HIF-1α and HIF-2α induce angiogenesis and improve muscle energy recovery

European Journal of Clinical Investigation

Volumn 44, Issue 10, 2014, Pages 989-999

  Niemi, Henna ^a   Honkonen, Krista ^a   Korpisalo, Petra ^a   Huusko, Jenni ^a   Kansanen, Emilia ^a   Merentie, Mari ^a   Rissanen, Tuomas T ^a   André, Helder ^b   Pereira, Teresa ^b   Poellinger, Lorenz ^b   Alitalo, Kari ^c   Ylä Herttuala, Seppo ^a,d  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UNIVERSITY OF HELSINKI   (Finland)

^d KUOPIO UNIVERSITY HOSPITAL   (Finland)

Author keywords

Angiogenesis; Gene therapy; HIF 1 ; HIF 2 ; Magnetic resonance spectroscopy; Skeletal muscle energy metabolism; Ultrasound imaging

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA;

ANGIOGENESIS; ANIMAL; C57BL MOUSE; CAPILLARY; CARDIAC MUSCLE; CORONARY BLOOD VESSEL; DRUG EFFECTS; GENE EXPRESSION; GENE THERAPY; GENE TRANSFER; HINDLIMB; ISCHEMIA; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; RABBIT; SKELETAL MUSCLE; VASCULARIZATION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CAPILLARIES; CORONARY VESSELS; GENE EXPRESSION; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; HINDLIMB; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; ISCHEMIA; MICE, INBRED C57BL; MUSCLE, SKELETAL; MYOCARDIUM; NEOVASCULARIZATION, PHYSIOLOGIC; RABBITS;

EID: 84908665955     PISSN: 00142972     EISSN: 13652362     Source Type: Journal    
DOI: 10.1111/eci.12333     Document Type: Article

References (35)

