Skin electroporation of a plasmid encoding hCAP-18/LL-37 host defense peptide promotes wound healing

Molecular Therapy

Volumn 22, Issue 4, 2014, Pages 734-742

  Steinstraesser, Lars ^a   Lam, Martin C ^b,c   Jacobsen, Frank ^b   Porporato, Paolo E ^c   Chereddy, Kiran Kumar ^c   Becerikli, Mustafa ^b   Stricker, Ingo ^b   Hancock, Robert EW ^d   Lehnhardt, Marcus ^b   Sonveaux, Pierre ^c   Préat, Véronique ^c   Vandermeulen, Gaëlle ^c  

^a European Medical School   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

^c UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CHEMOKINE RECEPTOR CXCR4; STROMAL CELL DERIVED FACTOR 1ALPHA; VASCULOTROPIN A; ANTIMICROBIAL CATIONIC PEPTIDE; CAP18 LIPOPOLYSACCHARIDE-BINDING PROTEIN;

ANALYSIS OF VARIANCE; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; COLORIMETRY; CONTROLLED STUDY; DIABETES MELLITUS; ELECTROPORATION; EPITHELIZATION; HOST RESISTANCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; KERATINOCYTE; LIMB ISCHEMIA; MOUSE; MUSCLE ATROPHY; NONHUMAN; PLASMID; PROTEIN FUNCTION; PROTEIN INDUCTION; PUNCH BIOPSY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKIN INJURY; UPREGULATION; WOUND HEALING; ADMINISTRATION AND DOSAGE; ANIMAL; CELL CULTURE; ELECTROCHEMOTHERAPY; GENE THERAPY; GENETICS; HUMAN; METABOLISM; PATHOLOGY;

BACTERIA (MICROORGANISMS); MUS;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CELLS, CULTURED; ELECTROCHEMOTHERAPY; GENETIC THERAPY; HUMANS; KERATINOCYTES; MICE; PLASMIDS; WOUND HEALING;

EID: 84897575852     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2013.258     Document Type: Article

References (50)

