Loss of HIF-1α in endothelial cells disrupts a hypoxia-driven VEGF autocrine loop necessary for tumorigenesis

Cancer Cell

Volumn 6, Issue 5, 2004, Pages 485-495

  Tang, Nan ^a   Wang, Lianchun ^b   Esko, Jeffrey ^b   Giordano, Frank J ^c   Huang, Yan ^c   Gerber, Hans Peter ^d   Ferrara, Napoleone ^d   Johnson, Randall S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; VASCULOTROPIN C; HYPOXIA INDUCIBLE FACTOR 1ALPHA; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ARTICLE; AUTOCRINE EFFECT; BLOOD VESSEL; CARCINOGENESIS; CELL HYPOXIA; CELL PROLIFERATION; CHEMOTAXIS; CONTROLLED STUDY; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; NEOVASCULARIZATION (PATHOLOGY); PRIORITY JOURNAL; PROTEIN EXPRESSION; WOUND HEALING; ANIMAL; CELL CULTURE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE; NEOPLASM; PATHOLOGY; PHYSIOLOGY; VASCULARIZATION;

ANIMALS; CELL HYPOXIA; CELL PROLIFERATION; CELLS, CULTURED; CHEMOTAXIS; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; TRANSCRIPTION FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; WOUND HEALING;

EID: 7944224442     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2004.09.026     Document Type: Article

References (54)

