Hypoxia-Induced Angiogenesis: Good and Evil

Genes and Cancer

Volumn 2, Issue 12, 2011, Pages 1117-1133

  Krock, Bryan L ^a   Skuli, Nicolas ^a,b   Simon, M Celeste ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

angiogenesis; anti angiogenic therapies; cancer; HIFs; hypoxia; vascular diseases

Indexed keywords

HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA;

ANGIOGENESIS; ARTICLE; BLINDNESS; CANCER THERAPY; CORONARY ARTERY ATHEROSCLEROSIS; DISEASE ASSOCIATION; DRUG TARGETING; HUMAN; HYPOXIA; MOLECULAR PATHOLOGY; NONHUMAN; PERIPHERAL OCCLUSIVE ARTERY DISEASE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TUMOR VASCULARIZATION;

EID: 84868612850     PISSN: 19476019     EISSN: 19476027     Source Type: Journal    
DOI: 10.1177/1947601911423654     Document Type: Article

References (190)

1. Semenza GL.Life with oxygen.Science. 2007;318:62-4.
2. Carmeliet P.Angiogenesis in life, disease and medicine.Nature. 2005;438:932-6.
3. Bertout JA,Patel SA,Simon MC.The impact of O2 availability on human cancer.Nat Rev Cancer. 2008;8:967-75.
4. Carreau A,Hafny-Rahbi BE,Matejuk A,Grillon C,Kieda C.Why is the partial oxygen pressure of human tissues a crucial parameter? Small molecules and hypoxia.J Cell Mol Med. 2011;15:1239-53.
5. Parmar K,Mauch P,Vergilio JA,Sackstein R,Down JD.Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia.Proc Natl Acad Sci U S A. 2007;104:5431-6.
6. Braun RD,Lanzen JL,Snyder SA,Dewhirst MW.Comparison of tumor and normal tissue oxygen tension measurements using OxyLite or microelectrodes in rodents.Am J Physiol Heart Circ Physiol. 2001;280:H2533-44.
7. Stockwell RA.Morphometry of cytoplasmic components of mammalian articular chondrocytes and corneal keratocytes: species and zonal variations of mitochondria in relation to nutrition.J Anat. 1991;175:251-61.
8. Keith B,Simon MC.Hypoxia-inducible factors, stem cells, and cancer.Cell. 2007;129:465-72.
9. Semenza GL,Wang GL.A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation.Mol Cell Biol. 1992;12:5447-54.
10. Wang GL,Semenza GL.Characterization of hypoxia-inducible factor 1 and regulation of DNA binding activity by hypoxia.J Biol Chem. 1993;268:21513-8.
11. Wang GL,Jiang BH,Rue EA,Semenza GL.Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension.Proc Natl Acad Sci U S A. 1995;92:5510-4.
12. Kewley RJ,Whitelaw ML,Chapman-Smith A.The mammalian basic helix-loop-helix/PAS family of transcriptional regulators.Int J Biochem Cell Biol. 2004;36:189-204.
13. Jain S,Maltepe E,Lu MM,Simon C,Bradfield CA.Expression of ARNT, ARNT2, HIF1 alpha, HIF2 alpha and Ah receptor mRNAs in the developing mouse.Mech Dev. 1998;73:117-23.
14. Keith B,Adelman DM,Simon MC.Targeted mutation of the murine arylhydrocarbon receptor nuclear translocator 2 (Arnt2) gene reveals partial redundancy with Arnt.Proc Natl Acad Sci U S A. 2001;98:6692-7.
15. Aragones J,Fraisl P,Baes M,Carmeliet P.Oxygen sensors at the crossroad of metabolism.Cell Metab. 2009;9:11-22.
16. Kaelin WG,Ratcliffe PJ.Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway.Mol Cell. 2008;30:393-402.
17. Jiang BH,Zheng JZ,Leung SW,Roe R,Semenza GL.Transactivation and inhibitory domains of hypoxia-inducible factor 1alpha: modulation of transcriptional activity by oxygen tension.J Biol Chem. 1997;272:19253-60.
18. Pugh CW,O'Rourke JF,Nagao M,Gleadle JM,Ratcliffe PJ.Activation of hypoxia-inducible factor-1: definition of regulatory domains within the alpha subunit.J Biol Chem. 1997;272:11205-14.
19. Wenger RH,Stiehl DP,Camenisch G.Integration of oxygen signaling at the consensus HRE.Sci STKE. 2005;2005:.
20. Mahon PC,Hirota K,Semenza GL.FIH-1: a novel protein that interacts with HIF-1alpha and VHL to mediate repression of HIF-1 transcriptional activity.Genes Dev. 2001;15:2675-86.
21. Jeong JW,Bae MK,Ahn MY, et al.Regulation and destabilization of HIF-1alpha by ARD1-mediated acetylation.Cell. 2002;111:709-20.
