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Topical antimicrobial photodynamic therapy improves angiogenesis in wounds of diabetic mice

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Abstract

We report the results of our investigations on the effect of antimicrobial photodynamic therapy (APDT) on angiogenesis in wounds of diabetic mice. For this, measurements were made on levels of nitric oxide (NO), vascular endothelial growth factor-A (VEGF-A), and markers of proinflammatory stress (phosphorylated nuclear factor kappa B and p38 mitogen-activated protein kinase) on day 3 post-wounding. For uninfected and infected wounds, the levels of NO, VEGF-A were lower and the levels of phospho-NF-kB-p65, phospho-p38MAPK were higher in diabetic mice compared with that in nondiabetic mice. For infected wounds, multiple APDT (fluence ~60 J/cm2) led to increase in NO, VEGF-A levels and a decrease in the phospho-NF-kB-p65, phospho-p38MAPK. Further, compared with aminoguanidine, and silver nitrate, multiple APDT was observed to result in a much improved proangiogenic response.

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References

  1. Maisch T (2009) A new strategy to destroy antibiotic resistant microorganisms: antimicrobial photodynamic treatment. Mini Rev Med Chem 9:974–983

    Article  CAS  PubMed  Google Scholar 

  2. Hashimoto MC, Prates RA, Kato IT, SC N´ n˜ e, Courrol LC, Ribeiro MS (2012) Antimicrobial photodynamic therapy on drug resistant Pseudomonas aeruginosa induced infection. An in vivo study. Photochem Photobiol 88:590–595

    Article  CAS  PubMed  Google Scholar 

  3. Vecchio D, Dai T, Huang L, Fantetti L, Roncucci G, Hamblin MR (2013) Antimicrobial photodynamic therapy with RLP068 kills methicilin resistant Staphylococcus aureus and improves wound healing in a mouse model of infected skin abrasion. J Biophotonics 6:733–742

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  4. Sharma M, Bansal H, Gupta PK (2005) Virulence of Pseudomonas aeruginosa cells surviving photodynamic treatment with toluidine blue. Curr Microbiol 50:277–280

    Article  CAS  PubMed  Google Scholar 

  5. Sahu K, Sharma M, Bansal H, Dube A, Gupta PK (2013) Topical photodynamic treatment with poly-L-lysine-chlorin p6 conjugate improves wound healing by reducing hyperinflammatory response in Pseudomonas aeruginosa infected wounds of mice. Lasers Med Sci 28:465–471

    Article  PubMed  Google Scholar 

  6. Sahu K, Sharma M, Sharma P, Verma Y, Rao KD, Bansal H, Dube A, Gupta PK (2014) Effect of poly-L-lysine-chlorin p6-mediated antimicrobial photodynamic treatment on collagen restoration in bacteria-infected wounds. Photomed Laser Surg 32:23–29

    Article  CAS  PubMed  Google Scholar 

  7. Morley S, Griffiths J, Philips G, Moseley H, O'Grady C, Mellish K, Lankester CL et al (2013) Phase IIa randomized, placebo-controlled study of antimicrobial photodynamic therapy in bacterially colonized, chronic leg ulcers and diabetic foot ulcers: a new approach to antimicrobial therapy. Br J Dermatol 168:617–624

    Article  CAS  PubMed  Google Scholar 

  8. Tardivo JP, Adami F, Correa JA, Pinhal MA, Baptista MS (2014) A clinical trial testing the efficacy of PDT in preventing amputation in diabetic patients. Photodiagnosis Photodyn Ther 11:342–350

    Article  PubMed  Google Scholar 

  9. Mannucci E, Genovese S, Monami M, Navalesi G, Dotta F, Anichini R et al (2014) Photodynamic topical antimicrobial therapy for infected foot ulcers in patients with diabetes: a randomized, double-blind, placebo-controlled study—the D.A.N.T.E (Diabetic ulcer Antimicrobial New Topical treatment Evaluation) study. Acta Diabetol 51:435–440

    Article  CAS  PubMed  Google Scholar 

  10. Brownlee M (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414:813–820

    Article  CAS  PubMed  Google Scholar 

  11. Brem H, Tomic-Canic M (2007) Cellular and molecular basis of wound healing in diabetes. J Clin Invest 117:1219–1222

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Costa PZ, Soares R (2013) Neovascularization in diabetes and its complications. Unraveling the angiogenic paradox. Life Sci 92:1037–1045

    Article  CAS  PubMed  Google Scholar 

  13. Zhang X, Jiang F, Kalkanis SN, Zhang Z, Hong X, Yang H, Chopp M (2007) Post-acute response of 9L gliosarcoma to Photofrin-mediated PDT in athymic nude mice. Lasers Med Sci 22:253–259

    Article  PubMed  Google Scholar 

  14. Hoober JK, Sery TW, Yamamoto N (1988) Photodynamic sensitizers from chlorophyll: purpurin-18 and chlorin p6. Photochem Photobiol 48:579–582

