Hypoxia-inducible factor-1 mediates activation of cultured vascular endothelial cells by inducing multiple angiogenic factors

Circulation Research

Volumn 93, Issue 7, 2003, Pages 664-673

  Yamakawa, Midori ^a   Liu, Louis X ^a   Date, Taro ^a   Belanger, Adam J ^a   Vincent, Karen A ^a   Akita, Geoffrey Y ^a   Kuriyama, Takayuki ^b   Cheng, Seng H ^a   Gregory, Richard J ^a   Jiang, Canwen ^a  

^a GENZYME CORPORATION   (United States)

^b CHIBA UNIVERSITY   (Japan)

Author keywords

Angiogenesis; Angiopoietins; Hypoxia; Hypoxia inducible factor 1; Vascular endothelial growth factor

Indexed keywords

ADENOVIRUS VECTOR; ANGIOGENIC FACTOR; ANGIOPOIETIN; ANGIOPOIETIN 2; ANGIOPOIETIN 4; DEFEROXAMINE; ETOPOSIDE; HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; UNCLASSIFIED DRUG; VASCULOTROPIN; ANGIOPOIETIN RECEPTOR; CASP3 PROTEIN, HUMAN; CASPASE; CASPASE 3; DNA BINDING PROTEIN; ENDOTHELIAL CELL GROWTH FACTOR; HIF1A PROTEIN, HUMAN; LYMPHOKINE; NUCLEAR PROTEIN; PLACENTA PROTEIN; PLATELET DERIVED GROWTH FACTOR; PRODUCT PLACENTA GROWTH FACTOR; PROTEIN TYROSINE KINASE; SIGNAL PEPTIDE; TRANSCRIPTION FACTOR; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 1;

ANGIOGENESIS; APOPTOSIS; ARTICLE; CELL CULTURE; CELL PROLIFERATION; CONTROLLED STUDY; EDEMA; ENDOTHELIUM CELL; FETUS; HEART MUSCLE CELL; HUMAN; HUMAN CELL; HYPOXIA; INFECTION; INFLAMMATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TRANSGENE; VASCULAR ENDOTHELIUM; BLOOD VESSEL; CELL DIVISION; CELL HYPOXIA; CELL MEMBRANE PERMEABILITY; CELL MOTION; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; GENE VECTOR; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY;

ANGIOGENESIS INDUCING AGENTS; ANGIOPOIETIN-2; ANGIOPOIETINS; APOPTOSIS; BLOOD VESSELS; CASPASE 3; CASPASES; CELL DIVISION; CELL HYPOXIA; CELL MEMBRANE PERMEABILITY; CELL MOVEMENT; CELLS, CULTURED; DEFEROXAMINE; DNA-BINDING PROTEINS; ENDOTHELIAL GROWTH FACTORS; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; GENETIC VECTORS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHOKINES; NUCLEAR PROTEINS; PLATELET-DERIVED GROWTH FACTOR; PREGNANCY PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, TIE-2; RNA, MESSENGER; TRANSCRIPTION FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 0141640863     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000093984.48643.D7     Document Type: Article

References (47)

