Upstream stimulatory factor 2 and hypoxia-inducible factor 2α (HIF2α) cooperatively activate HIF2 target genes during hypoxia

Molecular and Cellular Biology

Volumn 32, Issue 22, 2012, Pages 4595-4610

  Pawlus, Matthew R ^a   Wang, Liyi ^a   Ware, Katie ^a   Hu, Cheng Jun ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC HELIX LOOP HELIX LEUCINE ZIPPER TRANSCRIPTION FACTOR; HISTONE ACETYLTRANSFERASE PCAF; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; RNA POLYMERASE II; TRANSCRIPTION FACTOR; UPSTREAM STIMULATORY FACTOR 2;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CELL MOTILITY; CELL PROLIFERATION; CLONOGENESIS; CONTROLLED STUDY; EMBRYO; GENE ACTIVATION; GENE TARGETING; HUMAN; HUMAN CELL; HYPOXIA; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION;

ANIMALS; ANOXIA; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION, NEOPLASTIC; CREB-BINDING PROTEIN; HUMANS; MICE; MICE, KNOCKOUT; P300-CBP TRANSCRIPTION FACTORS; PLASMIDS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RNA POLYMERASE II; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION; UPSTREAM STIMULATORY FACTORS;

EID: 84868702904     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00724-12     Document Type: Article

References (113)

