Hypoxia inducible factor-1α directly regulates nuclear clusterin transcription by interacting with hypoxia response elements in the clusterin promoter

Molecules and Cells

Volumn 37, Issue 2, 2014, Pages 178-186

  Park, Jeongsook ^a   Park, So Yun ^a   Shin, Eunkyung ^a   Lee, Sun Hee ^a   Kim, Yoon Sook ^a   Lee, Dong Hoon ^a   Roh, Gu Seob ^a   Kim, Hyun Joon ^a   Kang, Sang Soo ^a   Cho, Gyeong Jae ^a   Jeong, Bo Young ^a   Kim, Hwajin ^a   Choi, Wan Sung ^a  

^a Gyeongsang National University   (South Korea)

Author keywords

HIF 1 ; Hypoxia response element; Nuclear clusterin; Promoter methylation; Prostate cancer

Indexed keywords

CLUSTERIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; OXYGEN; CLU PROTEIN, HUMAN; COBALT; COBALT CHLORIDE; HIF1A PROTEIN, HUMAN; ISOPROTEIN;

APOPTOSIS; ARTICLE; CANCER CELL; CARCINOGENESIS; CELL DEATH; CHROMATIN IMMUNOPRECIPITATION; DNA RESPONSIVE ELEMENT; GEL MOBILITY SHIFT ASSAY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HYPOXIA; INCUBATION TIME; LNCAP CELL LINE; MALE; POLYMERASE CHAIN REACTION; PROMOTER REGION; PROSTATE CANCER; PROTEIN PROTEIN INTERACTION; CELL HYPOXIA; CELL NUCLEUS; DNA METHYLATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; METABOLISM; PATHOLOGY; PROSTATE TUMOR; TUMOR CELL LINE;

APOPTOSIS; CELL HYPOXIA; CELL LINE, TUMOR; CELL NUCLEUS; CLUSTERIN; COBALT; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; OXYGEN; PROMOTER REGIONS, GENETIC; PROSTATIC NEOPLASMS; PROTEIN ISOFORMS;

EID: 84901397533     PISSN: 10168478     EISSN: 02191032     Source Type: Journal    
DOI: 10.14348/molcells.2014.2349     Document Type: Article

References (45)