1. Ferrara N, Alitalo K. Clinical applications of angiogenic growth factors and their inhibitors. Nat Med. 1999;5:1359-1364.
2. Isner JM. Myocardial gene therapy. Nature. 2002;415:234-239.
3. Larcher F, Murillas R, Bolontrade M, Conti CJ, Jorcano JL. VEGF/VPF overexpression in skin of transgenic mice induces angiogenesis, vascular hyperpermeability and accelerated tumor development. Oncogene. 1998;17:303-311.
4. Thurston G, Suri C, Smith K, McClain J, Sato TN, Yancopoulos GD, McDonald DM. Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science. 1999;286:2511-2514.
5. Blau HM, Banfi A. The well-tempered vessel. Nat Med. 2001;7:532-534.
6. Bruick RK, McKnight SL. Building better vasculature. Genes Dev. 2001;15:2497-2502.
7. Folkman J, D'Amore PA. Blood vessel formation: what is its molecular basis? Cell. 1996;87:1153-1155.
8. Risau W. Mechanisms of angiogenesis. Nature. 1997;386:671-674.
9. Wang GL, Semenza GL. Purification and characterization of hypoxia-inducible factor 1. J Biol Chem. 1995;270:1230-1237.
10. 2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol. 1999;15:551-578.
11. 2 sensing. Science. 2001;292:464-468.
12. 2-regulated prolyl hydroxylation. Science. 2001;292:468-472.
13. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ. The tumor suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature. 1999;399:271-275.
14. Epstein AC, Gleadle JM, McNeill LA, Hewitson KS, O'Rourke J, Mole DR, Mukherji M, Metzen E, Wilson MI, Dhanda A, Tian YM, Masson N, Hamilton DL, Jaakkola P, Barstead R, Hodgkin J, Maxwell PH, Pugh CW, Schofield CJ, Ratcliffe PJ. C elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell. 2001;107:43-54.
15. Kaelin WG Jr. How oxygen makes its presence felt. Genes Dev. 2002;16:1441-1445.
16. 2 homeostasis by hypoxia-inducible factor 1α. Genes Dev. 1998;12:149-162.
17. Vincent KA, Shyu K, Luo Y, Magner M, Tio RA, Jiang C, Goldberg MA, Akita GY, Gregory RJ, Isner JM. Angiogenesis is induced in a rabbit model of hindlimb ischemia by naked DNA encoding a HIF-1α/VP16 hybrid transcriptional factor. Circulation. 2000;102:2255-2261.
18. Shyu KG, Wang MT, Wang BW, Chang CC, Leu JG, Kuan P, Chang H. Intramyocardial injection of naked DNA encoding HIF-1α/VP16 hybrid to enhance angiogenesis in an acute myocardial infarction model in the rat. Cardiovasc Res. 2002;54:576-583.
19. Elson DA, Thurston G, Huang LE, Ginzinger DG, McDonald DM, Johnson RS, Arbeit JM. Induction of hypervascularity without leakage or inflammation in transgenic mice overexpressing hypoxia-inducible factor-1α. Genes Dev. 2001;15:2520-2532.
20. Davis S, Yancopoulos GD. The angiopoietins: yin and yang in angiogenesis. Curr Top Microbiol Immunol. 1999;237:173-185.
21. Davis S, Aldrich TH, Jones PF, Acheson A, Compton DL, Jain V, Ryan TE, Bruno J, Radziejewski C, Maisonpierre PC, Yancopoulos GD. Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell. 1996;87:1161-1169.
22. Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S, Sato TN, Yancopoulos GD. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell. 1996;87:1171-1180.
23. Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radziejewski C, Compton D, McClain J, Aldrich TH, Papadopoulos N, Daly TJ, Davis S, Sato TN, Yancopoulos GD. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science. 1997;277:55-60.
24. Holash J, Maisonpierre PC, Compton D, Boland P, Alexander CR, Zagzag D, Yancopoulos GD, Wiegand SJ. Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF. Science. 1999;284:1994-1998.
25. Holash J, Wiegand SJ, Yancopoulos GD. New model of tumor angiogenesis: dynamic balance between vessel regression and growth mediated by angiopoietins and VEGF. Oncogene. 1999;18:5356-5362.
26. Asahara T, Chen D, Takahashi T, Fujikawa K, Kearney M, Magner M, Yancopoulos GD, Isner JM. Tie2 receptor ligands, angiopoietin-1 and angiopoietin-2, modulate VEGF-induced postnatal neovascularization. Circ Res. 1998;83:233-240.
27. Visconti RP, Richardson CD, Sato TN. Orchestration of angiogenesis and arteriovenous contribution by angiopoietins and vascular endothelial growth factor (VEGF). Proc Natl Acad Sci U S A. 2002;99:8219-8224.
28. Valenzuela DM, Griffiths JA, Rojas J, Aldrich TH, Jones PF, Zhou H, McClain J, Copeland NG, Gilbert DJ, Jenkins NA, Huang T, Papadopoulos N, Maisonpierre PC, Davis S, Yancopoulos GD. Angiopoietins 3 and 4: diverging gene counterparts in mice and humans. Proc Natl Acad Sci U S A. 1999;96:1904-1909.
29. Mandriota SJ, Pepper MS. Regulation of angiopoietin-2 mRNA levels in bovine microvascular endothelial cells by cytokines and hypoxia. Circ Res. 1998;83:852-859.