1. Alfranca A, et al. 2002. c-Jun and hypoxia-inducible factor 1 functionally cooperate in hypoxia-induced gene transcription. Mol. Cell. Biol. 22:12-22.
2. Allen RR, Qi L, Higgins PJ. 2005. Upstream stimulatory factor regulates E box-dependent PAI-1 transcription in human epidermal keratinocytes. J. Cell. Physiol. 203:156-165.
3. Anderson CJ, Hoare SF, Ashcroft M, Bilsland AE, Keith WN. 2006. Hypoxic regulation of telomerase gene expression by transcriptional and post-transcriptional mechanisms. Oncogene 25:61-69.
4. Aprelikova O, Wood M, Tackett S, Chandramouli GV, Barrett JC. 2006. Role of ETS transcription factors in the hypoxia-inducible factor-2 target gene selection. Cancer Res. 66:5641-5647.
5. Arany Z, et al. 1996. An essential role for p300/CBP in the cellular response to hypoxia. Proc. Natl. Acad. Sci. U. S. A. 93:12969-12973.
6. Breen GA, Jordan EM. 1999. Transcriptional activation of the F(1)F(0) ATP synthase alpha-subunit initiator element by USF2 is mediated by p300. Biochim. Biophys. Acta 1428:169-176.
7. Breen GA, Jordan EM. 1998. Upstream stimulatory factor 2 activates the mammalian F1F0 ATP synthase alpha-subunit gene through an initiator element. Gene Expr. 7:163-170.
8. Breen GA, Jordan EM. 2000. Upstream stimulatory factor 2 stimulates transcription through an initiator element in the mouse cytochrome c oxidase subunit Vb promoter. Biochim. Biophys. Acta 1517:119-127.
9. Chang JT, Yang HT, Wang TC, Cheng AJ. 2005. Upstream stimulatory factor (USF) as a transcriptional suppressor of human telomerase reverse transcriptase (hTERT) in oral cancer cells. Mol. Carcinog. 44:183-192.
10. Chen L, et al. 2006. Human prolyl-4-hydroxylase alpha(I) transcription is mediated by upstream stimulatory factors. J. Biol. Chem. 281:10849-10855.
11. Cheung E, Mayr P, Coda-Zabetta F, Woodman PG, Boam DS. 1999. DNA-binding activity of the transcription factor upstream stimulatory factor 1 (USF-1) is regulated by cyclin-dependent phosphorylation. Biochem. J. 344(Pt 1):145-152.
12. Chiang CM, Roeder RG. 1995. Cloning of an intrinsic human TFIID subunit that interacts with multiple transcriptional activators. Science 267:531-536.
13. Compernolle V, et al. 2002. Loss of HIF-2alpha and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nat. Med. 8:702-710.
14. Corre S, Galibert MD. 2005. Upstream stimulating factors: highly versatile stress-responsive transcription factors. Pigment Cell Res. 18:337-348.
15. Corre S, et al. 2009. Target gene specificity of USF-1 is directed via p38-mediated phosphorylation-dependent acetylation. J. Biol. Chem. 284:18851-18862.
16. Coulson JM, et al. 2003. Upstream stimulatory factor activates the vasopressin promoter via multiple motifs, including a non-canonical E-box. Biochem. J. 369:549-561.
17. Dames SA, Martinez-Yamout M, De Guzman RN, Dyson HJ, Wright PE. 2002. Structural basis for Hif-1 alpha/CBP recognition in the cellular hypoxic response. Proc. Natl. Acad. Sci. U. S. A. 99:5271-5276.
18. Dimova EY, Kietzmann T. 2006. Cell type-dependent regulation of the hypoxia-responsive plasminogen activator inhibitor-1 gene by upstream stimulatory factor-2. J. Biol. Chem. 281:2999-3005.
19. Du H, Roy AL, Roeder RG. 1993. Human transcription factor USF stimulates transcription through the initiator elements of the HIV-1 and the Ad-ML promoters. EMBO J. 12:501-511.
20. Ebert BL, Bunn HF. 1998. Regulation of transcription by hypoxia requires a multiprotein complex that includes hypoxia-inducible factor 1, an adjacent transcription factor, and p300/CREB binding protein. Mol. Cell. Biol. 18:4089-4096.
21. Elvert G, et al. 2003. Cooperative interaction of hypoxia-inducible factor-2alpha (HIF-2alpha) and Ets-1 in the transcriptional activation of vascular endothelial growth factor receptor-2 (Flk-1). J. Biol. Chem. 278: 7520-7530.
22. Ema M, et al. 1999. Molecular mechanisms of transcription activation by HLF and HIF1alpha in response to hypoxia: their stabilization and redox signal-induced interaction with CBP/p300. EMBO J. 18:1905-1914.
23. Emerling BM, Weinberg F, Liu JL, Mak TW, Chandel NS. 2008. PTEN regulates p300-dependent hypoxia-inducible factor 1 transcriptional activity through Forkhead transcription factor 3a (FOXO3a). Proc. Natl. Acad. Sci. U. S. A. 105:2622-2627.
