Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1

Molecular and Cellular Biology

Volumn 16, Issue 9, 1996, Pages 4604-4613

  Forsythe, Jo A ^a   Jiang, Bing Hua ^b   Iyer, Narayan V ^b   Agani, Faton ^b   Leung, Sandra W ^b   Koos, Robert D ^a   Semenza, Gregg L ^b,c  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c JOHNS HOPKINS HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; ERYTHROPOIETIN; HELIX LOOP HELIX PROTEIN; HYPOXIA INDUCIBLE FACTOR 1; MESSENGER RNA; UNCLASSIFIED DRUG; VASCULOTROPIN;

ARTICLE; BINDING SITE; CELL HYPOXIA; DNA BINDING; DNA FLANKING REGION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; REPORTER GENE; TRANSCRIPTION INITIATION;

SIMIAE; SIMIAN VIRUS; SIMIAN VIRUS 40;

EID: 0029761644     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.16.9.4604     Document Type: Article

References (68)

1. Banai, S., D. Shweiki, A. Pinson, M. Chandra, G. Lazarovici, and E. Keshet. 1994. Upregulation of vascular endothelial growth factor expression induced by myocardial ischemia: implications for coronary angiogenesis. Cardiovasc. Res. 28:1176-1179.
2. Beck, I., S. Ramirez, R. Weinmann, and J. Caro. 1991. Enhancer element at the 3′-flanking region controls transcriptional response to hypoxia in the human erythropoietin gene. J. Biol. Chem. 266:15563-15566.
3. Beck, I., R. Weinmann, and J. Caro. 1993. Characterization of hypoxiaresponsive enhancer in the human erythropoietin gene shows presence of hypoxia-inducible 120-kd nuclear DNA-binding protein in erythropoietinproducing and nonproducing cells. Blood 82:704-711.
4. Burbach, K. M., A. Poland, and C. A. Bradfield. 1992. Cloning of the Ah-receptor cDNA reveals a distinctive ligand-activated transcription factor. Proc. Natl. Acad. Sci. USA 89:8185-8189.
5. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
6. Dolwick, K. M., H. I. Swanson, and C. A. Bradfield. 1993. In vitro analysis of Ah receptor domains involved in ligand-activated transcription. Proc. Natl. Acad. Sci. USA 90:8566-8570.
7. Ebert, B. L., J. D. Firth, and P. J. Ratcliffe. 1995. Hypoxia and mitochondrial inhibitors regulate expression of glucose transporter-1 via distinct cis-acting sequences. J. Biol. Chem. 270:29083-29089.
8. Fandrey, J., and H. F. Bunn. 1993. In vivo and in vitro regulation of erythropoietin mRNA: measurement by competitive polymerase chain reaction. Blood 81:617-623.
9. Ferrara, N., and W. J. Henzel. 1989. Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem. Biophys. Res. Commun. 161:851-858.
10. Ferrara, N., K. Houck, L. Jakman, and D. W. Leung. 1992. Molecular and biological properties of the vascular endothelial growth factor family of proteins. Endocrinol. Rev. 13:18-32.
11. Finkenzeller, G., A. Technau, and D. Marme. 1995. Hypoxia-induced transcription of the vascular endothelial growth factor gene is independent of functional AP-1 transcription factor. Biochem. Biophys. Res. Commun. 208: 432-439.
12. Firth, J. D., B. L. Ebert, C. W. Pugh, and P. J. Ratcliffe. 1994. Oxygen-regulated control elements in the phosphoglycerate kinase 1 and lactate dehydrogenase A genes: similarities with the erythropoietin 3′ enhancer. Proc. Natl. Acad. Sci. USA 91:6496-6500.
13. Firth, J. D., B. L. Ebert, and P. J. Ratcliffe. 1995. Hypoxic regulation of lactate dehydrogenase A: interaction between hypoxia-inducible factor 1 and cAMP response elements. J. Biol. Chem. 270:21021-21027.
14. Folkman, J., and Y. Shing. 1992. Angiogenesis. J. Biol. Chem. 267:10931-10934.
15. Gleadle, J. M., B. L. Ebert, J. D. Firth, and P. J. Ratcliffe. 1995. Regulation of angiogenic growth factor expression by hypoxia, transition metals, and chelating agents. Am. J. Physiol. 268:C1362-C1368.
16. Goldberg, M. A., C. C. Gaut, and H. F. Bunn. 1991. Erythropoietin mRNA levels are governed by both the rate of gene transcription and posttranscriptional events. Blood 77:271-277.
17. Goldberg, M. A., and T. J. Schneider. 1994. Similarities between the oxygen-sensing mechanisms regulating the expression of vascular endothelial growth factor and erythropoietin. J. Biol. Chem. 269:4355-4359.
18. Gospodarowicz, D., J. A. Abraham, and J. Schilling. 1989. Isolation of a vascular endothelial cell mitogen produced by pituitary-derived folliculostellate cells. Proc. Natl. Acad. Sci. USA 86:7311-7315.
