Deletion of prolyl hydroxylase domain proteins (PHD1, PHD3) stabilizes hypoxia inducible factor-1 alpha, promotes neovascularization, and improves perfusion in a murine model of hind-limb ischemia

Microvascular Research

Volumn 97, Issue , 2015, Pages 181-188

  Rishi, Muhammad T ^a,b   Selvaraju, Vaithinathan ^a   Thirunavukkarasu, Mahesh ^a   Shaikh, Inam A ^a,b   Takeda, Kotaro ^a   Fong, Guo Hua ^a   Palesty, J Alexander ^b   Sanchez, Juan A ^a   Maulik, Nilanjana ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b ST MARY S HOSPITAL   (United States)

Author keywords

Bcl 2; HIF; Hindlimb ischemia; Prolyl hydroxylase; VEGF

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE 1; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE 3; PROTEIN BCL 2; UNCLASSIFIED DRUG; VASCULOTROPIN; BCL2 PROTEIN, MOUSE; HIF1A PROTEIN, MOUSE; PHD1 PROTEIN, MOUSE; PHD3 PROTEIN, MOUSE; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ADULT; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY LIGATION; ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMORAL ARTERY LIGATION; FIBROSIS; HINDLIMB ISCHEMIA; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LASER DOPPLER FLOWMETRY; LIMB ISCHEMIA; LIMB PERFUSION; MALE; MOTOR PERFORMANCE; MOUSE; NONHUMAN; PERIPHERAL OCCLUSIVE ARTERY DISEASE; PICROSIRIUS RED STAINING; PROTEIN EXPRESSION; PROTEIN STABILITY; STAINING; ANIMAL; BLOOD FLOW; C57BL MOUSE; CONVALESCENCE; DEFICIENCY; DISEASE MODEL; GENE DELETION; GENETICS; HINDLIMB; ISCHEMIA; KNOCKOUT MOUSE; METABOLISM; MOTOR ACTIVITY; PATHOLOGY; PATHOPHYSIOLOGY; SKELETAL MUSCLE; TIME; VASCULARIZATION;

MURINAE; MUS;

ANIMALS; DISEASE MODELS, ANIMAL; FIBROSIS; GENE DELETION; HINDLIMB; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; ISCHEMIA; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; PROCOLLAGEN-PROLINE DIOXYGENASE; PROTEIN STABILITY; PROTO-ONCOGENE PROTEINS C-BCL-2; RECOVERY OF FUNCTION; REGIONAL BLOOD FLOW; TIME FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84918577369     PISSN: 00262862     EISSN: 10959319     Source Type: Journal    
DOI: 10.1016/j.mvr.2014.10.009     Document Type: Article

References (43)