24. Figueroa YG, et al. 2002. NF-kappaB plays a key role in hypoxiainducible factor-1-regulated erythropoietin gene expression. Exp. Hematol. 30:1419-1427.
25. Finger EC, Giaccia AJ. 2010. Hypoxia, inflammation, and the tumor microenvironment in metastatic disease. Cancer Metastasis Rev. 29:285-293.
26. Fink T, Ebbesen P, Zachar V. 2001. Quantitative gene expression profiles of human liver-derived cell lines exposed to moderate hypoxia. Cell. Physiol. Biochem. 11:105-114.
27. Fink T, Kazlauskas A, Poellinger L, Ebbesen P, Zachar V. 2002. Identification of a tightly regulated hypoxia-response element in the promoter of human plasminogen activator inhibitor-1. Blood 99:2077-2083.
28. Firth JD, Ebert BL, Pugh CW, Ratcliffe PJ. 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. U. S. A. 91:6496-6500.
29. Fitzpatrick TE, Graham CH. 1998. Stimulation of plasminogen activator inhibitor-1 expression in immortalized human trophoblast cells cultured under low levels of oxygen. Exp. Cell Res. 245:155-162.
30. Freedman SJ, et al. 2002. Structural basis for recruitment of CBP/p300 by hypoxia-inducible factor-1 alpha. Proc. Natl. Acad. Sci. U. S. A. 99: 5367-5372.
31. Galibert MD, Carreira S, Goding CR. 2001. The Usf-1 transcription factor is a novel target for the stress-responsive p38 kinase and mediates UV-induced tyrosinase expression. EMBO J. 20:5022-5031.
32. Gao E, Wang Y, Alcorn JL, Mendelson CR. 1997. The basic helix-loophelix-zipper transcription factor USF1 regulates expression of the surfactant protein-A gene. J. Biol. Chem. 272:23398-23406.
33. Gao E, Wang Y, Alcorn JL, Mendelson CR. 2003. Transcription factor USF2 is developmentally regulated in fetal lung and acts together with USF1 to induce SP-A gene expression. Am. J. Physiol. 284:L1027-L1036.
34. Gordan JD, Bertout JA, Hu CJ, Diehl JA, Simon MC. 2007. HIF-2alpha promotes hypoxic cell proliferation by enhancing c-myc transcriptional activity. Cancer Cell 11:335-347.
35. Goueli BS, Janknecht R. 2003. Regulation of telomerase reverse transcriptase gene activity by upstream stimulatory factor. Oncogene 22: 8042-8047.
36. Gregor PD, Sawadogo M, Roeder RG. 1990. The adenovirus major late transcription factor USF is a member of the helix-loop-helix group of regulatory proteins and binds to DNA as a dimer. Genes Dev. 4:1730-1740.
37. Greijer AE, et al. 2005. Up-regulation of gene expression by hypoxia is mediated predominantly by hypoxia-inducible factor 1 (HIF-1). J. Pathol. 206:291-304.
38. Gruber M, et al. 2007. Acute postnatal ablation of Hif-2alpha results in anemia. Proc. Natl. Acad. Sci. U. S. A. 104:2301-2306.
39. Gusterson R, et al. 2002. The transcriptional co-activators CBP and p300 are activated via phenylephrine through the p42/p44 MAPK cascade. J. Biol. Chem. 277:2517-2524.
40. Harris VK, Coticchia CM, List HJ, Wellstein A, Riegel AT. 2000. Mitogen-induced expression of the fibroblast growth factor-binding protein is transcriptionally repressed through a non-canonical E-box element. J. Biol. Chem. 275:28539-28548.
41. Hartsfield CL, Alam J, Choi AM. 1999. Differential signaling pathways of HO-1 gene expression in pulmonary and systemic vascular cells. Am. J. Physiol. 277:L1133-L1141.
42. Hock TD, Nick HS, Agarwal A. 2004. Upstream stimulatory factors, USF1 and USF2, bind to the human haem oxygenase-1 proximal promoter in vivo and regulate its transcription. Biochem. J. 383:209-218.
43. Hofbauer KH, et al. 2003. Oxygen tension regulates the expression of a group of procollagen hydroxylases. Eur. J. Biochem. 270:4515-4522.
44. Horikawa I, et al. 2002. Downstream E-box-mediated regulation of the human telomerase reverse transcriptase (hTERT) gene transcription: evidence for an endogenous mechanism of transcriptional repression. Mol. Biol. Cell 13:2585-2597.
45. Howcroft TK, et al. 1999. Upstream stimulatory factor regulates major histocompatibility complex class I gene expression: the U2DeltaE4 splice variant abrogates E-box activity. Mol. Cell. Biol. 19:4788-4797.
46. Hu CJ, et al. 2006. Differential regulation of the transcriptional activities of hypoxia-inducible factor 1 alpha (HIF-1alpha) and HIF-2alpha in stem cells. Mol. Cell. Biol. 26:3514-3526.
47. 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.
48. 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.