22. Richard DE,Berra E,Gothie E,Roux D,Pouyssegur J.p42/p44 mitogen-activated protein kinases phosphorylate hypoxia-inducible factor 1alpha (HIF-1alpha) and enhance the transcriptional activity of HIF-1.J Biol Chem. 1999;274:32631-7.
23. Sodhi A,Montaner S,Miyazaki H,Gutkind JS.MAPK and Akt act cooperatively but independently on hypoxia inducible factor-1alpha in rasV12 upregulation of VEGF.Biochem Biophys Res Commun. 2001;287:292-300.
24. Bae SH,Jeong JW,Park JA, et al.Sumoylation increases HIF-1alpha stability and its transcriptional activity.Biochem Biophys Res Commun. 2004;324:394-400.
25. Carbia-Nagashima A,Gerez J,Perez-Castro C, et al.RSUME, a small RWD-containing protein, enhances SUMO conjugation and stabilizes HIF-1alpha during hypoxia.Cell. 2007;131:309-23.
26. Berta MA,Mazure N,Hattab M,Pouyssegur J,Brahimi-Horn MC.SUMOylation of hypoxia-inducible factor-1alpha reduces its transcriptional activity.Biochem Biophys Res Commun. 2007;360:646-52.
27. Sumbayev VV,Budde A,Zhou J,Brune B.HIF-1 alpha protein as a target for S-nitrosation.FEBS Lett. 2003;535:106-12.
28. Cho H,Ahn DR,Park H,Yang EG.Modulation of p300 binding by posttranslational modifications of the C-terminal activation domain of hypoxia-inducible factor-1alpha.FEBS Lett. 2007;581:1542-8.
29. Lim JH,Lee YM,Chun YS,Chen J,Kim JE,Park JW.Sirtuin 1 modulates cellular responses to hypoxia by deacetylating hypoxia-inducible factor 1alpha.Mol Cell. 38:864-78.
30. Dioum EM,Chen R,Alexander MS, et al.Regulation of hypoxia-inducible factor 2alpha signaling by the stress-responsive deacetylase sirtuin 1.Science. 2009;324:1289-93.
31. Minet E,Michel G,Mottet D,Raes M,Michiels C.Transduction pathways involved in hypoxia-inducible factor-1 phosphorylation and activation.Free Radic Biol Med. 2001;31:847-55.
32. Cash TP,Pan Y,Simon MC.Reactive oxygen species and cellular oxygen sensing.Free Radic Biol Med. 2007;43:1219-25.
33. Ghosh G,Subramanian IV,Adhikari N, et al.Hypoxia-induced microRNA-424 expression in human endothelial cells regulates HIF-alpha isoforms and promotes angiogenesis.J Clin Invest. 120:4141-54.
34. Jung F,Palmer LA,Zhou N,Johns RA.Hypoxic regulation of inducible nitric oxide synthase via hypoxia inducible factor-1 in cardiac myocytes.Circ Res. 2000;86:319-25.
35. Iyer NV,Kotch LE,Agani F, et al.Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha.Genes Dev. 1998;12:149-62.
36. Ryan HE,Lo J,Johnson RS.HIF-1 alpha is required for solid tumor formation and embryonic vascularization.EMBO J. 1998;17:3005-15.
37. 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.
38. Carmeliet P,Dor Y,Herbert JM, et al.Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis.Nature. 1998;394:485-90.
39. Fong GH.Mechanisms of adaptive angiogenesis to tissue hypoxia.Angiogenesis. 2008;11:121-40.
40. Dzierzak E,Speck NA.Of lineage and legacy: the development of mammalian hematopoietic stem cells.Nat Immunol. 2008;9:129-36.
41. Lancrin C,Sroczynska P,Stephenson C,Allen T,Kouskoff V,Lacaud G.The haemangioblast generates haematopoietic cells through a haemogenic endothelium stage.Nature. 2009;457:892-5.
42. Adelman DM,Maltepe E,Simon MC.Multilineage embryonic hematopoiesis requires hypoxic ARNT activity.Genes Dev. 1999;13:2478-83.
43. Diez H,Fischer A,Winkler A, et al.Hypoxia-mediated activation of Dll4-Notch-Hey2 signaling in endothelial progenitor cells and adoption of arterial cell fate.Exp Cell Res. 2007;313:1-9.
44. Liu Y,Cox SR,Morita T,Kourembanas S.Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells: identification of a 5′ enhancer.Circ Res. 1995;77:638-43.
45. Levy AP,Levy NS,Wegner S,Goldberg MA.Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia.J Biol Chem. 1995;270:13333-40.
46. Forsythe JA,Jiang BH,Iyer NV, et al.Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1.Mol Cell Biol. 1996;16:4604-13.
47. Compernolle V,Brusselmans K,Acker T, et al.Loss of HIF-2alpha and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice.Nat Med. 2002;8:702-10.
