[go: up one dir, main page]
More Web Proxy on the site http://driver.im/
Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Strategies in the design of nanoparticles for therapeutic applications

Key Points

  • The development of the next generation of nanoparticle therapeutics — based on polymeric nanoparticles that combine the pre-eminent features of traditional delivery vectors such as liposomes and polymer-drug conjugates, but offer new flexibility to overcome some of the key barriers in the field — is gaining momentum.

  • To achieve intracellular drug delivery, strategies for overcoming various biological barriers — from the system level, to the organ level and to the cellular level — are needed. For intravenously injected engineered nanoparticles, the avoidance of multiple organ-level clearance mechanisms, such as those operating in the spleen and in the liver, must be compensated for if the carrier is to reach its intended destination. Ultimately, the effectiveness of any engineered nanoparticle will depend on the efficiency of the carrier to deliver its cargo to the intracellular site of action, which in many cases requires organelle-specific targeting.

  • The size, the surface characteristics and the shape of a nanoparticle have a key role in its biodistribution in vivo. The effects of size have been studied extensively with spherically shaped particles and some general trends have been noted. Particle size is also known to influence the mechanism of cellular internalization. However, current findings indicate that particle shape is just as important, if not more so, than size in controlling key aspects of both biodistribution and nanoparticle internalization.

  • Achieving tailored activated release of therapeutic cargo still represents a key barrier in the field of engineered nanoparticles. The predominant strategies so far incorporate materials that are enzymatically degradable, pH sensitive or reductively labile, which facilitate bond breaking between the drug and the carrier, or destabilization of the carrier on reaching the intended site of action.

Abstract

Engineered nanoparticles have the potential to revolutionize the diagnosis and treatment of many diseases; for example, by allowing the targeted delivery of a drug to particular subsets of cells. However, so far, such nanoparticles have not proved capable of surmounting all of the biological barriers required to achieve this goal. Nevertheless, advances in nanoparticle engineering, as well as advances in understanding the importance of nanoparticle characteristics such as size, shape and surface properties for biological interactions, are creating new opportunities for the development of nanoparticles for therapeutic applications. This Review focuses on recent progress important for the rational design of such nanoparticles and discusses the challenges to realizing the potential of nanoparticles.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Schematic representation of an engineered nanoparticle.
Figure 2: Modes of cellular internalization of nanoparticles and respective size limitations.
Figure 3: PRINT technology for generating microparticles and nanoparticles.
Figure 4: Stimuli-responsive engineered nanoparticles.

Similar content being viewed by others

References

  1. Davis, M. E., Chen, Z. & Shin, D. M. Nanoparticle therapeutics: an emerging treatment modality for cancer. Nature Rev. Drug Discov. 7, 771–782 (2008).

    Article  CAS  Google Scholar 

  2. Zhang, L. et al. Nanoparticles in medicine: therapeutic applications and developments. Clin. Pharmacol. Ther. 83, 761–769 (2008).

    Article  CAS  PubMed  Google Scholar 

  3. Park, J. et al. PEGylated PLGA nanoparticles for the improved delivery of doxorubicin. Nanomedicine 5, 410–418 (2009).

    Article  CAS  PubMed  Google Scholar 

  4. Wang, X. et al. HFT–T, a targeting nanoparticle, enhances specific delivery of paclitaxel to folate receptor-positive tumors. ACS Nano 3, 3165–3174 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Torchilin, V. P. Recent advances with liposomes as pharmaceutical carriers. Nature Rev. Drug Discov. 4, 145–160 (2005).

    Article  CAS  Google Scholar 

  6. Berry, G. et al. The use of cardiac biopsy to demonstrate reduced cardiotoxicity in AIDS Kaposi's sarcoma patients treated with pegylated liposomal doxorubicin. Ann. Oncol. 9, 711–716 (1998).

    Article  CAS  PubMed  Google Scholar 

  7. Ewer, M. S. et al. Cardiac safety of liposomal anthracyclines. Semin. Oncol. 31, 161–181 (2004).

    Article  CAS  PubMed  Google Scholar 

  8. Sharma, G., Anabousi, S., Ehrhardt, C. & Kumar, M. Liposomes as targeted drug delivery systems in the treatment of breast cancer. J. Drug Target. 14, 301–310 (2006).

    Article  CAS  PubMed  Google Scholar 

  9. Duncan, R. Polymer conjugates as anticancer nanomedicines. Nature Rev. Cancer 6, 688–701 (2006).

    Article  CAS  Google Scholar 

  10. Lammers, T. & Ulbrich, K. HPMA copolymers: 30 years of advances. Adv. Drug Deliv. Rev. 62, 119–121 (2010).

    Article  CAS  PubMed  Google Scholar 

  11. Kopecek, J. & Kopeckova, P. HPMA copolymers: origins, early developments, present, and future. Adv. Drug Deliv. Rev. 62, 122–149 (2010).

    Article  CAS  PubMed  Google Scholar 

  12. Fukumura, D. & Jain, R. K. Imaging angiogenesis and the microenvironment. APMIS 116, 695–715 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Fukumura, D. & Jain, R. K. Tumor microvasculature and microenvironment: targets for anti-angiogenesis and normalization. Microvasc. Res. 74, 72–84 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Jain, R. K. Transport of molecules across tumor vasculature. Cancer Metastasis Rev. 6, 559–593 (1987).

    Article  CAS  PubMed  Google Scholar 

  15. Owens III, D. E. & Peppas, N. A. Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles. Int. J. Pharm. 307, 93–102 (2006).

    Article  CAS  Google Scholar 

  16. Champion, J. A., Katare, Y. K. & Mitragotri, S. Particle shape: a new design parameter for micro- and nanoscale drug delivery carriers. J. Control. Release 121, 3–9 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Vinogradov, S. V., Bronich, T. K. & Kabanov, A. V. Nanosized cationic hydrogels for drug delivery: preparation, properties and interactions with cells. Adv. Drug Deliv. Rev. 54, 135–147 (2002).