    Article  CAS  PubMed  Google Scholar 

  15. Medicherla S, Wadsworth S, Cullen B, Silcock D, Ma JY, Mangadu R, Kerr I et al (2009) p38 MAPK inhibition reduces diabetes-induced impairment of wound healing. Diabetes Metab Syndr Obes 2:91–100

    PubMed Central  CAS  PubMed  Google Scholar 

  16. Zhu P, Ren M, Yang C, Hu YX, Ran JM, Yan L (2012) Involvement of RAGE, MAPK and NF-κB pathways in AGEs-induced MMP-9 activation in HaCaT keratinocytes. Exp Dermatol 21:123–129

    Article  CAS  PubMed  Google Scholar 

  17. Bien J, Sokolova O, Bozko P (2011) Characterization of virulence factors of Staphylococcus aureus: novel function of known virulence factors that are implicated in activation of airway epithelial proinflammatory response. J Pathog 2011:601905

    Article  PubMed Central  PubMed  Google Scholar 

  18. Son Y, Cheong YK, Kim NH, Chung HT, Kang DG, Pae HO (2011) Mitogen-activated protein kinases and reactive oxygen species: how can ROS activate MAPK pathways? J Signal Transduct 2011:792639

    PubMed Central  PubMed  Google Scholar 

  19. Kelleher ZT, Matsumoto A, Stamler JS, Marshall HE (2007) NOS2 regulation of NF-kappaB by S-nitrosylation of p65. J Biol Chem 282:30667–306772

    Article  CAS  PubMed  Google Scholar 

  20. Ozturk A, Fırat C, Parlakpınar H, Bay-Karabulut A, Kirimlioglu H, Gurlek A (2012) Beneficial effects of aminoguanidine on skin flap survival in diabetic rats. Exp Diabetes Res 2012:721256

    Article  PubMed Central  PubMed  Google Scholar 

  21. Tian M, Qing C, Niu Y, Dong J, Cao X, Song F, Ji X, Lu S (2013) Effect of aminoguanidine intervention on neutrophils in diabetes inflammatory cells wound healing. Exp Clin Endocrinol Diabetes 121:635–642

    Article  CAS  PubMed  Google Scholar 

  22. Atiyeh BB, Costagliola M, Hayek SN, Dibo SA (2007) Effect of silver on burn wound infection control and healing: review of the literature. Burns 33:139–148

    Article  PubMed  Google Scholar 

  23. Arora S, Ojha SK, Vohora D (2009) Characterisation of streptozotocin induced diabetes mellitus in Swiss albino mice. Global J Pharmacol 3:81–84

    Google Scholar 

  24. Zhao G, Usui ML, Underwood RA, Singh PK, James GA, Stewart PS et al (2012) Time course study of delayed wound healing in a biofilm-challenged diabetic mouse model. Wound Repair Regen 20:342–352

    Article  PubMed Central  PubMed  Google Scholar 

  25. Jagetia GC, Rajanikant GK, Mallikarjun Rao KV (2007) Ascorbic acid increases healing of excision wounds of mice whole body exposed to different doses of gamma-radiation. Burns 33:484–494

    Article  PubMed  Google Scholar 

  26. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD et al (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85

    Article  CAS  PubMed  Google Scholar 

  27. Kim YW, Byzova TV (2014) Oxidative stress in angiogenesis and vascular disease. Blood 123:625–631

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. Luo JD, Chen AF (2005) Nitric oxide: a newly discovered function on wound healing. Acta Pharmacol Sin 26:259–64

    Article  CAS  PubMed  Google Scholar 

  29. Witte MB, Barbul A (2002) Role of nitric oxide in wound repair. Am J Surg 183:406–412

    Article  CAS  PubMed  Google Scholar 

  30. Song S, Zhou F, Chen WR, Xing D (2013) PDT-induced HSP70 externalization up-regulates NO production via TLR2 signal pathway in macrophages. FEBS Lett 587:128–135

    Article  CAS  PubMed  Google Scholar 

  31. Herold S, Boccini F (2006) NO* release from MbFe(II)NO and HbFe(II)NO after oxidation by peroxynitrite. Inorg Chem 45:6933–6943

    Article  CAS  PubMed  Google Scholar 

  32. Tanaka M, Mroz P, Dai T, Huang L, Morimoto Y, Kinoshita M et al (2012) Photodynamic therapy can induce a protective innate immune response against murine bacterial arthritis via neutrophil accumulation. PLoS One 7, e39823

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  33. Jiang F, Zhang ZG, Katakowski M, Robin AM, Faber M, Zhang F, Chopp M (2004) Angiogenesis induced by photodynamic therapy in normal rat brains. Photochem Photobiol 79:494–498