48. Rankin EB,Rha J,Unger TL, et al.Hypoxia-inducible factor-2 regulates vascular tumorigenesis in mice.Oncogene. 2008;27:5354-8.
49. Maltepe E,Schmidt JV,Baunoch D,Bradfield CA,Simon MC.Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT.Nature. 1997;386:403-7.
50. Hu CJ,Iyer S,Sataur A,Covello KL,Chodosh LA,Simon MC.Differential regulation of the transcriptional activities of hypoxia-inducible factor 1 alpha (HIF-1alpha) and HIF-2alpha in stem cells.Mol Cell Biol. 2006;26:3514-26.
51. Peng J,Zhang L,Drysdale L,Fong GH.The transcription factor EPAS-1/hypoxia-inducible factor 2alpha plays an important role in vascular remodeling.Proc Natl Acad Sci U S A. 2000;97:8386-91.
52. 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.
53. Gruber M,Hu CJ,Johnson RS,Brown EJ,Keith B,Simon MC.Acute postnatal ablation of Hif-2alpha results in anemia.Proc Natl Acad Sci U S A. 2007;104:2301-6.
54. Yamashita T,Ohneda K,Nagano M, et al.Hypoxia-inducible transcription factor-2alpha in endothelial cells regulates tumor neovascularization through activation of ephrin A1.J Biol Chem. 2008;283:18926-36.
55. Skuli N,Liu L,Runge A, et al.Endothelial deletion of hypoxia-inducible factor-2alpha (HIF-2alpha) alters vascular function and tumor angiogenesis.Blood. 2009;114:469-77.
56. Tang N,Wang L,Esko J, et al.Loss of HIF-1alpha in endothelial cells disrupts a hypoxia-driven VEGF autocrine loop necessary for tumorigenesis.Cancer Cell. 2004;6:485-95.
57. Yim SH,Shah Y,Tomita S, et al.Disruption of the Arnt gene in endothelial cells causes hepatic vascular defects and partial embryonic lethality in mice.Hepatology. 2006;44:550-60.
58. Ben-Yosef Y,Miller A,Shapiro S,Lahat N.Hypoxia of endothelial cells leads to MMP-2-dependent survival and death.Am J Physiol Cell Physiol. 2005;289:C1321-31.
59. Hellstrom M,Phng LK,Hofmann JJ, et al.Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis.Nature. 2007;445:776-80.
60. Lobov IB,Renard RA,Papadopoulos N, et al.Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting.Proc Natl Acad Sci U S A. 2007;104:3219-24.
61. Suchting S,Freitas C,Le Noble F, et al.The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching.Proc Natl Acad Sci U S A. 2007;104:3225-30.
62. Gustafsson MV,Zheng X,Pereira T, et al.Hypoxia requires notch signaling to maintain the undifferentiated cell state.Dev Cell. 2005;9:617-28.
63. Patel NS,Li JL,Generali D,Poulsom R,Cranston DW,Harris AL.Up-regulation of delta-like 4 ligand in human tumor vasculature and the role of basal expression in endothelial cell function.Cancer Res. 2005;65:8690-7.
64. Folkman J.Angiogenesis in cancer, vascular, rheumatoid and other disease.Nat Med. 1995;1:27-31.
65. Parangi S,O'Reilly M,Christofori G, et al.Antiangiogenic therapy of transgenic mice impairs de novo tumor growth.Proc Natl Acad Sci U S A. 1996;93:2002-7.
66. Gutierrez LS,Suckow M,Lawler J,Ploplis VA,Castellino FJ.Thrombospondin 1-a regulator of adenoma growth and carcinoma progression in the APC(Min/+) mouse model.Carcinogenesis. 2003;24:199-207.
67. Hawighorst T,Velasco P,Streit M, et al.Thrombospondin-2 plays a protective role in multistep carcinogenesis: a novel host anti-tumor defense mechanism.EMBO J. 2001;20:2631-40.
68. Selak MA,Armour SM,MacKenzie ED, et al.Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase.Cancer Cell. 2005;7:77-85.
69. Kikuchi H,Pino MS,Zeng M,Shirasawa S,Chung DC.Oncogenic KRAS and BRAF differentially regulate hypoxia-inducible factor-1alpha and -2alpha in colon cancer.Cancer Res. 2009;69:8499-506.
70. Ravi R,Mookerjee B,Bhujwalla ZM, et al.Regulation of tumor angiogenesis by p53-induced degradation of hypoxia-inducible factor 1alpha.Genes Dev. 2000;14:34-44.
71. Hockel M,Schlenger K,Mitze M,Schaffer U,Vaupel P.Hypoxia and radiation response in human tumors.Semin Radiat Oncol. 1996;6:3-9.