    Article  CAS  PubMed  Google Scholar 

  18. Wong, J. et al. Suspensions for intravenous (IV) injection: a review of development, preclinical and clinical aspects. Adv. Drug Deliv. Rev. 60, 939–954 (2008).

    Article  CAS  PubMed  Google Scholar 

  19. Alexis, F., Pridgen, E., Molnar, L. K. & Farokhzad, O. C. Factors affecting the clearance and biodistribution of polymeric nanoparticles. Mol. Pharm. 5, 505–515 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Choi, H. S. et al. Renal clearance of quantum dots. Nature Biotech. 25, 1165–1170 (2007).

    Article  CAS  Google Scholar 

  21. Ilium, L. et al. Blood clearance and organ deposition of intravenously administered colloidal particles. The effects of particle size, nature and shape. Int. J. Pharm. 12, 135–146 (1982).

    Article  Google Scholar 

  22. Moghimi, S. M., Hedeman, H., Muir, I. S., Illum, L. & Davis, S. S. An investigation of the filtration capacity and the fate of large filtered sterically-stabilized microspheres in rat spleen. Biochim. Biophys. Acta 1157, 233–240 (1993).

    Article  CAS  PubMed  Google Scholar 

  23. Porter, C. J., Moghimi, S. M., Illum, L. & Davis, S. S. The polyoxyethylene/polyoxypropylene block copolymer poloxamer-407 selectively redirects intravenously injected microspheres to sinusoidal endothelial-cells of rabbit bone-marrow. FEBS Lett. 305, 62–66 (1992).

    Article  CAS  PubMed  Google Scholar 

  24. Mitragotri, S. & Lahann, J. Physical approaches to biomaterial design. Nature Mater. 8, 15–23 (2009).

    Article  CAS  Google Scholar 

  25. Barua, S. & Rege, K. Cancer-cell-phenotype-dependent differential intracellular trafficking of unconjugated quantum dots. Small 5, 370–376 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Moghimi, S. M., Hunter, A. C. & Murray, J. C. Long-circulating and target-specific nanoparticles: theory to practice. Pharmacol. Rev. 53, 283–318 (2001).

    CAS  PubMed  Google Scholar 

  27. Frank, M. M. & Fries, L. F. The role of complement in inflammation and phagocytosis. Immunol. Today 12, 322–326 (1991).

    Article  CAS  PubMed  Google Scholar 

  28. Leu, D., Manthey, B., Kreuter, J., Speiser, P. & Deluca, P. P. Distribution and elimination of coated polymethyl [2–C–14]methacrylate nanoparticles after intravenous injection in rats. J. Pharm. Sci. 73, 1433–1437 (1984).

    Article  CAS  PubMed  Google Scholar 

  29. Goppert, T. M. & Muller, R. H. Polysorbate-stabilized solid lipid nanoparticles as colloidal carriers for intravenous targeting of drugs to the brain: comparison of plasma protein adsorption patterns. J. Drug Target. 13, 179–187 (2005).

    Article  CAS  PubMed  Google Scholar 

  30. Moghimi, S. M. & Patel, H. M. Serum-mediated recognition of liposomes by phagocytic cells of the reticuloendothelial system — the concept of tissue specificity. Adv. Drug Deliv. Rev. 32, 45–60 (1998).

    Article  CAS  PubMed  Google Scholar 

  31. Dobrovolskaia, M. A. & Mcneil, S. E. Immunological properties of engineered nanomaterials. Nature Nanotech. 2, 469–478 (2007). Excellent perspective regarding formal guidelines for the testing of nanomaterials.

    Article  CAS  Google Scholar 

  32. Serda, R. E. et al. Mitotic trafficking of silicon microparticles. Nanoscale 1, 250–259 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Moghimi, S. M., Hamad, I., Andresen, T. L., Jorgensen, K. & Szebeni, J. Methylation of the phosphate oxygen moiety of phospholipid–methoxy(polyethylene glycol) conjugate prevents PEGylated liposome-mediated complement activation and anaphylatoxin production. FASEB J. 20, 2591–2593 (2006).

    Article  CAS  PubMed  Google Scholar 

  34. Hamad, I. et al. Complement activation by PEGylated single-walled carbon nanotubes is independent of C1q and alternative pathway turnover. Mol. Immunol. 45, 3797–3803 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Torchilin, V. P. & Trubetskoy, V. S. Which polymers can make nanoparticulate drug carriers long-circulating. Adv. Drug Deliv. Rev. 16, 141–155 (1995).

    Article  CAS  Google Scholar 

  36. Adams, M. L., Lavasanifar, A. & Kwon, G. S. Amphiphilic block copolymers for drug delivery. J. Pharm. Sci. 92, 1343–1355 (2003).

    Article  PubMed  Google Scholar 

  37. Otsuka, H., Nagasaki, Y. & Kataoka, K. PEGylated nanoparticles for biological and pharmaceutical applications. Adv. Drug Deliv. Rev. 55, 403–419 (2003).

    Article  CAS  PubMed  Google Scholar 

  38. Howard, M. D., Jay, M., Dziublal, T. D. & Lu, X. L. PEGylation of nanocarrier drug delivery systems: state of the art. J. Biomed. Nanotechnol. 4, 133–148 (2008).

    Article  CAS  Google Scholar 

  39. Yokoe, J. et al. Albumin-conjugated PEG liposome enhances tumor distribution of liposomal doxorubicin in rats. Int. J. Pharm. 353, 28–34 (2008).

    Article  CAS  PubMed  Google Scholar 

  40. Furumoto, K. et al. Effect of coupling of albumin onto surface of PEG liposome on its in vivo disposition. Int. J. Pharm. 329, 110–116 (2007).