1. Vinh, DC and Embil, JM (2005). Rapidly progressive soft tissue infections. Lancet Infect Dis 5: 501-513
2. Rice, LB (2003). Do we really need new anti-infective drugs? Curr Opin Pharmacol 3: 459-463
3. Grundmann, H, Aires-de-Sousa, M, Boyce, J and Tiemersma, E (2006). Emergence and resurgence of meticillin-resistant Staphylococcus aureus as a public-health threat. Lancet 368: 874-885
4. Hancock, RE and Sahl, HG (2006). Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechnol 24: 1551-1557
5. Sørensen, OE, Follin, P, Johnsen, AH, Calafat, J, Tjabringa, GS, Hiemstra, PS et al. (2001). Human cathelicidin, hCAP-18, is processed to the antimicrobial peptide LL-37 by extracellular cleavage with proteinase 3. Blood 97: 3951-3959
6. Steinstraesser, L, Koehler, T, Jacobsen, F, Daigeler, A, Goertz, O, Langer, S et al. (2008). Host defense peptides in wound healing. Mol Med 14: 528-537
7. Steinstraesser, L, Al-Benna, S, Kesting, M and Jacobsen, F (2009). Bioengineered human skin: Working the bugs out. Mol Ther 17: 405-408
8. Heilborn, JD, Nilsson, MF, Kratz, G, Weber, G, Sørensen, O, Borregaard, N et al. (2003). The cathelicidin anti-microbial peptide LL-37 is involved in re-epithelialization of human skin wounds and is lacking in chronic ulcer epithelium. J Invest Dermatol 120: 379-389
9. Nizet, V, Ohtake, T, Lauth, X, Trowbridge, J, Rudisill, J, Dorschner, RA et al. (2001). Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature 414: 454-457
10. Dressel, S, Harder, J, Cordes, J, Wittersheim, M, Meyer-Hoffert, U, Sunderkötter, C et al. (2010). Differential expression of antimicrobial peptides in margins of chronic wounds. Exp Dermatol 19: 628-632
11. Rivas-Santiago, B, Trujillo, V, Montoya, A, Gonzalez-Curiel, I, Castañeda-Delgado, J, Cardenas, A et al. (2012). Expression of antimicrobial peptides in diabetic foot ulcer. J Dermatol Sci 65: 19-26
12. Steinstraesser, L, Hirsch, T, Schulte, M, Kueckelhaus, M, Jacobsen, F, Mersch, EA et al. (2012). Innate defense regulator peptide 1018 in wound healing and wound infection. PLoS ONE 7: E39373
13. Schmidtchen, A, Frick, IM, Andersson, E, Tapper, H and Björck, L (2002). Proteinases of common pathogenic bacteria degrade and inactivate the antibacterial peptide LL-37. Mol Microbiol 46: 157-168
14. Carretero, M, Del Río, M, García, M, Escámez, MJ, Mirones, I, Rivas, L et al. (2004). A cutaneous gene therapy approach to treat infection through keratinocyte-Targeted overexpression of antimicrobial peptides. FASEB J 18: 1931-1933
15. Jacobsen, F, Mittler, D, Hirsch, T, Gerhards, A, Lehnhardt, M, Voss, B et al. (2005). Transient cutaneous adenoviral gene therapy with human host defense peptide hCAP-18/LL-37 is effective for the treatment of burn wound infections. Gene Ther 12: 1494-1502
16. Nikol, S (2007). Viral or non-viral angiogenesis gene transfer-New answers to old questions. Cardiovasc Res 73: 443-445
17. Thomas, CE, Ehrhardt, A and Kay, MA (2003). Progress and problems with the use of viral vectors for gene therapy. Nat Rev Genet 4: 346-358
18. Mäkinen, K, Manninen, H, Hedman, M, Matsi, P, Mussalo, H, Alhava, E et al. (2002). Increased vascularity detected by digital subtraction angiography after VEGF gene transfer to human lower limb artery: A randomized, placebo-controlled, doubleblinded phase II study. Mol Ther 6: 127-133
19. Vogt, PM, Thompson, S, Andree, C, Liu, P, Breuing, K, Hatzis, D et al. (1994). Genetically modified keratinocytes transplanted to wounds reconstitute the epidermis. Proc Natl Acad Sci USA 91: 9307-9311
20. Zhang, Z, Slobodianski, A, Ito, WD, Arnold, A, Nehlsen, J, Weng, S et al. (2011). Enhanced collateral growth by double transplantation of gene-nucleofected fibroblasts in ischemic hindlimb of rats. PLoS ONE 6: E19192
21. Nauta, A, Seidel, C, Deveza, L, Montoro, D, Grova, M, Ko, SH et al. (2013). Adiposederived stromal cells overexpressing vascular endothelial growth factor accelerate mouse excisional wound healing. Mol Ther 21: 445-455
22. Thomas-Virnig, CL, Centanni, JM, Johnston, CE, He, LK, Schlosser, SJ, Van Winkle, KF et al. (2009). Inhibition of multidrug-resistant Acinetobacter baumannii by nonviral expression of hCAP-18 in a bioengineered human skin tissue. Mol Ther 17: 562-569
23. Satkauskas, S, Bureau, MF, Puc, M, Mahfoudi, A, Scherman, D, Miklavcic, D et al. (2002). Mechanisms of in vivo DNA electrotransfer: Respective contributions of cell electropermeabilization and DNA electrophoresis. Mol Ther 5: 133-140
24. Pavselj, N and Préat, V (2005). DNA electrotransfer into the skin using a combination of one high-And one low-voltage pulse. J Control Release 106: 407-415
25. Vandermeulen, G, Staes, E, Vanderhaeghen, ML, Bureau, MF, Scherman, D and Préat, V (2007). Optimisation of intradermal DNA electrotransfer for immunisation. J Control Release 124: 81-87
26. Lee, PY, Chesnoy, S and Huang, L (2004). Electroporatic delivery of TGF-beta1 gene works synergistically with electric therapy to enhance diabetic wound healing in db/ db mice. J Invest Dermatol 123: 791-798