1. Adam D.J., et al. Bypass versus angioplasty in severe ischaemia of the leg (BASIL): multicentre, randomised controlled trial. Lancet 2005, 366:1925-1934.
2. -/-) attenuates ex vivo myocardial ischemia/reperfusion injury through hypoxia-inducible factor-1alpha transcription factor and its target genes in mice. Antioxid. Redox Signal. 2011, 15:1789-1797.
3. Adluri R.S., et al. Thioredoxin 1 enhances neovascularization and reduces ventricular remodeling during chronic myocardial infarction: a study using thioredoxin 1 transgenic mice. J. Mol. Cell. Cardiol. 2011, 50:239-247.
4. Aragones J., et al. Deficiency or inhibition of oxygen sensor Phd1 induces hypoxia tolerance by reprogramming basal metabolism. Nat. Genet. 2008, 40:170-180.
5. Belch J.J., et al. Critical issues in peripheral arterial disease detection and management: a call to action. Arch. Intern. Med. 2003, 163:884-892.
6. Belch J., et al. Effect of fibroblast growth factor NV1FGF on amputation and death: a randomised placebo-controlled trial of gene therapy in critical limb ischaemia. Lancet 2011, 377:1929-1937.
7. Berra E., et al. The hypoxia-inducible-factor hydroxylases bring fresh air into hypoxia signalling. EMBO Rep. 2006, 7:41-45.
8. Bruick R.K., McKnight S.L. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 2001, 294:1337-1340.
9. Cappell K.M., et al. Multiple cancer testis antigens function to support tumor cell mitotic fidelity. Mol. Cell. Biol. 2012, 32:4131-4140.
10. Carmeliet P. Angiogenesis in health and disease. Nat. Med. 2003, 9:653-660.
11. Couffinhal T., et al. Mouse model of angiogenesis. Am. J. Pathol. 1998, 152:1667-1679.
12. Criqui M.H., et al. Mortality over a period of 10years in patients with peripheral arterial disease. N. Engl. J. Med. 1992, 326:381-386.
13. Duca F.A., et al. Replication of obesity and associated signaling pathways through transfer of microbiota from obese-prone rats. Diabetes 2014, 63:1624-1636.
14. Epstein A.C., et al. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 2001, 107:43-54.
15. Ferrara N. Role of vascular endothelial growth factor in physiologic and pathologic angiogenesis: therapeutic implications. Semin. Oncol. 2002, 29:10-14.
16. Ferrara N., et al. The biology of VEGF and its receptors. Nat. Med. 2003, 9:669-676.
17. Folkman J. Tumor angiogenesis: therapeutic implications. N. Engl. J. Med. 1971, 285:1182-1186.
18. Folkman J. Angiogenesis. Biology of Endothelial Cells 1984, 412-428. Martinus-Nijhoff, Boston. E.A. Jaffe (Ed.).
19. Folkman J., Klagsbrun M. Angiogenic factors. Science 1987, 235:442-447.
20. Golomb B.A., et al. Peripheral arterial disease: morbidity and mortality implications. Circulation 2006, 114:688-699.
21. Harari-Steinberg O., et al. Identification of human nephron progenitors capable of generation of kidney structures and functional repair of chronic renal disease. EMBO Mol. Med. 2013, 5:1556-1568.
22. Helisch A., et al. Impact of mouse strain differences in innate hindlimb collateral vasculature. Arterioscler. Thromb. Vasc. Biol. 2006, 26:520-526.
23. Jones W.S., et al. Temporal trends and geographic variation of lower-extremity amputation in patients with peripheral artery disease: results from U.S. Medicare 2000-2008. J. Am. Coll. Cardiol. 2012, 60:2230-2236.
24. Lekas M., et al. Growth factor-induced therapeutic neovascularization for ischaemic vascular disease: time for a re-evaluation?. Curr. Opin. Cardiol. 2006, 21:376-384.
25. Limbourg A., et al. Evaluation of postnatal arteriogenesis and angiogenesis in a mouse model of hind-limb ischemia. Nat. Protoc. 2009, 4:1737-1746.
26. Lunde K., et al. Intracoronary injection of mononuclear bone marrow cells in acute myocardial infarction. N. Engl. J. Med. 2006, 355:1199-1209.
27. Messaoudi S., et al. Cardiac aldosterone overexpression prevents harmful effects of diabetes in the mouse heart by preserving capillary density. FASEB J. 2009, 23:2176-2185.
28. Myllyharju J. Prolyl 4-hydroxylases, key enzymes in the synthesis of collagens and regulation of the response to hypoxia, and their roles as treatment targets. Ann. Med. 2008, 40:402-417.
29. Nagel S., et al. Therapeutic manipulation of the HIF hydroxylases. Antioxid. Redox Signal. 2010, 12:481-501.
30. Nor J.E., et al. Vascular endothelial growth factor (VEGF)-mediated angiogenesis is associated with enhanced endothelial cell survival and induction of Bcl-2 expression. Am. J. Pathol. 1999, 154:375-384.
31. Norgren L., et al. Inter-society consensus for the management of peripheral arterial disease (TASC II). J. Vasc. Surg. 2007, 45(Suppl. S):S5-S67.
32. Oriowo B., et al. Targeted gene deletion of prolyl hydroxylase domain protein 3 triggers angiogenesis and preserves cardiac function by stabilizing hypoxia inducible factor 1 alpha following myocardial infarction. Curr. Pharm. Des. 2014, 20:1305-1310.
33. Ouriel K. Peripheral arterial disease. Lancet 2001, 358:1257-1264.
34. Ratajczak P., et al. Expression and localization of caveolins during postnatal development in rat heart: implication of thyroid hormone. J. Appl. Physiol. 2005, 99:244-251. (1985).
35. Raval Z., Losordo D.W. Cell therapy of peripheral arterial disease: from experimental findings to clinical trials. Circ. Res. 2013, 112:1288-1302.
36. Schachinger V., et al. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N. Engl. J. Med. 2006, 355:1210-1221.
37. Selvaraju V., et al. Molecular mechanisms of action and therapeutic uses of pharmacological inhibitors of HIF-prolyl 4-hydroxylases for treatment of ischemic diseases. Antioxid. Redox Signal. 2014, 20:2631-2665.
38. Semenza G.L. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 2003, 3:721-732.
39. Shizukuda Y., et al. Vascular endothelial growth factor-induced endothelial cell migration and proliferation depend on a nitric oxide-mediated decrease in protein kinase Cdelta activity. Circ. Res. 1999, 85:247-256.
40. Takeda K., et al. Placental but not heart defects are associated with elevated hypoxia-inducible factor alpha levels in mice lacking prolyl hydroxylase domain protein 2. Mol. Cell. Biol. 2006, 26:8336-8346.
41. Thirunavukkarasu M., et al. Simvastatin treatment inhibits hypoxia inducible factor 1-alpha-(HIF-1alpha)-prolyl-4-hydroxylase 3 (PHD-3) and increases angiogenesis after myocardial infarction in streptozotocin-induced diabetic rat. Int. J. Cardiol. 2013, 168:2474-2480.
42. Webber M.J., et al. Supramolecular nanostructures that mimic VEGF as a strategy for ischemic tissue repair. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:13438-13443.
43. Wu S., et al. Enhancement of angiogenesis through stabilization of hypoxia-inducible factor-1 by silencing prolyl hydroxylase domain-2 gene. Mol. Ther. 2008, 16:1227-1234.