Proteasomal inhibition attenuates transcriptional activity of hypoxia-inducible factor 1 (HIF-1) via specific effect on the HIF-1α C-terminal activation domain

Molecular and Cellular Biology

Volumn 26, Issue 15, 2006, Pages 5895-5907

  Kaluz, Stefan ^a,b   Kaluzová, Milota ^a,b   Stanbridge, Eric J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUTE OF VIROLOGY   (Slovakia)

Author keywords

[No Author keywords available]

Indexed keywords

BORTEZOMIB; CARBONATE DEHYDRATASE IX; CYSTEINE; GLUTATHIONE TRANSFERASE; HISTIDINE; HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROTEASOME; PROTEASOME INHIBITOR; PROTEIN P300; STAT2 PROTEIN; UBIQUITIN; VASCULOTROPIN;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CARBOXY TERMINAL ACTIVATION DOMAIN; CARBOXY TERMINAL SEQUENCE; CELL ACTIVITY; CELL LINE; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TARGETING; REGULATORY MECHANISM;

ANIMALS; ANOXIA; BIOLOGICAL MARKERS; BORONIC ACIDS; CARBONIC ANHYDRASES; CELL LINE; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; ISOENZYMES; P300-CBP TRANSCRIPTION FACTORS; PROTEASE INHIBITORS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STRUCTURE, TERTIARY; PYRAZINES; RECOMBINANT FUSION PROTEINS; TRANSCRIPTION, GENETIC; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 33746496671     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00552-06     Document Type: Article

References (63)

