EAF2 suppresses hypoxia-induced factor 1α transcriptional activity by disrupting its interaction with coactivator CBP/p300

Molecular and Cellular Biology

Volumn 34, Issue 6, 2014, Pages 1085-1099

  Chen, Zhu ^a   Liu, Xing ^a   Mei, Zhichao ^a   Wang, Zhou ^b   Xiao, Wuhan ^a  

^a INSTITUTE OF HYDROBIOLOGY   (China)

^b UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANOXIA; CELL DEATH; CELL LINE; CELL LINE, TUMOR; GLUCOSE; HEK293 CELLS; HEP G2 CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; P300-CBP TRANSCRIPTION FACTORS; PROMOTER REGIONS, GENETIC; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 84894284981     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00718-13     Document Type: Article

References (64)

1. Semenza GL. 2012. Hypoxia-inducible factors in physiology and medicine. Cell 148:399-408. http://dx.doi.org/10.1016/j.cell.2012.01.021.
2. Semenza GL. 2003. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3:721-732. http://dx.doi.org/10.1038/nrc1187.
3. Semenza GL. 2012. Molecular mechanisms mediating metastasis of hypoxic breast cancer cells. Trends Mol. Med. 18:534-543. http://dx.doi.org/10.1016/j.molmed.2012.08.001.
4. Greer SN, Metcalf JL, Wang Y, Ohh M. 2012. The updated biology of hypoxia-inducible factor. EMBO J. 31:2448-2460. http://dx.doi.org/10.1038/emboj.2012.125.
5. Majmundar AJ, Wong WJ, Simon MC. 2010. Hypoxia-inducible factors and the response to hypoxic stress. Mol. Cell 40:294-309. http://dx.doi.org/10.1016/j.molcel.2010.09.022.
6. Semenza GL. 2001. HIF-1, O(2), and the 3 PHDs: how animal cells signal hypoxia to the nucleus. Cell 107:1-3. http://dx.doi.org/10.1016/S0092-8674(01)00518-9.
7. Huang X, Ding L, Bennewith KL, Tong RT, Welford SM, Ang KK, Story M, Le QT, Giaccia AJ. 2009. Hypoxia-inducible mir-210 regulates normoxic gene expression involved in tumor initiation. Mol. Cell 35:856-867. http://dx.doi.org/10.1016/j.molcel.2009.09.006.
8. Tsai YP, Wu KJ. 2012. Hypoxia-regulated target genes implicated in tumor metastasis. J. Biomed. Sci. 19:102. http://dx.doi.org/10.1186/1423-0127-19-102.
9. Simone F, Luo RT, Polak PE, Kaberlein JJ, Thirman MJ. 2003. ELLassociated factor 2 (EAF2), a functional homolog of EAF1 with alternative ELL binding properties. Blood 101:2355-2362. http://dx.doi.org/10.1182/blood-2002-06-1664.
10. Xiao W, Zhang Q, Jiang F, Pins M, Kozlowski JM, Wang Z. 2003. Suppression of prostate tumor growth by U19, a novel testosteroneregulated apoptosis inducer. Cancer Res. 63:4698-4704. http://cancerres.aacrjournals.org/content/63/15/4698.long.
11. Xiao W, Zhang Q, Habermacher G, Yang X, Zhang AY, Cai X, Hahn J, Liu J, Pins M, Doglio L, Dhir R, Gingrich J, Wang Z. 2008. U19/Eaf2 knockout causes lung adenocarcinoma, B-cell lymphoma, hepatocellular carcinoma and prostatic intraepithelial neoplasia. Oncogene 27:1536-1544. http://dx.doi.org/10.1038/sj.onc.1210786.
12. Xiao W, Ai J, Habermacher G, Volpert O, Yang X, Zhang AY, Hahn J, Cai X, Wang Z. 2009. U19/Eaf2 binds to and stabilizes von Hippel-Lindau protein. Cancer Res. 69:2599-2606. http://dx.doi.org/10.1158/0008-5472.CAN-08-2595.