1. Blouw B., Song H., Tihan T., Bosze J., Ferrara N., Gerber H.P., Johnson R.S., Bergers G. The hypoxic response of tumors is dependent on their microenvironment. Cancer Cell. 4:2003;133-146
2. Cattelino A., Liebner S., Gallini R., Zanetti A., Balconi G., Corsi A., Bianco P., Wolburg H., Moore R., Oreda B., et al. The conditional inactivation of the beta-catenin gene in endothelial cells causes a defective vascular pattern and increased vascular fragility. J. Cell Biol. 162:2003;1111-1122
3. Constien R., Forde A., Liliensiek B., Grone H.J., Nawroth P., Hammerling G., Arnold B. Characterization of a novel EGFP reporter mouse to monitor Cre recombination as demonstrated by a Tie2 Cre mouse line. Genesis. 30:2001;36-44
4. Culic O., Gruwel M.L., Schrader J. Energy turnover of vascular endothelial cells. Am. J. Physiol. 273:1997;C205-C213
5. Dong Q.G., Bernasconi S., Lostaglio S., De Calmanovici R.W., Martin-Padura I., Breviario F., Garlanda C., Ramponi S., Mantovani A., Vecchi A. A general strategy for isolation of endothelial cells from murine tissues. Characterization of two endothelial cell lines from the murine lung and subcutaneous sponge implants. Arterioscler. Thromb. Vasc. Biol. 17:1997;1599-1604
6. Ema M., Taya S., Yokotani N., Sogawa K., Matsuda Y., Fujii-Kuriyama Y. A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1alpha regulates the VEGF expression and is potentially involved in lung and vascular development. Proc. Natl. Acad. Sci. USA. 94:1997;4273-4278
7. Ferrara N. Role of vascular endothelial growth factor in physiologic and pathologic angiogenesis. therapeutic implications Semin. Oncol. 29:2002;10-14
8. Ferrara N., Gerber H.P. The role of vascular endothelial growth factor in angiogenesis. Acta Haematol. 106:2001;148-156
9. Ferrara N., Gerber H.P., LeCouter J. The biology of VEGF and its receptors. Nat. Med. 9:2003;669-676
10. Flamme I., Frohlich T., von Reutern M., Kappel A., Damert A., Risau W. HRF, a putative basic helix-loop-helix-PAS-domain transcription factor is closely related to hypoxia-inducible factor-1 alpha and developmentally expressed in blood vessels. Mech. Dev. 63:1997;51-60
11. Folkman J. Tumor angiogenesis. therapeutic implications N. Engl. J. Med. 285:1971;1182-1186
12. Folkman J. Tumor angiogenesis and tissue factor. Nat. Med. 2:1996;167-168
13. Folkman J., Klagsbrun M. Angiogenic factors. Science. 235:1987;442-447
14. Fong G.H., Zhang L., Bryce D.M., Peng J. Increased hemangioblast commitment, not vascular disorganization, is the primary defect in flt-1 knock-out mice. Development. 126:1999;3015-3025
15. Gabhann F.M., Popel A.S. Model of competitive binding of vascular endothelial growth factor and placental growth factor to VEGF receptors on endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 286:2004;H153-H164
16. Gerber H.P., Condorelli F., Park J., Ferrara N. Differential transcriptional regulation of the two vascular endothelial growth factor receptor genes. Flt-1, but not Flk-1/KDR, is up-regulated by hypoxia. J. Biol. Chem. 272:1997;23659-23667
17. Gerber H.P., Hillan K.J., Ryan A.M., Kowalski J., Keller G.A., Rangell L., Wright B.D., Radtke F., Aguet M., Ferrara N. VEGF is required for growth and survival in neonatal mice. Development. 126:1999;1149-1159
18. Gille H., Kowalski J., Li B., LeCouter J., Moffat B., Zioncheck T.F., Pelletier N., Ferrara N. Analysis of biological effects and signaling properties of Flt-1 (VEGFR-1) and KDR (VEGFR-2). A reassessment using novel receptor-specific vascular endothelial growth factor mutants. J. Biol. Chem. 276:2001;3222-3230
19. Griffiths J.R., McSheehy P.M., Robinson S.P., Troy H., Chung Y.L., Leek R.D., Williams K.J., Stratford I.J., Harris A.L., Stubbs M. Metabolic changes detected by in vivo magnetic resonance studies of HEPA-1 wild-type tumors and tumors deficient in hypoxia-inducible factor-1beta (HIF-1beta). evidence of an anabolic role for the HIF-1 pathway Cancer Res. 62:2002;688-695
20. Hanahan D., Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell. 86:1996;353-364
21. Hiratsuka S., Maru Y., Okada A., Seiki M., Noda T., Shibuya M. Involvement of Flt-1 tyrosine kinase (vascular endothelial growth factor receptor-1) in pathological angiogenesis. Cancer Res. 61:2001;1207-1213
22. Hu C.J., Wang L.Y., Chodosh L.A., Keith B., Simon M.C. Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Mol. Cell. Biol. 23:2003;9361-9374
23. Iyer N.V., Kotch L.E., Agani F., Leung S.W., Laughner E., Wenger R.H., Gassmann M., Gearhart J.D., Lawler A.M., Yu A.Y., Semenza G.L. Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev. 12:1998;149-162
24. Jain S., Maltepe E., Lu M.M., Simon C., Bradfield C.A. Expression of ARNT, ARNT2, HIF1 alpha, HIF2 alpha and Ah receptor mRNAs in the developing mouse. Mech. Dev. 73:1998;117-123
25. Jussila L., Alitalo K. Vascular growth factors and lymphangiogenesis. Physiol. Rev. 82:2002;673-700
26. Kisanuki Y.Y., Hammer R.E., Miyazaki J., Williams S.C., Richardson J.A., Yanagisawa M. Tie2-Cre transgenic mice. a new model for endothelial cell-lineage analysis in vivo Dev. Biol. 230:2001;230-242
