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Shifting cold to hot tumors by nanoparticle-loaded drugs and products

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Abstract

Cold tumors lack antitumor immunity and are resistant to therapy, representing a major challenge in cancer medicine. Because of the immunosuppressive spirit of the tumor microenvironment (TME), this form of tumor has a low response to immunotherapy, radiotherapy, and also chemotherapy. Cold tumors have low infiltration of immune cells and a high expression of co-inhibitory molecules, such as immune checkpoints and immunosuppressive molecules. Therefore, targeting TME and remodeling immunity in cold tumors can improve the chance of tumor repression after therapy. However, tumor stroma prevents the infiltration of inflammatory cells and hinders the penetration of diverse molecules and drugs. Nanoparticles are an intriguing tool for the delivery of immune modulatory agents and shifting cold to hot tumors. In this review article, we discuss the mechanisms underlying the ability of nanoparticles loaded with different drugs and products to modulate TME and enhance immune cell infiltration. We also focus on newest progresses in the design and development of nanoparticle-based strategies for changing cold to hot tumors. These include the use of nanoparticles for targeted delivery of immunomodulatory agents, such as cytokines, small molecules, and checkpoint inhibitors, and for co-delivery of chemotherapy drugs and immunomodulatory agents. Furthermore, we discuss the potential of nanoparticles for enhancing the efficacy of cancer vaccines and cell therapy for overcoming resistance to treatment.

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References

  1. O’Neill RE, Cao X. Co-stimulatory and co-inhibitory pathways in cancer immunotherapy. Adv Cancer Res. 2019;143:145–94.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Zhang J, Shi Z, Xu X, Yu Z, Mi J. The influence of microenvironment on tumor immunotherapy. FEBS J. 2019;286(21):4160–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Zhang J, Huang D, Saw PE, Song E. Turning cold tumors hot: from molecular mechanisms to clinical applications. Trends Immunol. 2022;43(7):523–45.

    Article  CAS  PubMed  Google Scholar 

  4. Bonaventura P, Shekarian T, Alcazer V, Valladeau-Guilemond J, Valsesia-Wittmann S, Amigorena S, et al. Cold tumors: a therapeutic challenge for immunotherapy. Front Immunol. 2019;10:168.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Wang M, Wang S, Desai J, Trapani JA, Neeson PJ. Therapeutic strategies to remodel immunologically cold tumors. Clin Transl Immunol. 2020;9(12):e1226.

    Article  Google Scholar 

  6. Banu SPNS, Narayan S. Biomaterial based nanocarriers for delivering immunomodulatory agents. Nanomed Res J. 2021;6(3):195–217.

    Google Scholar 

  7. Park W, Heo Y-J, Han DK. New opportunities for nanoparticles in cancer immunotherapy. Biomater Res. 2018;22:1–10.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Fontana F, Liu D, Hirvonen J, Santos HA. Delivery of therapeutics with nanoparticles: what’s new in cancer immunotherapy? Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2017;9(1):e1421.

    Article  Google Scholar 

  9. Lee MS, Dees EC, Wang AZ. Nanoparticle-delivered chemotherapy: old drugs in new packages. Oncology (Williston Park). 2017;31(3):198–208.

    PubMed  Google Scholar 

  10. Chidambaram M, Manavalan R, Kathiresan K. Nanotherapeutics to overcome conventional cancer chemotherapy limitations. J Pharm Pharm Sci. 2011;14(1):67–77.

    Article  PubMed  Google Scholar 

  11. Wang M, Zhao J, Zhang L, Wei F, Lian Y, Wu Y, et al. Role of tumor microenvironment in tumorigenesis. J Cancer. 2017;8(5):761.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Lyssiotis CA, Kimmelman AC. Metabolic interactions in the tumor microenvironment. Trends Cell Biol. 2017;27(11):863–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Mohme M, Riethdorf S, Pantel K. Circulating and disseminated tumour cells—mechanisms of immune surveillance and escape. Nat Rev Clin Oncol. 2017;14(3):155–67.

    Article  CAS  PubMed  Google Scholar 

  14. Chow MT, Möller A, Smyth MJ, editors (2012) Inflammation and immune surveillance in cancer. Semin Cancer Biol: Elsevier.

  15. Fearon DT. The carcinoma-associated fibroblast expressing fibroblast activation protein and escape from immune surveillance. Cancer Immunol Res. 2014;2(3):187–93.

    Article  CAS  PubMed  Google Scholar 

  16. Denton AE, Roberts EW, Fearon DT. Stromal cells in the tumor microenvironment. Stromal Immunol. 2018;1060:99–114.

    CAS  Google Scholar 

  17. Lambrechts D, Wauters E, Boeckx B, Aibar S, Nittner D, Burton O, et al. Phenotype molding of stromal cells in the lung tumor microenvironment. Nat Med. 2018;24(8):1277–89.

    Article  CAS  PubMed  Google Scholar 

  18. Gajewski TF, Schreiber H, Fu Y-X. Innate and adaptive immune cells in the tumor microenvironment. Nat Immunol. 2013;14(10):1014–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Fu C, Jiang A. Dendritic cells and CD8 T cell immunity in tumor microenvironment. Front Immunol. 2018;9:3059.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Hadrup S, Donia M, Thor SP. Effector CD4 and CD8 T cells and their role in the tumor microenvironment. Cancer Microenviron. 2013;6:123–33.

    Article  CAS  PubMed  Google Scholar 

  21. Xie Q, Ding J, Chen Y. Role of CD8+ T lymphocyte cells: Interplay with stromal cells in tumor microenvironment. Acta Pharmaceutica Sinica B. 2021;11(6):1365–78.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Fricke I, Gabrilovich DI. Dendritic cells and tumor microenvironment: a dangerous liaison. Immunol Invest. 2006;35(3–4):459–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Wicherska-Pawłowska K, Wróbel T, Rybka J. Toll-like receptors (TLRs), NOD-like receptors (NLRs), and RIG-I-like receptors (RLRs) in innate immunity TLRs, NLRs, and RLRs ligands as immunotherapeutic agents for hematopoietic diseases. Int J Mol Sci. 2021;22(24):13397.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Liu Z, Han C, Fu Y-X. Targeting innate sensing in the tumor microenvironment to improve immunotherapy. Cell Mol Immunol. 2020;17(1):13–26.

    Article  CAS  PubMed  Google Scholar 

  25. Verneau J, Sautés-Fridman C, Sun C-M. Dendritic cells in the tumor microenvironment: prognostic and theranostic impact. Semin Immunol. 2020;48:101410.

    Article  CAS  PubMed  Google Scholar 

  26. Vitale M, Cantoni C, Pietra G, Mingari MC, Moretta L. Effect of tumor cells and tumor microenvironment on NK-cell function. Eur J Immunol. 2014;44(6):1582–92.

    Article  CAS  PubMed  Google Scholar 

  27. Myers JA, Schirm D, Bendzick L, Hopps R, Selleck C, Hinderlie P, et al. Balanced engagement of activating and inhibitory receptors mitigates human NK cell exhaustion. JCI insight. 2022;7(15):e150079.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Tallerico R, Todaro M, Di Franco S, Maccalli C, Garofalo C, Sottile R, et al. Human NK cells selective targeting of colon cancer–initiating cells: a role for natural cytotoxicity receptors and MHC class I molecules. J Immunol. 2013;190(5):2381–90.

    Article  CAS  PubMed  Google Scholar 

  29. Wörmann S, Diakopoulos K, Lesina M, Algül H. The immune network in pancreatic cancer development and progression. Oncogene. 2014;33(23):2956–67.

    Article  PubMed  Google Scholar 

  30. Harden JL, Egilmez NK. Indoleamine 2,3-dioxygenase and dendritic cell tolerogenicity. Immunol Invest. 2012;41(6–7):738–64. https://doi.org/10.3109/08820139.2012.676122.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Tanaka A, Sakaguchi S. Regulatory T cells in cancer immunotherapy. Cell Res. 2017;27(1):109–18.

    Article  CAS  PubMed  Google Scholar 

  32. Giannotta C, Autino F, Massaia M. The immune suppressive tumor microenvironment in multiple myeloma: the contribution of myeloid-derived suppressor cells. Front Immunol. 2023;13:1102471.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Sionov RV, Fridlender ZG, Granot Z. The multifaceted roles neutrophils play in the tumor microenvironment. Cancer Microenviron. 2015;8:125–58.

    Article  CAS  PubMed  Google Scholar 

  34. Genin M, Clement F, Fattaccioli A, Raes M, Michiels C. M1 and M2 macrophages derived from THP-1 cells differentially modulate the response of cancer cells to etoposide. BMC Cancer. 2015;15(1):1–14.

    Article  CAS  Google Scholar 

  35. Keeley T, Costanzo-Garvey DL, Cook LM. Unmasking the many faces of tumor-associated neutrophils and macrophages: considerations for targeting innate immune cells in cancer. Trends in cancer. 2019;5(12):789–98.

    Article  CAS  PubMed  Google Scholar 

  36. Viallard C, Larrivée B. Tumor angiogenesis and vascular normalization: alternative therapeutic targets. Angiogenesis. 2017;20(4):409–26.

    Article  CAS  PubMed  Google Scholar 

  37. Muz B, de la Puente P, Azab F, Kareem AA. The role of hypoxia in cancer progression, angiogenesis, metastasis, and resistance to therapy. Hypoxia. 2015;3:83–92.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Kumar V, Gabrilovich DI. Hypoxia-inducible factors in regulation of immune responses in tumour microenvironment. Immunology. 2014;143(4):512–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Taylor S, Spugnini EP, Assaraf YG, Azzarito T, Rauch C, Fais S. Microenvironment acidity as a major determinant of tumor chemoresistance: proton pump inhibitors (PPIs) as a novel therapeutic approach. Drug Resist Updates. 2015;23:69–78.

    Article  Google Scholar 

  40. Tomaszewski W, Sanchez-Perez L, Gajewski TF, Sampson JH. Brain tumor microenvironment and host state: implications for immunotherapy. Clin Cancer Res. 2019;25(14):4202–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Zhang S, Kohli K, Black RG, Yao L, Spadinger SM, He Q, et al. Systemic interferon-γ increases MHC class I expression and T-cell infiltration in cold tumors: results of a phase 0 clinical trial. Cancer Immunol Res. 2019;7(8):1237–43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Mirlekar B. Tumor promoting roles of IL-10, TGF-β, IL-4, and IL-35: Its implications in cancer immunotherapy. SAGE Open Med. 2022;10:20503121211069012.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Zhang Y, Guan X-Y, Jiang P. Cytokine and chemokine signals of T-cell exclusion in tumors. Front Immunol. 2020;11:594609.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Popovic A, Jaffee EM, Zaidi N. Emerging strategies for combination checkpoint modulators in cancer immunotherapy. J Clin Investig. 2018;128(8):3209–18.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Mortezaee K. Immune escape: a critical hallmark in solid tumors. Life Sci. 2020;258:118110.

    Article  CAS  PubMed  Google Scholar 

  46. Mu Q, Najafi M. Resveratrol for targeting the tumor microenvironment and its interactions with cancer cells. Int Immunopharmacol. 2021;98:107895.