    Article  CAS  PubMed  Google Scholar 

  41. Ogawara, K. et al. Pre-coating with serum albumin reduces receptor-mediated hepatic disposition of polystyrene nanosphere: implications for rational design of nanoparticles. J. Control. Release 100, 451–455 (2004).

    Article  CAS  PubMed  Google Scholar 

  42. Conner, S. D. & Schmid, S. L. Regulated portals of entry into the cell. Nature 422, 37–44 (2003).

    Article  CAS  PubMed  Google Scholar 

  43. Rejman, J., Oberle, V., Zuhorn, I. S. & Hoekstra, D. Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem. J. 377, 159–169 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Hillaireau, H. & Couvreur, P., Nanocarriers' entry into the cell: relevance to drug delivery. Cell. Mol. Life Sci. 66, 2873–2896 (2009).

    Article  CAS  PubMed  Google Scholar 

  45. Decuzzi, P., Pasqualini, R., Arap, W. & Ferrari, M. Intravascular delivery of particulate systems: does geometry really matter? Pharm. Res. 26, 235–243 (2009).

    Article  CAS  PubMed  Google Scholar 

  46. Champion, J. A. & Mitragotri, S. Shape induced inhibition of phagocytosis of polymer particles. Pharm. Res. 26, 244–249 (2009).

    Article  CAS  PubMed  Google Scholar 

  47. Muro, S. et al. Control of endothelial targeting and intracellular delivery of therapeutic enzymes by modulating the size and shape of ICAM-1-targeted carriers. Mol. Ther. 16, 1450–1458 (2008).

    Article  CAS  PubMed  Google Scholar 

  48. Geng, Y., et al. Shape effects of filaments versus spherical particles in flow and drug delivery. Nature Nanotech. 2, 249–255 (2007).

    Article  CAS  Google Scholar 

  49. Gratton, S. E., Napier, M. E., Ropp, P. A., Tian, S. M. & DeSimone, J. M. Microfabricated particles for engineered drug therapies: elucidation into the mechanisms of cellular internalization of PRINT particles. Pharm. Res. 25, 2845–2852 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Gratton, S. E. et al. The effect of particle design on cellular internalization pathways. Proc. Natl Acad. Sci. USA 105, 11613–11618 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  51. Champion, J. A. & Mitragotri, S. Role of target geometry in phagocytosis. Proc. Natl Acad. Sci. USA 103, 4930–4934 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Doshi, N. & Mitragotri, S. Designer biomaterials for nanomedicine. Adv. Funct. Mater. 19, 3843–3854 (2009).

    Article  CAS  Google Scholar 

  53. Lee, S. Y., Ferrari, M. & Decuzzi, P. Shaping nano-/micro-particles for enhanced vascular interaction in laminar flows. Nanotechnology 20, 495101–495111 (2009).

    Article  CAS  PubMed  Google Scholar 

  54. Decuzzi, P. et al. Size and shape effects in the biodistribution of intravascularly injected particles. J. Control. Release 141, 320–327 (2010).

    Article  CAS  PubMed  Google Scholar 

  55. Drummond, D. C., Meyer, O., Hong, K. L., Kirpotin, D. B. & Papahadjopoulos, D. Optimizing liposomes for delivery of chemotherapeutic agents to solid tumors. Pharmacol. Rev. 51, 691–743 (1999).

    CAS  PubMed  Google Scholar 

  56. Thevenot, P., Hu, W. J. & Tang, L. P. Surface chemistry influences implant biocompatibility. Curr. Top. Med. Chem. 8, 270–280 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Wang, Y. X., Robertson, J. L., Spillman, W. B. & Claus, R. O. Effects of the chemical structure and the surface properties of polymeric biomaterials on their biocompatibility. Pharm. Res. 21, 1362–1373 (2004).

    Article  CAS  PubMed  Google Scholar 

  58. Braun, K., Pipkorn, R. & Waldeck, W. Development and characterization of drug delivery systems for targeting mammalian cells and tissues: a review. Curr. Med. Chem. 12, 1841–1858 (2005).

    Article  CAS  PubMed  Google Scholar 

  59. Byrne, J. D., Betancourt, T. & Brannon-Peppas, L. Active targeting schemes for nanoparticle systems in cancer therapeutics. Adv. Drug Deliv. Rev. 60, 1615–1626 (2008). Provides a recent overview of cancer targeting strategies.

    Article  CAS  PubMed  Google Scholar 

  60. Maeda, H., Greish, K. & Fang, J. The EPR effect and polymeric drugs: a paradigm shift for cancer chemotherapy in the 21st century. Adv. Polym. Sci. 193, 103–121 (2006).

    Article  CAS  Google Scholar 

  61. Matsumura, Y. & Maeda, H. A new concept for macromolecular therapeutics in cancer-chemotherapy — mechanism of tumoritropic accumulation of proteins and the antitumor agent Smancs. Cancer Res. 46, 6387–6392 (1986).

    CAS  PubMed  Google Scholar 

  62. Salazar, M. D. & Ratnam, M. The folate receptor: what does it promise in tissue-targeted therapeutics? Cancer Metastasis Rev. 26, 141–152 (2007).

    Article  CAS  PubMed  Google Scholar 

  63. Low, P. S., Henne, W. A. & Doorneweerd, D. D. Discovery and development of folic-acid-based receptor targeting for imaging and therapy of cancer and inflammatory diseases. Acc. Chem. Res. 41, 120–129 (2008).

    Article  CAS  PubMed  Google Scholar 

  64. Gabizon, A., Shmeeda, H., Horowitz, A. T. & Zalipsky, S. Tumor cell targeting of liposome-entrapped drugs with phospholipid-anchored folic acid–PEG conjugates. Adv. Drug Deliv. Rev. 56, 1177–1192 (2004).