1. Norgren L, Hiatt WR, Dormandy JA, Nehler MR, Harris KA, Fowkes FG. Inter-Society Consensus for the Management of Peripheral Arterial Disease (TASC II). J Vasc Surg 2007;45(Suppl S):S5-67.
2. Grech ED. Pathophysiology and investigation of coronary artery disease. BMJ 2003;326:1027-30.
3. Rissanen TT, Yla-Herttuala S. Current status of cardiovascular gene therapy. Mol Ther 2007;15:1233-47.
4. Yla-Herttuala S, Alitalo K. Gene transfer as a tool to induce therapeutic vascular growth. Nat Med 2003;9:694-701.
5. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003;9:669-76.
6. Rissanen TT, Korpisalo P, Markkanen JE, Liimatainen T, Orden MR, Kholova I et al. Blood flow remodels growing vasculature during vascular endothelial growth factor gene therapy and determines between capillary arterialization and sprouting angiogenesis. Circulation 2005;112:3937-46.
7. Rissanen TT, Korpisalo P, Karvinen H, Liimatainen T, Laidinen S, Grohn OH et al. High-resolution ultrasound perfusion imaging of therapeutic angiogenesis. JACC Cardiovasc Imaging 2008;1:83-91.
8. 2 tension. Proc Natl Acad Sci U S A 1995;92:5510-4.
9. Lendahl U, Lee KL, Yang H, Poellinger L. Generating specificity and diversity in the transcriptional response to hypoxia. Nat Rev Genet 2009;10:821-32.
10. Jaakkola P, Mole DR, Tian YM, Wilson MI, Gielbert J, Gaskell SJ et al. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 2001;292:468-72.
11. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999;399:271-5.
12. Hirota K, Semenza GL. Regulation of angiogenesis by hypoxia-inducible factor 1. Crit Rev Oncol Hematol 2006;59:15-26.
13. 2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev 1998;12:149-62.
14. Patel TH, Kimura H, Weiss CR, Semenza GL, Hofmann LV. Constitutively active HIF-1alpha improves perfusion and arterial remodeling in an endovascular model of limb ischemia. Cardiovasc Res 2005;68:144-54.
15. Tian H, McKnight SL, Russell DW. Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells. Genes Dev 1997;11:72-82.
16. Wiesener MS, Turley H, Allen WE, Willam C, Eckardt KU, Talks KL et al. Induction of endothelial PAS domain protein-1 by hypoxia: characterization and comparison with hypoxia-inducible factor-1alpha. Blood 1998;92:2260-8.
17. Tian H, Hammer RE, Matsumoto AM, Russell DW, McKnight SL. The hypoxia-responsive transcription factor EPAS1 is essential for catecholamine homeostasis and protection against heart failure during embryonic development. Genes Dev 1998;12:3320-4.
18. Scortegagna M, Ding K, Oktay Y, Gaur A, Thurmond F, Yan LJ et al. Multiple organ pathology, metabolic abnormalities and impaired homeostasis of reactive oxygen species in Epas1-/- mice. Nat Genet 2003;35:331-40.
19. Takeda N, Maemura K, Imai Y, Harada T, Kawanami D, Nojiri T et al. Endothelial PAS domain protein 1 gene promotes angiogenesis through the transactivation of both vascular endothelial growth factor and its receptor, Flt-1. Circ Res 2004;95:146-53.
20. Makinen K, Manninen H, Hedman M, Matsi P, Mussalo H, Alhava E et al. Increased vascularity detected by digital subtraction angiography after VEGF gene transfer to human lower limb artery: a randomized, placebo-controlled. Double-Blinded Phase II Study. Mol Ther 2002;6:127-33.
21. Hedman M, Hartikainen J, Syvanne M, Stjernvall J, Hedman A, Kivela A et al. 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 2003;107:2677-83.
22. Korpisalo P, Karvinen H, Rissanen TT, Kilpijoki J, Marjomaki V, Baluk P et al. Vascular endothelial growth factor-A and platelet-derived growth factor-B combination gene therapy prolongs angiogenic effects via recruitment of interstitial mononuclear cells and paracrine effects rather than improved pericyte coverage of angiogenic vessels. Circ Res 2008;103:1092-9.
23. Huusko J, Merentie M, Dijkstra MH, Ryhanen MM, Karvinen H, Rissanen TT et al. The effects of VEGF-R1 and VEGF-R2 ligands on angiogenic responses and left ventricular function in mice. Cardiovasc Res 2010;86:122-30.
24. Rissanen TT, Markkanen JE, Arve K, Rutanen J, Kettunen MI, Vajanto I et al. Fibroblast growth factor 4 induces vascular permeability, angiogenesis and arteriogenesis in a rabbit hindlimb ischemia model. FASEB J 2003;17:100-2.
25. Korpisalo P, Rissanen TT, Bengtsson T, Liimatainen T, Laidinen S, Karvinen H et al. Therapeutic angiogenesis with placental growth factor improves exercise tolerance of ischaemic rabbit hindlimbs. Cardiovasc Res 2008;80:263-70.
26. Holscher M, Silter M, Krull S, von AM, Hesse A, Schwartz P et al. Cardiomyocyte-specific prolyl-4-hydroxylase domain 2 knock out protects from acute myocardial ischemic injury. J Biol Chem 2011;286:11185-94.
27. Hyvarinen J, Hassinen IE, Sormunen R, Maki JM, Kivirikko KI, Koivunen P et al. Hearts of hypoxia-inducible factor prolyl 4-hydroxylase-2 hypomorphic mice show protection against acute ischemia-reperfusion injury. J Biol Chem 2010;285:13646-57.
28. Pajusola K, Kunnapuu J, Vuorikoski S, Soronen J, Andre H, Pereira T et al. Stabilized HIF-1alpha is superior to VEGF for angiogenesis in skeletal muscle via adeno-associated virus gene transfer. FASEB J 2005;19:1365-7.
29. Skuli N, Majmundar AJ, Krock BL, Mesquita RC, Mathew LK, Quinn ZL et al. Endothelial HIF-2alpha regulates murine pathological angiogenesis and revascularization processes. J Clin Invest 2012;122:1427-43.
30. Koh MY, Lemos R Jr, Liu X, Powis G. The hypoxia-associated factor switches cells from HIF-1alpha- to HIF-2alpha-dependent signaling promoting stem cell characteristics, aggressive tumor growth and invasion. Cancer Res 2011;71:4015-27.
31. Holmquist-Mengelbier L, Fredlund E, Lofstedt T, Noguera R, Navarro S, Nilsson H et al. Recruitment of HIF-1alpha and HIF-2alpha to common target genes is differentially regulated in neuroblastoma: HIF-2alpha promotes an aggressive phenotype. Cancer Cell 2006;10:413-23.
32. Kim JW, Tchernyshyov I, Semenza GL, Dang CV. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 2006;3:177-85.
33. Papandreou I, Cairns RA, Fontana L, Lim AL, Denko NC. HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab 2006;3:187-97.
34. Westerblad H, Bruton JD, Katz A. Skeletal muscle: energy metabolism, fiber types, fatigue and adaptability. Exp Cell Res 2010;316:3093-9.
35. Greiner A, Esterhammer R, Messner H, Biebl M, Muhlthaler H, Fraedrich G et al. High-energy phosphate metabolism during incremental calf exercise in patients with unilaterally symptomatic peripheral arterial disease measured by phosphor 31 magnetic resonance spectroscopy. J Vasc Surg 2006;43:978-86.