    Article  CAS  PubMed  Google Scholar 

  47. Pelly VS, Moeini A, Roelofsen LM, Bonavita E, Bell CR, Hutton C, et al. Anti-inflammatory drugs remodel the tumor immune environment to enhance immune checkpoint blockade efficacy. Cancer Discov. 2021;11(10):2602–19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Tekpli X, Lien T, Røssevold AH, Nebdal D, Borgen E, Ohnstad HO, et al. An independent poor-prognosis subtype of breast cancer defined by a distinct tumor immune microenvironment. Nat Commun. 2019;10(1):5499.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Vasan N, Baselga J, Hyman DM. A view on drug resistance in cancer. Nature. 2019;575(7782):299–309.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Rezaei M, Danilova ND, Soltani M, Savvateeva LV, Tarasov VV, Ganjalikhani-Hakemi M, et al. Cancer vaccine in cold tumors: clinical landscape, challenges, and opportunities. Curr Cancer Drug Targets. 2022;22(6):437–53.

    Article  CAS  PubMed  Google Scholar 

  51. Runcie KD, Dallos MC. Prostate cancer immunotherapy—finally in from the cold? Curr Oncol Rep. 2021;23(8):88.

    Article  PubMed  Google Scholar 

  52. De Nunzio C, Andriole GL, Thompson IM Jr, Freedland SJ. Smoking and prostate cancer: a systematic review. Eur Urol Focus. 2015;1(1):28–38.

    Article  PubMed  Google Scholar 

  53. Tian M, Ma W, Chen Y, Yu Y, Zhu D, Shi J, Zhang Y. Impact of gender on the survival of patients with glioblastoma. Biosci Rep. 2018;38(6):BSR20180752.

    Article  PubMed  PubMed Central  Google Scholar 

  54. McFarlane T, Zajac JD, Cheung AS. Gender-affirming hormone therapy and the risk of sex hormone-dependent tumours in transgender individuals—a systematic review. Clin Endocrinol (Oxf). 2018;89(6):700–11.

    Article  CAS  PubMed  Google Scholar 

  55. Allegra A, Caserta S, Genovese S, Pioggia G, Gangemi S. Gender differences in oxidative stress in relation to cancer susceptibility and survival. Antioxidants. 2023;12(6):1255.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Galon J, Bruni D. Approaches to treat immune hot, altered and cold tumours with combination immunotherapies. Nat Rev Drug Discov. 2019;18(3):197–218.

    Article  CAS  PubMed  Google Scholar 

  57. Kather JN, Suarez-Carmona M, Charoentong P, Weis C-A, Hirsch D, Bankhead P, et al. Topography of cancer-associated immune cells in human solid tumors. Elife. 2018;7:e36967.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Bernatchez C, Haymaker C, Tannir NM, Kluger H, Tetzlaff M, Bentebibel SE, et al. A CD122-biased agonist increases CD8+ T Cells and natural killer cells in the tumor microenvironment; making cold tumors hot with NKTR-214. Cough. 2016;5(1):3.

    Google Scholar 

  59. Wargo JA, Reddy SM, Reuben A, Sharma P. Monitoring immune responses in the tumor microenvironment. Curr Opin Immunol. 2016;41:23–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Burkholder B, Huang R-Y, Burgess R, Luo S, Jones VS, Zhang W, et al. (2014) Tumor-induced perturbations of cytokines and immune cell networks. Biochimica et Biophysica Acta (BBA)-Revi Cancer. 1845;2:182–201.

    Google Scholar 

  61. De Guillebon E, Dardenne A, Saldmann A, Séguier S, Tran T, Paolini L, et al. Beyond the concept of cold and hot tumors for the development of novel predictive biomarkers and the rational design of immunotherapy combination. Int J Cancer. 2020;147(6):1509–18.

    Article  PubMed  Google Scholar 

  62. Fan H, Shi Y, Wang H, Li Y, Mei J, Xu J, Liu C. GBP5 identifies immuno-hot tumors and predicts the therapeutic response to immunotherapy in NSCLC. Int J General Med. 2023;16:1757–69.

    Article  CAS  Google Scholar 

  63. Li X, Luo L, Jiang M, Zhu C, Shi Y, Zhang J, et al. Cocktail strategy for ‘cold’tumors therapy via active recruitment of CD8+ T cells and enhancing their function. J Control Release. 2021;334:413–26.

    Article  CAS  PubMed  Google Scholar 

  64. Zhao Z, Liu H, Zhou X, Fang D, Ou X, Ye J, et al. Necroptosis-related lncRNAs: predicting prognosis and the distinction between the cold and hot tumors in gastric cancer. J Oncol. 2021;2021:6718443.

    Article  PubMed  PubMed Central  Google Scholar 

  65. O’Connor JP, Rose CJ, Waterton JC, Carano RA, Parker GJ, Jackson A. Imaging intratumor heterogeneity: role in therapy response, resistance, and clinical outcome. Clin Cancer Res. 2015;21(2):249–57.

    Article  CAS  PubMed  Google Scholar 

  66. Wang L, Geng H, Liu Y, Liu L, Chen Y, Wu F, et al. Hot and cold tumors: immunological features and the therapeutic strategies. MedComm. 2023;4(5):e343.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Nassar KW, Tan AC. The mutational landscape of mucosal melanoma. Semin Cancer Biol. 2020;61:139–48.

    Article  CAS  PubMed  Google Scholar 

  68. O’Brien SM, Klampatsa A, Thompson JC, Martinez MC, Hwang W-T, Rao AS, et al. Function of human tumor-infiltrating lymphocytes in early-stage non–small cell lung cancer. Cancer Immunol Res. 2019;7(6):896–909.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Lazdun Y, Si H, Creasy T, Ranade K, Higgs BW, Streicher K, Durham NM. A new pipeline to predict and confirm tumor neoantigens predict better response to immune checkpoint blockade. Mol Cancer Res. 2021;19(3):498–506.

    Article  CAS  PubMed  Google Scholar 

  70. Gameiro SF, Evans AM, Mymryk JS. The tumor immune microenvironments of HPV+ and HPV−head and neck cancers. WIREs Mechanisms of Disease. 2022;14(2):e1539.

    Article  CAS  PubMed  Google Scholar 

  71. Kanavy HE, Gerstenblith MR. Ultraviolet radiation and melanoma. Semin Cutan Med Surg. 2011;30:222–8.

    Article  CAS  PubMed  Google Scholar 

  72. Ernst SM, Mankor JM, van Riet J, von der Thüsen JH, Dubbink HJ, Aerts JG, et al. Tobacco smoking-related mutational signatures in classifying smoking-associated and nonsmoking-associated NSCLC. J Thorac Oncol. 2023;18(4):487–98.

    Article  CAS  PubMed  Google Scholar 

  73. Farling KB. Bladder cancer: risk factors, diagnosis, and management. Nurse Pract. 2017;42(3):26–33.

    Article  PubMed  Google Scholar 

  74. Gormley M, Creaney G, Schache A, Ingarfield K, Conway DI. Reviewing the epidemiology of head and neck cancer: definitions, trends and risk factors. Br Dent J. 2022;233(9):780–6.

    Article  PubMed  PubMed Central  Google Scholar 

  75. Schwartz MR, Luo L, Berwick M. Sex differences in melanoma. Current Epidemiol Rep. 2019;6:112–8.

    Article  Google Scholar 

  76. Frega S, Ferro A, Bonanno L, Guarneri V, Conte P, Pasello G. Sex-based heterogeneity in non-small cell lung cancer (NSCLC) and response to immune checkpoint inhibitors (ICIs): a narrative review. Precision Cancer Medi. 2021;4:100251.

    Google Scholar 

  77. Gul ZG, Liaw CW, Mehrazin R. Gender differences in incidence, diagnosis, treatments, and outcomes in clinically localized bladder and renal cancer. Urology. 2021;151:176–81. https://doi.org/10.1016/j.urology.2020.05.067.

    Article  PubMed  Google Scholar 

  78. Park J-O, Nam I-C, Kim C-S, Park S-J, Lee D-H, Kim H-B, et al. Sex Differences in the prevalence of head and neck cancers: a 10-year follow-up study of 10 million healthy people. Cancers (Basel). 2022;14(10):2521.

    Article  CAS  PubMed  Google Scholar 

  79. Liu J, Chen Z, Li Y, Zhao W, Wu J, Zhang Z. PD-1/PD-L1 checkpoint inhibitors in tumor immunotherapy. Front Pharmacol. 2021;12:731798.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Toor SM, Nair VS, Decock J, Elkord E. Immune checkpoints in the tumor microenvironment. Semin Cancer Biol. 2020;65:1–12.

    Article  CAS  PubMed  Google Scholar 

  81. Giannone G, Ghisoni E, Genta S, Scotto G, Tuninetti V, Turinetto M, Valabrega G. Immuno-metabolism and microenvironment in cancer: key players for immunotherapy. Int J Mol Sci. 2020;21(12):4414.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Chyuan I-T, Chu C-L, Hsu P-N. Targeting the tumor microenvironment for improving therapeutic effectiveness in cancer immunotherapy: focusing on immune checkpoint inhibitors and combination therapies. Cancers. 2021;13(6):1188.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Ma Y, Conforti R, Aymeric L, Locher C, Kepp O, Kroemer G, Zitvogel L. How to improve the immunogenicity of chemotherapy and radiotherapy. Cancer Metastasis Rev. 2011;30:71–82.

    Article  CAS  PubMed  Google Scholar 

  84. Galassi C, Klapp V, Yamazaki T, Galluzzi L. Molecular determinants of immunogenic cell death elicited by radiation therapy. Immunol Rev. 2023;321:20–32.

    Article  PubMed  PubMed Central  Google Scholar 

  85. Wang Q, Ju X, Wang J, Fan Y, Ren M, Zhang H. Immunogenic cell death in anticancer chemotherapy and its impact on clinical studies. Cancer Lett. 2018;438:17–23.

    Article  CAS  PubMed  Google Scholar 

  86. Fabian KP, Kowalczyk JT, Reynolds ST, Hodge JW. Dying of stress: chemotherapy, radiotherapy, and small-molecule inhibitors in immunogenic cell death and immunogenic modulation. Cells. 2022;11(23):3826.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Ludgate CM. Optimizing cancer treatments to induce an acute immune response: radiation Abscopal effects, PAMPs, and DAMPs. Clin Cancer Res. 2012;18(17):4522–5.

    Article  CAS  PubMed  Google Scholar 

  88. Garg AD, Agostinis P. Cell death and immunity in cancer: from danger signals to mimicry of pathogen defense responses. Immunol Rev. 2017;280(1):126–48.

    Article  CAS  PubMed  Google Scholar 

  89. Nkune NW, Simelane NWN, Montaseri H, Abrahamse H. Photodynamic therapy-mediated immune responses in three-dimensional tumor models. Int J Mol Sci. 2021;22(23):12618.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Li W, Yang J, Luo L, Jiang M, Qin B, Yin H, et al. Targeting photodynamic and photothermal therapy to the endoplasmic reticulum enhances immunogenic cancer cell death. Nat Commun. 2019;10(1):3349.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Panzarini E, Inguscio V, Dini L. Immunogenic cell death: can it be exploited in photodynamic therapy for cancer? BioMed Res Int. 2013. https://doi.org/10.1155/2013/482160.

    Article  PubMed  Google Scholar 

  92. Wang S-B, Zhang C, Ye J-J, Zou M-Z, Liu C-J, Zhang X-Z. Near-infrared light responsive nanoreactor for simultaneous tumor photothermal therapy and carbon monoxide-mediated anti-inflammation. ACS Cent Sci. 2020;6(4):555–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Lima-Sousa R, Melo BL, Alves CG, Moreira AF, Mendonça AG, Correia IJ, de Melo-Diogo D. Combining photothermal-photodynamic therapy mediated by nanomaterials with immune checkpoint blockade for metastatic cancer treatment and creation of immune memory. Adv Func Mater. 2021;31(29):2010777.