1. Andersen, C.L., Schepeler, T., Thorsen, K., Birkenkamp-Demtroder, K., Mansilla, F., Aaltonen, L.A., Laurberg, S., and Orntoft, T.F. (2007). Clusterin expression in normal mucosa and colorectal cancer. Mol. Cell. Proteomics 6, 1039-1048. (Pubitemid 47019405)
2. Bettuzzi, S. (2009). Chapter 1: Introduction. Adv. Cancer Res. 104, 1-8.
3. Bettuzzi, S., Scorcioni, F., Astancolle, S., Davalli, P., Scaltriti, M., and Corti, A. (2002). Clusterin (SGP-2) transient overexpression decreases proliferation rate of SV40-immortalized human prostate epithelial cells by slowing down cell cycle progression. Oncogene 21, 4328-4334. (Pubitemid 34753840)
4. Chen, N., Chen, X., Huang, R., Zeng, H., Gong, J., Meng, W., Lu, Y., Zhao, F., Wang, L., and Zhou, Q. (2009). BCL-xL is a target gene regulated by hypoxia-inducible factor-1{alpha}. J. Biol. Chem. 284, 10004-10012.
5. Cochrane, D.R., Wang, Z., Muramaki, M., Gleave, M.E., and Nelson, C.C. (2007). Differential regulation of clusterin and its isoforms by androgens in prostate cells. J. Biol. Chem. 282, 2278-2287. (Pubitemid 47076744)
6. de Silva, H.V., Harmony, J.A., Stuart, W.D., Gil, C.M., and Robbins, J. (1990). Apolipoprotein J: structure and tissue distribution. Biochemistry 29, 5380-5389. (Pubitemid 20193947)
7. Forsythe, J.A., Jiang, B.H., Iyer, N.V., Agani, F., Leung, S.W., Koos, R.D., and Semenza, G.L. (1996). Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 16, 4604-4613. (Pubitemid 26272112)
8. Gleave, M., and Miyake, H. (2005). Use of antisense oligonucleotides targeting the cytoprotective gene, clusterin, to enhance androgen- and chemo-sensitivity in prostate cancer. World J. Urol. 23, 38-46. (Pubitemid 40430679)
9. Higashimura, Y., Nakajima, Y., Yamaji, R., Harada, N., Shibasaki, F., Nakano, Y., and Inui, H. (2011). Up-regulation of glyceraldehyde-3-phosphate dehydrogenase gene expression by HIF-1 activity depending on Sp1 in hypoxic breast cancer cells. Arch. Biochem. Biophys. 509, 1-8.
10. Holmquist-Mengelbier, L., Fredlund, E., Lofstedt, T., Noguera, R., Navarro, S., Nilsson, H., Pietras, A., Vallon-Christersson, J., Borg, A., Gradin, K., et al. (2006). Recruitment of HIF-1alpha and HIF-2alpha to common target genes is differentially regulated in neuroblastoma: HIF-2alpha promotes an aggressive phenotype. Cancer Cell 10, 413-423. (Pubitemid 44693470)
11. Kase, S., He, S., Sonoda, S., Kitamura, M., Spee, C., Wawrousek, E., Ryan, S.J., Kannan, R., and Hinton, D.R. (2010). alphaB-crystallin regulation of angiogenesis by modulation of VEGF. Blood 115, 3398-3406.
12. Kevans, D., Gorman, S., Tosetto, M., Sheahan, K., O'Donoghue, D., Mulcahy, H., and O'Sullivan, J. (2012). Clusterin and chemotherapy sensitivity under normoxic and graded hypoxic conditions in colorectal cancer. J. Gastrointest. Cancer 43, 305-313.
13. Kim, N., and Choi, W.S. (2011). Proapoptotic role of nuclear clusterin in brain. Anat. Cell Biol. 44, 169-175.
14. Kim, N., Yoo, J.C., Han, J.Y., Hwang, E.M., Kim, Y.S., Jeong, E.Y., Sun, C.H., Yi, G.S., Roh, G.S., Kim, H.J., et al. (2011). Human nuclear clusterin mediates apoptosis by interacting with Bcl-XL through C-terminal coiled coil domain. J. Cell Physiol. 227, 1157-1167.
15. Kim, N., Han, J.Y., Roh, G.S., Kim, H.J., Kang, S.S., Cho, G.J., Park, J.Y., and Choi, W.S. (2012). Nuclear clusterin is associated with neuronal apoptosis in the developing rat brain upon ethanol exposure. Alcohol Clin. Exp. Res. 36, 72-82.
16. Lee, D.H., Ha, J.H., Kim, Y., Bae, K.H., Park, J.Y., Choi, W.S., Yoon, H.S., Park, S.G., Park, B.C., Yi, G.S., et al. (2011). Interaction of a putative BH3 domain of clusterin with anti-apoptotic Bcl-2 family proteins as revealed by NMR spectroscopy. Biochem. Biophys. Res. Commun. 408, 541-547.
17. Leskov, K.S., Klokov, D.Y., Li, J., Kinsella, T.J., and Boothman, D.A. (2003). Synthesis and functional analyses of nuclear clusterin, a cell death protein. J. Biol. Chem. 278, 11590-11600. (Pubitemid 36792721)
18. Liao, F.T., Lee, Y.J., Ko, J.L., Tsai, C.C., Tseng, C.J., and Sheu, G.T. (2009). Hepatitis delta virus epigenetically enhances clusterin expression via histone acetylation in human hepatocellular carcinoma cells. J. Gen. Virol. 90, 1124-1134.
19. Loboda, A., Jozkowicz, A., and Dulak, J. (2010). HIF-1 and HIF-2 transcription factors - similar but not identical. Mol. Cells 29, 435-442.
20. Lund, P., Weisshaupt, K., Mikeska, T., Jammas, D., Chen, X., Kuban, R.J., Ungethum, U., Krapfenbauer, U., Herzel, H.P., Schafer, R., et al. (2006). Oncogenic HRAS suppresses clusterin expression through promoter hypermethylation. Oncogene 25, 4890-4903. (Pubitemid 44201180)
21. Millar, N.L., Reilly, J.H., Kerr, S.C., Campbell, A.L., Little, K.J., Leach, W.J., Rooney, B.P., Murrell, G.A., and McInnes, I.B. (2012). Hypoxia: a critical regulator of early human tendinopathy. Ann. Rheum. Dis. 71, 302-310.
