Mechanism of sustained release of vascular endothelial growth factor in accelerating experimental diabetic healing

Journal of Investigative Dermatology

Volumn 129, Issue 9, 2009, Pages 2275-2287

  Brem, Harold ^a   Kodra, Arber ^a   Golinko, Michael S ^a   Entero, Hyacinth ^g   Stojadinovic, Olivera ^b   Wang, Vincent M ^c   Sheahan, Claudia M ^d   Weinberg, Alan D ^e   Woo, Savio L C ^e   Ehrlich, H Paul ^f   Tomic Canic, Marjana ^b  

^a NEW YORK UNIVERSITY   (United States)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^c RUSH UNIVERSITY MEDICAL CENTER   (United States)

^d LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^f PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

^g NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; COLLAGEN; DL 312; EPIDERMAL GROWTH FACTOR; LONG ACTING INSULIN; NOVOLIN 30/70; UNCLASSIFIED DRUG; VASCULOTROPIN 165; WOUND HEALING PROMOTING AGENT; ZINC FINGER PROTEIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; COLLAGEN SYNTHESIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC FOOT; DRUG DOSE COMPARISON; DRUG MEGADOSE; EPITHELIZATION; FEMALE; FOOT ULCER; GENE TRANSFER; GRANULATION TISSUE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; IN VIVO STUDY; KERATINOCYTE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SKIN FIBROBLAST; SUSTAINED DRUG RELEASE; TENSILE STRENGTH; VIRAL GENE DELIVERY SYSTEM; WOUND; WOUND CLOSURE; WOUND HEALING;

ADENOVIRIDAE; ANIMALS; COLLAGEN; DIABETES MELLITUS; EPITHELIUM; FEMALE; GENE THERAPY; GRANULATION TISSUE; HUMANS; MICE; MICE, INBRED NOD; REGENERATION; TENSILE STRENGTH; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WOUND HEALING;

EID: 70349748588     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2009.26     Document Type: Article

References (62)