1. Adams, J. 2003. The proteasome: structure, function, and role in the cell. Cancer Treat. Rev. 29(Suppl. 1):3-9.
2. Adams, J. 2004. The development of proteasome inhibitors as anticancer drugs. Cancer Cell 5:417-421.
3. Adams, J. 2004. The proteasome: a suitable antineoplastic target. Nat. Rev. Cancer 4:349-360.
4. Arany, Z., L. E. Huang, R. Eckner, S. Bhattacharya, C. Jiang, M. A. Goldberg, H. F. Bunn, and D. M. Livingston. 1996. An essential role for p300/CBP in the cellular response to hypoxia. Proc. Natl. Acad. Sci. USA 93:12969-12973.
5. Bhattacharya, S., R. Eckner, S. Grossman, E. Oldread, Z. Arany, A. D'Andrea, and D. M. Livingston. 1996. Cooperation of Stat2 and p300/CBP in signaling induced by interferon-α. Nature 383:344-347.
6. Bhattacharya, S., C. L. Michels, M. K. Leung, Z. P. Arany, A. L. Kung, and D. M. Livingston. 1999. Functional role of p35srj, a novel p300/CBP binding protein during transactivation by HIF-1. Genes Dev. 13:64-75.
7. Blagosklonny, M. V., W. G. An, L. Y. Romanova, J. Trepel, T. Fojo, and L. Neckers. 1998. p53 inhibits hypoxia-inducible factor-stimulated transcription. J. Biol. Chem. 273:11995-11998.
8. Bruick, R. K., and S. L. McKnight. 2001. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294:1337-1340.
9. Damert, A., E. Ikeda, and W. Risau. 1997. Activator-protein-1 binding potentiates the hypoxia-inducible factor-1-mediated hypoxia-induced transcriptional activation of vascular-endothelial growth factor expression in C6 glioma cells. Biochem. J. 327:419-423.
10. Dames, S. A., M. Martinez-Yamout, R. N. De Guzman, H. J. Dyson, and P. Wright. 2002. Structural basis for Hif·1 alpha/CBP recognition in the cellular hypoxic response. Proc. Natl. Acad. Sci. USA 99:5271-5276.
11. Epstein, A. C., J. M. Gleadle, L. A. McNeil, K. S. Hewitson, J. O'Rourke, D. R. Mole, M. Mukherji, E. Metzen, M. I. Wilson, A. Dhanda, Y. M. Tian, N. Massen, D. L. Hamilton, P. Jaakkola, R. Barstead, J. Hodgkin, P. H. Maxwell, C. W. Pugh, C. J. Schofield, and P. J. Ratcliffe. 2001. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107:43-54.
12. Freedman, S. J., Z. Y. Sun, F. Poy, A. L. Kung, D. M. Livingston, G. Wagner, and M. J. Eck. 2002. Structural basis for recruitment of CBP/p300 by hypoxia-inducible factor-1 alpha. Proc. Natl. Acad. Sci. USA 99:5367-5372.
13. Giaccia, A., B. G. Siim, and R. S. Johnson. 2003. HIF-1 as a target for drug development. Nat. Rev. Drug Discov. 2:803-811.
14. Gradin, K., C. Takasaki, Y. Fujii-Kuriyama, and K. Sogawa. 2002. The transcriptional activation function of the HIF-like factor requires phosphorylation at a conserved threonine. J. Biol. Chem. 277:23508-23514.
15. Gu, J., J. Milligan, and L. E. Huang. 2001. Molecular mechanism of hypoxia-inducible factor 1α-p300 interaction. J. Biol. Chem. 276:3550-3554.
16. Harris, A. L. 2002. Hypoxia-a key regulatory factor in tumour growth. Nat. Rev. Cancer 2:38-46.
17. Haupt, Y., R. Maya, A. Kazaz, and M. Oren. 1997. Mdm2 promotes rapid degradation of p53. Nature 387:296-299.
18. Hershko, A., and A. Ciechanover. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425-479.
19. Hideshima, T., D. Chauhan, P. Richardson, C. Mitsiades, N. Mitsiades, T. Hayashi, N. Munschi, L. Dang, A. Castro, and V. Palombela. 2002. NF-κB as a therapeutic target in multiple myeloma. J. Biol. Chem. 277:16639-16647.
20. 2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. USA 95:7987-7992.
21. Huang, L. E., and H. F. Bunn. 2003. Hypoxia-inducible factor and its biomedical relevance. J. Biol. Chem. 278:19575-19578.
22. Ivan, M., and W. G. Kaelin, Jr. 2001. The von Hippel-Lindau tumor suppressor protein. Curr. Opin. Genet. Dev. 11:27-34.
23. 2 sensing. Science 292:464-468.
24. Ivanov, S., S. Y. Liao, A. Ivanova, A. Danilkovitch-Miagkova, N. Tarasova, G. Weirich, M. J. Merril, M. A. Proescholdt, E. H. Oldfield, J. Lee, J. Zavada, A. Waheed, W. Sly, M. I. Lerman, and E. J. Stanbridge. 2001. Expression of hypoxia-inducible cell-surface transmembrane carbonic anhydrases in human cancer. Am. J. Pathol. 158:905-919.
25. 2-regulated prolyl hydroxylation. Science 292:468-472.
26. Jianii, B. H., J. Z. Zheng, S. W. Leung, R. Roe, and G. L. Semenza. 1997. Transactivation and inhibitory domains of hypoxia-induciblc factor 1 alpha. J. Biol. Chem. 272:19253-19260.