27. Marti, G, Ferguson, M, Wang, J, Byrnes, C, Dieb, R, Qaiser, R et al. (2004). Electroporative transfection with KGF-1 DNA improves wound healing in a diabetic mouse model. Gene Ther 11: 1780-1785
28. Liu, L, Marti, GP, Wei, X, Zhang, X, Zhang, H, Liu, YV et al. (2008). Agedependent impairment of HIF-1alpha expression in diabetic mice: Correction with electroporation-facilitated gene therapy increases wound healing, angiogenesis, and circulating angiogenic cells. J Cell Physiol 217: 319-327
29. Porporato, PE, Payen, VL, De Saedeleer, CJ, Préat, V, Thissen, JP, Feron, O et al. (2012). Lactate stimulates angiogenesis and accelerates the healing of superficial and ischemic wounds in mice. Angiogenesis 15: 581-592
30. Couffinhal, T, Silver, M, Zheng, LP, Kearney, M, Witzenbichler, B and Isner, JM (1998). Mouse model of angiogenesis. Am J Pathol 152: 1667-1679
31. Sonveaux, P, Martinive, P, DeWever, J, Batova, Z, Daneau, G, Pelat, M et al. (2004). Caveolin-1 expression is critical for vascular endothelial growth factor-induced ischemic hindlimb collateralization and nitric oxide-mediated angiogenesis. Circ Res 95: 154-161
32. Bosch-Marce, M, Okuyama, H, Wesley, JB, Sarkar, K, Kimura, H, Liu, YV et al. (2007). Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia. Circ Res 101: 1310-1318
33. Botusan, IR, Sunkari, VG, Savu, O, Catrina, AI, Grünler, J, Lindberg, S et al. (2008). Stabilization of HIF-1alpha is critical to improve wound healing in diabetic mice. Proc Natl Acad Sci USA 105: 19426-19431
34. Chesnoy, S and Huang, L (2002). Enhanced cutaneous gene delivery following intradermal injection of naked DNA in a high ionic strength solution. Mol Ther 5: 57-62
35. Meuli, M, Liu, Y, Liggitt, D, Kashani-Sabet, M, Knauer, S, Meuli-Simmen, C et al. (2001). Efficient gene expression in skin wound sites following local plasmid injection. J Invest Dermatol 116: 131-135
36. Sivamani, RK, Garcia, MS and Isseroff, RR (2007). Wound re-epithelialization: Modulating keratinocyte migration in wound healing. Front Biosci 12: 2849-2868
37. Miklavcic, D, Pucihar, G, Pavlovec, M, Ribaric, S, Mali, M, Macek-Lebar, A et al. (2005). The effect of high frequency electric pulses on muscle contractions and antitumor efficiency in vivo for a potential use in clinical electrochemotherapy. Bioelectrochemistry 65: 121-128
38. Ferraro, B, Heller, LC, Cruz, YL, Guo, S, Donate, A and Heller, R (2011). Evaluation of delivery conditions for cutaneous plasmid electrotransfer using a multielectrode array. Gene Ther 18: 496-500
39. Daugimont, L, Baron, N, Vandermeulen, G, Pavselj, N, Miklavcic, D, Jullien, MC et al. (2010). Hollow microneedle arrays for intradermal drug delivery and DNA electroporation. J Membr Biol 236: 117-125
40. Heller, LC, Jaroszeski, MJ, Coppola, D, McCray, AN, Hickey, J and Heller, R (2007). Optimization of cutaneous electrically mediated plasmid DNA delivery using novel electrode. Gene Ther 14: 275-280
41. André, FM, Gehl, J, Sersa, G, Préat, V, Hojman, P, Eriksen, J et al. (2008). Efficiency of high-And low-voltage pulse combinations for gene electrotransfer in muscle, liver, tumor, and skin. Hum Gene Ther 19: 1261-1271
42. Gallucci, RM, Sloan, DK, Heck, JM, Murray, AR and O'Dell, SJ (2004). Interleukin 6 indirectly induces keratinocyte migration. J Invest Dermatol 122: 764-772
43. Sehgal, PB (1990). Interleukin-6: Molecular pathophysiology. J Invest Dermatol 94(6 Suppl): 2S-6S.
44. Niyonsaba, F, Ushio, H, Nakano, N, Ng, W, Sayama, K, Hashimoto, K et al. (2007). Antimicrobial peptides human beta-defensins stimulate epidermal keratinocyte migration, proliferation and production of proinflammatory cytokines and chemokines. J Invest Dermatol 127: 594-604
45. Carretero, M, Escámez, MJ, García, M, Duarte, B, Holguín, A, Retamosa, L et al. (2008). In vitro and in vivo wound healing-promoting activities of human cathelicidin LL-37. J Invest Dermatol 128: 223-236
46. Ferraro, B, Cruz, YL, Baldwin, M, Coppola, D and Heller, R (2010). Increased perfusion and angiogenesis in a hindlimb ischemia model with plasmid FGF-2 delivered by noninvasive electroporation. Gene Ther 17: 763-769
47. Koczulla, R, von Degenfeld, G, Kupatt, C, Krötz, F, Zahler, S, Gloe, T et al. (2003). An angiogenic role for the human peptide antibiotic LL-37/hCAP-18. J Clin Invest 111: 1665-1672
48. Rodríguez-Martínez, S, Cancino-Diaz, JC, Vargas-Zuñiga, LM and Cancino-Diaz, ME (2008). LL-37 regulates the overexpression of vascular endothelial growth factor (VEGF) and c-IAP-2 in human keratinocytes. Int J Dermatol 47: 457-462
49. Marie, C, Vandermeulen, G, Quiviger, M, Richard, M, Préat, V and Scherman, D (2010). pFARs, plasmids free of antibiotic resistance markers, display high-level transgene expression in muscle, skin and tumour cells. J Gene Med 12: 323-332
50. Lin, ZQ, Kondo, T, Ishida, Y, Takayasu, T and Mukaida, N (2003). Essential involvement of IL-6 in the skin wound-healing process as evidenced by delayed wound healing in IL-6-deficient mice. J Leukoc Biol 73: 713-721.