1. Abbott CA, Callington AL, Ashe H, Bath S, Every LC, Griffiths J et al. (2002) The North-West diabetes foot care study: incidence of, and risk factors for, new diabetic foot ulceration in a community-based patient cohort. Diabet Med 19(3):377-384
2. Aoyama T, Yamamoto S, Kanematsu A, Ogawa O, Tabata Y (2003) Local delivery of matrix metalloproteinase gene prevents the onset of renal sclerosis in streptozotocin-induced diabetic mice. Tissue Eng 9:1289-1299
3. Bikle DD, Oda Y, Xie Z (2004) Calcium and 1,25(OH)2D: interacting drivers of epidermal differentiation. J Steroid Biochem Mol Biol 89-90:355-360
4. Brem H, Erlich P, Tsakayannis D, Folkman J et al. (1997) Delay of wound healing by the angiogenesis inhibitor TNP-470. Surgical Forum 48:714-716
5. Brem H, Stojadinovic O, Diegelmann RF, Entero H, Lee B, Pastar I et al. (2007) Molecular markers in patients with chronic wounds to guide surgical debridement. Mol Med 13:30-39
6. Brkovic A, Sirois MG (2007) Vascular permeability induced by VEGF family members in vivo: role of endogenous PAF and NO synthesis. J Cell Biochem 100(3):727-737
7. Chandler LA, Gu DL, Ma C, Gonzalez AM, Doukas J, Nguyen T et al. (2000) Matrix-enabled gene transfer for cutaneous wound repair. Wound Repair Regen 8:473-479
8. Chang DS, Su H, Tang GL, Brevetti LS, Sarkar R, Wang R et al. (2003) Adeno-associated viral vector-mediated gene transfer of VEGF normalizes skeletal muscle oxygen tension and induces arteriogenesis in ischemic rat hindlimb. Mol Ther 7:44-51
9. Cho CH, Sung HK, Kim KT, Cheon HG, Oh GT, Hong HJ et al. (2006) COMP-angiopoietin-1 promotes wound healing through enhanced angiogenesis, lymphangiogenesis, and blood flow in a diabetic mouse model. Proc Natl Acad Sci USA 103:4946-4951
10. Crombleholme TM (2000) Adenoviral-mediated gene transfer in wound healing. Wound Repair Regen 8:460-472
11. Davidson JM, Krieg T, Eming SA (2000) Particle-mediated gene therapy of wounds. Wound Repair Regen 8:452-459
12. Davis WA, Norman PE, Bruce DG, Davis TM (2006) Predictors, consequences and costs of diabetes-related lower extremity amputation complicating type 2 diabetes: the Fremantle Diabetes Study. Diabeto-logia 49:2634-2641
13. Eming SA, Whitsitt JS, He L, Krieg T, Morgan JR, Davidson JM (1999) Particle-mediated gene transfer of PDGF isoforms promotes wound repair. J Invest Dermatol 112:297-302
14. Faglia E, Clerici G, Clerissi J, Gabrielli L, Losa S, Mantero M et al. (2006) Early and five-year amputation and survival rate of diabetic patients with critical limb ischemia: data of a cohort study of 564 patients. Eur J Vasc Endovasc Surg 32:484-490
15. Ferrara N (1999) Molecular and biological properties of vascular endothelial growth factor. J Mol Med 77:527-543 (Pubitemid 29426311)
16. Folkman J (2007) Angiogenesis: an organizing principle for drug discovery? Nature Rev 6:273-286 (Pubitemid 46505878)
17. Galeano M, Deodato B, Altavilla D, Cucinotta D, Arsic N, Marini H et al. (2003) Adeno-associated viral vector-mediated human vascular en-dothelial growth factor gene transfer stimulates angiogenesis and wound healing in the genetically diabetic mouse. Diabetologia 46:546-555
18. Gavard J, Gutkind JS (2006) VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat Cell Biol 8:1223-1234
19. Gibran NS, Jang YC, Isik FF, Greenhalgh DG, Muffley LA, Underwood RA et al. (2002) Diminished neuropeptide levels contribute to the impaired cutaneous healing response associated with diabetes mellitus. J Surg Res 108:122-128
20. Griffoen AW, Molema G (2000) Angiogenesis: potentials for pharmacological intervention in the treatment of cancer, cardiovascular diseases, and chronic inflammation. Pharmacol Rev 52:237-268
21. Harvey BG, Maroni J, O?Donoghue KA, Chu KW, Muscat JC, Pippo AL et al. (2002) Safety of local delivery of low- and intermediate-dose adenovirus gene transfer vectors to individuals with a spectrum of morbid conditions. Hum Gene Ther 13:15-63 (Pubitemid 34075172)
22. Hedman M, Hartikainen J, Syvanne M, Stjernvall J, Hedman A, Kivela A et al. (2003) Safety and feasibility of catheter-based local intracoronary vascular endothelial growth factor gene transfer in the prevention of postangioplasty and in-stent restenosis and in the treatment of chronic myocardial ischemia: phase II results of the Kuopio Angiogenesis Trial (KAT). Circulation 107:2677-2683