27. Kroon M.E., Koolwijk P., van der Vecht B., van Hinsbergh V.W. Hypoxia in combination with FGF-2 induces tube formation by human microvascular endothelial cells in a fibrin matrix. involvement of at least two signal transduction pathways J. Cell Sci. 114:2001;825-833
28. Li G., Gustafson-Brown C., Hanks S.K., Nason K., Arbeit J.M., Pogliano K., Wisdom R.M., Johnson R.S. c-Jun is essential for organization of the epidermal leading edge. Dev. Cell. 4:2003;865-877. a
29. Li J., Zhang Y.P., Kirsner R.S. Angiogenesis in wound repair. angiogenic growth factors and the extracellular matrix Microsc. Res. Tech. 60:2003;107-114. b
30. McClain S.A., Simon M., Jones E., Nandi A., Gailit J.O., Tonnesen M.G., Newman D., Clark R.A. Mesenchymal cell activation is the rate-limiting step of granulation tissue induction. Am. J. Pathol. 149:1996;1257-1270
31. Michiels C., Arnould T., Remacle J. Endothelial cell responses to hypoxia. initiation of a cascade of cellular interactions Biochim. Biophys. Acta. 1497:2000;1-10
32. O'Reilly M.S., Boehm T., Shing Y., Fukai N., Vasios G., Lane W.S., Flynn E., Birkhead J.R., Olsen B.R., Folkman J. Endostatin. an endogenous inhibitor of angiogenesis and tumor growth Cell. 88:1997;277-285
33. Park S.K., Dadak A.M., Haase V.H., Fontana L., Giaccia A.J., Johnson R.S. Hypoxia-induced gene expression occurs solely through the action of hypoxia-inducible factor 1alpha (HIF-1alpha). role of cytoplasmic trapping of HIF-2alpha Mol. Cell. Biol. 23:2003;4959-4971
34. Passaniti A., Taylor R.M., Pili R., Guo Y., Long P.V., Haney J.A., Pauly R.R., Grant D.S., Martin G.R. A simple, quantitative method for assessing angiogenesis and antiangiogenic agents using reconstituted basement membrane, heparin, and fibroblast growth factor. Lab. Invest. 67:1992;519-528
35. Phillips P.G., Birnby L.M., Narendran A. Hypoxia induces capillary network formation in cultured bovine pulmonary microvessel endothelial cells. Am. J. Physiol. 268:1995;L789-L800
36. Pugh C.W., Ratcliffe P.J. Regulation of angiogenesis by hypoxia. role of the HIF system Nat. Med. 9:2003;677-684
37. Rabbany S.Y., Heissig B., Hattori K., Rafii S. Molecular pathways regulating mobilization of marrow-derived stem cells for tissue revascularization. Trends Mol. Med. 9:2003;109-117
38. Rafii S., Lyden D., Benezra R., Hattori K., Heissig B. Vascular and haematopoietic stem cells. novel targets for anti-angiogenesis therapy? Nat. Rev. Cancer. 2:2002;826-835
39. Ryan H.E., Lo J., Johnson R.S. HIF-1 alpha is required for solid tumor formation and embryonic vascularization. EMBO J. 17:1998;3005-3015
40. Scortegagna M., Ding K., Oktay Y., Gaur A., Thurmond F., Yan L.J., Marck B.T., Matsumoto A.M., Shelton J.M., Richardson J.A., et al. Multiple organ pathology, metabolic abnormalities and impaired homeostasis of reactive oxygen species in Epas1-/- mice. Nat. Genet. 35:2003;331-340
41. Seagroves T.N., Ryan H.E., Lu H., Wouters B.G., Knapp M., Thibault P., Laderoute K., Johnson R.S. Transcription factor HIF-1 is a necessary mediator of the pasteur effect in mammalian cells. Mol. Cell. Biol. 21:2001;3436-3444
42. Seagroves T.N., Hadsell D., McManaman J., Palmer C., Liao D., McNulty W., Welm B., Wagner K.U., Neville M., Johnson R.S. HIF1alpha is a critical regulator of secretory differentiation and activation, but not vascular expansion, in the mouse mammary gland. Development. 130:2003;1713-1724
43. Semenza G.L. Hypoxia-inducible factor 1. control of oxygen homeostasis in health and disease Pediatr. Res. 49:2001;614-617
44. Semenza G.L. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer. 3:2003;721-732
45. Shalaby F., Rossant J., Yamaguchi T.P., Gertsenstein M., Wu X.F., Breitman M.L., Schuh A.C. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature. 376:1995;62-66
46. Shibuya M. Structure and dual function of vascular endothelial growth factor receptor-1 (Flt-1). Int. J. Biochem. Cell Biol. 33:2001;409-420
47. Singer A.J., Clark R.A. Cutaneous wound healing. N. Engl. J. Med. 341:1999;738-746
48. Sowter H.M., Raval R.R., Moore J.W., Ratcliffe P.J., Harris A.L. Predominant role of hypoxia-inducible transcription factor (Hif)-1alpha versus Hif-2alpha in regulation of the transcriptional response to hypoxia. Cancer Res. 63:2003;6130-6134
49. Ten V.S., Pinsky D.J. Endothelial response to hypoxia. physiologic adaptation and pathologic dysfunction Curr. Opin. Crit. Care. 8:2002;242-250
50. Thomlinson R.H., Gray L.H. The histological structure of some human lung cancers and the possible implications for radiotherapy. Br. J. Cancer. 9:1955;539-549
51. Tian H., McKnight S.L., Russell D.W. Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells. Genes Dev. 11:1997;72-82
52. Tonnesen M.G., Feng X., Clark R.A. Angiogenesis in wound healing. J. Investig. Dermatol. Symp. Proc. 5:2000;40-46
53. Tretyakov A.V., Farber H.W. Endothelial cell tolerance to hypoxia. Potential role of purine nucleotide phosphates. J. Clin. Invest. 95:1995;738-744
54. Waltenberger J., Mayr U., Pentz S., Hombach V. Functional upregulation of the vascular endothelial growth factor receptor KDR by hypoxia. Circulation. 94:1996;1647-1654