    Article  CAS  PubMed  Google Scholar 

  65. Daniels, T. R., Delgado, T., Rodriguez, J. A., Helguera, G. & Penichet, M. L. The transferrin receptor part I: biology and targeting with cytotoxic antibodies for the treatment of cancer. Clin. Immunol. 121, 144–158 (2006).

    Article  CAS  PubMed  Google Scholar 

  66. Daniels, T. R., Delgado, T., Helguera, G. & Penichet, M. L. The transferrin receptor part II: targeted delivery of therapeutic agents into cancer cells. Clin. Immunol. 121, 159–176 (2006).

    Article  CAS  PubMed  Google Scholar 

  67. Choi, C. H., Alabi, C. A., Webster, P. & Davis, M. E. Mechanism of active targeting in solid tumors with transferrin-containing gold nanoparticles. Proc. Natl Acad. Sci. USA. 107, 1235–1240 (2010).

    Article  PubMed  Google Scholar 

  68. Sung, J. C., Pulliam, B. L. & Edwards, D. A. Nanoparticles for drug delivery to the lungs. Trends Biotechnol. 25, 563–570 (2007).

    Article  CAS  PubMed  Google Scholar 

  69. Roger, E., Lagarce, F., Garcion, E. & Benoit, J. P. Biopharmaceutical parameters to consider in order to alter the fate of nanocarriers after oral delivery. Nanomedicine 5, 287–306 (2010).

    Article  CAS  PubMed  Google Scholar 

  70. Abra, R. M., Bosworth, M. E. & Hunt, C. A. Liposome disposition in vivo: effects of pre-dosing with lipsomes. Res. Commun. Chem. Pathol. Pharmacol. 29, 349–360 (1980).

    CAS  PubMed  Google Scholar 

  71. Souhami, R. L., Patel, H. M. & Ryman, B. E. The effect of reticuloendothelial blockade on the blood clearance and tissue distribution of liposomes. Biochim. Biophys. Acta 674, 354–371 (1981).

    Article  CAS  PubMed  Google Scholar 

  72. Moghimi, S. M. & Davis, S. S. Innovations in avoiding particle clearance from blood by Kupffer cells: cause for reflection. Crit. Rev. Ther. Drug Carrier Syst. 11, 31–59 (1994).

    CAS  PubMed  Google Scholar 

  73. Simberg, D. et al. Biomimetic amplification of nanoparticle homing to tumors. Proc. Natl Acad. Sci. USA 104, 932–936 (2007). Details an innovative strategy for amplifying tumour targeting.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Passirani, C., Barratt, G., Devissaguet, J. P. & Labarre, D. Long-circulating nanoparticles bearing heparin or dextran covalently bound to poly(methyl methacrylate). Pharm. Res. 15, 1046–1050 (1998).

    Article  CAS  PubMed  Google Scholar 

  75. Socha, M. et al. Increase in the vascular residence time of propranolol-loaded nanoparticles coated with heparin. J. Nanosci. Nanotechnol. 8, 2369–2376 (2008).

    Article  CAS  PubMed  Google Scholar 

  76. Oldenborg, P. A., Gresham, H. D., Chen, Y. M., Izui, S. & Lindberg, F. P. Lethal autoimmune hemolytic anemia in CD47-deficient nonobese diabetic (NOD) mice. Blood 99, 3500–3504 (2002).

    Article  CAS  PubMed  Google Scholar 

  77. Shiratori, I. et al. Down-regulation of basophil function by human CD200 and human herpesvirus-8 CD200. J. Immunol. 175, 4441–4449 (2005).

    Article  CAS  PubMed  Google Scholar 

  78. Bareford, L. M. & Swaan, P. W. Endocytic mechanisms for targeted drug delivery. Adv. Drug Deliv. Rev. 59, 748–758 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Torchilin, V. P. Cell penetrating peptide-modified pharmaceutical nanocarriers for intracellular drug and gene delivery. Biopolymers 90, 604–610 (2008).

    Article  CAS  PubMed  Google Scholar 

  80. Davis, M. E. et al. Evidence of RNAi in humans from systemically administered siRNA via targeted nanoparticles. Nature 464, 1067–1070 (2010). First example of dose-dependent accumulation of targeted nanoparticles in human tumours following systemic injection.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Davis, M. E. The first targeted delivery of siRNA in humans via a self-assembling, cyclodextrin polymer-based nanoparticle: from concept to clinic. Mol. Pharm. 6, 659–668 (2009).

    Article  CAS  PubMed  Google Scholar 

  82. Napier, M. E. & DeSimone, J. M. Nanoparticle drug delivery platform. Polymer Rev. 47, 321–327 (2007).

    Article  CAS  Google Scholar 

  83. Gratton, S. E. et al. The pursuit of a scalable nanofabrication platform for use in material and life science applications. Acc. Chem. Res. 41, 1685–1695 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Euliss, L. E., DuPont, J. A., Gratton, S. & DeSimone, J. Imparting size, shape, and composition control of materials for nanomedicine. Chem. Soc. Rev. 35, 1095–1104 (2006).

    Article  CAS  PubMed  Google Scholar 

  85. Rolland, J. et al. Direct fabrication and harvesting of monodisperse, shape-specific nanobiomaterials. J. Am. Chem. Soc. 127, 10096–10100 (2005).

    Article  CAS  PubMed  Google Scholar 

  86. Oupicky, D., Konak, C., Ulbrich, K., Wolfert, M. A. & Seymour, L. W. DNA delivery systems based on complexes of DNA with synthetic polycations and their copolymers. J. Control. Release 65, 149–171 (2000).

    Article  CAS  PubMed  Google Scholar 

  87. Gary, D. J., Puri, N. & Won, Y. Y. Polymer-based siRNA delivery: perspectives on the fundamental and phenomenological distinctions from polymer-based DNA delivery. J. Control. Release 121, 64–73 (2007).