23. Huang N, Khan A, Ashrafpour H, Neligan PC, Forrest CR, Kontos CD et al. (2006) Efficacy and mechanism of adenovirus-mediated VEGF-165 gene therapy for augmentation of skin flap viability. Am J Physiol Heart Circ Physiol 291:H127-37
24. Iwaguro H, Yamaguchi J, Kalka C, Murasawa S, Masuda H, Hayashi S et al. (2002) Endothelial progenitor cell vascular endothelial growth factor gene transfer for vascular regeneration. Circulation 105:732-738
25. Jho SH, Vouthounis C, Lee B, Stojadinovic O, Im MJ, Brem H et al. (2005) The book of opposites: the role of the nuclear receptor co-regulators in the suppression of epidermal genes by retinoic acid and thyroid hormone receptors. J Invest Dermatol 124:1034-1043
26. Keswani SG, Katz AB, Lim FY, Zoltick P, Radu A, Alaee D et al. (2004) Adenoviral mediated gene transfer of PDGF-B enhances wound healing in type I and type II diabetic wounds. Wound Repair Regen 12:497-504
27. Laitinen M, Hartikainen J, Hiltunen MO, Eranen J, Kiviniemi M, Narvanen O et al. (2000) Catheter-mediated vascular endothelial growth factor gene transfer to human coronary arteries after angioplasty. Hum Gene Ther 11:263-270
28. Lavery LA, Armstrong DG, Murdoch DP, Peters EJ, Lipsky BA (2007) Validation of the Infectious Diseases Society of America?s diabetic foot infection classification system. Clin Infect Dis 44:562-565
29. Lavery LA, Armstrong DG, Wunderlich RP, Mohler MJ, Wendel CS, Lipsky BA (2006) Risk factors for foot infections in individuals with diabetes. Diabetes Care 29:1288-1293
30. Lee B, Vouthounis C, Stojadinovic O, Brem H, Im M, Tomic-Canic M (2005a) From an enhanceosome to a repressosome: molecular antagonism between glucocorticoids and EGF leads to inhibition of wound healing. J Mol Biol 345:1083-1097
31. Lee JA, Conejero JA, Mason JM, Parrett BM, Wear-Maggitti KD, Grant RT et al. (2005b) Lentiviral transfection with the PDGF-B gene improves diabetic wound healing. Plast Reconstr Surg 116:532-538
32. Levy RJ, Song C, Tallapragada S, DeFelice S, Hinson JT, Vyavahare N et al. (2001) Localized adenovirus gene delivery using antiviral IgG complexation. Gene Ther 8:659-667
33. Li Y, Hazarika S, Xie D, Pippen AM, Kontos CD, Annex BH (2007) In mice with type 2 diabetes, a vascular endothelial growth factor (VEGF)-activating transcription factor modulates VEGF signaling and induces therapeutic angiogenesis after hindlimb ischemia. Diabetes 56:656-665
34. Malay DS, Margolis DJ, Hoffstad OJ, Bellamy S (2006) The incidence and risks of failure to heal after lower extremity amputation for the treatment of diabetic neuropathic foot ulcer. J Foot Ankle Surg 45:366-374
35. Marston WA, Hanft J, Norwood P, Pollak R (2003) The efficacy and safety of dermagraft in improving the healing of chronic diabetic foot ulcers: results of a prospective randomized trial. Diabetes Care 26:1701-1705
36. Michaels Jt, Dobryansky M, Galiano RD, Bhatt KA, Ashinoff R, Ceradini DJ et al. (2005) Topical vascular endothelial growth factor reverses delayed wound healing secondary to angiogenesis inhibitor administration. Wound Repair Regen 13:506-512
37. Nawar EW, Niska RW, Xu J (2007) National Hospital Ambulatory Medical Care Survey: 2005 emergency department summary. Advance Data, 386:1-32
38. Radoja N, Komine M, Jho SH, Blumenberg M, Tomic-Canic M (2000) Novel mechanism of steroid action in skin through glucocorticoid receptor monomers. Mol Cell Biol 20:4328-4339
39. Raja, Sivamani K, Garcia MS, Isseroff RR (2007) Wound re-epithelialization: modulating keratinocyte migration in wound healing. Front Biosci 12:2849-2868
40. Rathur HM, Boulton AJ (2007) The diabetic foot. Clin Dermatol 25:109-120
41. Rivard A, Silver M, Chen D, Kearney M, Magner M, Annex B et al. (1999) Rescue of diabetes-related impairment of angiogenesis by intramuscular gene therapy with adeno-VEGF. Am J Pathol 154:355-363
42. Robinson CJ, Stringer SE (2001) The splice variants of vascular endothelial growth factor (VEGF) and their receptors. J Cell Sci 114:853-865
43. Romano Di Peppe S, Mangoni A, Zambruno G, Spinetti G, Melillo G, Napolitano M et al. (2002) Adenovirus-mediated VEGF(165) gene transfer enhances wound healing by promoting angiogenesis in CD1 diabetic mice. Gene Ther 9:1271-1277