72. Hockel M,Vaupel P.Biological consequences of tumor hypoxia.Semin Oncol. 2001;28:36-41.
73. Vaupel P,Kelleher DK,Hockel M.Oxygen status of malignant tumors: pathogenesis of hypoxia and significance for tumor therapy.Semin Oncol. 2001;28:29-35.
74. Comerford KM,Wallace TJ,Karhausen J,Louis NA,Montalto MC,Colgan SP.Hypoxia-inducible factor-1-dependent regulation of the multidrug resistance (MDR1) gene.Cancer Res. 2002;62:3387-94.
75. Maxwell PH,Dachs GU,Gleadle JM, et al.Hypoxia-inducible factor-1 modulates gene expression in solid tumors and influences both angiogenesis and tumor growth.Proc Natl Acad Sci U S A. 1997;94:8104-9.
76. Oh H,Takagi H,Suzuma K,Otani A,Matsumura M,Honda Y.Hypoxia and vascular endothelial growth factor selectively up-regulate angiopoietin-2 in bovine microvascular endothelial cells.J Biol Chem. 1999;274:15732-9.
77. Zhang L,Yang N,Park JW, et al.Tumor-derived vascular endothelial growth factor up-regulates angiopoietin-2 in host endothelium and destabilizes host vasculature, supporting angiogenesis in ovarian cancer.Cancer Res. 2003;63:3403-12.
78. Gu J,Yamamoto H,Ogawa M, et al.Hypoxia-induced up-regulation of angiopoietin-2 in colorectal cancer.Oncol Rep. 2006;15:779-83.
79. Maisonpierre PC,Suri C,Jones PF, et al.Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis.Science. 1997;277:55-60.
80. Thurston G,Suri C,Smith K, et al.Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1.Science. 1999;286:2511-4.
81. Mazzieri R,Pucci F,Moi D, et al.Targeting the ANG2/TIE2 axis inhibits tumor growth and metastasis by impairing angiogenesis and disabling rebounds of proangiogenic myeloid cells.Cancer Cell. 2011;19:512-26.
82. Suri C,Jones PF,Patan S, et al.Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis.Cell. 1996;87:1171-80.
83. Han ZB,Ren H,Zhao H, et al.Hypoxia-inducible factor (HIF)-1 alpha directly enhances the transcriptional activity of stem cell factor (SCF) in response to hypoxia and epidermal growth factor (EGF).Carcinogenesis. 2008;29:1853-61.
84. Sun L,Hui AM,Su Q, et al.Neuronal and glioma-derived stem cell factor induces angiogenesis within the brain.Cancer Cell. 2006;9:287-300.
85. Matsui J,Wakabayashi T,Asada M,Yoshimatsu K,Okada M.Stem cell factor/c-kit signaling promotes the survival, migration, and capillary tube formation of human umbilical vein endothelial cells.J Biol Chem. 2004;279:18600-7.
86. Litz J,Krystal GW.Imatinib inhibits c- kit-induced hypoxia-inducible factor-1alpha activity and vascular endothelial growth factor expression in small cell lung cancer cells.Mol Cancer Ther. 2006;5:1415-22.
87. Fasanaro P,D'Alessandra Y,Di Stefano V, et al.MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3.J Biol Chem. 2008;283:15878-83.
88. Ceradini DJ,Kulkarni AR,Callaghan MJ, et al.Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1.Nat Med. 2004;10:858-64.
89. Kioi M,Vogel H,Schultz G,Hoffman RM,Harsh GR,Brown JM.Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice.J Clin Invest. 2010;120:694-705.
90. Kawanaka T,Kubo A,Ikushima H,Sano T,Takegawa Y,Nishitani H.Prognostic significance of HIF-2alpha expression on tumor infiltrating macrophages in patients with uterine cervical cancer undergoing radiotherapy.J Med Invest. 2008;55:78-86.
91. Imtiyaz HZ,Williams EP,Hickey MM, et al.Hypoxia-inducible factor 2alpha regulates macrophage function in mouse models of acute and tumor inflammation.J Clin Invest. 2010;120:2699-714.
92. Cramer T,Yamanishi Y,Clausen BE, et al.HIF-1alpha is essential for myeloid cell-mediated inflammation.Cell. 2003;112:645-57.
93. Paez-Ribes M,Allen E,Hudock J, et al.Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis.Cancer Cell. 2009;15:220-31.
94. Ebos JM,Lee CR,Cruz-Munoz W,Bjarnason GA,Christensen JG,Kerbel RS.Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis.Cancer Cell. 2009;15:232-9.
95. Bergers G,Hanahan D.Modes of resistance to anti-angiogenic therapy.Nat Rev Cancer. 2008;8:592-603.
96. Dorrell MI,Aguilar E,Scheppke L,Barnett FH,Friedlander M.Combination angiostatic therapy completely inhibits ocular and tumor angiogenesis.Proc Natl Acad Sci U S A. 2007;104:967-72.