13. Liu JX, Zhang D, Xie X, Ouyang G, Liu X, Sun Y, Xiao W. 2013. Eaf1 and Eaf2 negatively regulate canonical Wnt/beta-catenin signaling. Development 140:1067-1078. http://dx.doi.org/10.1242/dev.086157.
14. Zhou J, Feng X, Ban B, Liu J, Wang Z, Xiao W. 2009. Elongation factor ELL (eleven-nineteen lysine-rich leukemia) acts as a transcription factor for direct thrombospondin-1 regulation. J. Biol. Chem. 284:19142-19152. http://dx.doi.org/10.1074/jbc.M109.010439.
15. Luo W, Hu H, Chang R, Zhong J, Knabel M, O'Meally R, Cole RN, Pandey A, Semenza GL. 2011. Pyruvate kinase M2 is a PHD3-stimulated coactivator for hypoxia-inducible factor 1. Cell 145:732-744. http://dx.doi.org/10.1016/j.cell.2011.03.054.
16. Xie XW, Liu JX, Hu B, Xiao W. 2011. Zebrafish foxo3b negatively regulates canonical Wnt signaling to affect early embryogenesis. PLoS One 6:e24469. http://dx.doi.org/10.1371/journal.pone.0024469.
17. Pawlus MR, Wang L, Ware K, Hu CJ. 2012. Upstream stimulatory factor 2 and hypoxia-inducible factor 2alpha (HIF2alpha) cooperatively activate HIF2 target genes during hypoxia. Mol. Cell. Biol. 32:4595-4610. http://dx.doi.org/10.1128/MCB.00724-12.
18. Feng X, Liu X, Zhang W, Xiao W. 2011. p53 directly suppresses BNIP3 expression to protect against hypoxia-induced cell death. EMBO J. 30:3397-3415. http://dx.doi.org/10.1038/emboj.2011.248.
19. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ. 1999. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399:271-275. http://dx.doi.org/10.1038/20459.
20. Khan MN, Bhattacharyya T, Andrikopoulos P, Esteban MA, Barod R, Connor T, Ashcroft M, Maxwell PH, Kiriakidis S. 2011. Factor inhibiting HIF (FIH-1) promotes renal cancer cell survival by protecting cells from HIF-1alpha-mediated apoptosis. Br. J. Cancer 104:1151-1159. http://dx.doi.org/10.1038/bjc.2011.73.
21. Ivan M, Kondo K, Yang H, Kim W, Valiando J, Ohh M, Salic A, Asara JM, Lane WS, Kaelin WG, Jr. 2001. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292:464-468. http://dx.doi.org/10.1126/science.1059817.
22. Dioum EM, Chen R, Alexander MS, Zhang Q, Hogg RT, Gerard RD, Garcia JA. 2009. Regulation of hypoxia-inducible factor 2alpha signaling by the stress-responsive deacetylase sirtuin 1. Science 324:1289-1293. http://dx.doi.org/10.1126/science.1169956.
23. Wang GL, Semenza GL. 1993. General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc. Natl. Acad. Sci. U. S. A. 90:4304-4308. http://dx.doi.org/10.1073/pnas.90.9.4304.
24. Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, Semenza GL. 1996. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 16:4604-4613.
25. Bruick RK. 2000. Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia. Proc. Natl. Acad. Sci. U. S. A. 97:9082-9087. http://dx.doi.org/10.1073/pnas.97.16.9082.
26. Mahon PC, Hirota K, Semenza GL. 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. http://dx.doi.org/10.1101/gad.924501.
27. Sowter HM, Ratcliffe PJ, Watson P, Greenberg AH, Harris AL. 2001. HIF-1-dependent regulation of hypoxic induction of the cell death factors BNIP3 and NIX in human tumors. Cancer Res. 61:6669-6673. http://cancerres.aacrjournals.org/content/61/18/6669.full.
28. Kallio PJ, Okamoto K, O'Brien S, Carrero P, Makino Y, Tanaka H, Poellinger L. 1998. Signal transduction in hypoxic cells: inducible nuclear translocation and recruitment of the CBP/p300 coactivator by the hypoxia-inducible factor-1alpha. EMBO J. 17:6573-6586. http://dx.doi.org/10.1093/emboj/17.22.6573.
