Topical prolyl hydroxylase domain-2 silencing improves diabetic murine wound closure

Wound Repair and Regeneration

Volumn 19, Issue 4, 2011, Pages 481-486

  Wetterau, Meredith ^a   George, Finny ^a   Weinstein, Andrew ^a   Nguyen, Phuong D ^a   Tutela, John Paul ^a   Knobel, Denis ^a   Cohen Ba, Oriana ^a   Warren, Stephen M ^a   Saadeh, Pierre B ^a  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; FIBROBLAST GROWTH FACTOR 2; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROTEIN; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; ENZYME ACTIVE SITE; GENE SILENCING; HISTOLOGY; MOUSE; NONHUMAN; PHOTOMETRY; PRIORITY JOURNAL; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE DOMAIN 2; RNA ANALYSIS; RNA INTERFERENCE; SHAM PROCEDURE; STENT; WESTERN BLOTTING; WOUND; WOUND CLOSURE;

ANIMALS; DIABETES MELLITUS; DISEASE MODELS, ANIMAL; FIBROBLAST GROWTH FACTOR 2; GENE SILENCING; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; PROCOLLAGEN-PROLINE DIOXYGENASE; RNA, MESSENGER; RNA, SMALL INTERFERING; SKIN; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WOUND HEALING;

EID: 79960103014     PISSN: 10671927     EISSN: 1524475X     Source Type: Journal    
DOI: 10.1111/j.1524-475X.2011.00697.x     Document Type: Article

References (37)