    Article  CAS  PubMed  Google Scholar 

  88. Saito, G., Swanson, J. A. & Lee, K. D. Drug delivery strategy utilizing conjugation via reversible disulfide linkages: role and site of cellular reducing activities. Adv. Drug Deliv. Rev. 55, 199–215 (2003).

    Article  CAS  PubMed  Google Scholar 

  89. Niculescu-Duvaz, I. Technology evaluation: gemtuzumab ozogamicin, Celltech Group. Curr. Opin. Mol. Ther. 2, 691–696 (2000).

    CAS  PubMed  Google Scholar 

  90. Petros, R. A., Ropp, P. A. & DeSimone, J. M. Reductively labile PRINT particles for the delivery of doxorubicin to HeLa cells. J. Am. Chem. Soc. 130, 5008–5009 (2008).

    Article  CAS  PubMed  Google Scholar 

  91. Oh, J. K. et al. Biodegradable nanogels prepared by atom transfer radical polymerization as potential drug delivery carriers: synthesis, biodegradation, in vitro release, and bioconjugation. J. Am. Chem. Soc. 129, 5939–5945 (2007).

    Article  CAS  PubMed  Google Scholar 

  92. Kirpotin, D., Hong, K., Mullah, N., Papahadjopoulos, D. & Zalipsky, S. Liposomes with detachable polymer coating: destabilization and fusion of dioleoylphosphatidylethanolamine vesicles triggered by cleavage of surface-grafted poly(ethylene glycol). FEBS Lett. 388, 115–118 (1996).

    Article  CAS  PubMed  Google Scholar 

  93. Torchilin, V. P. Targeted pharmaceutical nanocarriers for cancer therapy and imaging. AAPS J. 9, E128–E147 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Oh, K. T., Yin, H. Q., Lee, E. S. & Bae, Y. H. Polymeric nanovehicles for anticancer drugs with triggering release mechanisms. J. Mater. Chem. 17, 3987–4001 (2007).

    Article  CAS  Google Scholar 

  95. Ganta, S., Devalapally, H., Shahiwala, A. & Amiji, M. A review of stimuli-responsive nanocarriers for drug and gene delivery. J. Control. Release 126, 187–204 (2008). Comprehensive review of stimuli-responsive materials used in targeted drug delivery.

    Article  CAS  PubMed  Google Scholar 

  96. Sinha, R., Kim, G. J., Nie, S. M. & Shin, D. M. Nanotechnology in cancer therapeutics: bioconjugated nanoparticles for drug delivery. Mol. Cancer Ther. 5, 1909–1917 (2006).

    Article  CAS  PubMed  Google Scholar 

  97. Patri, A. K. et al. Synthesis and in vitro testing of J591 antibody–dendrimer conjugates for targeted prostate cancer therapy. Bioconjug. Chem. 15, 1174–1181 (2004).

    Article  CAS  PubMed  Google Scholar 

  98. Chang, S. S. et al. Prostate-specific membrane antigen is produced in tumor-associated neovasculature. Clin. Cancer Res. 5, 2674–2681 (1999).

    CAS  PubMed  Google Scholar 

  99. Milowsky, M. I. et al. Vascular targeted therapy with anti-prostate-specific membrane antigen monoclonal antibody J591 in advanced solid tumors. J. Clin. Oncol. 25, 540–547 (2007).

    Article  CAS  PubMed  Google Scholar 

  100. Aina, O. H. et al. From combinatorial chemistry to cancer-targeting peptides. Mol. Pharm. 4, 631–651 (2007). Recent review detailing the use of peptides as cancer targeting ligands.

    Article  CAS  PubMed  Google Scholar 

  101. Pierschbacher, M. D. & Ruoslahti, E. Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature 309, 30–33 (1984).

    Article  CAS  PubMed  Google Scholar 

  102. Stupack, D. G. & Cheresh, D. A. Integrins and angiogenesis. Curr. Top. Dev. Biol. 64, 207–238 (2004).

    Article  CAS  PubMed  Google Scholar 

  103. Cheresh, D. A. Structure, function and biological properties of integrin alpha v beta 3 on human-melanoma cells. Cancer Metastasis Rev. 10, 3–10 (1991).

    Article  CAS  PubMed  Google Scholar 

  104. Murphy, E. A. et al. Nanoparticle-mediated drug delivery to tumor vasculature suppresses metastasis. Proc. Natl Acad. Sci. USA 105, 9343–9348 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  105. Danhier, F. et al. Targeting of tumor endothelium by RGD-grafted PLGA-nanoparticles loaded with paclitaxel. J. Control. Release 140, 166–173 (2009).

    Article  CAS  PubMed  Google Scholar 

  106. Schliemann, C. et al. In vivo biotinylation of the vasculature in B-cell lymphoma identifies BST-2 as a target for antibody-based therapy. Blood 115, 736–744 (2010).

    Article  CAS  PubMed  Google Scholar 

  107. Ruoslahti, E., Bhatia, S. N. & Sailor, M. J. Targeting of drugs and nanoparticles to tumors. J. Cell Biol. 188, 759–768 (2010). Describes the advantages of vascular targeting of nanoparticles to tumours.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Jacobson, B. S., Stolz, D. B. & Schnitzer, J. E. Identification of endothelial cell-surface proteins as targets for diagnosis and treatment of disease. Nature Med. 2, 482–484 (1996).

    Article  CAS  PubMed  Google Scholar 

  109. Carson-Walter, E. B. et al. Cell surface tumor endothelial markers are conserved in mice and humans. Cancer Res. 61, 6649–6655 (2001).