29. Lim JH, Lee YM, Chun YS, Chen J, Kim JE, Park JW. 2010. Sirtuin 1 modulates cellular responses to hypoxia by deacetylating hypoxiainducible factor 1alpha. Mol. Cell 38:864-878. http://dx.doi.org/10.1016/j.molcel.2010.05.023.
30. Huang Y, Lei L, Liu D, Jovin I, Russell R, Johnson RS, Di Lorenzo A, Giordano FJ. 2012. Normal glucose uptake in the brain and heart requires an endothelial cell-specific HIF-1alpha-dependent function. Proc. Natl. Acad. Sci. U. S. A. 109:17478-17483. http://dx.doi.org/10.1073/pnas.1209281109.
31. Chaika NV, Gebregiworgis T, Lewallen ME, Purohit V, Radhakrishnan P, Liu X, Zhang B, Mehla K, Brown RB, Caffrey T, Yu F, Johnson KR, Powers R, Hollingsworth MA, Singh PK. 2012. MUC1 mucin stabilizes and activates hypoxia-inducible factor 1 alpha to regulate metabolism in pancreatic cancer. Proc. Natl. Acad. Sci. U. S. A. 109:13787-13792. http://dx.doi.org/10.1073/pnas.1203339109.
32. Semenza GL. 2011. Regulation of metabolism by hypoxia-inducible factor 1. Cold Spring Harbor Symp. Quant. Biol. 76:347-353. http://dx.doi.org/10.1101/sqb.2011.76.010678.
33. Finley LW, Carracedo A, Lee J, Souza A, Egia A, Zhang J, Teruya-Feldstein J, Moreira PI, Cardoso SM, Clish CB, Pandolfi PP, Haigis MC. 2011. SIRT3 opposes reprogramming of cancer cell metabolism through HIF1alpha destabilization. Cancer Cell 19:416-428. http://dx.doi.org/10.1016/j.ccr.2011.02.014.
34. Rey S, Luo W, Shimoda LA, Semenza GL. 2011. Metabolic reprogramming by HIF-1 promotes the survival of bone marrow-derived angiogenic cells in ischemic tissue. Blood 117:4988-4998. http://dx.doi.org/10.1182/blood-2010-11-321190.
35. Zhong L, D'Urso A, Toiber D, Sebastian C, Henry RE, Vadysirisack DD, Guimaraes A, Marinelli B, Wikstrom JD, Nir T, Clish CB, Vaitheesvaran B, Iliopoulos O, Kurland I, Dor Y, Weissleder R, Shirihai OS, Ellisen LW, Espinosa JM, Mostoslavsky R. 2010. The histone deacetylase Sirt6 regulates glucose homeostasis via Hif1alpha. Cell 140:280-293. http://dx.doi.org/10.1016/j.cell.2009.12.041.
36. Agbor TA, Cheong A, Comerford KM, Scholz CC, Bruning U, Clarke A, Cummins EP, Cagney G, Taylor CT. 2011. Small ubiquitin-related modifier (SUMO)-1 promotes glycolysis in hypoxia. J. Biol. Chem. 286:4718-4726. http://dx.doi.org/10.1074/jbc.M110.115931.
37. Ogiwara H, Ui A, Otsuka A, Satoh H, Yokomi I, Nakajima S, Yasui A, Yokota J, Kohno T. 2011. Histone acetylation by CBP and p300 at double-strand break sites facilitates SWI/SNF chromatin remodeling and the recruitment of non-homologous end joining factors. Oncogene 30:2135-2146. http://dx.doi.org/10.1038/onc.2010.592.
38. Cui L, Miao J, Furuya T, Fan Q, Li X, Rathod PK, Su XZ. 2008. Histone acetyltransferase inhibitor anacardic acid causes changes in global gene expression during in vitro Plasmodium falciparum development. Eukaryot. Cell 7:1200-1210. http://dx.doi.org/10.1128/EC.00063-08.
39. Balasubramanyam K, Swaminathan V, Ranganathan A, Kundu TK. 2003. Small molecule modulators of histone acetyltransferase p300. J. Biol. Chem. 278:19134-19140. http://dx.doi.org/10.1074/jbc.M301580200.