97. Mabjeesh NJ,Escuin D,LaVallee TM, et al.2ME2 inhibits tumor growth and angiogenesis by disrupting microtubules and dysregulating HIF.Cancer Cell. 2003;3:363-75.
98. Ricker JL,Chen Z,Yang XP,Pribluda VS,Swartz GM,Van Waes C.2-methoxyestradiol inhibits hypoxia-inducible factor 1alpha, tumor growth, and angiogenesis and augments paclitaxel efficacy in head and neck squamous cell carcinoma.Clin Cancer Res. 2004;10:8665-73.
99. Kang SH,Cho HT,Devi S, et al.Antitumor effect of 2-methoxyestradiol in a rat orthotopic brain tumor model.Cancer Res. 2006;66:11991-7.
100. Zhang H,Qian DZ,Tan YS, et al.Digoxin and other cardiac glycosides inhibit HIF-1alpha synthesis and block tumor growth.Proc Natl Acad Sci U S A. 2008;105:19579-86.
101. Hede K.Low-dose anthracyclines may block HIF-1 and stop tumor growth.J Natl Cancer Inst. 2009;101:368-70.
102. Yamazaki Y,Hasebe Y,Egawa K,Nose K,Kunimoto S,Ikeda D.Anthracyclines, small-molecule inhibitors of hypoxia-inducible factor-1 alpha activation.Biol Pharm Bull. 2006;29:1999-2003.
103. Lee K,Qian DZ,Rey S,Wei H,Liu JO,Semenza GL.Anthracycline chemotherapy inhibits HIF-1 transcriptional activity and tumor-induced mobilization of circulating angiogenic cells.Proc Natl Acad Sci U S A. 2009;106:2353-8.
104. Kong D,Park EJ,Stephen AG, et al.Echinomycin, a small-molecule inhibitor of hypoxia-inducible factor-1 DNA-binding activity.Cancer Res. 2005;65:9047-55.
105. Lee K,Zhang H,Qian DZ,Rey S,Liu JO,Semenza GL.Acriflavine inhibits HIF-1 dimerization, tumor growth, and vascularization.Proc Natl Acad Sci U S A. 2009;106:17910-5.
106. Shin DH,Chun YS,Lee DS,Huang LE,Park JW.Bortezomib inhibits tumor adaptation to hypoxia by stimulating the FIH-mediated repression of hypoxia-inducible factor-1.Blood. 2008;111:3131-6.
107. Chun YS,Yeo EJ,Choi E, et al.Inhibitory effect of YC-1 on the hypoxic induction of erythropoietin and vascular endothelial growth factor in Hep3B cells.Biochem Pharmacol. 2001;61:947-54.
108. Kim HL,Yeo EJ,Chun YS,Park JW.A domain responsible for HIF-1alpha degradation by YC-1, a novel anticancer agent.Int J Oncol. 2006;29:255-60.
109. Selvin E,Erlinger TP.Prevalence of and risk factors for peripheral arterial disease in the United States: results from the National Health and Nutrition Examination Survey, 1999-2000.Circulation. 2004;110:738-43.
110. Lau JF,Weinberg MD,Olin JW.Peripheral artery disease. Part 1: clinical evaluation and noninvasive diagnosis.Nat Rev Cardiol. 2011;8:405-18.
111. Weinberg MD,Lau JF,Rosenfield K,Olin JW.Peripheral artery disease: Part 2. Medical and endovascular treatment.Nat Rev Cardiol. 2011;8:429-44.
112. Kelly BD,Hackett SF,Hirota K, et al.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.
113. Manalo DJ,Rowan A,Lavoie T, et al.Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1.Blood. 2005;105:659-69.
114. 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.
115. Ho TK,Rajkumar V,Ponticos M, et al.Increased endogenous angiogenic response and hypoxia-inducible factor-1alpha in human critical limb ischemia.J Vasc Surg. 2006;43:125-33.
116. Bosch-Marce M,Okuyama H,Wesley JB, et al.Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia.Circ Res. 2007;101:1310-8.
117. Zeymer U,Parhofer KG,Pittrow D, et al.Risk factor profile, management and prognosis of patients with peripheral arterial disease with or without coronary artery disease: results of the prospective German REACH registry cohort.Clin Res Cardiol. 2009;98:249-56.
118. Isner JM.Cancer and atherosclerosis: the broad mandate of angiogenesis.Circulation. 1999;99:1653-5.
119. Moulton KS,Vakili K,Zurakowski D, et al.Inhibition of plaque neovascularization reduces macrophage accumulation and progression of advanced atherosclerosis.Proc Natl Acad Sci U S A. 2003;100:4736-41.
120. Vink A,Schoneveld AH,Lamers D, et al.HIF-1 alpha expression is associated with an atheromatous inflammatory plaque phenotype and upregulated in activated macrophages.Atherosclerosis. 2007;195:e69-75.