    CAS  PubMed  Google Scholar 

  110. Sugahara, K. N. et al. Tissue-penetrating delivery of compounds and nanoparticles into tumors. Cancer Cell 16, 510–520 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Chan, J. M. et al. Spatiotemporal controlled delivery of nanoparticles to injured vasculature. Proc. Natl Acad. Sci. USA 107, 2213–2218 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  112. Renschler, M. F., Bhatt, R. R., Dower, W. J. & Levy, R. Synthetic peptide ligands of the antigen binding receptor induce programmed cell death in a human B-cell lymphoma. Proc. Natl Acad. Sci. USA 91, 3623–3627 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Pennell, C. A. & Scott, D. W. Lymphoma models for B cell activation and tolerance. IV. Growth inhibition by anti-Ig of CH31 and CH33 B lymphoma cells. Eur. J. Immunol. 16, 1577–1581 (1986).

    Article  CAS  PubMed  Google Scholar 

  114. Miller, R. A., Maloney, D. G., Warnke, R. & Levy, R. Treatment of B-cell lymphoma with monoclonal anti-idiotype antibody. N. Engl. J. Med. 306, 517–522 (1982).

    Article  CAS  PubMed  Google Scholar 

  115. Pouton, C. W., Wagstaff, K. M., Roth, D. M., Moseley, G. W. & Jans, D. A. Targeted delivery to the nucleus. Adv. Drug Deliv. Rev. 59, 698–717 (2007).

    Article  CAS  PubMed  Google Scholar 

  116. Hodoniczky, J., Sims, C. G., Best, W. M., Bentel, J. M. & Wilce, J. A. The intracellular and nuclear-targeted delivery of an antiandrogen drug by carrier peptides. Biopolymers 90, 595–603 (2008).

    Article  CAS  PubMed  Google Scholar 

  117. Misra, R. & Sahoo, S. K. Intracellular trafficking of nuclear localization signal conjugated nanoparticles for cancer therapy. Eur. J. Pharm. Sci. 39, 152–163 (2010).

    Article  CAS  PubMed  Google Scholar 

  118. Vasir, J. K. & Labhasetwar, V. Biodegradable nanoparticles for cytosolic delivery of therapeutics. Adv. Drug Deliv. Rev. 59, 718–728 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Zhang, Z. H. et al. Biomimetic nanocarrier for direct cytosolic drug delivery. Angew. Chem. Int. Ed. Engl. 48, 9171–9175 (2009).

    Article  CAS  PubMed  Google Scholar 

  120. Mukhopadhyay, A. & Weiner, H. Delivery of drugs and macromolecules to mitochondria. Adv. Drug Deliv. Rev. 59, 729–738 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Boddapati, S. V., D'Souza, G. G., Erdogan, S., Torchilin, V. P. & Weissig, V. Organelle-targeted nanocarriers: specific delivery of liposomal ceramide to mitochondria enhances its cytotoxicity in vitro and in vivo. Nano Lett. 8, 2559–2563 (2008).

    Article  CAS  PubMed  Google Scholar 

  122. Yamada, Y. & Harashima, H. Mitochondrial drug delivery systems for macromolecule and their therapeutic application to mitochondrial diseases. Adv. Drug Deliv. Rev. 60, 1439–1462 (2008).

    Article  CAS  PubMed  Google Scholar 

  123. Yousif, L. F., Stewart, K. M. & Kelley, S. O. Targeting mitochondria with organelle-specific compounds: strategies and applications. ChemBioChem 10, 1939–1950 (2009).

    Article  CAS  PubMed  Google Scholar 

  124. Terlecky, S. R. & Koepke, J. I. Drug delivery to peroxisomes: employing unique trafficking mechanisms to target protein therapeutics. Adv. Drug Deliv. Rev. 59, 739–747 (2007).

    Article  CAS  PubMed  Google Scholar 

  125. Breunig, M., Bauer, S. & Goefferich, A. Polymers and nanoparticles: intelligent tools for intracellular targeting? Eur. J. Pharm. Biopharm. 68, 112–128 (2008).

    Article  CAS  PubMed  Google Scholar 

  126. Callahan, J. & Kopecek, J. Semitelechelic HPMA copolymers functionalized with triphenylphosphonium as drug carriers for membrane transduction and mitochondrial localization. Biomacromolecules 7, 2347–2356 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Hoshino, A. et al. Quantum dots targeted to the assigned organelle in living cells. Microbiol. Immunol. 48, 985–994 (2004).

    Article  CAS  PubMed  Google Scholar 

  128. Wagstaff, K. M. & Jans, D. A. Importins and beyond: non-conventional nuclear transport mechanisms. Traffic 10, 1188–1198 (2009).

    Article  CAS  PubMed  Google Scholar 

  129. Pante, N. & Kann, M. Nuclear pore complex is able to transport macromolecules with diameters of similar to 39 nm. Mol. Biol. Cell 13, 425–434 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Chan, C. K. & Jans, D. A. Using nuclear targeting signals to enhance non-viral gene transfer. Immunol. Cell Biol. 80, 119–130 (2002).

    Article  CAS  PubMed  Google Scholar 

  131. Chan, C. K., Senden, T. & Jans, D. A. Supramolecular structure and nuclear targeting efficiency determine the enhancement of transfection by modified polylysines. Gene Ther. 7, 1690–1697 (2000).

    Article  CAS  PubMed  Google Scholar 

  132. Farokhzad, O. C. & Langer, R. Impact of nanotechnology on drug delivery. ACS Nano 3, 16–20 (2009). Excellent description of the new opportunities afforded by targeted drug delivery.

    Article  CAS  PubMed  Google Scholar 

  133. Jatzkewitz, H. Incorporation of physiologically-active substances into a colloidal blood plasma substitute. I. Incorporation of mescaline peptide into polyvinylpyrrolidone. Hoppe-Seylers Z. Physiol. Chem. 297, 149–156 (1954) (in German).