    Article  CAS  Google Scholar 

  94. Kong C, Chen X. Combined photodynamic and photothermal therapy and immunotherapy for cancer treatment: a review. Int J Nanomed. 2022;17:6427.

    Article  Google Scholar 

  95. Jurj A, Braicu C, Pop L-A, Tomuleasa C, Gherman CD, Berindan-Neagoe I. The new era of nanotechnology, an alternative to change cancer treatment. Drug Des Devel Ther. 2017;11:2871–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Paul W, Sharma CP. Inorganic nanoparticles for targeted drug delivery. Biointegr Med Implant Mater. 2020. https://doi.org/10.1016/B978-0-08-102680-9.00013-5.

    Article  Google Scholar 

  97. Zhao J, Lee P, Wallace J, M, P Melancon M,. Gold nanoparticles in cancer therapy: efficacy, biodistribution, and toxicity. Curr Pharm Des. 2015;21(29):4240–51.

    Article  CAS  PubMed  Google Scholar 

  98. Goddard ZR, Marín MJ, Russell DA, Searcey M. Active targeting of gold nanoparticles as cancer therapeutics. Chem Soc Rev. 2020;49(23):8774–89.

    Article  CAS  PubMed  Google Scholar 

  99. Beik J, Khateri M, Khosravi Z, Kamrava SK, Kooranifar S, Ghaznavi H, Shakeri-Zadeh A. Gold nanoparticles in combinatorial cancer therapy strategies. Coord Chem Rev. 2019;387:299–324.

    Article  CAS  Google Scholar 

  100. Fu Q, Zhang X, Song J, Yang H. Plasmonic gold nanoagents for cancer imaging and therapy. View. 2021;2(5):20200149.

    Article  CAS  Google Scholar 

  101. Zhao S, Yu X, Qian Y, Chen W, Shen J. Multifunctional magnetic iron oxide nanoparticles: an advanced platform for cancer theranostics. Theranostics. 2020;10(14):6278.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Espinosa A, Di Corato R, Kolosnjaj-Tabi J, Flaud P, Pellegrino T, Wilhelm C. Duality of iron oxide nanoparticles in cancer therapy: amplification of heating efficiency by magnetic hyperthermia and photothermal bimodal treatment. ACS Nano. 2016;10(2):2436–46.

    Article  CAS  PubMed  Google Scholar 

  103. Bazak R, Houri M, El Achy S, Kamel S, Refaat T. Cancer active targeting by nanoparticles: a comprehensive review of literature. J Cancer Res Clin Oncol. 2015;141:769–84.

    Article  CAS  PubMed  Google Scholar 

  104. Lappas CM. The immunomodulatory effects of titanium dioxide and silver nanoparticles. Food Chem Toxicol. 2015;85:78–83.

    Article  CAS  PubMed  Google Scholar 

  105. Alyassin Y, Sayed EG, Mehta P, Ruparelia K, Arshad MS, Rasekh M, et al. Application of mesoporous silica nanoparticles as drug delivery carriers for chemotherapeutic agents. Drug Discov Today. 2020;25(8):1513–20.

    Article  CAS  PubMed  Google Scholar 

  106. Barkat A, Beg S, Panda SK, Alharbi KS, Rahman M, Ahmed FJ. Functionalized mesoporous silica nanoparticles in anticancer therapeutics. Semin Cancer Biol. 2021;69:365–75.

    Article  CAS  PubMed  Google Scholar 

  107. Sabio RM, Meneguin AB, Ribeiro TC, Silva RR, Chorilli M. New insights towards mesoporous silica nanoparticles as a technological platform for chemotherapeutic drugs delivery. Int J Pharm. 2019;564:379–409.

    Article  CAS  PubMed  Google Scholar 

  108. Rao PV, Nallappan D, Madhavi K, Rahman S, Jun Wei L, Gan SH. Phytochemicals and biogenic metallic nanoparticles as anticancer agents. Oxid Med Cell Longev. 2016. https://doi.org/10.1155/2016/3685671.

    Article  PubMed  PubMed Central  Google Scholar 

  109. Tu X, Ma Y, Cao Y, Huang J, Zhang M, Zhang Z. PEGylated carbon nanoparticles for efficient in vitro photothermal cancer therapy. J Mater Chem B. 2014;2(15):2184–92.

    Article  CAS  PubMed  Google Scholar 

  110. Xu G, Liu S, Niu H, Lv W. Functionalized mesoporous carbon nanoparticles for targeted chemo-photothermal therapy of cancer cells under near-infrared irradiation. RSC Adv. 2014;4(64):33986–97.

    Article  CAS  Google Scholar 

  111. Sadeghi MS, Sangrizeh FH, Jahani N, Abedin MS, Chaleshgari S, Ardakan AK, et al. Graphene oxide nanoarchitectures in cancer therapy: drug and gene delivery, phototherapy, immunotherapy, and vaccine development. Environ Res. 2023;237:117027.

    Article  CAS  PubMed  Google Scholar 

  112. Li K, Liu B. Polymer-encapsulated organic nanoparticles for fluorescence and photoacoustic imaging. Chem Soc Rev. 2014;43(18):6570–97.

    Article  CAS  PubMed  Google Scholar 

  113. Lu Y, Yue Z, Xie J, Wang W, Zhu H, Zhang E, Cao Z. Micelles with ultralow critical micelle concentration as carriers for drug delivery. Nat Biomed Eng. 2018;2(5):318–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Chen L, Zang F, Wu H, Li J, Xie J, Ma M, et al. Using PEGylated magnetic nanoparticles to describe the EPR effect in tumor for predicting therapeutic efficacy of micelle drugs. Nanoscale. 2018;10(4):1788–97.

    Article  CAS  PubMed  Google Scholar 

  115. Khalid M, El-Sawy HS. Polymeric nanoparticles: promising platform for drug delivery. Int J Pharm. 2017;528(1–2):675–91.

    Google Scholar 

  116. Wang Y, Lin Y-X, Qiao S-L, An H-W, Ma Y, Qiao Z-Y, et al. Polymeric nanoparticles promote macrophage reversal from M2 to M1 phenotypes in the tumor microenvironment. Biomaterials. 2017;112:153–63.

    Article  CAS  PubMed  Google Scholar 

  117. Duan Y, Dhar A, Patel C, Khimani M, Neogi S, Sharma P, et al. A brief review on solid lipid nanoparticles: Part and parcel of contemporary drug delivery systems. RSC Adv. 2020;10(45):26777–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Guimarães D, Cavaco-Paulo A, Nogueira E. Design of liposomes as drug delivery system for therapeutic applications. Int J Pharm. 2021;601:120571.

    Article  PubMed  Google Scholar 

  119. Souto EB, Baldim I, Oliveira WP, Rao R, Yadav N, Gama FM, Mahant S. SLN and NLC for topical, dermal, and transdermal drug delivery. Expert Opin Drug Deliv. 2020;17(3):357–77.

    Article  CAS  PubMed  Google Scholar 

  120. Baek J-S, Cho C-W. Controlled release and reversal of multidrug resistance by co-encapsulation of paclitaxel and verapamil in solid lipid nanoparticles. Int J Pharm. 2015;478(2):617–24.

    Article  CAS  PubMed  Google Scholar 

  121. Wilson RJ, Li Y, Yang G, Zhao C-X. Nanoemulsions for drug delivery. Particuology. 2022;64:85–97.

    Article  CAS  Google Scholar 

  122. Meldolesi J. Exosomes and ectosomes in intercellular communication. Curr Biol. 2018;28(8):R435–44.

    Article  CAS  PubMed  Google Scholar 

  123. Batrakova EV, Kim MS. Using exosomes, naturally-equipped nanocarriers, for drug delivery. J Control Release. 2015;219:396–405.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Kibria G, Ramos EK, Wan Y, Gius DR, Liu H. Exosomes as a drug delivery system in cancer therapy: potential and challenges. Mol Pharm. 2018;15(9):3625–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Kaur D, Jain K, Mehra NK, Kesharwani P, Jain NK. A review on comparative study of PPI and PAMAM dendrimers. J Nanopart Res. 2016;18:1–14.

    Article  CAS  Google Scholar 

  126. Chauhan AS. Dendrimers for drug delivery. Molecules. 2018;23(4):938.

    Article  PubMed  PubMed Central  Google Scholar 

  127. Zhou J, Wang G, Chen Y, Wang H, Hua Y, Cai Z. Immunogenic cell death in cancer therapy: present and emerging inducers. J Cell Mol Med. 2019;23(8):4854–65.

    Article  PubMed  PubMed Central  Google Scholar 

  128. Ashrafizadeh M, Farhood B, Musa AE, Taeb S, Najafi M. The interactions and communications in tumor resistance to radiotherapy: therapy perspectives. Int Immunopharmacol. 2020;87:106807.

    Article  CAS  PubMed  Google Scholar 

  129. Zhu M, Yang M, Zhang J, Yin Y, Fan X, Zhang Y, et al. Immunogenic cell death induction by ionizing radiation. Front Immunol. 2021;12:705361.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Khodamoradi E, Hoseini-Ghahfarokhi M, Amini P, Motevaseli E, Shabeeb D, Musa AE, et al. Targets for protection and mitigation of radiation injury. Cell Mol Life Sci. 2020;77:3129–59.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Liu P, Zhao L, Zitvogel L, Kepp O, Kroemer G. Immunogenic cell death (ICD) enhancers—Drugs that enhance the perception of ICD by dendritic cells. Immunol Rev. 2023;32:7–19.

    Google Scholar 

  132. Martins I, Wang Y, Michaud M, Ma Y, Sukkurwala A, Shen S, et al. Molecular mechanisms of ATP secretion during immunogenic cell death. Cell Death Differ. 2014;21(1):79–91.

    Article  CAS  PubMed  Google Scholar 

  133. Yahyapour R, Salajegheh A, Safari A, Amini P, Rezaeyan A, Amraee A, Najafi M. Radiation-induced non-targeted effect and carcinogenesis; implications in clinical radiotherapy. J Biomed Phys Eng. 2018;8(4):435.

    CAS  PubMed  PubMed Central  Google Scholar 

  134. Moloudi K, Khani A, Najafi M, Azmoonfar R, Azizi M, Nekounam H, et al. Critical parameters to translate gold nanoparticles as radiosensitizing agents into the clinic. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2023;15:e1886.

    Article  CAS  PubMed  Google Scholar 

  135. Maggiorella L, Barouch G, Devaux C, Pottier A, Deutsch E, Bourhis J, et al. Nanoscale radiotherapy with hafnium oxide nanoparticles. Future Oncol. 2012;8(9):1167–81.

    Article  CAS  PubMed  Google Scholar 

  136. Zhang P, Darmon A, Marill J, Mohamed Anesary N, Paris S. Radiotherapy-activated hafnium oxide nanoparticles produce abscopal effect in a mouse colorectal cancer model. Int J Nanomed. 2020;15:3843–50.

    Article  CAS  Google Scholar 

  137. Siva S, MacManus MP, Martin RF, Martin OA. Abscopal effects of radiation therapy: a clinical review for the radiobiologist. Cancer Lett. 2015;356(1):82–90.

    Article  CAS  PubMed  Google Scholar 

  138. Grass GD, Krishna N, Kim S. The immune mechanisms of abscopal effect in radiation therapy. Curr Probl Cancer. 2016;40(1):10–24.