121. Attanasio S,Snell J.Therapeutic angiogenesis in the management of critical limb ischemia: current concepts and review.Cardiol Rev. 2009;17:115-20.
122. Deindl E,Buschmann I,Hoefer IE, et al.Role of ischemia and of hypoxia-inducible genes in arteriogenesis after femoral artery occlusion in the rabbit.Circ Res. 2001;89:779-86.
123. Couffinhal T,Silver M,Zheng LP,Kearney M,Witzenbichler B,Isner JM.Mouse model of angiogenesis.Am J Pathol. 1998;152:1667-79.
124. Niiyama H,Huang NF,Rollins MD,Cooke JP.Murine model of hindlimb ischemia.J Vis Exp. 2009 1035;23:.
125. Mesquita RC,Skuli N,Kim MN, et al.Hemodynamic and metabolic diffuse optical monitoring in a mouse model of hindlimb ischemia.Biomed Opt Express. 2010;1:1173-87.
126. Limbourg A,Korff T,Napp LC,Schaper W,Drexler H,Limbourg FP.Evaluation of postnatal arteriogenesis and angiogenesis in a mouse model of hind-limb ischemia.Nat Protoc. 2009;4:1737-46.
127. Scholz D,Ziegelhoeffer T,Helisch A, et al.Contribution of arteriogenesis and angiogenesis to postocclusive hindlimb perfusion in mice.J Mol Cell Cardiol. 2002;34:775-87.
128. Heil M,Eitenmuller I,Schmitz-Rixen T,Schaper W.Arteriogenesis versus angiogenesis: similarities and differences.J Cell Mol Med. 2006;10:45-55.
129. Sarkar K,Fox-Talbot K,Steenbergen C,Bosch-Marce M,Semenza GL.Adenoviral transfer of HIF-1alpha enhances vascular responses to critical limb ischemia in diabetic mice.Proc Natl Acad Sci U S A. 2009;106:18769-74.
130. Brem H,Tomic-Canic M,Entero H, et al.The synergism of age and db/db genotype impairs wound healing.Exp Gerontol. 2007;42:523-31.
131. 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.
132. Catrina SB,Okamoto K,Pereira T,Brismar K,Poellinger L.Hyperglycemia regulates hypoxia-inducible factor-1alpha protein stability and function.Diabetes. 2004;53:3226-32.
133. Mace KA,Yu DH,Paydar KZ,Boudreau N,Young DM.Sustained expression of Hif-1alpha in the diabetic environment promotes angiogenesis and cutaneous wound repair.Wound Repair Regen. 2007;15:636-45.
134. Liu L,Marti GP,Wei X, et al.Age-dependent 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. 2008;217:319-27.
135. Botusan IR,Sunkari VG,Savu O, et al.Stabilization of HIF-1alpha is critical to improve wound healing in diabetic mice.Proc Natl Acad Sci U S A. 2008;105:19426-31.
136. Asahara T,Takahashi T,Masuda H, et al.VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells.EMBO J. 1999;18:3964-72.
137. Grant MB,May WS,Caballero S, et al.Adult hematopoietic stem cells provide functional hemangioblast activity during retinal neovascularization.Nat Med. 2002;8:607-12.
138. Rehman J,Li J,Orschell CM,March KL.Peripheral blood "endothelial progenitor cells" are derived from monocyte/macrophages and secrete angiogenic growth factors.Circulation. 2003;107:1164-9.
139. Okuyama H,Krishnamachary B,Zhou YF,Nagasawa H,Bosch-Marce M,Semenza GL.Expression of vascular endothelial growth factor receptor 1 in bone marrow-derived mesenchymal cells is dependent on hypoxia-inducible factor 1.J Biol Chem. 2006;281:15554-63.
140. Moeller LC,Cao X,Dumitrescu AM,Seo H,Refetoff S.Thyroid hormone mediated changes in gene expression can be initiated by cytosolic action of the thyroid hormone receptor beta through the phosphatidylinositol 3-kinase pathway.Nucl Recept Signal. 2006;4:e020.
141. Javed MJ,Mead LE,Prater D, et al.Endothelial colony forming cells and mesenchymal stem cells are enriched at different gestational ages in human umbilical cord blood.Pediatr Res. 2008;64:68-73.
142. Bertolini F.Chemotherapy and the tumor microenvironment: the contribution of circulating endothelial cells.Cancer Metastasis Rev. 2008;27:95-101.
143. Martin-Padura I,Bertolini F.Circulating endothelial cells as biomarkers for angiogenesis in tumor progression.Front Biosci (Schol Ed). 2009;1:304-18.
144. Zhang X,Liu L,Wei X, et al.Impaired angiogenesis and mobilization of circulating angiogenic cells in HIF-1alpha heterozygous-null mice after burn wounding.Wound Repair Regen. 2010;18:193-201.