    Article  CAS  PubMed  Google Scholar 

  134. Jatzkewitz, H. An ein kolloidales blutplasma-ersatzmittel (polyvinylpyrrolidon) gebundenes peptamin (glycyl-L-leucyl-mezcalin) als neuartige depotform fur biologisch aktive primare amine (mezcalin). Z. Naturforsch. B 10, 27–31 (1955) (in German).

    Article  Google Scholar 

  135. Bangham, A. D. & Horne, R. W. Negative staining of phospholipids and their structural modification by surface-active agents as observed in the electron microscope. J. Mol. Biol. 8, 660–668 (1964).

    Article  CAS  PubMed  Google Scholar 

  136. Bangham, A. D., Standish, M. M. & Watkins, J. C. Diffusion of univalent ions across lamellae of swollen phospholipids. J. Mol. Biol. 13, 238–252 (1965).

    Article  CAS  PubMed  Google Scholar 

  137. Ringsdorf, H. Structure and properties of pharmacologically active polymers. J. Polym. Sci. Pol. Sym. 135–153 (1975).

  138. Scheffel, U., Rhodes, B. A., Natarajan T. K. & Wagner, H. N. Albumin microspheres for study of reticuloendothelial system. J. Nucl. Med. 13, 498–503 (1972).

    CAS  PubMed  Google Scholar 

  139. Gradishar, W. J. et al. Phase III trial of nanoparticle albumin-bound paclitaxel compared with polyethylated castor oil-based paclitaxel in women with breast cancer. J. Clin. Oncol. 23, 7794–7803 (2005).

    Article  CAS  PubMed  Google Scholar 

  140. Kopf, H., Joshi, R. K., Soliva, M. & Speiser, P. Study on micelle polymerization in the presence of low-molecular-weight drugs. 1. Production and isolation of nanoparticles, residual monomer determination, physical–chemical data. Pharm. Ind. 38, 281–284 (1976).

    CAS  Google Scholar 

  141. Kreuter, J. Nanoparticles — a historical perspective. Int. J. Pharm. 331, 1–10 (2007). Describes the early history in the development of polymer nanoparticles for drug delivery.

    Article  CAS  PubMed  Google Scholar 

  142. US Food and Drug Administration. Drugs. US FDA website [online],http://www.accessdata.fda.gov/scripts/cder/drugsatfda/index.cfm (2010).

  143. Kim, T. Y. et al. Phase I and pharmacokinetic study of Genexol-PM, a cremophor-free, polymeric micelle-formulated paclitaxel, in patients with advanced malignancies. Clin. Cancer Res. 10, 3708–3716 (2004).

    Article  CAS  PubMed  Google Scholar 

  144. Lee, K. S. et al. Multicenter phase II trial of Genexol-PM, a Cremophor-free, polymeric micelle formulation of paclitaxel, in patients with metastatic breast cancer. Breast Cancer Res. Treat. 108, 241–250 (2008).

    Article  CAS  PubMed  Google Scholar 

  145. Lim, W. T. et al. Phase I pharmacokinetic study of a weekly liposomal paclitaxel formulation (Genexol R-PM) in patients with solid tumors. Ann. Oncol. 21, 382–388 (2010).

    Article  CAS  PubMed  Google Scholar 

  146. Brem, H. et al. Biocompatibility of a biodegradable, controlled-release polymer in the rabbit brain. Sel. Cancer Ther. 5, 55–65 (1989).

    Article  CAS  PubMed  Google Scholar 

  147. Brem, H. et al. Placebo-controlled trial of safety and efficacy of intraoperative controlled delivery by biodegradable polymers of chemotherapy for recurrent gliomas. Lancet 345, 1008–1012 (1995).

    Article  CAS  PubMed  Google Scholar 

  148. National Cancer Institute. Understanding cancer series: angiogenesis. National Cancer Institute website [online], http://www.cancer.gov/cancertopics/understandingcancer/angiogenesis/allpages (2005).

  149. Neri, D. & Bicknell, R. Tumour vascular targeting. Nature Rev. Cancer 5, 436–446 (2005).

    Article  CAS  Google Scholar 

  150. Desgrosellier, J. S. & Cheresh, D. A. Integrins in cancer: biological implications and therapeutic opportunities. Nature Rev. Cancer 10, 9–22 (2010). Comprehensive review of the role of integrin targeting in cancer therapeutics.

    Article  CAS  Google Scholar 

  151. Rolland, J. P. et al. Solvent-resistant photocurable “liquid teflon” for microfluidic device fabrication. J. Am. Chem. Soc. 126, 2322–2323 (2004).

    Article  CAS  PubMed  Google Scholar 

  152. Kelly, J. Y. & DeSimone, J. M. Shape-specific, monodisperse nano-molding of protein particles. J. Am. Chem. Soc. 130, 5438–5439 (2008).

    Article  CAS  PubMed  Google Scholar 

  153. Gratton, S. E. et al. Nanofabricated particles for engineered drug therapies: a preliminary biodistribution study of PRINT nanoparticles. J. Control. Release 121, 10–18 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Merkel, T. J. et al. Scalable, shape-specific, top-down fabrication methods for the synthesis of engineered colloidal particles. Langmuir 11 Dec 2009 (doi:10.1021/la903890h).

  155. Meng, F., Hennink, W. E. & Zhong, Z. Reduction-sensitive polymers and bioconjugates for biomedical applications. Biomaterials 30, 2180–2198 (2009).

    Article  CAS  PubMed  Google Scholar 

  156. Duncan, R. Designing polymer conjugates as lysosomotropic nanomedicines. Biochem. Soc. Trans. 35, 56–60 (2007).

    Article  CAS  PubMed  Google Scholar 

  157. Folkman, J. & Long, D. M. The use of silicone rubber as a carrier for prolonged drug therapy. J. Surg. Res. 4, 139–142 (1964).