    Article  PubMed  Google Scholar 

  139. Bonvalot S, Le Pechoux C, De Baere T, Kantor G, Buy X, Stoeckle E, et al. First-in-human study testing a new radioenhancer using nanoparticles (NBTXR3) activated by radiation therapy in patients with locally advanced soft tissue sarcomas. Clin Cancer Res. 2017;23(4):908–17. https://doi.org/10.1158/1078-0432.Ccr-16-1297.

    Article  CAS  PubMed  Google Scholar 

  140. Bonvalot S, Rutkowski PL, Thariat J, Carrère S, Ducassou A, Sunyach M-P, et al. NBTXR3, a first-in-class radioenhancer hafnium oxide nanoparticle, plus radiotherapy versus radiotherapy alone in patients with locally advanced soft-tissue sarcoma (ActInSarc): a multicentre, phase 2–3, randomised, controlled trial. Lancet Oncol. 2019;20(8):1148–59. https://doi.org/10.1016/S1470-2045(19)30326-2.

    Article  CAS  PubMed  Google Scholar 

  141. Vanmeerbeek I, Sprooten J, De Ruysscher D, Tejpar S, Vandenberghe P, Fucikova J, et al. Trial watch: chemotherapy-induced immunogenic cell death in immuno-oncology. Oncoimmunology. 2020;9(1):1703449.

    Article  PubMed  PubMed Central  Google Scholar 

  142. Liu Z, Xu X, Liu K, Zhang J, Ding D, Fu R. Immunogenic cell death in hematological malignancy therapy. Adv Sci. 2023;10(13):2207475.

    Article  CAS  Google Scholar 

  143. Kim D-Y, Pyo A, Yun M, Thangam R, You S-H, Zhang Y, et al. Imaging calreticulin for early detection of immunogenic cell death during anticancer treatment. J Nucl Med. 2021;62(7):956–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Zhao C-Y, Cheng R, Yang Z, Tian Z-M. Nanotechnology for cancer therapy based on chemotherapy. Molecules. 2018;23(4):826.

    Article  PubMed  PubMed Central  Google Scholar 

  145. Fu L, Ma X, Liu Y, Xu Z, Sun Z. Applying nanotechnology to boost cancer immunotherapy by promoting immunogenic cell death. Chin Chem Lett. 2022;33(4):1718–28.

    Article  CAS  Google Scholar 

  146. Duan X, Chan C, Lin W. Nanoparticle-mediated immunogenic cell death enables and potentiates cancer immunotherapy. Angew Chem Int Ed. 2019;58(3):670–80.

    Article  CAS  Google Scholar 

  147. Duan X, Chan C, Lin W. Nanoparticle-mediated immunogenic cell death enables and potentiates cancer immunotherapy. Angew Chem Int Ed Engl. 2019;58(3):670–80. https://doi.org/10.1002/anie.201804882.

    Article  CAS  PubMed  Google Scholar 

  148. Guo J, Yu Z, Sun D, Zou Y, Liu Y, Huang L. Two nanoformulations induce reactive oxygen species and immunogenetic cell death for synergistic chemo-immunotherapy eradicating colorectal cancer and hepatocellular carcinoma. Mol Cancer. 2021;20(1):10. https://doi.org/10.1186/s12943-020-01297-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Liu J, Li Z, Zhao D, Feng X, Wang C, Li D, Ding J. Immunogenic cell death-inducing chemotherapeutic nanoformulations potentiate combination chemoimmunotherapy. Mater Des. 2021;202:109465.

    Article  CAS  Google Scholar 

  150. Wang Y, Wang Z, Chen B, Yin Q, Pan M, Xia H, et al. Cooperative self-assembled nanoparticle induces sequential immunogenic cell death and toll-like receptor activation for synergistic chemo-immunotherapy. Nano Lett. 2021;21(10):4371–80. https://doi.org/10.1021/acs.nanolett.1c00977.

    Article  CAS  PubMed  Google Scholar 

  151. Overchuk M, Weersink RA, Wilson BC, Zheng G. Photodynamic and photothermal therapies: synergy opportunities for nanomedicine. ACS Nano. 2023;17(9):7979–8003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Kadkhoda J, Tarighatnia A, Barar J, Aghanejad A, Davaran S. Recent advances and trends in nanoparticles based photothermal and photodynamic therapy. Photodiagnosis Photodyn Ther. 2022;37:102697.

    Article  CAS  PubMed  Google Scholar 

  153. Bucharskaya A, Maslyakova G, Terentyuk G, Yakunin A, Avetisyan Y, Bibikova O, et al. Towards effective photothermal/photodynamic treatment using plasmonic gold nanoparticles. Int J Mol Sci. 2016;17(8):1295.

    Article  PubMed  PubMed Central  Google Scholar 

  154. Zhang H, Zhou F, Yang Q, Huang M. Targeting the oral tumor microenvironment by nanoparticles: a review of progresses. J Drug Deliv Sci Technol. 2023;91:105248.

    Article  Google Scholar 

  155. Qin L, Wu J. Targeting anticancer immunity in oral cancer: drugs, products, and nanoparticles. Environ Res. 2023;239:116751.

    Article  CAS  PubMed  Google Scholar 

  156. Yang M, Li J, Gu P, Fan X. The application of nanoparticles in cancer immunotherapy: targeting tumor microenvironment. Bioactive Mater. 2021;6(7):1973–87.

    Article  CAS  Google Scholar 

  157. Lu H. TLR agonists for cancer immunotherapy: tipping the balance between the immune stimulatory and inhibitory effects. Front Immunol. 2014;5:83.

    Article  PubMed  PubMed Central  Google Scholar 

  158. Chakraborty S, Ye J, Wang H, Sun M, Zhang Y, Sang X, Zhuang Z. Application of toll-like receptors (TLRs) and their agonists in cancer vaccines and immunotherapy. Front Immunol. 2023;14:1227833.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Ma F, Zhang J, Zhang J, Zhang C. The TLR7 agonists imiquimod and gardiquimod improve DC-based immunotherapy for melanoma in mice. Cell Mol Immunol. 2010;7(5):381–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Keshavarz A, Pourbagheri-Sigaroodi A, Zafari P, Bagheri N, Ghaffari SH, Bashash D. Toll-like receptors (TLRs) in cancer; with an extensive focus on TLR agonists and antagonists. IUBMB Life. 2021;73(1):10–25.

    Article  CAS  PubMed  Google Scholar 

  161. Chen X, Zhang Y, Fu Y. The critical role of Toll-like receptor-mediated signaling in cancer immunotherapy. Med Drug Discov. 2022;14:100122.

    Article  CAS  Google Scholar 

  162. Sultan H, Salazar AM, Celis E. Poly-ICLC, a multi-functional immune modulator for treating cancer. Semin Immunol. 2020;49:101414.

    Article  CAS  PubMed  Google Scholar 

  163. Zhang Y, Yuan T, Li Z, Luo C, Wu Y, Zhang J, et al. Hyaluronate-based self-stabilized nanoparticles for immunosuppression reversion and immunochemotherapy in osteosarcoma treatment. ACS Biomater Sci Eng. 2021;7(4):1515–25. https://doi.org/10.1021/acsbiomaterials.1c00081.

    Article  CAS  PubMed  Google Scholar 

  164. Huang Y, Nahar S, Alam MDM, Hu S, McVicar DW, Yang D. Reactive oxygen species-sensitive biodegradable mesoporous silica nanoparticles harboring theravac elicit tumor-specific immunity for colon tumor treatment. ACS Nano. 2023;17(20):19740–52. https://doi.org/10.1021/acsnano.3c03195.

    Article  CAS  PubMed  Google Scholar 

  165. Tambunlertchai S, Geary SM, Naguib YW, Salem AK. Investigating silver nanoparticles and resiquimod as a local melanoma treatment. Eur J Pharm Biopharm. 2023;183:1–12.

    Article  CAS  PubMed  Google Scholar 

  166. Kim H, Niu L, Larson P, Kucaba TA, Murphy KA, James BR, et al. Polymeric nanoparticles encapsulating novel TLR7/8 agonists as immunostimulatory adjuvants for enhanced cancer immunotherapy. Biomaterials. 2018;164:38–53. https://doi.org/10.1016/j.biomaterials.2018.02.034.

    Article  CAS  PubMed  Google Scholar 

  167. Bahmani B, Gong H, Luk BT, Haushalter KJ, DeTeresa E, Previti M, et al. Intratumoral immunotherapy using platelet-cloaked nanoparticles enhances antitumor immunity in solid tumors. Nat Commun. 2021;12(1):1999.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Widmer J, Thauvin C, Mottas I, Nguyen VN, Delie F, Allémann E, Bourquin C. Polymer-based nanoparticles loaded with a TLR7 ligand to target the lymph node for immunostimulation. Int J Pharm. 2018;535(1):444–51. https://doi.org/10.1016/j.ijpharm.2017.11.031.

    Article  CAS  PubMed  Google Scholar 

  169. Yin W, Qian S. Delivery of cisplatin and resiquimod in nanomicelles for the chemoimmunotherapy of ovarian cancer. Cancer Nanotechnology. 2022;13(1):8. https://doi.org/10.1186/s12645-021-00094-8.

    Article  CAS  Google Scholar 

  170. Zhang H, Tang WL, Kheirolomoom A, Fite BZ, Wu B, Lau K, et al. Development of thermosensitive resiquimod-loaded liposomes for enhanced cancer immunotherapy. J Control Release. 2021;330:1080–94. https://doi.org/10.1016/j.jconrel.2020.11.013.

    Article  CAS  PubMed  Google Scholar 

  171. Kakwere H, Zhang H, Ingham ES, Nura-Raie M, Tumbale SK, Allen R, et al. Systemic immunotherapy with micellar resiquimod-polymer conjugates triggers a robust antitumor response in a breast cancer model. Adv Healthc Mater. 2021;10(10):e2100008. https://doi.org/10.1002/adhm.202100008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Singh B, Maharjan S, Pan DC, Zhao Z, Gao Y, Zhang YS, Mitragotri S. Imiquimod-gemcitabine nanoparticles harness immune cells to suppress breast cancer. Biomaterials. 2022;280:121302. https://doi.org/10.1016/j.biomaterials.2021.121302.

    Article  CAS  PubMed  Google Scholar 

  173. Gondan AIB, Ruiz-de-Angulo A, Zabaleta A, Blanco NG, Cobaleda-Siles BM, García-Granda MJ, et al. Effective cancer immunotherapy in mice by polyIC-imiquimod complexes and engineered magnetic nanoparticles. Biomaterials. 2018;170:95–115.

    Article  Google Scholar 

  174. Yan W, Li Y, Zou Y, Zhu R, Wu T, Yuan W, et al. Co-delivering irinotecan and imiquimod by pH-responsive micelle amplifies anti-tumor immunity against colorectal cancer. Int J Pharm. 2023;648:123583. https://doi.org/10.1016/j.ijpharm.2023.123583.

    Article  CAS  PubMed  Google Scholar 

  175. Wen YH, Hsieh PI, Chiu HC, Chiang CW, Lo CL, Chiang YT. Precise delivery of doxorubicin and imiquimod through pH-responsive tumor microenvironment-active targeting micelles for chemo- and immunotherapy. Mater Today Bio. 2022;17:100482. https://doi.org/10.1016/j.mtbio.2022.100482.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Bagchi S, Yuan R, Engleman EG. Immune checkpoint inhibitors for the treatment of cancer: clinical impact and mechanisms of response and resistance. Annu Rev Pathol. 2021;16:223–49.