19. Hoffman, E. C., H. Reyes, F.-F. Chu, F. Sander, L. H. Conley, B. A. Brooks, and O. Hankinson. 1991. Cloning of a factor required for activity of the Ah (dioxin) receptor. Science 252:954-958.
20. Ikeda, E., M. G. Achen, G. Breier, and W. Risau. 1995. Hypoxia-induced transcriptional activation and increased mRNA stability of vascular endothelial growth factor in C6 glioma cells. J. Biol. Chem. 270:19761-19766.
21. Iyer, N. V., and G. L. Semenza. 1996. Unpublished data.
22. Jelkmann, W. 1992. Erythropoietin: structure, control of production, and function. Physiol. Rev. 72:449-489.
23. Jiang, B.-H., E. Rue, G. L. Wang, R. Roe, and G. L. Semenza. Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. J. Biol. Chem., in press.
24. Klagsbrun, M., and S. Soker. 1993. VEGF/VPF: the angiogenesis factor found? Curr. Biol. 3:699-702.
25. Krantz, S. B. 1991. Erythropoietin. Blood 77:419-434.
26. Ladoux, A., and C. Frelin. 1993. Hypoxia is a strong inducer of vascular endothelial growth factor mRNA expression in the heart. Biochem. Biophys. Res. Commun. 195:1005-1010.
27. Lee, P., B.-H. Jiang, G. L. Semenza, J. Alam, and A. Choi. Unpublished data.
28. Leung, D. W., G. Cachianes, W. J. Kuang, D. V. Goeddel, and N. Ferrara. 1989. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246:1306-1309.
29. Levy, A. P., N. S. Levy, and M. A. Goldberg. 1996. Post-transcriptional regulation of vascular endothelial growth factor by hypoxia. J. Biol. Chem. 271:2746-2753.
30. Levy, A. P., N. S. Levy, J. Loscalzo, A. Calderone, N. Takahashi, K.-T. Yeo, G. Koren, W. S. Colucci, and M. A. Goldberg. 1995. Regulation of vascular endothelial growth factor in cardiac myocytes. Circ. Res. 76:758-766.
31. Levy, A. P., N. S. Levy, S. Wegner, and M. A. Goldberg. 1995. Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia. J. Biol. Chem. 270:13333-13340.
32. Li, H., L. Dong, and J. P. Whitlock, Jr. 1994. Transcriptional activation function of the mouse Ah receptor nuclear translocator. J. Biol. Chem. 269:29098-28105.
33. Liu, Y., S. R. Cox, T. Morita, and S. Kourembanas. 1995. Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells. Circ. Res. 77:638-643.
34. Lowenstein, C., and G. L. Semenza. Unpublished data.
35. Ma, Q., L. Dong, and J. P. Whitlock, Jr. 1995. Transcriptional activation by the mouse Ah receptor: interplay between multiple stimulatory and inhibitory functions. J. Biol. Chem. 270:12697-12703.
36. Madan, A., and P. T. Curtin. 1993. A 24-base-pair sequence 3′ to the human erythropoietin gene contains a hypoxia-responsive transcriptional enhancer. Proc. Natl. Acad. Sci. USA 90:3928-3932.
37. Martin, C., A. Yu, B.-H. Jiang, A. R. Hohimer, L. E. Davis, and G. L. Semenza. Unpublished data.
38. Melillo, G., T. Musso, A. Sica, L. S. Taylor, G. W. Cox, and L. Varesio. 1995. A hypoxia-responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter. J. Exp. Med. 182:1683-1693.
39. Miller, J. W., A. P. Adamis, D. T. Shima, P. A. D'Amore, R. S. Moulton, M. S. O'Reilly, J. Folkman, H. F. Dvorak, L. F. Brown, B. Berse, T.-K. Yeo, and K.-T. Yeo. 1994. Vascular endothelial growth factor/vascular permeability factor is temporally and spatially correlated with ocular angiogenesis in a primate model. Am. J. Pathol. 145:574-584.
40. Minchenko, A., S. Salceda, T. Bauer, and J. Caro. 1994. Hypoxia regulatory elements of the human vascular endothelial growth factor gene. Cell. Mol. Biol. Res. 40:35-39.
41. Nomura, M., S. Yamagishi, S. Harada, Y. Hayashi, T. Yamashima, J. Yamashita, and H. Yamamoto. 1995. Possible participation of autocrine and paracrine vascular endothelial growth factors in hypoxia-induced proliferation of endothelial cells and pericytes. J. Biol. Chem. 270:28316-28324.
42. Pierce, E. A., R. L. Avery, E. D. Foley, L. P. Aiello, and L. E. H. Smith. 1995. Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization. Proc. Natl. Acad. Sci. USA 92:905-909.
43. Plate, K. H., G. Breier, B. Millauer, A. Ullrich, and W. Risau. 1993. Upregulation of vascular endothelial growth factor and its cognate receptors in a rat glioma model of tumor angiogenesis. Cancer Res. 53:5822-5827.
44. Plate, K. H., G. Breier, H. A. Weich, and W. Risau. 1992. Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature (London) 359:845-848.