145. Andrikopoulou E,Zhang X,Sebastian R, et al.Current Insights into the role of HIF-1 in cutaneous wound healing.Curr Mol Med. 2011;11:218-35.
146. Schioppa T,Uranchimeg B,Saccani A, et al.Regulation of the chemokine receptor CXCR4 by hypoxia.J Exp Med. 2003;198:1391-402.
147. Chang EI,Loh SA,Ceradini DJ, et al.Age decreases endothelial progenitor cell recruitment through decreases in hypoxia-inducible factor 1alpha stabilization during ischemia.Circulation. 2007;116:2818-29.
148. Aragones J,Schneider M,Van Geyte K, et al.Deficiency or inhibition of oxygen sensor Phd1 induces hypoxia tolerance by reprogramming basal metabolism.Nat Genet. 2008;40:170-80.
149. Schneider M,Van Geyte K,Fraisl P, et al.Loss or silencing of the PHD1 prolyl hydroxylase protects livers of mice against ischemia/reperfusion injury.Gastroenterology. 2010;138:1143 e1-54 2.
150. Huang B,Wu P,Bowker-Kinley MM,Harris RA.Regulation of pyruvate dehydrogenase kinase expression by peroxisome proliferator-activated receptor-alpha ligands, glucocorticoids, and insulin.Diabetes. 2002;51:276-83.
151. Gordan JD,Thompson CB,Simon MC.HIF and c-Myc: sibling rivals for control of cancer cell metabolism and proliferation.Cancer Cell. 2007;12:108-13.
152. Bertout JA,Majmundar AJ,Gordan JD, et al.HIF2alpha inhibition promotes p53 pathway activity, tumor cell death, and radiation responses.Proc Natl Acad Sci U S A. 2009;106:14391-6.
153. Habib GB,Heibig J,Forman SA, et al.Influence of coronary collateral vessels on myocardial infarct size in humans: results of phase I thrombolysis in myocardial infarction (TIMI) trial. The TIMI Investigators.Circulation. 1991;83:739-46.
154. Sabia PJ,Powers ER,Ragosta M,Sarembock IJ,Burwell LR,Kaul S.An association between collateral blood flow and myocardial viability in patients with recent myocardial infarction.N Engl J Med. 1992;327:1825-31.
155. Schultz A,Lavie L,Hochberg I, et al.Interindividual heterogeneity in the hypoxic regulation of VEGF: significance for the development of the coronary artery collateral circulation.Circulation. 1999;100:547-52.
156. Resar JR,Roguin A,Voner J, et al.Hypoxia-inducible factor 1alpha polymorphism and coronary collaterals in patients with ischemic heart disease.Chest. 2005;128:787-91.
157. Hlatky MA,Quertermous T,Boothroyd DB, et al.Polymorphisms in hypoxia inducible factor 1 and the initial clinical presentation of coronary disease. Am Heart J. 2007;154:1035-42.
158. Gnarra JR,Ward JM,Porter FD, et al.Defective placental vasculogenesis causes embryonic lethality in VHL-deficient mice.Proc Natl Acad Sci U S A. 1997;94:9102-7.
159. Elson DA,Thurston G,Huang LE, et al.Induction of hypervascularity without leakage or inflammation in transgenic mice overexpressing hypoxia-inducible factor-1alpha.Genes Dev. 2001;15:2520-32.
160. Kim WY,Safran M,Buckley MR, et al.Failure to prolyl hydroxylate hypoxia-inducible factor alpha phenocopies VHL inactivation in vivo.EMBO J. 2006;25:4650-62.
161. Mazzone M,Dettori D,Leite de,Oliveira R, et al.Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization.Cell. 2009;136:839-51.
162. Grimm C,Wenzel A,Groszer M, et al.HIF-1-induced erythropoietin in the hypoxic retina protects against light-induced retinal degeneration.Nat Med. 2002;8:718-24.
163. Sasaki H,Fukuda S,Otani H, et al.Hypoxic preconditioning triggers myocardial angiogenesis: a novel approach to enhance contractile functional reserve in rat with myocardial infarction.J Mol Cell Cardiol. 2002;34:335-48.
164. Fadini GP,Miorin M,Facco M, et al.Circulating endothelial progenitor cells are reduced in peripheral vascular complications of type 2 diabetes mellitus.J Am Coll Cardiol. 2005;45:1449-57.
165. Rey S,Lee K,Wang CJ, et al.Synergistic effect of HIF-1alpha gene therapy and HIF-1-activated bone marrow-derived angiogenic cells in a mouse model of limb ischemia.Proc Natl Acad Sci U S A. 2009;106:20399-404.
166. Vincent KA,Shyu KG,Luo Y, et al.Angiogenesis is induced in a rabbit model of hindlimb ischemia by naked DNA encoding an HIF-1alpha/VP16 hybrid transcription factor.Circulation. 2000;102:2255-61.