44. Rosengart TK, Lee LY, Patel SR, Kligfield PD, Okin PM, Hackett NR et al. (1999a) Six-month assessment of a phase I trial of angiogenic gene therapy for the treatment of coronary artery disease using direct intramyocardial administration of an adenovirus vector expressing the VEGF121 cDNA. Ann Surg 230:466-70; discussion 462-470
45. Rosengart TK, Lee LY, Patel SR, Sanborn TA, Parikh M, Bergman GW et al. (1999b) Angiogenesis gene therapy: phase I assessment of direct intramyocardial administration of an adenovirus vector expressing VEGF121 cDNA to individuals with clinically significant severe coronary artery disease. Circulation 100:468-474
46. Saaristo A, Tammela T, Farkkila A, Karkkainen M, Suominen E, Yla-Herttuala S et al. (2006) Vascular endothelial growth factor-C accelerates diabetic wound healing. Am J Pathol 169:1080-1087
47. Shimpo M, Ikeda U, Maeda Y, Takahashi M, Miyashita H, Mizukami H et al. (2002) AAV-mediated VEGF gene transfer into skeletal muscle stimulates angiogenesis and improves blood flow in a rat hindlimb ischemia model. Cardiovasc Res 53:993-1001
48. Smiell JM (1998) Clinical safety of becaplermin (rhPDGF-BB) gel. Becapler-min Studies Group. Am J Surg 176:S68-73
49. Smiell JM, Wieman TJ, Steed DL, Perry BH, Sampson AR, Schwab BH (1999) Efficacy and safety of becaplermin (recombinant human platelet-derived growth factor-BB) in patients with nonhealing, lower extremity diabetic ulcers: a combined analysis of four randomized studies. Wound Repair Regen 7:335-346
50. Steed DL (1995) Clinical evaluation of recombinant human platelet-derived growth factor for the treatment of lower extremity diabetic ulcers. Diabetic Ulcer Study Group. J Vasc Surg 21:71-8; discussion 79-81
51. Steed DL (2006) Clinical evaluation of recombinant human platelet-derived growth factor for the treatment of lower extremity ulcers. Plast Reconstr Surg 117:143S-9S; discussion S150-1
52. Stewart DJ, Hilton JD, Arnold JM, Gregoire J, Rivard A, Archer SL et al. (2006) Angiogenic gene therapy in patients with nonrevascularizable ischemic heart disease: a phase 2 randomized, controlled trial of AdVEGF(121) (AdVEGF121) versus maximum medical treatment. Gene Ther 13:1503-1511
53. Stojadinovic O, Brem H, Vouthounis C, Lee B, Fallon J, Stallcup M et al. (2005) Molecular pathogenesis of chronic wounds: the role of betacatenin and c-myc in the inhibition of epithelialization and wound healing. Am J Pathol 167:59-69
54. Stojadinovic O, Lee B, Vouthounis C, Vukelic S, Pastar I, Blumenberg M et al. (2006) Novel genomic effects of glucocorticoids in epidermal keratinocytes: inhibition of apoptosis, IFNgamma pathway and wound healing along with promotion of terminal differentiation. J Biol Chem 262(6):4021-4034
55. Stojadinovic O, Pastar I, Vukelic S, Mahoney MG, Brennan D, Krzyzanowska A et al. (2008) Deregulation of keratinocyte differentiation and activation: a hallmark of venous ulcers. J Cell Mol Med 12(68):2675-2690
56. Stojadinovic O, Kodra A, Golinko M, Tomic-Canic M, Brem H (2007) A novel non-angiogenic mechanism of VEGF: Stimulation of keratinocyte and fibroblast migration. Wound Repair and Regen 15:A30 (Abstr.)
57. Vajanto I, Rissanen TT, Rutanen J, Hiltunen MO, Tuomisto TT, Arve K et al. (2002) Evaluation of angiogenesis and side effects in ischemic rabbit hindlimbs after intramuscular injection of adenoviral vectors encoding VEGF and LacZ. J Gene Med 4:371-380
58. Valensi P, Girod I, Baron F, Moreau-Defarges T, Guillon P (2005) Quality of life and clinical correlates in patients with diabetic foot ulcers. Diabetes Metab 31:263-271
59. Veves A, Falanga V, Armstrong DG, Sabolinski ML (2001) Graftskin, a human skin equivalent, is effective in the management of noninfected neuropathic diabetic foot ulcers: a prospective randomized multicenter clinical trial. Diabetes Care 24:290-295
60. Witte MB, Kiyama T, Barbul A (2002) Nitric oxide enhances experimental wound healing in diabetes. Br J Surg 89:1594-1601
61. Yamagishi S, Yonekura H, Yamamoto Y, Fujimori H, Sakurai S, Tanaka N et al. (1999) Vascular endothelial growth factor acts as a pericyte mitogen under hypoxic conditions. Lab Invest 79:501-509
62. Yao F, Eriksson E (2000) Gene therapy in wound repair and regeneration. Wound Repair Regen 8:443-451