1. Laing P., The development and complications of diabetic foot ulcers. Am J Surg 1998; 176: 11S-9S. (Pubitemid 28460653)
2. Capla JM, Grogan RH, Callaghan MJ, Galiano RD, Tepper OM, Ceradini DJ, Gurtner GC., Diabetes impairs endothelial progenitor cell-mediated blood vessel formation in response to hypoxia. Plast Reconstr Surg 2006; 119: 59-70. (Pubitemid 46360247)
3. Tepper OM, Galiano RD, Capla JM, Kalka C, Gagne PJ, Jacobowitz GR, Levine JP, Gurtner GC., Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation 2002; 106: 2781-6. (Pubitemid 35396976)
4. Abaci A, Oguzhan A, Kahraman S, Eryol NK, Unal S, ArinÃ? H, Ergin A., Effect of diabetes mellitus on formation of coronary collateral vessels. Circulation 199; 99: 2239-42. (Pubitemid 29201128)
5. Haffner SM, Lehto S, Ronnemaa T, Pyörälä K, Laakso M., Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N Engl J Med 1998; 339: 229-34. (Pubitemid 28350165)
6. Shintani S, Murohara T, Ideka H, Ueno T, Honma T, Katoh A, Sasaki K, Shimada T, Oike Y, Imaizumi T., Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation 2001; 103: 2776-9. (Pubitemid 32550062)
7. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M, Magner M, Isner JM, Asahara T., Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 1999; 5: 434-8. (Pubitemid 29180584)
8. Martin A, Komada MR, Sane DC., Abnormal angiogenesis in diabetes mellitus. Med Res Rev 2003; 23: 117-45. (Pubitemid 36241095)
9. Isner JM, Asahara T., Angiogenesis and vasculogenesis as therapeutic strategies for postnatal neovascularization. J Clin Invest 1999; 103: 1231-6. (Pubitemid 29218292)
10. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, Isner JM., Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 1999; 85: 221-8. (Pubitemid 29377293)
11. Bardos J, Ashcroft M., Negative and positive regulation of HIF-1: a complex network. Biochem Biophys Acta 2005; 1775: 107-20. (Pubitemid 40982561)
12. Pepper MS, Ferrara N, Orci L, Montesano R., Potent synergism between vascular endothelial growth factor and basic fibroblast growth factor in the induction of angiogenesis in vitro. Biochem Biophys Res Commun 1992; 189: 824-31. (Pubitemid 23032448)
13. Cao R, Brakenhielm E, Pawliuk R, Wariaro D, Post MJ, Wahlberg E, Leboulch P, Cao Y., Angiogenic synergism, vasular stability and improvement of hind-limb ischemia by the combination of PDGF-BB and FGF-2. Nat Med 2003; 9: 604-13. (Pubitemid 36597108)
14. Asahara T, Bauters C, Zheng LP, Takeshita S, Bunting S, Ferrara N, Symes JF, Isner JM., Synergistic effect of vascular endothelial growth factor and basic fibroblast growth factor on angiogenesis in vivo. Circulation 1995; 92: 11365-71.
15. Kano MR, Morishita Y, Iwata C, Iwasaka S, Watabe T, Ouchi Y, Miyazono K, Miyazawa K., VEGF-A and FGF-2 synergistically promote neoangiogenesis through enhancement of endogenous PDGF-B-PDGFR beta signaling. J Cell Sci 2005; 118: 3759-68. (Pubitemid 41309422)
16. Kelly BD, Hackett SF, Hirota K, Oshima Y, Cai Z, Berg-Dixon S, Rowan A, Yan Z, Campochiaro PA, Semenza GL., Cell type-specific regulation of angiogenic growth factor gene expression and induction of angiogenesis in nonischemic tissue by a constitutively active form of hypoxia-inducible factor-1. Circ Res 2003; 93: 1074-81. (Pubitemid 37485038)
17. Appelhoff RJ, Tian YM, Raval RR, Turley H, Harris AL, Pugh CW, Ratcliffe PJ, Gleadle JM., Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor. J Biol Chem 2004; 279: 38458-65. (Pubitemid 39295997)
18. Wu S, Nishiyama N, Kano M, Morishita Y, Miyazono K, Itaka K, Chung UI, Kataoka K., Enhancement of angiogenesis through stabilization of hypoxia-inducible factor-1 by silencing prolyl hydroxylase domain-2 gene. Mol Ther 2008; 16: 1227-34. (Pubitemid 351866053)
19. Takeda K, Cowan A, Fong GH., Essential role of prolyl hydroxylase domain protein-2 in oxygen homeostasis of the adult vascular system. Circulation 2007; 116: 774-81. (Pubitemid 47255995)
20. Scherr M, Morgan M, Eder M., Gene silencing mediated by small interfering RNAs in mammalian cells. Curr Med Chem 2003; 10: 245-56. (Pubitemid 36131657)
21. Thanik VD, Greives MR, Lerman OZ, Seiser N, Dec W, Chang CC, Warren SM, Levine JP, aadeh PB., Topical matrix-based siRNA silences local gene expression in a murine wound model. Gene Ther 2007; 14: 1305-8. (Pubitemid 47299955)
22. Takashima A., Establishment of fibroblast cultures. Curr Protoc Cell Biol 1998; 2.1.1-12. Available at
23. Galiano RD, Michaels, J, V, Dobryansky M, Levine JP, Gurtner GC., Quantitative and reproducible murine model of excisional wound healing. Wound Repair Regen 2004; 12: 485-92. (Pubitemid 39007049)
24. Michaels J, Churgin SS, Blechman KM, Greives MR, Aarabi S, Galiano RD, Gurtner GC., db/db mice exhibit severe wound-healing impairments compared with other murine diabetic strains in a silicone-splinted excisional wound model. Wound Repair Regen 2007; 15: 665-70. (Pubitemid 47493885)
25. Feener EP, King GL., Vascular dysfunction in diabetes mellitus. Lancet 1997; 350: SI9-13. (Pubitemid 27303531)
26. Mace KA, Yu DH, Paydar KZ, Boudreau N, Young DM., Sustained expression of HIF-1α in the diabetic environment promotes angiogenesis and cutaneous wound repair. Wound Repair Regen 2007; 15: 636-45. (Pubitemid 47493890)
27. Simons M, Annex BH, Laham RJ, Kleiman N, Henry T, Dauerman H, Udelson JE, Gervino EV, Pike M, Whitehouse MJ, Moon T, Chronos NA., Pharmacological treatment of coronary artery disease with recombinant fibroblast growth factor-2: double blind, randomized controlled clinical trial. Circulation 2002; 105: 788-93. (Pubitemid 34174916)
28. Liu R, Bal HS, Desta T, Behl Y, Graves DT., Tumor necrosis factor-alpha mediates diabetes-enhanced apoptosis of matrix-producing cells and impairs diabetic healing. Am J Pathol 2006; 168: 757-64. (Pubitemid 43327728)
29. Desta T, Li J, Chino T, Graves DT., Altered fibroblast proliferation and apoptosis in diabetic gingival wounds. J Dent Res 2010; 89: 609-14. Epub March 30, 2010.
30. Siqueira MF, Li J, Chehab L, Desta T Chino T, Krothpali N, Behl Y, Alikhani M, Yang J, Braasch C, Graves DT., Impaired wound healing in mouse models of diabetes is mediated by TNF-alpha dysregulation and associated with enhanced activation of forkhead box O1 (FOXO1). Diabetologia 2010; 53: 378-88. Epub November 10, 2009.
31. Lerman OZ, Galiano RD, Armour M, Levine JP, Gurtner GC., Cellular dysfunction in the diabetic fibroblast: impairment in migration, vascular endothelial growth factor production, and response to hypoxia. Am J Pathol 2003; 162: 303-12. (Pubitemid 36042012)
32. McMahon S, Charbonneau M, Grandmont S, Richard DE, Dubois CM., Transforming growth factor beta1 induces hypoxia-inducible factor-1 stabilization through selective inhibition of PHD2 expression. J Biol Chem 2006; 281: 24171-81. Epub June 30, 2006. (Pubitemid 44274191)
33. Velander P, Theopold C, Hirsch T, Bleiziffer O, Zuhaili B, Fossum M, Hoeller D, Gheerardyn R, Chen M, Visovatti S, Svensson H, Yao F, Eriksson E., Impaired wound healing in an acute diabetic pig model and the effects of local hyperglycemia. Wound Repair Regen 2008; 16: 288-93. (Pubitemid 351342136)
34. Gleich LL, Biddinger PW, Duperier FD, Gluckman JL., Tumor angiogenesis as a prognostic indicator in T2-T4 oral cavity squamous cell carcinoma: a clinical-pathologic correlation. Head Neck 1997; 19: 276-80. (Pubitemid 27273105)
35. Henry TD, Annex BH, McKendall GR, Azrin MA, Lopez JJ, Giordano FJ, Shah PK, Willerson JT, Benza RL, Berman DS, Gibson CM, Bajamonde A, Rundle AC, Fine J, McCluskey ER, VIVA Investigators. The VIVA trial: vascular endothelial growth factor in ischemia for vascular angiogenesis. Circulation 2003; 107: 1359-65. (Pubitemid 36350732)
36. Lee SH, Schloss DJ, Swain JL., Maintenance of vascular integrity in the embryo requires signaling through the fibroblast growth factor receptor. J Biol Chem 2000; 275: 3367. 9-86.
37. Elson DA, Thurston G, Huang LE, Ginzinger DG, McDonald DM, Johnson RS, Arbeit JM., Induction of hypervascularity without leakage of inflammation in transgenic mice overexpressing hypoxia-inducible factor 1-α. Genes Dev 2001; 15: 2520-32. (Pubitemid 32937863)