Hypoxic induction of an HIF-1α-dependent bFGF autocrine loop drives angiogenesis in human endothelial cells

Blood

Volumn 107, Issue 7, 2006, Pages 2705-2712

  Calvani, Maura ^a   Rapisarda, Annamaria ^a   Uranchimeg, Badarch ^a   Shoemaker, Robert H ^a   Melillo, Giovanni ^a,b  

^a SAIC FREDERICK INC   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; MATRIGEL; PLATELET DERIVED GROWTH FACTOR BB; SMALL INTERFERING RNA; SOMATOMEDIN C; TOPOTECAN; VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; ENDOTHELIUM CELL; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HYPOXIA; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 33645504221     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2005-09-3541     Document Type: Article

References (42)

1. Folkman J, D'Amore PA. Blood vessel formation: what is its molecular basis? Cell. 1996;87:1153-1155.
2. Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature. 2000;407:249-257.
3. Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell. 1996;86:353-364.
4. Acker T, Plate KH. Role of hypoxia in tumor angiogenesis-molecular and cellular angiogenic crosstalk. Cell Tissue Res. 2003;314:145-155.
5. Bicknell R, Harris AL. Novel angiogenic signaling pathways and vascular targets. Annu Rev Pharmacol Toxicol. 2004;44:219-238.
6. Folkman J. Fundamental concepts of the angiogenic process. Curr Mol Med. 2003;3:643-651.
7. 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;92:5510-5514.
8. Ivan M, Kondo K, Yang H, et al. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science. 2001;292:464-468.
9. Epstein AC, Gleadle JM, McNeill LA, 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.
10. Zhong H, Chiles K, Feldser D, et al. Modulation of hypoxia-inducible factor 1alpha expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: implications for tumor angiogenesis and therapeutics. Cancer Res. 2000;60:1541-1545.
11. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer. 2003;3:721-732.
12. Zundel W, Schindler C, Haas-Kogan D, et al. Loss of PTEN facilitates HIF-1-mediated gene expression. Genes Dev. 2000;14:391-396.
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;73:117-123.
14. 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.
15. 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;12:3320-3324.
16. Wiesener MS, Jurgensen JS, Rosenberger C, et al. Widespread hypoxia-inducible expression of HIF-2alpha in distinct cell populations of different organs. FASEB J. 2003;17:271-273.
17. 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. 1997;63:51-60.
18. 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 U S A. 1997;94:4273-4278.
19. Wiesener MS, Turley H, Allen WE, et al. Induction of endothelial PAS domain protein-1 by hypoxia: characterization and comparison with hypoxiainducible factor-1alpha. Blood. 1998;92:2260-2268.
20. Rapisarda A, Uranchimeg B, Sordet O, Pommier Y, Shoemaker RH, Melillo G. Topoisomerase I-mediated inhibition of hypoxia-inducible factor 1: mechanism and therapeutic implications. Cancer Res. 2004;64:1475-1482.
21. Kelly BD, Hackett SF, Hirota K, et al. Cell typespecific 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;93:1074-1081.
22. Yamakawa M, Liu LX, Date T, et al. Hypoxia-inducible factor-1 mediates activation of cultured vascular endothelial cells by inducing multiple angiogenic factors. Circ Res. 2003;93:664-673.
23. Zhang SX, Gozal D, Sachleben LR Jr, Rane M, Klein JB, Gozal E. Hypoxia induces an autocrine-paracrine survival pathway via platelet-derived growth factor (PDGF)-B/PDGF-beta receptor/phosphatidylinositol 3-kinase/Akt signaling in RN46A neuronal cells. FASEB J. 2003;17:1709-1711.
24. Raval RR, Lau KW, Tran MG, et al. Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-associated renal cell carcinoma. Mol Cell Biol. 2005;25:5675-5686.
25. Manalo DJ, Rowan A, Lavoie T, et al. Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood. 2005;105:659-669.
26. 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;6:485-495.
27. Scortegagna M, Ding K, Oktay Y, et al. Multiple organ pathology, metabolic abnormalities and impaired homeostasis of reactive oxygen species in Epas1-/- mice. Nat Genet. 2003;35:331-340.
28. 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;97:8386-8391.
29. Park SK, Dadak AM, Haase VH, Fontana L, Giaccia AJ, Johnson RS. 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. 2003;23:4959-4971.
30. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med. 1971;285:1182-1186.
31. Rapisarda A, Uranchimeg B, Scudiero DA, et al. Identification of small molecule inhibitors of hypoxia-inducible factor 1 transcriptional activation pathway. Cancer Res. 2002;62:4316-4324.
32. Rapisarda A, Zalek J, Hollingshead M, et al. Schedule-dependent inhibition of hypoxia-inducible factor-1alpha protein accumulation, angiogenesis, and tumor growth by topotecan in U251-HRE glioblastoma xenografts. Cancer Res. 2004;64:6845-6848.
33. Petrangolini G, Pratesi G, De Cesare M, et al. Antiangiogenic effects of the novel camptothecin ST1481 (gimatecan) in human tumor xenografts. Mol Cancer Res. 2003;1:863-870.
34. Clements MK, Jones CB, Cumming M, Daoud SS. Antiangiogenic potential of camptothecin and topotecan. Cancer Chemother Pharmacol. 1999;44:411-416.
35. Kusaka M, Sudo K, Matsutani E, et al. Cytostatic inhibition of endothelial cell growth by the angiogenesis inhibitor TNP-470 (AGM-1470). Br J Cancer. 1994;69:212-216.
36. Kiaris H, Chatzistamou I, Kalofoutis C, Koutselini H, Piperi C, Kalofoutis A. Tumour-stroma interactions in carcinogenesis: basic aspects and perspectives. Mol Cell Biochem. 2004;261:117-122.
37. Moeller BJ, Cao Y, Li CY, Dewhirst MW. Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell. 2004;5:429-441.
38. Semenza GL. Intratumoral hypoxia, radiation resistance, and HIF-1. Cancer Cell. 2004;5:405-406.
39. Berger AP, Kofler K, Bektic J, et al. Increased growth factor production in a human prostatic stromal cell culture model caused by hypoxia. Prostate. 2003;57:57-65.
40. Li J, Shworak NW, Simons M. Increased responsiveness of hypoxic endothelial cells to FGF2 is mediated by HIF-1alpha-dependent regulation of enzymes involved in synthesis of heparan sulfate FGF2-binding sites. J Cell Sci. 2002;115:1951-1959.
41. Bos R, van Diest PJ, de Jong JS, van der Groep P, van der Valk P, van der Wall E. Hypoxia-inducible factor-1alpha is associated with angiogenesis, and expression of bFGF, PDGF-BB, and EGFR in invasive breast cancer. Histopathology. 2005;46:31-36.
42. Kroon ME, Koolwijk P, van der Vecht B, van Hinsbergh VW. 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. 2001;114:825-833.