27. Kallio, P. J., W. J. Wilson, S. O'Brien, Y. Makino, and L. Poellinger. 1999. Regulation of the hypoxia-inducible transcription factor 1 alpha by the ubiquitin-proteasome pathway. J. Biol. Chem. 274:6519-6525.
28. Kaluz, S., M. Kaluzová, R. Opavský, S. Pastorekovâ, A. Gibadulinová, F. Dequiedt, R. Kettmann, and J. Pastorek. 1999. Transcriptional regulation of the MN/CA 9 gene coding for the tumor-associated carbonic anhydrase IX. Identification and characterization of a proximal silencer clement. J. Biol. Chem. 274:32588-32595.
29. Kaluz, S., M. Kaluzová, A. Chrastina, P. L. Olive, S. Pasloreková, J. Pastorek, M. I. Lerman, and E. J. Stanbridge. 2002. Lowered oxygen tension induces expression of the hypoxia marker MN/carbonic anhydrase IX in the absence of hypoxia-inducible factor 1α stabilization: a role for phosphatidylinositol 3′-kinase. Cancer Res. 62:4469-4477.
30. Kaluz, S., M. Kaluzová, and E. J. Stanbridge. 2003. Expression of the hypoxia marker carbonic anhydrase IX is critically dependent on SP1 activity. Identification of a novel type of hypoxia-responsive enhancer. Cancer Res. 63:917-922.
31. Kaluzová, M., S. Pasloreková, E. Švaslová, J. Pastorek, E. J. Stanbridge, and S. Kaluz. 2001. Characterization of the MN/CA 9 promoter proximal region-a role for SP and AP1 factors. Biochem. J. 359:669-677.
32. Kaluzová, M., S. Kaluz, M. I. Lerman, and E. J. Stanbridge. 2004. DNA damage is a prerequisite for p53-mediated proteasomal degradation of HIF-1α in hypoxic cells and downregulation of the hypoxia marker carbonic anhydrase IX. Mol. Cell. Biol. 24:5757-5766.
33. Karin, M., Y. Cao, F. R. Greten, and Z. W. Li. 2002. NF-κB in cancer: from innocent bystander to major culprit. Nat. Rev. Cancer 2:301-310.
34. Kisselev, A. F., and A. L. Goldherg. 2001. Proteasome inhibitors: from research tools to drug candidates. Chem. Biol. 8:739-758.
35. Kubbutat, M. H., S. N. Jones, and K. H. Vousden. 1997. Regulation of p53 stability by Mdm2. Nature 387:299-303.
36. Kung, A. L., S. Wang, J. M. Klco, W. G. Kaelin, and D. M. Livingston. 2000. Suppression of tumor growth through disruption of hypoxia-inducible signaling. Nat. Med. 6:1335-1340.
37. Kung, A. L., S. D. Zabludoff, D. S. France, S. J. Freedman, E. A. Tanner, A. Vieira, S. Cornell-Kennon, J. Lee, B. Wang, J. Wang, K. Memmert, H. U. Naegeli, F. Petersen, M. J. Eck, K. W. Bair, A. W. Wood, and D. M. Livingston. 2004. Small molecule blockade of transcriptional coactivation of the hypoxia-inducible pathway. Cancer Cell 6:33-43.
38. Lando, D., D. J. Peet, J. J. Gorman, D. A. Whelan, M. L. Whitelaw, and R. K. Bruick. 2002. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev. 16:1466-1471.
39. Lando, D., D. J. Peet, D. A. Whelan, J. J. Gorman, and M. L. Whitelaw. 2002. Asparagine hydroxylation of the HIF transactivation domain: a hypoxic switch. Science 295:858-861.
40. LeBlanc, R., L. P. Catley, T. Hideshima, S. Lentzsch, C. S. Mitsiades, N. Mitsiades, D. Neuburg, O. Goloubeva, C. S. Pien, J. Adams, D. Gupta, P. G. Richardson, N. C. Munshi, and K. C. Anderson. 2002. Proteasome inhibitor PS-341 inhibits human myeloma cell growth in vivo and prolongs survival in a murine model. Cancer Res. 62:4996-5000.
41. Lipford, J. R., G. T. Smith, Y. Chi, and R. J. Deshaies. 2005. A putative stimulatory role for activator turnover in gene expression. Science 438:113-116.
42. Lonard, D. M., Z. Nawaz, C. L. Smith, and B. W. O'Malley. 2000. The 26S proteasome is required for estrogen receptor-α and coactivator turnover and for efficient estrogen receptor-α transactivation. Mol. Cell 5:939-948.
43. Loncaster, J. A., A. L. Harris, S. E. Davidson, J. P. Logue, R. D. Hunter, C. C. Wykoff, J. Pastorek, P. J. Ratcliffe, I. J. Stratford, and C. M. L. West. 2001. Carbonic anhydrase (CAIX) expression, a potential new intrinsic marker of hypoxia: correlations with tumor oxygen measurements and prognosis in locally advanced carcinoma of the cervix. Cancer Res. 61:6394-6399.
44. Mabjeesh, N. J., D. E. Post, M. T. Willard, B. Kaur, E. G. Van Meir, J. W. Simmons, and H. Zhong. 2002. Geldanamycin induces degradation of hypoxia-inducible factor 1α protein via the proteasome pathway in prostate cancer cells. Cancer Res. 62:2478-2482.