40. Sun Y, Jiang X, Chen S, Price BD. 2006. Inhibition of histone acetyltransferase activity by anacardic acid sensitizes tumor cells to ionizing radiation. FEBS Lett. 580:4353-4356. http://dx.doi.org/10.1016/j.febslet.2006.06.092.
41. Nitin N, Carlson AL, Muldoon T, El-Naggar AK, Gillenwater A, Richards-Kortum R. 2009. Molecular imaging of glucose uptake in oral neoplasia following topical application of fluorescently labeled deoxy-glucose. Int. J. Cancer 124:2634-2642. http://dx.doi.org/10.1002/ijc.24222.
42. Vlashi E, Lagadec C, Vergnes L, Matsutani T, Masui K, Poulou M, Popescu R, Della Donna L, Evers P, Dekmezian C, Reue K, Christofk H, Mischel PS, Pajonk F. 2011. Metabolic state of glioma stem cells and nontumorigenic cells. Proc. Natl. Acad. Sci. U. S. A. 108:16062-16067. http://dx.doi.org/10.1073/pnas.1106704108.
43. Gordan JD, Simon MC. 2007. Hypoxia-inducible factors: central regulators of the tumor phenotype. Curr. Opin. Genet. Dev. 17:71-77. http://dx.doi.org/10.1016/j.gde.2006.12.006.
44. Hu CJ, Wang LY, Chodosh LA, Keith B, Simon MC. 2003. Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Mol. Cell. Biol. 23:9361-9374. http://dx.doi.org/10.1128/MCB.23.24.9361-9374.2003.
45. Hu CJ, Iyer S, Sataur A, Covello KL, Chodosh LA, Simon MC. 2006. Differential regulation of the transcriptional activities of hypoxiainducible factor 1 alpha (HIF-1alpha) and HIF-2alpha in stem cells. Mol. Cell. Biol. 26:3514-3526. http://dx.doi.org/10.1128/MCB.26.9.3514-3526.2006.
46. Hu CJ, Sataur A, Wang L, Chen H, Simon MC. 2007. The N-terminal transactivation domain confers target gene specificity of hypoxiainducible factors HIF-1alpha and HIF-2alpha. Mol. Biol. Cell 18:4528-4542. http://dx.doi.org/10.1091/mbc.E06-05-0419.
47. Maranchie JK, Vasselli JR, Riss J, Bonifacino JS, Linehan WM, Klausner RD. 2002. The contribution of VHL substrate binding and HIF1-alpha to the phenotype of VHL loss in renal cell carcinoma. Cancer Cell 1:247-255. http://dx.doi.org/10.1016/S1535-6108(02)00044-2.
48. Acker T, Diez-Juan A, Aragones J, Tjwa M, Brusselmans K, Moons L, Fukumura D, Moreno-Murciano MP, Herbert JM, Burger A, Riedel J, Elvert G, Flamme I, Maxwell PH, Collen D, Dewerchin M, Jain RK, Plate KH, Carmeliet P. 2005. Genetic evidence for a tumor suppressor role of HIF-2alpha. Cancer Cell 8:131-141. http://dx.doi.org/10.1016/j.ccr.2005.07.003.
49. Raval RR, Lau KW, Tran MG, Sowter HM, Mandriota SJ, Li JL, Pugh CW, Maxwell PH, Harris AL, Ratcliffe PJ. 2005. Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindauassociated renal cell carcinoma. Mol. Cell. Biol. 25:5675-5686. http://dx.doi.org/10.1128/MCB.25.13.5675-5686.2005.
50. Holmquist-Mengelbier L, Fredlund E, Lofstedt T, Noguera R, Navarro S, Nilsson H, Pietras A, Vallon-Christersson J, Borg A, Gradin K, Poellinger L, Pahlman S. 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. http://dx.doi.org/10.1016/j.ccr.2006.08.026.
51. Rankin EB, Rha J, Unger TL, Wu CH, Shutt HP, Johnson RS, Simon MC, Keith B, Haase VH. 2008. Hypoxia-inducible factor-2 regulates vascular tumorigenesis in mice. Oncogene 27:5354-5358. http://dx.doi.org/10.1038/onc.2008.160.