22. Nakamura, E., Abreu-e-Lima, P., Awakura, Y., Inoue, T., Kamoto, T., Ogawa, O., Kotani, H., Manabe, T., Zhang, G.J., Kondo, K., et al. (2006). Clusterin is a secreted marker for a hypoxia-inducible factor-independent function of the von Hippel-Lindau tumor suppressor protein. Am. J. Pathol. 168, 574-584. (Pubitemid 43271155)
23. Otrock, Z.K., Hatoum, H.A., Awada, A.H., Ishak, R.S., and Shamseddine, A.I. (2009). Hypoxia-inducible factor in cancer angiogenesis: structure, regulation and clinical perspectives. Crit. Rev. Oncol. Hematol. 70, 93-102.
24. Park, S.Y., Kim, J.B., and Han, Y.M. (2007). REST is a key regulator in brain-specific homeobox gene expression during neuronal differentiation. J. Neurochem. 103, 2565-2574.
25. 2, a chemical inducer of hypoxia-inducible factor-1, and hypoxia reduce apoptotic cell death in hepatoma cell line HepG2. Ann. N Y Acad. Sci. 973, 443-447.
26. Poulios, E., Trougakos, I.P., and Gonos, E.S. (2006). Comparative effects of hypoxia on normal and immortalized human diploid fibroblasts. Anticancer Res. 26, 2165-2168. (Pubitemid 43989485)
27. Pucci, S., Bonanno, E., Pichiorri, F., Angeloni, C., and Spagnoli, L.G. (2004). Modulation of different clusterin isoforms in human colon tumorigenesis. Oncogene 23, 2298-2304. (Pubitemid 38496784)
28. Rauhala, H.E., Porkka, K.P., Saramaki, O.R., Tammela, T.L., and Visakorpi, T. (2008). Clusterin is epigenetically regulated in prostate cancer. Int. J. Cancer 123, 1601-1609.
29. Rizzi, F., and Bettuzzi, S. (2009). Clusterin (CLU) and prostate cancer. Adv. Cancer Res. 105, 1-19.
30. Rizzi, F., and Bettuzzi, S. (2010). The clusterin paradigm in prostate and breast carcinogenesis. Endocr. Relat. Cancer 17, R1-17.
31. Rizzi, F., Coletta, M., and Bettuzzi, S. (2009). Chapter 2: Clusterin (CLU): From one gene and two transcripts to many proteins. Adv. Cancer Res. 104, 9-23.
32. Rosemblit, N., and Chen, C.L. (1994). Regulators for the rat clusterin gene: DNA methylation and cis-acting regulatory elements. J. Mol. Endocrinol. 13, 69-76. (Pubitemid 24253333)
33. Rosenberg, M.E., and Silkensen, J. (1995). Clusterin: physiologic and pathophysiologic considerations. Int. J. Biochem. Cell Biol. 27, 633-645.
34. Sala, A., Bettuzzi, S., Pucci, S., Chayka, O., Dews, M., and Thomas-Tikhonenko, A. (2009). Regulation of CLU gene expression by oncogenes and epigenetic factors implications for tumorigenesis. Adv. Cancer Res. 105, 115-132.
35. Salnikow, K., Donald, S.P., Bruick, R.K., Zhitkovich, A., Phang, J.M., and Kasprzak, K.S. (2004). Depletion of intracellular ascorbate by the carcinogenic metals nickel and cobalt results in the induction of hypoxic stress. J. Biol. Chem. 279, 40337-40344. (Pubitemid 39287619)
36. Schepeler, T., Mansilla, F., Christensen, L.L., Orntoft, T.F., and Andersen, C.L. (2007). Clusterin expression can be modulated by changes in TCF1-mediated Wnt signaling. J. Mol. Signal. 2, 6.
37. 2 homeostasis. Curr. Opin. Genet. Dev. 8, 588-594.
38. 2, and the 3 PHDs: how animal cells signal hypoxia to the nucleus. Cell 107, 1-3.
39. Serrano, A., Redondo, M., Tellez, T., Castro-Vega, I., Roldan, M.J., Mendez, R., Rueda, A., and Jimenez, E. (2009). Regulation of clusterin expression in human cancer via DNA methylation. Tumour. Biol. 30, 286-291.
40. Shannan, B., Seifert, M., Leskov, K., Willis, J., Boothman, D., Tilgen, W., and Reichrath, J. (2006). Challenge and promise: roles for clusterin in pathogenesis, progression and therapy of cancer. Cell Death Differ. 13, 12-19.
41. Trougakos, I.P., and Gonos, E.S. (2002). Clusterin/apolipoprotein J in human aging and cancer. Int. J. Biochem. Cell Biol. 34, 1430-1448. (Pubitemid 35245400)
42. Trougakos, I.P., So, A., Jansen, B., Gleave, M.E., and Gonos, E.S. (2004). Silencing expression of the clusterin/apolipoprotein j gene in human cancer cells using small interfering RNA induces spontaneous apoptosis, reduced growth ability, and cell sensitization to genotoxic and oxidative stress. Cancer Res. 64, 1834-1842. (Pubitemid 38428709)
43. Wiesener, M.S., Jurgensen, J.S., Rosenberger, C., Scholze, C.K., Horstrup, J.H., Warnecke, C., Mandriota, S., Bechmann, I., Frei, U.A., Pugh, C.W., et al. (2003). Widespread hypoxia-inducible expression of HIF-2alpha in distinct cell populations of different organs. FASEB J. 17, 271-273.
44. Wilson, M.R., and Easterbrook-Smith, S.B. (2000). Clusterin is a secreted mammalian chaperone. Trends Biochem. Sci. 25, 95-98. (Pubitemid 30122416)
45. Yamaji, R., Fujita, K., Takahashi, S., Yoneda, H., Nagao, K., Masuda, W., Naito, M., Tsuruo, T., Miyatake, K., Inui, H., et al. (2003). Hypoxia up-regulates glyceraldehyde-3-phosphate dehydrogenase in mouse brain capillary endothelial cells: involvement of Na+/Ca2+ exchanger. Biochim. Biophys. Acta. 1593, 269-276. (Pubitemid 36173495)