45. Mackay, H., D. Hedley, P. Major, C. Townsley, M. Mackenzie, M. Vincent, P. Degendorfer, M. S. Tsao, T. Nicklee, D. Birle, J. Wright, L. Siu, M. Moore, and A. Oza. 2005. A phase II trial with pharmacodynamic endpoints of the proteasome inhibitor bortezomib in patients with metastatic colorectal cancer. Clin. Cancer Res. 11:5526-5533.
46. Mahon, P. C., K. Hirota, and G. L. Semenza. 2001. FIH-1: a novel protein that interacts with HIF-1alpha and VHL to mediate repression of HIF-1 transcriptional activity. Genes Dev. 15:2675-2686.
47. Maxwell, P. H., M. Wiesener, G.-W. Chang, S. Clifford, E. Vaux, M. Cockman, C. C. Wykoff, C. Pugh, E. Maher, and P. J. Ratcliffe. 1999. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature (London) 399:271-275.
48. Mizukami, Y., J. Li, X. Zhang, M. A. Zimmer, O. Iliopoulos, and D. C. Chung. 2004. Hypoxia-inducible factor-1-independent regulation of vascular endothelial growth factor by hypoxia in colon cancer. Cancer Res. 64:1765-1772.
49. Ohh, M., C. W. Park, M. Ivan, M. A. Hoffman, T. Y. Kim, L. E. Huang, N. Pavletich, V. Chau, and W. G. Kaelin, Jr. 2000. Ubiquitination of hypoxia-inducible factor requires direct binding to the β-domain of the von Hippel-Lindau protein. Nat. Cell Biol. 2:423-427.
50. Olive, P. L., C. Aquino-Parsons, S. H. MacPhail, S.-Y. Liao, J. A. Raleigh, M. I. Lerman, and E. J. Stanbridge. 2001. Carbonic anhydrase 9 as an endogenous marker for hypoxic cells in cervical cancer. Cancer Res. 61:8924-8929.
51. Pal, S., K. P. Claffey, H. T. Cohen, and D. Mukhopadhyay. 1998. Activation of Sp-1 mediated vascular permeability factor/vascular endothelial growth factor transcription requires specific interaction with protein kinase C ξ. J. Biol. Chem. 273:26277-26280.
52. Pugh, C. W., J. F. O'Rourke, M. Nagao, J. M. Gleadle, and P. J. Ratcliffe. 1997. Activation of hypoxia-inducible factor-1; definition of regulatory domains within the alpha subunit. J. Biol. Chem. 272:11205-11214.
53. Ralajová, M., M. Zat'ovičová, R. Kettman, J. Pastorek, and S. Pastoreková. 2004. Induction by hypoxia combined with low glucose or low bicarbonate and high posttranslational stability upon reoxygenation contribute to carbonic anhydrase IX expression in cancer cells. Int. J. Oncol. 24:995-1004.
54. Rocarro, A. M., T. Hideshima, N. Raje, S. Kumar, K. Ishitsuka, H. Yasui, N. Shiraishi, D. Ribatti, B. Nico, A. Vacca, F. Dammacco, P. G. Richardson, and K. C. Anderson. 2006. Bortezomib mediates antiangiogenesis in multiple myeloma via direct and indirect effects on endothelial cells. Cancer Res. 66:184-191.
55. Salceda, S., and J. Caro. 1997. Hypoxia-inducible factor 1α (HIF-1α) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. J. Biol. Chem. 272:22642-22647.
56. Sang, N., D. P. Stiehl, J. Bohensky, I. Leschinsky, V. Srinivas, and J. Caro. 2003. MAPK signaling up-regulates the activity of hypoxia-inducible factors by its effects on p300. J. Biol. Chem. 278:14013-14019.
57. 2 homeostasis by hypoxia-inducible factor 1. Annu. Rev. Cell Dev. Biol. 15:551-578.
58. Semenza, G. L. 2003. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3:721-732.
59. Sowter, H. M., R. R. Raval, J. Moore, P. J. Ratcliffe, and A. Harris. 2003. Predominant role of hypoxia-inducible transcription factor (HIF)-1α versus HIF-2α in regulation of the transcriptional response to hypoxia. Cancer Res. 63:6130-6134.
60. Vo, N., and R. H. Goodman. 2001. CREB-binding protein and p300 in transcriptional regulation. J. Biol. Chem. 276:13505-13508.
61. Wang, D., R. Moriggl, D. Stravopodis, N. Carpino, J.-C. Marine, S. Teglund, J. Feng, and J. N. Ihle. 2000. A small amphipathic α-helical region is required for transcriptional activities and proteasome-dependent turnover of the tyrosine-phosphorylated Stat5. EMBO J. 19:392-399.
62. 2 tension. Proc. Natl. Acad. Sci. USA 92:5510-5514.
63. Wykoff, C. C., N. J. Beasley, P. H. Watson, K. J. Turner, J. Pastorek, A. Sibtain, G. D. Wilson, H. Turley, K. L. Talks, P. H. Maxwell, C. W. Pugh, P. J. Ratcliffe, and A. L. Harris. 2000. Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res. 60:7075-7083.