    Article  CAS  PubMed  Google Scholar 

  177. Marei HE, Hasan A, Pozzoli G, Cenciarelli C. Cancer immunotherapy with immune checkpoint inhibitors (ICIs): potential, mechanisms of resistance, and strategies for reinvigorating T cell responsiveness when resistance is acquired. Cancer Cell Int. 2023;23(1):64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Nagasaki J, Ishino T, Togashi Y. Mechanisms of resistance to immune checkpoint inhibitors. Cancer Sci. 2022;113(10):3303.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Shi C, Wang Y, Xue J, Zhou X. Immunotherapy for EGFR-mutant advanced non-small-cell lung cancer: current status, possible mechanisms and application prospects. Front Immunol. 2022;13:940288.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Zhao Y, Yang W, Huang Y, Cui R, Li X, Li B. Evolving roles for targeting CTLA-4 in cancer immunotherapy. Cell Physiol Biochem. 2018;47(2):721–34.

    Article  CAS  PubMed  Google Scholar 

  181. Chauvin J-M, Zarour HM. TIGIT in cancer immunotherapy. J Immunother Cancer. 2020;8(2):000957.

    Article  Google Scholar 

  182. Chu X, Tian W, Wang Z, Zhang J, Zhou R. Co-inhibition of TIGIT and PD-1/PD-L1 in cancer immunotherapy: mechanisms and clinical trials. Mol Cancer. 2023;22(1):1–31.

    Google Scholar 

  183. Dong M, Yu T, Zhang Z, Zhang J, Wang R, Tse G, et al. ICIs-related cardiotoxicity in different types of cancer. J Cardiovasc Develop Dis. 2022;9(7):203.

    CAS  Google Scholar 

  184. Boone CE, Wang L, Gautam A, Newton IG, Steinmetz NF. Combining nanomedicine and immune checkpoint therapy for cancer immunotherapy. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2022;14(1):e1739.

    Article  PubMed  Google Scholar 

  185. Badiee P, Maritz MF, Dmochowska N, Cheah E, Thierry B. Intratumoral Anti-PD-1 nanoformulation improves its biodistribution. ACS Appl Mater Interface. 2022;14(14):15881–93. https://doi.org/10.1021/acsami.1c22479.

    Article  CAS  Google Scholar 

  186. Ordikhani F, Uehara M, Kasinath V, Dai L, Eskandari SK, Bahmani B, et al. Targeting antigen-presenting cells by anti-PD-1 nanoparticles augments antitumor immunity. JCI Insight. 2018. https://doi.org/10.1172/jci.insight.122700.

    Article  PubMed  PubMed Central  Google Scholar 

  187. Wu Y, Gu W, Li L, Chen C, Xu ZP. Enhancing PD-1 gene silence in T lymphocytes by comparing the delivery performance of two inorganic nanoparticle platforms. Nanomaterials. 2019;9(2):159.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  188. Wu Y, Gu W, Li J, Chen C, Xu ZP. Silencing PD-1 and PD-L1 with nanoparticle-delivered small interfering RNA increases cytotoxicity of tumor-infiltrating lymphocytes. Nanomedicine. 2019;14(8):955–67.

    Article  CAS  PubMed  Google Scholar 

  189. Jeong W-j, Bu J, Han Y, Drelich AJ, Nair A, Král P, Hong S. Nanoparticle Conjugation stabilizes and multimerizes β-hairpin peptides to effectively target PD-1/PD-L1 β-sheet-rich interfaces. J Am Chem Soc. 2020;142(4):1832–7.

    Article  CAS  PubMed  Google Scholar 

  190. Zhang Z, Wang Q, Liu Q, Zheng Y, Zheng C, Yi K, et al. Dual-locking nanoparticles disrupt the PD-1/PD-L1 pathway for efficient cancer immunotherapy. Adv Mater. 2019;31(51):1905751. https://doi.org/10.1002/adma.201905751.

    Article  CAS  Google Scholar 

  191. Zhang B, Wang Y, Wang S, Tang Y, Li Z, Lin L, et al. Precise RNA editing: cascade self-uncloaking dual-prodrug nanoassemblies based on CRISPR/Cas13a for pleiotropic immunotherapy of PD-L1-resistant colorectal cancer. Adv Func Mater. 2023;33(46):2305630. https://doi.org/10.1002/adfm.202305630.

    Article  CAS  Google Scholar 

  192. Lan X, Zhu W, Huang X, Yu Y, Xiao H, Jin L, et al. Microneedles loaded with anti-PD-1–cisplatin nanoparticles for synergistic cancer immuno-chemotherapy. Nanoscale. 2020;12(36):18885–98.

    Article  CAS  PubMed  Google Scholar 

  193. Xu S, Cui F, Huang D, Zhang D, Zhu A, Sun X, et al. PD-L1 monoclonal antibody-conjugated nanoparticles enhance drug delivery level and chemotherapy efficacy in gastric cancer cells. Int J Nanomed. 2019;14:17–32.

    Article  CAS  Google Scholar 

  194. Mu X, Zhang M, Wei A, Yin F, Wang Y, Hu K, Jiang J. Doxorubicin and PD-L1 siRNA co-delivery with stem cell membrane-coated polydopamine nanoparticles for the targeted chemoimmunotherapy of PCa bone metastases. Nanoscale. 2021;13(19):8998–9008.

    Article  CAS  PubMed  Google Scholar 

  195. Zhu W, Bai Y, Zhang N, Yan J, Chen J, He Z, et al. A tumor extracellular pH-sensitive PD-L1 binding peptide nanoparticle for chemo-immunotherapy of cancer. J Mater Chem B. 2021;9(20):4201–10.

    Article  CAS  PubMed  Google Scholar 

  196. Cai S, Chen Z, Wang Y, Wang M, Wu J, Tong Y, et al. Reducing PD-L1 expression with a self-assembled nanodrug: an alternative to PD-L1 antibody for enhanced chemo-immunotherapy. Theranostics. 2021;11(4):1970–81. https://doi.org/10.7150/thno.45777.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  197. Zou M-Z, Liu W-L, Li C-X, Zheng D-W, Zeng J-Y, Gao F, et al. A Multifunctional biomimetic nanoplatform for relieving hypoxia to enhance chemotherapy and inhibit the PD-1/PD-L1 Axis. Small. 2018;14(28):1801120. https://doi.org/10.1002/smll.201801120.

    Article  CAS  Google Scholar 

  198. Liang J, Wang H, Ding W, Huang J, Zhou X, Wang H, et al. Nanoparticle-enhanced chemo-immunotherapy to trigger robust antitumor immunity. Sci Adv. 2020;6(35):eabc646.

    Article  Google Scholar 

  199. Sun Z, Zhang Y, Cao D, Wang X, Yan X, Li H, et al. PD-1/PD-L1 pathway and angiogenesis dual recognizable nanoparticles for enhancing chemotherapy of malignant cancer. Drug Deliv. 2018;25(1):1746–55. https://doi.org/10.1080/10717544.2018.1509907.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  200. Jhunjhunwala S, Hammer C, Delamarre L. Antigen presentation in cancer: insights into tumour immunogenicity and immune evasion. Nat Rev Cancer. 2021;21(5):298–312.

    Article  CAS  PubMed  Google Scholar 

  201. Gupta RG, Li F, Roszik J, Lizée G. Exploiting tumor neoantigens to target cancer evolution: current challenges and promising therapeutic approaches. Cancer Discov. 2021;11(5):1024–39.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  202. Accolla R, Lombardo L, Abdallah R, Raval G, Forlani G, Tosi G. Boosting the MHC class II-restricted tumor antigen presentation to CD4+ T helper cells: a critical issue for triggering protective immunity and re-orienting the tumor microenvironment toward an anti-tumor state. Front Oncol. 2014;4:79407.

    Article  Google Scholar 

  203. Sánchez-Paulete A, Teijeira A, Cueto FJ, Garasa S, Pérez-Gracia JL, Sánchez-Arráez A, et al. Antigen cross-presentation and T-cell cross-priming in cancer immunology and immunotherapy. Annal Oncol. 2017;28:xii44–55.

    Article  Google Scholar 

  204. Zwiorek K, Bourquin C, Battiany J, Winter G, Endres S, Hartmann G, Coester C. Delivery by cationic gelatin nanoparticles strongly increases the immunostimulatory effects of CpG oligonucleotides. Pharm Res. 2008;25:551–62.

    Article  CAS  PubMed  Google Scholar 

  205. Thomas SN, Vokali E, Lund AW, Hubbell JA, Swartz MA. Targeting the tumor-draining lymph node with adjuvanted nanoparticles reshapes the anti-tumor immune response. Biomaterials. 2014;35(2):814–24. https://doi.org/10.1016/j.biomaterials.2013.10.003.

    Article  CAS  PubMed  Google Scholar 

  206. Lin AY, Almeida JP, Bear A, Liu N, Luo L, Foster AE, Drezek RA. Gold nanoparticle delivery of modified CpG stimulates macrophages and inhibits tumor growth for enhanced immunotherapy. PLoS ONE. 2013;8(5):e63550. https://doi.org/10.1371/journal.pone.0063550.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  207. Schumacher TN, Schreiber RD. Neoantigens in cancer immunotherapy. Science. 2015;348(6230):69–74.

    Article  CAS  PubMed  Google Scholar 

  208. Bobisse S, Foukas PG, Coukos G, Harari A. Neoantigen-based cancer immunotherapy. Ann Transl Med. 2016;4(14):262.

    Article  PubMed  PubMed Central  Google Scholar 

  209. Wirth TC, Kühnel F. Neoantigen targeting—dawn of a new era in cancer immunotherapy? Front Immunol. 2017;8:1848.

    Article  PubMed  PubMed Central  Google Scholar 

  210. Solbrig CM, Saucier-Sawyer JK, Cody V, Saltzman WM, Hanlon DJ. Polymer nanoparticles for immunotherapy from encapsulated tumor-associated antigens and whole tumor cells. Mol Pharm. 2007;4(1):47–57. https://doi.org/10.1021/mp060107e.

    Article  CAS  PubMed  Google Scholar 

  211. Tan S, Sasada T, Bershteyn A, Yang K, Ioji T, Zhang Z. Combinational delivery of lipid-enveloped polymeric nanoparticles carrying different peptides for anti-tumor immunotherapy. Nanomedicine (Lond). 2014;9(5):635–47. https://doi.org/10.2217/nnm.13.67.

    Article  CAS  PubMed  Google Scholar 

  212. Xu Z, Wang Y, Zhang L, Huang L. Nanoparticle-delivered transforming growth factor-β siRNA enhances vaccination against advanced melanoma by modifying tumor microenvironment. ACS Nano. 2014;8(4):3636–45. https://doi.org/10.1021/nn500216y.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  213. Arbelaez CA, Estrada J, Gessner MA, Glaus C, Morales AB, Mohn D, et al. A nanoparticle vaccine that targets neoantigen peptides to lymphoid tissues elicits robust antitumor T cell responses. NPJ Vaccin. 2020;5(1):106. https://doi.org/10.1038/s41541-020-00253-9.

    Article  CAS  Google Scholar 

  214. Ni Q, Zhang F, Liu Y, Wang Z, Yu G, Liang B, et al. A bi-adjuvant nanovaccine that potentiates immunogenicity of neoantigen for combination immunotherapy of colorectal cancer. Sci Adv. 2020;6(12):6eaaw6071.