45. Pugh, C. W., C. C. Tan, R. W. Jones, and P. J. Ratcliffe. 1991. Functional analysis of an oxygen-regulated transcriptional enhancer lying 3′ to the mouse erythropoietin gene. Proc. Natl. Acad. Sci. USA 88:10553-10557.
46. Ratcliffe, P. J. 1994. Molecular biology of erythropoietin. Kidney Int. 44: 887-904.
47. Reisz-Porszasz, S., M. R. Probst, B. N. Fukunaga, and O. Hankinson. 1994. Identification of functional domains of the aryl hydrocarbon receptor nuclear translocator protein (ARNT). Mol. Cell. Biol. 14:6075-6086.
48. Reyes, H., S. Reisz-Porszasz, and O. Hankinson. 1992. Identification of the Ah receptor nuclear translocator protein (Arnt) as a component of the DNA binding form of the Ah receptor. Science 256:1193-1195.
49. Schuster, S. J., E. V. Badiavas, P. Costa-Giomi, R. Weinmann, A. J. Erslev, and J. Caro. 1987. Stimulation of erythropoietin gene transcription during hypoxia and cobalt exposure. Blood 73:13-16.
50. Semenza, G. L., S. Leung, B.-H. Jiang, and A. Giallongo. Unpublished data.
51. Semenza, G. L., M. K. Nejfelt, S. M. Chi, and S. E. Antonarakis. 1991. Hypoxia-inducible nuclear factors bind to an enhancer element located 3′ to the human erythropoietin gene. Proc. Natl. Acad. SCi. USA 88:5680-5684.
52. Semenza, G. L., P. H. Roth, H.-M. Fang, and G. L. Wang. 1994. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J. Biol. Chem. 269:23757-23763.
53. Semenza, G. L., and G. L. Wang. 1992. 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. 12:5447-5454.
54. Shima, D. T., M. Kuroki, U. Deutsch, Y.-S. Ng, A. P. Adamis, and P. A. D'Amore. 1996. The mouse gene for vascular endothelial growth factor: genomic structure, definition of the transcriptional unit, and characterization of transcriptional and post-transcriptional regulatory sequences. J. Biol. Chem. 271:3877-3883.
55. Shweiki, D., A. Itin, D. Soffer, and E. Keshet. 1992. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature (London) 359:843-845.
56. Sogawa, K. R. Nakano, A. Kobayashi, Y. Kikuchi, N. Ohe, N. Matsushita, and Y. Fujii-Kuriyama. 1995. Possible function of Ah receptor nuclear translocator (Arnt) homodimer in transcriptional regulation. Proc. Natl. Acad. Sci. USA 92:1936-1940.
57. Stein, I., M. Neeman, D. Shweiki, A. Itin, and E. Keshet. 1995. Stabilization of vascular endothelial growth factor mRNA by hypoxia and hypoglycemia and coregulation with other ischemia-induced genes. Mol. Cell. Biol. 15: 5363-5368.
58. Swanson, H. I., W. K. Chan, and C. A. Bradfield. 1995. DNA binding specificities and pairing rules of the Ah receptor, ARNT, and SIM proteins. J. Biol. Chem. 270:26292-26302.
59. Tan, C. C., and P. J. Ratclilfe. 1991. Effect of inhibitors of oxidative phosphorylation on erythropoietin mRNA in isolated perfused rat kidneys. Am. J. Physiol. 261:F982-F987.
60. Tischer, E., S. R. Mitchell, T. Hartman, M. Silva, D. Gospodarowicz, J. C. Fiddes, and J. A. Abraham. 1991. The human gene for vascular endothelial growth factor: multiple protein forms are encoded through alternative exon splicing. J. Biol. Chem. 266:11947-11954.
61. 2 tension. Proc. Natl. Acad. Sci. USA 92:5510-5514.
62. Wang, G. L., and G. L. Semenza. 1993. General involvement of hypoxia-inducible factor in transcriptional response to hypoxia. Proc. Natl. Acad. Sci. USA 90:4304-4308.
63. Wang, G. L., and G. L. Semenza. 1993. Characterization of hypoxia-inducible factor 1 and regulation of DNA binding activity by hypoxia. J. Biol. Chem. 268:21513-21518.
64. Wang, G. L., and G. L. Semenza. 1993. Desferrioxamine induces erythropoietin gene expression and hypoxia-inducible factor 1 DNA-binding activity: implications for models of hypoxia signal transduction. Blood 82:3610-3615.
65. Wang, G. L., and G. L. Semenza. 1995. Purification and characterization of hypoxia-inducible factor 1. J. Biol. Chem. 270:1230-1237.
66. Wenger, R. H., A. Rolfs, H. H. Marti, C. Bauer, and M. Gassmann. 1995. Hypoxia, a novel inducer of acute phase gene expression in a human hepatoma cell line. J. Biol. Chem. 270:27865-27870.
67. Whitelaw, M. L., J.-A. Gustafsson, and L. Poellinger. 1994. Identification of transactivation and repression functions of the dioxin receptor and its basic helix-loop-helix/PAS partner factor Arnt: inducible versus constitutive modes of regulation. Mol. Cell. Biol. 14:8343-8355.
68. Wiener, C. M., G. Booth, and G. L. Semenza. Unpublished data.