    Article  CAS  PubMed  Google Scholar 

  158. Breslow, D. S. Biologically active synthetic polymers. Pure Appl. Chem. 46, 103–113 (1976).

    Article  CAS  Google Scholar 

  159. Regelson, W. Advances in intraperitoneal (intracavitary) administration of synthetic polymers for immunotherapy and chemotherapy. J. Bioact. Compat. Polym. 1, 84–107 (1986).

    Article  CAS  Google Scholar 

  160. Gregoriadis, G. Drug entrapment in liposomes. FEBS Lett. 36, 292–296 (1973).

    Article  CAS  PubMed  Google Scholar 

  161. Kramer, P. A. Albumin microspheres as vehicles for achieving specificity in drug delivery. J. Pharm. Sci. 63, 1646–1647 (1974).

    Article  CAS  PubMed  Google Scholar 

  162. Gurny, R., Peppas, N. A., Harrington, D. D. & Banker, G. S. Development of biodegradable and injectable lattices for controlled release of potent drugs. Drug Dev. Ind. Pharm. 7, 1–25 (1981).

    Article  CAS  Google Scholar 

  163. Klibanov, A. L., Maruyama, K., Torchilin, V. P. & Huang, L. Amphipathic polyethyleneglycols effectively prolong the circulation time of liposomes. FEBS Lett. 268, 235–237 (1990).

    Article  CAS  PubMed  Google Scholar 

  164. Kattan, J. et al. Phase I clinical trial and pharmacokinetic evaluation of Doxorubicin carried by polyisohexylcyanoacrylate nanoparticles. Invest. New Drugs 10, 191–199 (1992).

    Article  CAS  PubMed  Google Scholar 

  165. Gref, R. et al. Biodegradable long-circulating polymeric nanospheres. Science 263, 1600–1603 (1994).

    Article  CAS  PubMed  Google Scholar 

  166. Kreuter, J., Alyautdin, R. N., Kharkevich, D. A. & Ivanov, A. A. Passage of peptides through the blood–brain barrier with colloidal polymer particles (nanoparticles). Brain Res. 674, 171–174 (1995).

    Article  CAS  PubMed  Google Scholar 

  167. Malik, N., Evagorou, E. G. & Duncan, R. Dendrimer-platinate: a novel approach to cancer chemotherapy. Anticancer Drugs 10, 767–776 (1999).

    Article  CAS  PubMed  Google Scholar 

  168. Vasey, P. et al. Phase I clinical and pharmacokinetic study of PKI [N-(2-hydroxypropyl)methacrylamide copolymer doxorubicin]: first member of a new class of chemotherapeutic agents — drug–polymer conjugates. Clin. Cancer Res. 5, 83–94 (1999).

    CAS  PubMed  Google Scholar 

  169. Seymour, L. W. et al. Hepatic drug targeting: phase I evaluation of polymer-bound doxorubicin. J. Clin. Oncol. 20, 1668–1676 (2002).

    Article  CAS  PubMed  Google Scholar 

  170. Danson, S. et al. Phase I dose escalation and pharmacokinetic study of pluronic polymer-bound doxorubicin (SP1049C) in patients with advanced cancer. Br. J. Cancer 90, 2085–2091 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Kukowska-Latallo, J. F. et al. Nanoparticle targeting of anticancer drug improves therapeutic response in animal model of human epithelial cancer. Cancer Res. 65, 5317–5324 (2005).

    Article  CAS  PubMed  Google Scholar 

  172. Lee, C. C. et al. A single dose of doxorubicin-functionalized bow-tie dendrimer cures mice bearing C-26 colon carcinomas. Proc. Natl Acad. Sci. USA 103, 16649–16654 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Ahmed, F. et al. Shrinkage of a rapidly growing tumor by drug-loaded polymersomes: pH-triggered release through copolymer degradation. Mol. Pharm. 3, 340–350 (2006).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank S. Gratton, K. Herlihy, J. Kelly, T. Merkle, M. Napier and J. Wang for help with figures. R.A.P. is supported by the National Science Foundation under CHE-1004878 and CHE-0840518. J.M.D. is supported by the Science and Technology Centers program of the National Science Foundation under CHE-9876674; the National Institutes of Health (NIH) Program Project Grant PO1-GM059299; NIH Grant U54-CA119343 (the Carolina Center for Cancer Nanotechnology Excellence); DARPA 07-4627; Liquidia Technologies; the Office of Naval Research N00014-08-1-0978; the William R. Kenan Jr, Distinguished Professorship; and the Chancellor's Eminent Professorship at the University of North Carolina at Chapel Hill, USA.

Author information

Authors and Affiliations

Authors

Ethics declarations

Competing interests

Joseph M. DeSimone is co-founder of a company called Liquidia Technologies which has licensed the PRINT technology. As such, J.M.D. is a member of the Board of Directors and is a consultant at Liquidia. He also has an equity position in the company.

Related links

Related links

FURTHER INFORMATION

Robby A. Petros's homepage

Joseph M. DeSimone's homepage

Glossary

Therapeutic index

In the case of the anticancer drug doxorubicin, which displays dose-limiting cardiotoxicity, the therapeutic index is the amount of drug in the tumour compared with the amount of drug in the heart.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Petros, R., DeSimone, J. Strategies in the design of nanoparticles for therapeutic applications. Nat Rev Drug Discov 9, 615–627 (2010). https://doi.org/10.1038/nrd2591

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrd2591

This article is cited by

Search

Quick links

Nature Briefing: Translational Research

Sign up for the Nature Briefing: Translational Research newsletter — top stories in biotechnology, drug discovery and pharma.

Get what matters in translational research, free to your inbox weekly. Sign up for Nature Briefing: Translational Research