    Article  Google Scholar 

  215. Zhu J, Ji Z, Wang J, Sun R, Zhang X, Gao Y, et al. Tumor-inhibitory effect and immunomodulatory activity of fullerol C60(OH)x. Small. 2008;4(8):1168–75. https://doi.org/10.1002/smll.200701219.

    Article  CAS  PubMed  Google Scholar 

  216. Liu Y, Jiao F, Qiu Y, Li W, Qu Y, Tian C, et al. Immunostimulatory properties and enhanced TNF- alpha mediated cellular immunity for tumor therapy by C60(OH)20 nanoparticles. Nanotechnology. 2009;20(41):415102. https://doi.org/10.1088/0957-4484/20/41/415102.

    Article  CAS  PubMed  Google Scholar 

  217. Eble JA, Niland S. The extracellular matrix in tumor progression and metastasis. Clin Exp Metastasis. 2019;36(3):171–98. https://doi.org/10.1007/s10585-019-09966-1.

    Article  CAS  PubMed  Google Scholar 

  218. Yoo J, Seo BK, Park EK, Kwon M, Jeong H, Cho KR, et al. Tumor stiffness measured by shear wave elastography correlates with tumor hypoxia as well as histologic biomarkers in breast cancer. Cancer Imaging. 2020;20(1):1–10.

    Article  Google Scholar 

  219. Salavati H, Debbaut C, Pullens P, Ceelen W. Interstitial fluid pressure as an emerging biomarker in solid tumors. Biochimica et Biophysica Acta (BBA) Rev Cancer. 2022;1877:188792.

    Article  CAS  Google Scholar 

  220. Zhang T, Jia Y, Yu Y, Zhang B, Xu F, Guo H. Targeting the tumor biophysical microenvironment to reduce resistance to immunotherapy. Adv Drug Del Rev. 2022;186:114319.

    Article  CAS  Google Scholar 

  221. Parodi A, Haddix SG, Taghipour N, Scaria S, Taraballi F, Cevenini A, et al. Bromelain surface modification increases the diffusion of silica nanoparticles in the tumor extracellular matrix. ACS Nano. 2014;8(10):9874–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  222. Kanapathipillai M, Mammoto A, Mammoto T, Kang JH, Jiang E, Ghosh K, et al. Inhibition of mammary tumor growth using lysyl oxidase-targeting nanoparticles to modify extracellular matrix. Nano Lett. 2012;12(6):3213–7. https://doi.org/10.1021/nl301206p.

    Article  CAS  PubMed  Google Scholar 

  223. Zhang B, Shen S, Liao Z, Shi W, Wang Y, Zhao J, et al. Targeting fibronectins of glioma extracellular matrix by CLT1 peptide-conjugated nanoparticles. Biomaterials. 2014;35(13):4088–98.

    Article  CAS  PubMed  Google Scholar 

  224. Zhang B, Jiang T, Shen S, She X, Tuo Y, Hu Y, et al. Cyclopamine disrupts tumor extracellular matrix and improves the distribution and efficacy of nanotherapeutics in pancreatic cancer. Biomaterials. 2016;103:12–21. https://doi.org/10.1016/j.biomaterials.2016.06.048.

    Article  CAS  PubMed  Google Scholar 

  225. Duan S, Sun F, Qiao P, Zhu Z, Geng M, Gong X, et al. Detachable dual-targeting nanoparticles for improving the antitumor effect by extracellular matrix depletion. ACS Biomater Sci Eng. 2023;9(3):1437–49. https://doi.org/10.1021/acsbiomaterials.2c01179.

    Article  CAS  PubMed  Google Scholar 

  226. Lee S, Han H, Koo H, Na JH, Yoon HY, Lee KE, et al. Extracellular matrix remodeling in vivo for enhancing tumor-targeting efficiency of nanoparticle drug carriers using the pulsed high intensity focused ultrasound. J Control Release. 2017;263:68–78. https://doi.org/10.1016/j.jconrel.2017.02.035.

    Article  CAS  PubMed  Google Scholar 

  227. Wang L, Dou J, Jiang W, Wang Q, Liu Y, Liu H, Wang Y. Enhanced intracellular transcytosis of nanoparticles by degrading extracellular matrix for deep tissue radiotherapy of pancreatic adenocarcinoma. Nano Lett. 2022;22(17):6877–87. https://doi.org/10.1021/acs.nanolett.2c01005.

    Article  CAS  PubMed  Google Scholar 

  228. Fang T, Zhang J, Zuo T, Wu G, Xu Y, Yang Y, et al. Chemo-photothermal combination cancer therapy with ROS scavenging, extracellular matrix depletion, and tumor immune activation by telmisartan and diselenide-paclitaxel prodrug loaded nanoparticles. ACS Appl Mater Interfaces. 2020;12(28):31292–308.

    Article  CAS  PubMed  Google Scholar 

  229. Xiao M, He J, Yin L, Chen X, Zu X, Shen Y. Tumor-associated macrophages: critical players in drug resistance of breast cancer. Front Immunol. 2021. https://doi.org/10.3389/fimmu.2021.799428.

    Article  PubMed  PubMed Central  Google Scholar 

  230. Lafta HA, AbdulHussein AH, Al-Shalah SA, Alnassar YS, Mohammed NM, Akram SM, et al. Tumor-associated macrophages (TAMs) in cancer resistance; modulation by natural products. Curr Top Med Chem. 2023;23(12):1104–22.

    Article  CAS  PubMed  Google Scholar 

  231. Chaudhary B, Elkord E. Regulatory T cells in the tumor microenvironment and cancer progression: role and therapeutic targeting. Vaccines. 2016;4(3):28. https://doi.org/10.3390/vaccines4030028.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  232. Zhang Y, Hughes KR, Raghani RM, Ma J, Orbach S, Jeruss JS, Shea LD. Cargo-free immunomodulatory nanoparticles combined with anti-PD-1 antibody for treating metastatic breast cancer. Biomaterials. 2021;269:120666. https://doi.org/10.1016/j.biomaterials.2021.120666.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  233. Sun M, Gu P, Yang Y, Yu L, Jiang Z, Li J, et al. Mesoporous silica nanoparticles inflame tumors to overcome anti-PD-1 resistance through TLR4-NFκB axis. J Immunother Cancer. 2021. https://doi.org/10.1136/jitc-2021-002508.

    Article  PubMed  PubMed Central  Google Scholar 

  234. Guo X-Y, Zhang J-Y, Shi X-Z, Wang Q, Shen W-L, Zhu W-W, Liu L-K. Upregulation of CSF-1 is correlated with elevated TAM infiltration and poor prognosis in oral squamous cell carcinoma. Am J Transl Res. 2020;12(10):6235.

    CAS  PubMed  PubMed Central  Google Scholar 

  235. Li M, Li M, Yang Y, Liu Y, Xie H, Yu Q, et al. Remodeling tumor immune microenvironment via targeted blockade of PI3K-γ and CSF-1/CSF-1R pathways in tumor associated macrophages for pancreatic cancer therapy. J Control Release. 2020;321:23–35.

    Article  CAS  PubMed  Google Scholar 

  236. Ries CH, Cannarile MA, Hoves S, Benz J, Wartha K, Runza V, et al. Targeting tumor-associated macrophages with anti-CSF-1R antibody reveals a strategy for cancer therapy. Cancer Cell. 2014;25(6):846–59.

    Article  CAS  PubMed  Google Scholar 

  237. Kumar V, Donthireddy L, Marvel D, Condamine T, Wang F, Lavilla-Alonso S, et al. Cancer-associated fibroblasts neutralize the anti-tumor effect of CSF1 receptor blockade by inducing PMN-MDSC infiltration of tumors. Cancer Cell. 2017;32(5):654-68.e5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  238. Almahariq MF, Quinn TJ, Kesarwani P, Kant S, Miller CR, Chinnaiyan P. Inhibition of colony-stimulating factor-1 receptor enhances the efficacy of radiotherapy and reduces immune suppression in glioblastoma. In Vivo. 2021;35(1):119–29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  239. Ramesh A, Brouillard A, Kumar S, Nandi D, Kulkarni A. Dual inhibition of CSF1R and MAPK pathways using supramolecular nanoparticles enhances macrophage immunotherapy. Biomaterials. 2020;227:119559.

    Article  CAS  PubMed  Google Scholar 

  240. Alhudaithi SS, Almuqbil RM, Zhang H, Bielski ER, Du W, Sunbul FS, et al. Local targeting of lung-tumor-associated macrophages with pulmonary delivery of a CSF-1R inhibitor for the treatment of breast cancer lung metastases. Mol Pharm. 2020;17(12):4691–703.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  241. Sun Y, Cronin MF, Mendonca MC, Guo J, O’Driscoll CM. Sialic acid-targeted cyclodextrin-based nanoparticles deliver CSF-1R siRNA and reprogram tumour-associated macrophages for immunotherapy of prostate cancer. Eur J Pharm Sci. 2023;185:106427.

    Article  CAS  PubMed  Google Scholar 

  242. Tu MM, Abdel-Hafiz HA, Jones RT, Jean A, Hoff KJ, Duex JE, et al. Inhibition of the CCL2 receptor, CCR2, enhances tumor response to immune checkpoint therapy. Commun Biol. 2020;3(1):720.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  243. Liu Y, Tiruthani K, Wang M, Zhou X, Qiu N, Xiong Y, et al. Tumor-targeted gene therapy with lipid nanoparticles inhibits tumor-associated adipocytes and remodels the immunosuppressive tumor microenvironment in triple-negative breast cancer. Nanoscale Horizons. 2021;6(4):319–29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  244. Wang Y, Tiruthani K, Li S, Hu M, Zhong G, Tang Y, et al. mRNA delivery of a bispecific single-domain antibody to polarize tumor-associated macrophages and synergize immunotherapy against liver malignancies. Adv Mater. 2021;33(23):2007603.

    Article  CAS  Google Scholar 

  245. Gu X, Gao Y, Wang P, Wang L, Peng H, He Y, et al. Nano-delivery systems focused on tumor microenvironment regulation and biomimetic strategies for treatment of breast cancer metastasis. J Control Release. 2021;333:374–90.

    Article  CAS  PubMed  Google Scholar 

  246. Mardani R, Hamblin MR, Taghizadeh M, Banafshe HR, Nejati M, Mokhtari M, et al. Nanomicellar-curcumin exerts its therapeutic effects via affecting angiogenesis, apoptosis, and T cells in a mouse model of melanoma lung metastasis. Pathol Res Pract. 2020;216(9):153082.

    Article  CAS  PubMed  Google Scholar 

  247. Zheng Y, Jia R, Li J, Tian X, Qian Y. Curcumin-and resveratrol-co-loaded nanoparticles in synergistic treatment of hepatocellular carcinoma. J Nanobiotechnol. 2022;20(1):339.

    Article  CAS  Google Scholar 

  248. Lin M, Yao W, Xiao Y, Dong Z, Huang W, Zhang F, et al. Resveratrol-modified mesoporous silica nanoparticle for tumor-targeted therapy of gastric cancer. Bioengineered. 2021;12(1):6343–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  249. Li C, Xu Y, Zhang J, Zhang Y, He W, Ju J, et al. The effect of resveratrol, curcumin and quercetin combination on immuno-suppression of tumor microenvironment for breast tumor-bearing mice. Sci Rep. 2023;13(1):13278.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  250. Kuo I-M, Lee J-J, Wang Y-S, Chiang H-C, Huang C-C, Hsieh P-J, et al. Potential enhancement of host immunity and anti-tumor efficacy of nanoscale curcumin and resveratrol in colorectal cancers by modulated electro-hyperthermia. BMC Cancer. 2020;20:1–13.