52. Qing G, Simon MC. 2009. Hypoxia inducible factor-2alpha: a critical mediator of aggressive tumor phenotypes. Curr. Opin. Genet. Dev. 19:60-66. http://dx.doi.org/10.1016/j.gde.2008.12.001.
53. Mastrogiannaki M, Matak P, Keith B, Simon MC, Vaulont S, Peyssonnaux C. 2009. HIF-2alpha, but not HIF-1alpha, promotes iron absorption in mice. J. Clin. Invest. 119:1159-1166. http://dx.doi.org/10.1172/JCI38499.
54. Imtiyaz HZ, Williams EP, Hickey MM, Patel SA, Durham AC, Yuan LJ, Hammond R, Gimotty PA, Keith B, Simon MC. 2010. Hypoxiainducible factor 2alpha regulates macrophage function in mouse models of acute and tumor inflammation. J. Clin. Invest. 120:2699-2714. http://dx.doi.org/10.1172/JCI39506.
55. Mazumdar J, Hickey MM, Pant DK, Durham AC, Sweet-Cordero A, Vachani A, Jacks T, Chodosh LA, Kissil JL, Simon MC, Keith B. 2010. HIF-2alpha deletion promotes Kras-driven lung tumor development. Proc. Natl. Acad. Sci. U. S. A. 107:14182-14187. http://dx.doi.org/10.1073/pnas.1001296107.
56. Koh MY, Darnay BG, Powis G. 2008. Hypoxia-associated factor, a novel E3-ubiquitin ligase, binds and ubiquitinates hypoxia-inducible factor 1alpha, leading to its oxygen-independent degradation. Mol. Cell. Biol. 28:7081-7095. http://dx.doi.org/10.1128/MCB.00773-08.
57. Hubbi ME, Luo W, Baek JH, Semenza GL. 2011. MCM proteins are negative regulators of hypoxia-inducible factor 1. Mol. Cell 42:700-712. http://dx.doi.org/10.1016/j.molcel.2011.03.029.
58. Jeong JW, Bae MK, Ahn MY, Kim SH, Sohn TK, Bae MH, Yoo MA, Song EJ, Lee KJ, Kim KW. 2002. Regulation and destabilization of HIF-1alpha by ARD1-mediated acetylation. Cell 111:709-720. http://dx.doi.org/10.1016/S0092-8674(02)01085-1.
59. Hubbi ME, Gilkes DM, Baek JH, Semenza GL. 2012. Four-and-a-half LIM domain proteins inhibit transactivation by hypoxia-inducible factor 1. J. Biol. Chem. 287:6139-6149. http://dx.doi.org/10.1074/jbc.M111.278630.
60. Makino Y, Cao R, Svensson K, Bertilsson G, Asman M, Tanaka H, Cao Y, Berkenstam A, Poellinger L. 2001. Inhibitory PAS domain protein is a negative regulator of hypoxia-inducible gene expression. Nature 414:550-554. http://dx.doi.org/10.1038/35107085.
61. Rohwer N, Zasada C, Kempa S, Cramer T. 2013. The growing complexity of HIF-1alpha's role in tumorigenesis: DNA repair and beyond. Oncogene 32:3569-3576. http://dx.doi.org/10.1038/onc.2012.510.
62. Lu X, Kang Y. 2010. Hypoxia and hypoxia-inducible factors: master regulators of metastasis. Clin. Cancer Res. 16:5928-5935. http://dx.doi.org/10.1158/1078-0432.CCR-10-1360.
63. Yoo YG, Hayashi M, Christensen J, Huang LE. 2009. An essential role of the HIF-1alpha-c-Myc axis in malignant progression. Ann. N. Y. Acad. Sci. 1177:198-204. http://dx.doi.org/10.1111/j.1749-6632.2009.05043.x.
64. Blagosklonny MV, An WG, Romanova LY, Trepel J, Fojo T, Neckers L. 1998. p53 inhibits hypoxia-inducible factor-stimulated transcription. J. Biol. Chem. 273:11995-11998. http://dx.doi.org/10.1074/jbc.273.20.11995.