30. Oh H, Takagi H, Suzuma K, Otani A, Matsumura M, Honda Y. Hypoxia and vascular endothelial growth factor selectively upregulated angiopoietin-2 in bovine microvascular endothelial cells. J Biol Chem. 1999;274:15732-15739.
31. Krikun G, Schatz F, Finlay T, Kadner S, Mesia A, Gerrets R, Lockwood CJ. Expression of angiopoietin-2 by human endometrial endothelial cells: regulation by hypoxia and inflammation. Biochem Biophys Res Commun. 2000;275:159-163.
32. Mandriota SJ, Pyke C, Di Sanza C, Quinodoz P, Pittet B, Pepper MS. Hypoxia-inducible angiopoietin-2 expression is mimicked by iodonium compounds and occurs in the rat brain and skin in response to systemic hypoxia and tissue ischemia. Am J Pathol. 2000;156:2077-2089.
33. Willam C, Koehne P, Jurgensen JS, Grafe M, Wagner KD, Bachmann S, Frei U, Eckardt KU. Tie2 receptor expression is stimulated by hypoxia and proinflammatory cytokines in human endothelial cells. Circ Res. 2000;87:370-377.
34. Ray PS, Estrada-Hernandez T, Sasaki H, Zhu L, Maulik N. Early effects of hypoxia/reoxygenation on VEGF, Ang-1, Ang-2 and their receptors in the rat myocardium: implications for myocardial angiogenesis. Mol Cell Biochem. 2000;213:145-153.
35. Yuan HT, Yang SP, Woolf AS. Hypoxia upregulates angiopoietin-2, a Tie-2 ligand, in mouse mesangial cells. Kidney Int. 2000;58:1912-1919.
36. Abdulmalek K, Ashur F, Ezer N, Ye F, Magder S, Hussain SN. Differential expression of Tie-2 receptors and angiopoietins in response to in vivo hypoxia in rats. Am J Physiol Lung Cell Mol Physiol. 2001;281: L582-L590.
37. Jiang C, Lu H, Vincent KA, Shankara S, Belanger AJ, Cheng SH, Akita GY, Kelly RA, Goldberg MA, Gregory RJ. Gene expression profiles in human cardiac cells subjected to hypoxia or expressing a hybrid form of HIF-1α. Physiol Genomics. 2002;8:23-32.
38. Jiang BH, Rue E, Wang GL, Roe R, Semenza GL. Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. J Biol Chem. 1996;271:17771-17778.
39. Lee H, Goetzl EJ, An S. Lysophosphatidic acid and sphingosine 1-phosphate stimulate endothelial cell wound healing. Am J Physiol Cell Physiol. 2000;278:C612-C618.
40. Belanger A, Lu H, Date T, Liu LX, Vincent KA, Akita GY, Cheng SH, Gregory RJ, Jiang C. Hypoxia upregulates expression of peroxisome proliferator-activated receptor γ angiopoietin-related gene (PGAR) in cardiomyocytes: role of hypoxia inducible factor 1α. J Mol Cell Cardiol. 2002;34:765-774.
41. Shyu KG, Manor O, Magner M, Yancopoulos GD, Isner JM. Direct intramuscular injection of plasmid DNA encoding angiopoietin-1 but not angiopoietin-2 augments revascularization in the rabbit ischemic hindlimb. Circulation. 1998;98:2081-2087.
42. Teichert-Kuliszewska K, Maisonpierre PC, Jones N, Campbell AI, Master Z, Bendeck MP, Alitalo K, Dumont DJ, Yancopoulos GD, Stewart DJ. Biological action of angiopoietin-2 in a fibrin matrix model of angiogenesis is associated with activation of Tie2. Cardiovasc Res. 2001;49:659-670.
43. Papapetropoulos A, Garcia-Cardena G, Dengler TJ, Maisonpierre PC, Yancopoulos GD, Sessa WC. Direct actions of angiopoietin-1 on human endothelium: evidence for network stabilization, cell survival, and interaction with other angiogenic growth factors. Lab Invest. 1999;79:213-223.
44. Cao R, Brakenhielm E, Pawliuk R, Wariaro D, Post MJ, Wahlberg E, Leboulch P, Cao Y. Angiogenic synergism, vascular stability and improvement of hind-limb ischemia by a combination of PDGF-BB and FGF-2. Nat Med. 2003;9:604-613.
45. Carmeliet P, Moons L, Luttun A, Vincenti V, Compernolle V, De Mol M, Wu Y, Bono F, Devy L, Beck H, Scholz D, Acker T, DiPalma T, Dewerchin M, Noel A, Stalmans I, Barra A, Blacher S, Vandendriessche T, Ponten A, Eriksson U, Plate KH, Foidart JM, Schaper W, Charnock-Jones DS, Hicklin DJ, Herbert JM, Collen D, Persico MG. Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med. 2001;7:575-583.
46. Luttun A, Tjwa M, Moons L, Wu Y, Angelillo-Scherrer A, Liao F, Nagy JA, Hooper A, Priller J, De Klerck B, Compernolle V, Daci E, Bohlen P, Dewerchin M, Herbert JM, Fava R, Matthys P, Carmeliet G, Collen D, Dvorak HF, Hicklin DJ, Carmeliet P. Revascularization of ischemic tissues by P1GF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis by anti-Flt1. Nat Med. 2002;8:831-840.
47. Pipp F, Heil M, Issbrucker K, Ziegelhoeffer T, Martin S, van den Heuvel J, Weich H, Fernandez B, Golomb G, Carmeliet P, Schaper W, Clauss M. VEGFR-1-selective VEGF homologue P1GF is arteriogenic: evidence for a monocyte-mediated mechanism. Circ Res. 2003;92:378-385.