    Article  Google Scholar 

  251. Ashkbar A, Rezaei F, Attari F, Ashkevarian S. Treatment of breast cancer in vivo by dual photodynamic and photothermal approaches with the aid of curcumin photosensitizer and magnetic nanoparticles. Sci Rep. 2020;10(1):21206.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  252. Xiao Z, Su Z, Han S, Huang J, Lin L, Shuai X. Dual pH-sensitive nanodrug blocks PD-1 immune checkpoint and uses T cells to deliver NF-κB inhibitor for antitumor immunotherapy. Sci Adv. 2020;6(6):7785.

    Article  Google Scholar 

  253. Ghoreyshi N, Ghahremanloo A, Javid H, Homayouni Tabrizi M, Hashemy SI. Effect of folic acid-linked chitosan-coated PLGA-based curcumin nanoparticles on the redox system of glioblastoma cancer cells. Phytochem Anal. 2023;34(8):950–8.

    Article  CAS  PubMed  Google Scholar 

  254. Xue D, Hsu E, Fu Y-X, Peng H. Next-generation cytokines for cancer immunotherapy. Antibody Therap. 2021;4(2):123–33.

    Article  CAS  Google Scholar 

  255. Mirlekar B, Pylayeva-Gupta Y. IL-12 family cytokines in cancer and immunotherapy. Cancers (Basel). 2021;13(2):167.

    Article  CAS  PubMed  Google Scholar 

  256. Todorović-Raković N. The role of cytokines in the evolution of cancer: IFN-γ paradigm. Cytokine. 2022;151:155442.

    Article  PubMed  Google Scholar 

  257. Klein C, Waldhauer I, Nicolini VG, Freimoser-Grundschober A, Nayak T, Vugts DJ, et al. Cergutuzumab amunaleukin (CEA-IL2v), a CEA-targeted IL-2 variant-based immunocytokine for combination cancer immunotherapy: overcoming limitations of aldesleukin and conventional IL-2-based immunocytokines. Oncoimmunology. 2017;6(3):e1277306. https://doi.org/10.1080/2162402x.2016.1277306.

    Article  PubMed  PubMed Central  Google Scholar 

  258. Johannsen M, Spitaleri G, Curigliano G, Roigas J, Weikert S, Kempkensteffen C, et al. The tumour-targeting human L19-IL2 immunocytokine: preclinical safety studies, phase I clinical trial in patients with solid tumours and expansion into patients with advanced renal cell carcinoma. Eur J Cancer. 2010;46(16):2926–35. https://doi.org/10.1016/j.ejca.2010.07.033.

    Article  CAS  PubMed  Google Scholar 

  259. Saif A, Rossi AJ, Sarnaik A, Hernandez JM, Zager JS. Efficacy of neoadjuvant intratumoral darleukin/fibromun (L19IL2 + L19TNF) in patients with clinical stage IIIB/C melanoma (Neo-DREAM). Ann Surg Oncol. 2022;29(6):3377–8. https://doi.org/10.1245/s10434-022-11447-x.

    Article  PubMed  Google Scholar 

  260. Barberio AE, Smith SG, Correa S, Nguyen C, Nhan B, Melo M, et al. Cancer cell coating nanoparticles for optimal tumor-specific cytokine delivery. ACS Nano. 2020;14(9):11238–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  261. Liu X, Gao X, Zheng S, Wang B, Li Y, Zhao C, et al. Modified nanoparticle mediated IL-12 immunogene therapy for colon cancer. Nanomed Nanotechnol Biol Med. 2017;13(6):1993–2004.

    Article  CAS  Google Scholar 

  262. Shin H, Kang S, Won C, Min D-H. Enhanced local delivery of engineered IL-2 mRNA by porous silica nanoparticles to promote effective antitumor immunity. ACS Nano. 2023;17(17):17554–67. https://doi.org/10.1021/acsnano.3c06733.

    Article  CAS  PubMed  Google Scholar 

  263. Kim J, Kang S, Kim KW, Heo M-G, Park D-I, Lee J-H, et al. Nanoparticle delivery of recombinant IL-2 (BALLkine-2) achieves durable tumor control with less systemic adverse effects in cancer immunotherapy. Biomaterials. 2022;280:121257. https://doi.org/10.1016/j.biomaterials.2021.121257.

    Article  CAS  PubMed  Google Scholar 

  264. Shimizu T, Kishida T, Hasegawa U, Ueda Y, Imanishi J, Yamagishi H, et al. Nanogel DDS enables sustained release of IL-12 for tumor immunotherapy. Biochem Biophys Res Commun. 2008;367(2):330–5. https://doi.org/10.1016/j.bbrc.2007.12.112.

    Article  CAS  PubMed  Google Scholar 

  265. Barberio AE, Smith SG, Pires IS, Iyer S, Reinhardt F, Melo MB, et al. Layer-by-layer interleukin-12 nanoparticles drive a safe and effective response in ovarian tumors. Bioeng Transl Med. 2023;8(2):e10453.

    Article  CAS  PubMed  Google Scholar 

  266. Li Y, Su Z, Zhao W, Zhang X, Momin N, Zhang C, et al. Multifunctional oncolytic nanoparticles deliver self-replicating IL-12 RNA to eliminate established tumors and prime systemic immunity. Nat Cancer. 2020;1(9):882–93. https://doi.org/10.1038/s43018-020-0095-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  267. Liu J-Q, Zhang C, Zhang X, Yan J, Zeng C, Talebian F, et al. Intratumoral delivery of IL-12 and IL-27 mRNA using lipid nanoparticles for cancer immunotherapy. J Control Release. 2022;345:306–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  268. Lai I, Swaminathan S, Baylot V, Mosley A, Dhanasekaran R, Gabay M, Felsher DW. Lipid nanoparticles that deliver IL-12 messenger RNA suppress tumorigenesis in MYC oncogene-driven hepatocellular carcinoma. J Immunother Cancer. 2018;6(1):125. https://doi.org/10.1186/s40425-018-0431-x.

    Article  PubMed  PubMed Central  Google Scholar 

  269. Zhao Y, Song Q, Yin Y, Wu T, Hu X, Gao X, et al. Immunochemotherapy mediated by thermosponge nanoparticles for synergistic anti-tumor effects. J Control Release. 2018;269:322–36. https://doi.org/10.1016/j.jconrel.2017.11.037.

    Article  CAS  PubMed  Google Scholar 

  270. Zhao P, Tian Y, Lu Y, Zhang J, Tao A, Xiang G, Liu Y. Biomimetic calcium carbonate nanoparticles delivered IL-12 mRNA for targeted glioblastoma sono-immunotherapy by ultrasound-induced necroptosis. J Nanobiotechnol. 2022;20(1):525. https://doi.org/10.1186/s12951-022-01731-z.

    Article  CAS  Google Scholar 

  271. Thaker PH, Brady WE, Lankes HA, Odunsi K, Bradley WH, Moore KN, et al. A phase I trial of intraperitoneal GEN-1, an IL-12 plasmid formulated with PEG-PEI-cholesterol lipopolymer, administered with pegylated liposomal doxorubicin in patients with recurrent or persistent epithelial ovarian, fallopian tube or primary peritoneal cancers: An NRG Oncology/Gynecologic Oncology Group study. Gynecol Oncol. 2017;147(2):283–90. https://doi.org/10.1016/j.ygyno.2017.08.001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  272. Shaw AR, Suzuki M. Recent advances in oncolytic adenovirus therapies for cancer. Curr Opin Virol. 2016;21:9–15.

    Article  PubMed Central  Google Scholar 

  273. Guo ZS, Liu Z, Bartlett DL. Oncolytic immunotherapy: dying the right way is a key to eliciting potent antitumor immunity. Front Oncol. 2014;4:74.

    Article  PubMed  PubMed Central  Google Scholar 

  274. Li F, Sheng Y, Hou W, Sampath P, Byrd D, Thorne S, Zhang Y. CCL5-armed oncolytic virus augments CCR5-engineered NK cell infiltration and antitumor efficiency. J Immunother Cancer. 2020. https://doi.org/10.1136/jitc-2019-000131.

    Article  PubMed  PubMed Central  Google Scholar 

  275. Wang X, Zhong L, Zhao Y. Oncolytic adenovirus: a tool for reversing the tumor microenvironment and promoting cancer treatment. Oncol Rep. 2021;45(4):1–9.

    Article  Google Scholar 

  276. Zhao Y, Liu Z, Li L, Wu J, Zhang H, Zhang H, et al. Oncolytic adenovirus: prospects for cancer immunotherapy. Front Microbiol. 2021;12:707290.

    Article  PubMed  PubMed Central  Google Scholar 

  277. Kalus P, De Munck J, Vanbellingen S, Carreer L, Laeremans T, Broos K, et al. Oncolytic herpes simplex virus type 1 induces immunogenic cell death resulting in maturation of BDCA-1+ myeloid dendritic cells. Int J Mol Sci. 2022;23(9):4865.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  278. Gebremeskel S, Nelson A, Walker B, Oliphant T, Lobert L, Mahoney D, Johnston B. Natural killer T cell immunotherapy combined with oncolytic vesicular stomatitis virus or reovirus treatments differentially increases survival in mouse models of ovarian and breast cancer metastasis. J Immunother Cancer. 2021. https://doi.org/10.1136/jitc-2020-002096.

    Article  PubMed  PubMed Central  Google Scholar 

  279. Martini V, D’Avanzo F, Maggiora PM, Varughese FM, Sica A, Gennari A. Oncolytic virotherapy: new weapon for breast cancer treatment. Ecancermedicalscience. 2020;14:1149.

    Article  PubMed  PubMed Central  Google Scholar 

  280. Niavarani S-R, Lawson C, Boudaud M, Simard C, Tai L-H. Oncolytic vesicular stomatitis virus-based cellular vaccine improves triple-negative breast cancer outcome by enhancing natural killer and CD8+ T-cell functionality. J Immunother Cancer. 2020. https://doi.org/10.1136/jitc-2019-000465.

    Article  PubMed  PubMed Central  Google Scholar 

  281. Fournier P, Bian H, Szeberényi J, Schirrmacher V. Analysis of three properties of Newcastle disease virus for fighting cancer: tumor-selective replication, antitumor cytotoxicity, and immunostimulation. Methods Mol Biol. 2012;797:177–204. https://doi.org/10.1007/978-1-61779-340-0_13.

    Article  CAS  PubMed  Google Scholar 

  282. Ma F, Cao Y, Yan J, Lu Z, Sun L, Hussain Z, et al. Multifunctional hybrid oncolytic virus-mimicking nanoparticles for targeted induce of tumor-specific pyroptosis and enhanced anti-tumor immune response in melanoma. Nano Today. 2024;54:102063. https://doi.org/10.1016/j.nantod.2023.102063.

    Article  CAS  Google Scholar 

  283. Jabir MS, Al-Shammari AM, Ali ZO, Albukhaty S, Sulaiman GM, Jawad SF, et al. Combined oncolytic virotherapy gold nanoparticles as synergistic immunotherapy agent in breast cancer control. Sci Rep. 2023;13(1):16843. https://doi.org/10.1038/s41598-023-42299-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  284. Wu F, Li Y, Meng Y, Cai X, Shi J, Li J, et al. An ion-enhanced oncolytic virus-like nanoparticle for tumor immunotherapy. Angew Chem. 2022;134(45):e202210487.