167. Pajusola K,Kunnapuu J,Vuorikoski S, 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.
168. Kajiwara H,Luo Z,Belanger AJ, et al.A hypoxic inducible factor-1 alpha hybrid enhances collateral development and reduces vascular leakage in diabetic rats.J Gene Med. 2009;11:390-400.
169. Rajagopalan S,Olin J,Deitcher S, et al.Use of a constitutively active hypoxia-inducible factor-1alpha transgene as a therapeutic strategy in no-option critical limb ischemia patients: phase I dose-escalation experience.Circulation. 2007;115:1234-43.
170. Li J,Post M,Volk R, et al.PR39, a peptide regulator of angiogenesis.Nat Med. 2000;6:49-55.
171. Wang GL,Semenza GL.Desferrioxamine induces erythropoietin gene expression and hypoxia-inducible factor 1 DNA-binding activity: implications for models of hypoxia signal transduction.Blood. 1993;82:3610-5.
172. Hofbauer KH,Gess B,Lohaus C,Meyer HE,Katschinski D,Kurtz A.Oxygen tension regulates the expression of a group of procollagen hydroxylases.Eur J Biochem. 2003;270:4515-22.
173. Grosfeld A,Stolze IP,Cockman ME, et al.Interaction of hydroxylated collagen IV with the von hippel-lindau tumor suppressor.J Biol Chem. 2007;282:13264-9.
174. Friedman DS,O'Colmain BJ,Munoz B, et al.Prevalence of age-related macular degeneration in the United States.Arch Ophthalmol. 2004;122:564-72.
175. Brown DM,Kaiser PK,Michels M, et al.Ranibizumab versus verteporfin for neovascular age-related macular degeneration.N Engl J Med. 2006;355:1432-44.
176. Lux A,Llacer H,Heussen FM,Joussen AM.Non-responders to bevacizumab (Avastin) therapy of choroidal neovascular lesions.Br J Ophthalmol. 2007;91:1318-22.
177. Inoue Y,Yanagi Y,Matsuura K,Takahashi H,Tamaki Y,Araie M.Expression of hypoxia-inducible factor 1alpha and 2alpha in choroidal neovascular membranes associated with age-related macular degeneration.Br J Ophthalmol. 2007;91:1720-1.
178. Mowat FM,Luhmann UF,Smith AJ, et al.HIF-1alpha and HIF-2alpha are differentially activated in distinct cell populations in retinal ischaemia.PLoS One. 2010;5:e11103.
179. Morita M,Ohneda O,Yamashita T, et al.HLF/HIF-2alpha is a key factor in retinopathy of prematurity in association with erythropoietin.EMBO J. 2003;22:1134-46.
180. Weidemann A,Krohne TU,Aguilar E, et al.Astrocyte hypoxic response is essential for pathological but not developmental angiogenesis of the retina.Glia. 2010;58:1177-85.
181. Yoshida T,Zhang H,Iwase T,Shen J,Semenza GL,Campochiaro PA.Digoxin inhibits retinal ischemia-induced HIF-1alpha expression and ocular neovascularization.FASEB J. 2010;24:1759-67.
182. Sears JE,Hoppe G,Ebrahem Q,Anand-Apte B.Prolyl hydroxylase inhibition during hyperoxia prevents oxygen-induced retinopathy.Proc Natl Acad Sci U S A. 2008;105:19898-903.
183. Casanovas O,Hicklin DJ,Bergers G,Hanahan D.Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors.Cancer Cell. 2005;8:299-309.
184. Stenman JM,Rajagopal J,Carroll TJ,Ishibashi M,McMahon J,McMahon AP.Canonical Wnt signaling regulates organ-specific assembly and differentiation of CNS vasculature.Science. 2008;322:1247-50.
185. Xu Q,Wang Y,Dabdoub A, et al.Vascular development in the retina and inner ear: control by Norrin and Frizzled-4, a high-affinity ligand-receptor pair.Cell. 2004;116:883-95.
186. Phng LK,Potente M,Leslie JD, et al.Nrarp coordinates endothelial Notch and Wnt signaling to control vessel density in angiogenesis.Dev Cell. 2009;16:70-82.
187. Ye X,Wang Y,Cahill H, et al.Norrin, frizzled-4, and Lrp5 signaling in endothelial cells controls a genetic program for retinal vascularization.Cell. 2009;139:285-98.
188. Liebner S,Corada M,Bangsow T, et al.Wnt/ beta-catenin signaling controls development of the blood-brain barrier.J Cell Biol. 2008;183:409-17.
189. Mazumdar J,O'Brien WT,Johnson RS, et al.O2 regulates stem cells through Wnt/beta-catenin signalling.Nat Cell Biol. 12:1007-13.
190. Kaidi A,Williams AC,Paraskeva C.Interaction between beta-catenin and HIF-1 promotes cellular adaptation to hypoxia.Nat Cell Biol. 2007;9:210-7.