    Article  CAS  PubMed  Google Scholar 

  34. Zhang X, Jiang F, Zhang ZG, Kalkanis SN, Hong X, Decarvalho AC, Chen J, Yang H, Robin AM, Chopp M (2005) Low-dose photodynamic therapy increases endothelial cell proliferation and VEGF expression in nude mice brain. Lasers Med Sci 20:74–79

    Article  PubMed  Google Scholar 

  35. Simonetti O, Cirioni O, Goteri G et al (2008) Temporin A is effective in MRSA-infected wounds through bactericidal activity and acceleration of wound repair in a murine model. Peptides 29:520–528

    Article  CAS  PubMed  Google Scholar 

  36. Frank H, Park S, Rich J, Lee JC (2011) Reduced neutrophil apoptosis in diabetic mice during staphylococcal infection leads to prolonged TNFα production and reduced neutrophil clearance. PLoS One 6, e23633

    Article  Google Scholar 

  37. Shibata T, Nagata K, Kobayashi Y (2010) The mechanism underlying the appearance of late apoptotic neutrophils and subsequent TNF-α production at a late stage during Staphylococcus aureus bioparticle-induced peritoneal inflammation in inducible NO synthase deficient mice. Biochim Biophys Acta 1802:1105–1111

    Article  CAS  PubMed  Google Scholar 

  38. Im SS, Osborne TF (2012) Protection from bacterial toxin induced apoptosis in macrophages requires the lipogenic transcription factor sterol regulatory element binding protein 1a. Mol Cell Biol 32:2196–2202

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. Power C, Wang JH, Sookai S, Street JT, Redmond HP (2001) Bacterial wall products induce down-regulation of vascular endothelial growth factor receptors on endothelial cells via a CD14-dependent mechanism: implications for surgical wound healing. J Surg Res 101:138–145

    Article  CAS  PubMed  Google Scholar 

  40. Zubkov MV, Fuchs BM, Eilers H, Burkill PH, Amann R (1999) Determination of total protein content of bacterial cells by SYPRO staining and flow cytometry. Appl Environ Microbiol 65:3251–3257

    PubMed Central  CAS  PubMed  Google Scholar 

  41. Ipaktchi K, Mattar A, Niederbichler AD, Hoesel LM, Vollmannshauser S, Hemmila MR et al (2007) Topical p38 MAPK inhibition reduces bacterial growth in an in vivo burn wound model. Surgery 142:86–89

    Article  PubMed Central  PubMed  Google Scholar 

  42. Ho FM, Lin WW, Chen BC, Chao CM, Yang CR, Lin LY et al (2006) High glucose induced apoptosis in human vascular endothelial cells is mediated through NF-kappaB and c-Jun NH2-terminal kinase pathway and prevented by PI3K/Akt/eNOS pathway. Cell Signal 18:391–399

    Article  CAS  PubMed  Google Scholar 

  43. Tabruyn SP, Griffioen AW (2008) NF-kappa B: a new player in angiostatic therapy. Angiogenesis 11:101–106

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  44. Marchi E, Vargas FS, Acencio MM, Antonangelo L, Teixeira LR, Light RW (2009) Low doses of silver nitrate induce pleurodesis with a limited systemic response. Respirology 14:885–889

    Article  PubMed  Google Scholar 

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Acknowledgment

The authors acknowledge help of Shri Anupam Chowdhury in establishment of wound infection and biochemical measurements.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics statement

All the experimental procedures involving animals were approved by the Institutional Animal Ethics Committee, in accordance with the guidelines of the Committee for Purpose of Care and Supervision of Experimental Animals (CPCSEA), Department of Environment and Forests, Government of India. The animals were housed individually in cages with free access to food and water and maintained on a 12-h light/dark cycle at 22 °C (±2 °C). All the animal manipulations involving wounds were carried out in anesthetized conditions, and animals were kept on warm cotton pads for recovery from anesthesia. Animals were euthanized by cervical dislocation. All research animals were treated humanely, and all efforts were made to minimize the animal suffering and the number of animals killed.

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Authors and Affiliations

  1. Laser Biomedical Applications and Instrumentation Division, R&D Block-D, Raja Ramanna Centre for Advanced Technology, Indore, 452 013, Madhya Pradesh, India

    Khageswar Sahu, Mrinalini Sharma, Alok Dube & Pradeep Kumar Gupta

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  1. Khageswar Sahu
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  2. Mrinalini Sharma
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  3. Alok Dube
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  4. Pradeep Kumar Gupta
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Correspondence to Khageswar Sahu.

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Sahu, K., Sharma, M., Dube, A. et al. Topical antimicrobial photodynamic therapy improves angiogenesis in wounds of diabetic mice. Lasers Med Sci 30, 1923–1929 (2015). https://doi.org/10.1007/s10103-015-1784-8

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  • DOI: https://doi.org/10.1007/s10103-015-1784-8

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