    Article  Google Scholar 

  285. Chan JD, Lai J, Slaney CY, Kallies A, Beavis PA, Darcy PK. Cellular networks controlling T cell persistence in adoptive cell therapy. Nat Rev Immunol. 2021;21(12):769–84.

    Article  CAS  PubMed  Google Scholar 

  286. Fuentes-Antrás J, Guevara-Hoyer K, Baliu-Piqué M, García-Sáenz JAn, Pérez-Segura P, Pandiella A, Ocaña A,. Adoptive cell therapy in breast cancer: a current perspective of next-generation medicine. Front Oncol. 2020;10:605633.

    Article  PubMed  PubMed Central  Google Scholar 

  287. Haslauer T, Greil R, Zaborsky N, Geisberger R. CAR T-cell therapy in hematological malignancies. Int J Mol Sci. 2021;22(16):8996.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  288. Kirtane K, Elmariah H, Chung CH, Abate-Daga D. Adoptive cellular therapy in solid tumor malignancies: review of the literature and challenges ahead. J Immunother Cancer. 2021;9(7):2723.

    Article  Google Scholar 

  289. Balakrishnan PB, Sweeney EE. Nanoparticles for enhanced adoptive T cell therapies and future perspectives for CNS tumors. Front Immunol. 2021;12:600659.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  290. Zheng C, Zhang J, Chan HF, Hu H, Lv S, Na N, et al. Engineering nano-therapeutics to boost adoptive cell therapy for cancer treatment. Small Methods. 2021;5(5):2001191.

    Article  CAS  Google Scholar 

  291. Prazeres PHDM, Ferreira H, Costa PAC, da Silva W, Alves MT, Padilla M, et al. Delivery of plasmid DNA by ionizable lipid nanoparticles to induce CAR expression in T cells. Int J Nanomed. 2023;18:5891–904.

    Article  CAS  Google Scholar 

  292. Zhang F, Stephan SB, Ene CI, Smith TT, Holland EC, Stephan MT. Nanoparticles that reshape the tumor milieu create a therapeutic window for effective T-cell therapy in solid malignancies. Cancer Res. 2018;78(13):3718–30. https://doi.org/10.1158/0008-5472.Can-18-0306.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  293. Siriwon N, Kim YJ, Siegler E, Chen X, Rohrs JA, Liu Y, Wang P. CAR-T cells surface-engineered with drug-encapsulated nanoparticles can ameliorate intratumoral T-cell hypofunction. Cancer Immunol Res. 2018;6(7):812–24. https://doi.org/10.1158/2326-6066.CIR-17-0502.

    Article  CAS  PubMed  Google Scholar 

  294. Braunstein MJ, Kucharczyk J, Adams S. Targeting toll-like receptors for cancer therapy. Target Oncol. 2018;13(5):583–98.

    Article  PubMed  Google Scholar 

  295. Qin M, Li Y, Yang X, Wu H. Safety of Toll-like receptor 9 agonists: a systematic review and meta-analysis. Immunopharmacol Immunotoxicol. 2014;36(4):251–60.

    Article  CAS  PubMed  Google Scholar 

  296. Zhou L, Zou M, Xu Y, Lin P, Lei C, Xia X. Nano drug delivery system for tumor immunotherapy: next-generation therapeutics. Front Oncol. 2022. https://doi.org/10.3389/fonc.2022.864301.

    Article  PubMed  PubMed Central  Google Scholar 

  297. Raja J, Ludwig JM, Gettinger SN, Schalper KA, Kim HS. Oncolytic virus immunotherapy: future prospects for oncology. J Immunother Cancer. 2018;6:1–13.

    Article  Google Scholar 

  298. Schirrmacher V. Cancer vaccines and oncolytic viruses exert profoundly lower side effects in cancer patients than other systemic therapies: a comparative analysis. Biomedicines. 2020;8(3):61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  299. Rasa A, Alberts P. Oncolytic virus preclinical toxicology studies. J Appl Toxicol. 2023;43(5):620–48.

    Article  CAS  PubMed  Google Scholar 

  300. Ajam-Hosseini M, Akhoondi F, Doroudian M. Nano based-oncolytic viruses for cancer therapy. Crit Rev Oncol Hematol. 2023;185:103980. https://doi.org/10.1016/j.critrevonc.2023.103980.

    Article  PubMed  Google Scholar 

  301. Myers G. Immune-related adverse events of immune checkpoint inhibitors: a brief review. Curr Oncol. 2018;25(5):342–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  302. Ashrafizadeh M, Zarrabi A, Hushmandi K, Zarrin V, Moghadam ER, Zabolian A, et al. PD-1/PD-L1 axis regulation in cancer therapy: the role of long non-coding RNAs and microRNAs. Life Sci. 2020;256:117899. https://doi.org/10.1016/j.lfs.2020.117899.

    Article  CAS  PubMed  Google Scholar 

  303. Bai R, Lv Z, Xu D, Cui J. Predictive biomarkers for cancer immunotherapy with immune checkpoint inhibitors. Biomark Res. 2020;8(1):34.

    Article  PubMed  PubMed Central  Google Scholar 

  304. Kawashima S, Togashi Y. Resistance to immune checkpoint inhibitors and the tumor microenvironment. Exp Dermatol. 2023;32(3):240–9.

    Article  CAS  PubMed  Google Scholar 

  305. Gupta R, Kadhim MM, Turki Jalil A, Qasim Alasheqi M, Alsaikhan F, Khalimovna Mukhamedova N, et al. The interactions of docetaxel with tumor microenvironment. Int Immunopharmacol. 2023;119:110214. https://doi.org/10.1016/j.intimp.2023.110214.

    Article  CAS  PubMed  Google Scholar 

  306. Yu D-L, Lou Z-P, Ma F-Y, Najafi M. The interactions of paclitaxel with tumour microenvironment. Int Immunopharmacol. 2022;105:108555. https://doi.org/10.1016/j.intimp.2022.108555.

    Article  CAS  PubMed  Google Scholar 

  307. Moslehi M, Moazamiyanfar R, Dakkali MS, Rezaei S, Rastegar-Pouyani N, Jafarzadeh E, et al. Modulation of the immune system by melatonin; implications for cancer therapy. Int Immunopharmacol. 2022;108:108890. https://doi.org/10.1016/j.intimp.2022.108890.

    Article  CAS  PubMed  Google Scholar 

  308. Mu Q, Najafi M. Resveratrol for targeting the tumor microenvironment and its interactions with cancer cells. Int Immunopharmacol. 2021. https://doi.org/10.1016/j.intimp.2021.107895.

    Article  PubMed  Google Scholar 

  309. Qin Y, Zhang H, Li Y, Xie T, Yan S, Wang J, et al. Promotion of ICD via nanotechnology. Macromol Biosci. 2023;23(9):2300093.

    Article  CAS  Google Scholar 

  310. Hernández Á-P, Juanes-Velasco P, Landeira-Viñuela A, Bareke H, Montalvillo E, Góngora R, Fuentes M. Restoring the immunity in the tumor microenvironment: insights into immunogenic cell death in onco-therapies. Cancers (Basel). 2021;13(11):2821.

    Article  PubMed  Google Scholar 

  311. Birmpilis AI, Paschalis A, Mourkakis A, Christodoulou P, Kostopoulos IV, Antimissari E, et al. Immunogenic cell death, DAMPs and prothymosin α as a putative anticancer immune response biomarker. Cells. 2022;11(9):1415.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  312. Chen S, Song Z, Zhang A. Small-molecule immuno-oncology therapy: advances, challenges and new directions. Curr Top Med Chem. 2019;19(3):180–5.

    Article  CAS  PubMed  Google Scholar 

  313. Qiu Y, Su M, Liu L, Tang Y, Pan Y, Sun J. Clinical application of cytokines in cancer immunotherapy. Drug Des Devel Ther. 2021;15:2269–87.

    Article  PubMed  PubMed Central  Google Scholar 

  314. Lee SN, Jin SM, Shin HS, Lim YT. Chemical strategies to enhance the therapeutic efficacy of toll-like receptor agonist based cancer immunotherapy. Acc Chem Res. 2020;53(10):2081–93. https://doi.org/10.1021/acs.accounts.0c00337.

    Article  CAS  PubMed  Google Scholar 

  315. Keshavarz M, Miri SM, Behboudi E, Arjeini Y, Dianat-Moghadam H, Ghaemi A. Oncolytic virus delivery modulated immune responses toward cancer therapy: challenges and perspectives. Int Immunopharmacol. 2022;108:108882.

    Article  CAS  PubMed  Google Scholar 

  316. Howard F, Muthana M. Designer nanocarriers for navigating the systemic delivery of oncolytic viruses. Nanomedicine. 2020;15(1):93–110.

    Article  CAS  PubMed  Google Scholar 

  317. Kepp O, Senovilla L, Kroemer G. Immunogenic cell death inducers as anticancer agents. Oncotarget. 2014;5(14):5190.

    Article  PubMed  PubMed Central  Google Scholar 

  318. Pol J, Vacchelli E, Aranda F, Castoldi F, Eggermont A, Cremer I, et al. Trial Watch: immunogenic cell death inducers for anticancer chemotherapy. Oncoimmunology. 2015;4(4):e1008866.

    Article  PubMed  PubMed Central  Google Scholar 

  319. Mazari SA, Ali E, Abro R, Khan FSA, Ahmed I, Ahmed M, et al. Nanomaterials: applications, waste-handling, environmental toxicities, and future challenges—a review. J Environ Chem Eng. 2021;9(2):105028.

    Article  CAS  Google Scholar 

  320. Muhammad Q, Jang Y, Kang SH, Moon J, Kim WJ, Park H. Modulation of immune responses with nanoparticles and reduction of their immunotoxicity. Biomater Sci. 2020;8(6):1490–501.

    Article  CAS  PubMed  Google Scholar 

  321. Colaço M, Marques AP, Jesus S, Duarte A, Borges O. Safe-by-design of glucan nanoparticles: size matters when assessing the immunotoxicity. Chem Res Toxicol. 2020;33(4):915–32.

    Article  PubMed  Google Scholar 

  322. Sonin D, Pochkaeva E, Zhuravskii S, Postnov V, Korolev D, Vasina L, et al. Biological safety and biodistribution of chitosan nanoparticles. Nanomaterials. 2020;10(4):810.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  323. Lee Y, Jeong M, Park J, Jung H, Lee H. Immunogenicity of lipid nanoparticles and its impact on the efficacy of mRNA vaccines and therapeutics. Exp Mol Med. 2023;55(10):2085–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  324. Simón M, Jørgensen JT, Norregaard K, Kjaer A. 18F-FDG positron emission tomography and diffusion-weighted magnetic resonance imaging for response evaluation of nanoparticle-mediated photothermal therapy. Sci Rep. 2020;10(1):7595.

    Article  PubMed  PubMed Central  Google Scholar 

  325. Liu X, Wang M, Jiang Y, Zhang X, Shi C, Zeng F, et al. Magnetic resonance imaging nanoprobe quantifies nitric oxide for evaluating M1/M2 macrophage polarization and prognosis of cancer treatments. ACS Nano. 2023;17(24):24854–66.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors are thankful to the Deanship of Scientific Research, King Khalid University, Abha, Saudi Arabia, for financially supporting this work through the small Research Group Project under Grant No. R.G.P.2/44/45.

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Ahmad, I., Altameemi, K.K.A., Hani, M.M. et al. Shifting cold to hot tumors by nanoparticle-loaded drugs and products. Clin Transl Oncol (2024). https://doi.org/10.1007/s12094-024-03577-3

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