49. Hu J, et al. 2011. Interaction of HIF and USF signaling pathways in human genes flanked by hypoxia-response elements and E-box palindromes. Mol. Cancer Res. 9:1520-1536.
50. Huang LE, et al. 1997. Erythropoietin gene regulation depends on heme-dependent oxygen sensing and assembly of interacting transcription factors. Kidney Int. 51:548-552.
51. Huang S, Li X, Yusufzai TM, Qiu Y, Felsenfeld G. 2007. USF1 recruits histone modification complexes and is critical for maintenance of a chromatin barrier. Mol. Cell. Biol. 27:7991-8002.
52. Jiang S, Galindo MR, Jarrett HW. 2010. Purification and identification of a transcription factor, USF-2, binding to E-box element in the promoter of human telomerase reverse transcriptase (hTERT). Proteomics 10:203-211.
53. Kaelin Jr WG. 2011. Cancer and altered metabolism: potential importance of hypoxia-inducible factor and 2-oxoglutarate-dependent dioxygenases. Cold Spring Harbor Symp. Quant. Biol. 76:335-345.
54. Kallio PJ, et al. 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.
55. Kasper LH, et al. 2005. Two transactivation mechanisms cooperate for the bulk of HIF-1-responsive gene expression. EMBO J. 24:3846-3858.
56. Keith B, Johnson RS, Simon MC. 2012. HIF1alpha and HIF2alpha: sibling rivalry in hypoxic tumour growth and progression. Nat. Rev. Cancer 12:9-22.
57. Kietzmann T, Roth U, Jungermann K. 1999. Induction of the plasminogen activator inhibitor-1 gene expression by mild hypoxia via a hypoxia response element binding the hypoxia-inducible factor-1 in rat hepatocytes. Blood 94:4177-4185.
58. Kimura D, et al. 2002. Hypoxia enhances the expression of plasminogen activator inhibitor-1 in human lung cancer cells, EBC-1. Tohoku J. Exp. Med. 196:259-267.
59. Kokubo T, et al. 1993. Identification of TFIID components required for transcriptional activation by upstream stimulatory factor. J. Biol. Chem. 268:17554-17558.
60. Kondo K, Kim WY, Lechpammer M, Kaelin Jr WG, 2003. Inhibition of HIF2alpha is sufficient to suppress pVHL-defective tumor growth. PLoS Biol. 1:E83. doi:10.1371/journal.pbio.0000083.
61. Koshiji M, et al. 2004. HIF-1alpha induces cell cycle arrest by functionally counteracting Myc. EMBO J. 23:1949-1956.
62. Krones A, Jungermann K, Kietzmann T. 2001. Cross-talk between the signals hypoxia and glucose at the glucose response element of the L-type pyruvate kinase gene. Endocrinology 142:2707-2718.
63. Lee PJ, et al. 1997. Hypoxia-inducible factor-1 mediates transcriptional activation of the heme oxygenase-1 gene in response to hypoxia. J. Biol. Chem. 272:5375-5381.
64. Li B, Takeda K, Yokoyama S, Shibahara S. 2008. A prolyl-hydroxylase inhibitor, ethyl-3,4-dihydroxybenzoate, induces haem oxygenase-1 expression in human cells through a mechanism independent of hypoxiainducible factor-1alpha. J. Biochem. 144:643-654.
65. Li QJ, et al. 2003. MAP kinase phosphorylation-dependent activation of Elk-1 leads to activation of the co-activator p300. EMBO J. 22:281-291.
66. Liao H, Hyman MC, Lawrence DA, Pinsky DJ. 2007. Molecular regulation of the PAI-1 gene by hypoxia: contributions of Egr-1, HIF-1alpha, and C/EBPalpha. FASEB J. 21:935-949.
67. Lou F, et al. 2007. The opposing effect of hypoxia-inducible factor-2alpha on expression of telomerase reverse transcriptase. Mol. Cancer Res. 5:793-800.
68. Madan A, Curtin PT. 1993. A 24-base-pair sequence 3= to the human erythropoietin gene contains a hypoxia-responsive transcriptional enhancer. Proc. Natl. Acad. Sci. U. S. A. 90:3928-3932.
69. Mastrogiannaki M, et al. 2012. Deletion of HIF-2alpha in the enterocytes decreases the severity of tissue iron loading in hepcidin knockout mice. Blood 119:587-590.
70. Meisterernst M, Horikoshi M, Roeder RG. 1990. Recombinant yeast TFIID, a general transcription factor, mediates activation by the genespecific factor USF in a chromatin assembly assay. Proc. Natl. Acad. Sci. U. S. A. 87:9153-9157.
71. Merika M, Williams AJ, Chen G, Collins T, Thanos D. 1998. Recruitment of CBP/p300 by the IFN beta enhanceosome is required for synergistic activation of transcription. Mol. Cell 1:277-287.
72. Minamino T, Mitsialis SA, Kourembanas S. 2001. Hypoxia extends the life span of vascular smooth muscle cells through telomerase activation. Mol. Cell. Biol. 21:3336-3342.
73. Moriuchi M, Moriuchi H, Margolis DM, Fauci AS. 1999. USF/c-Myc enhances, while Yin-Yang 1 suppresses, the promoter activity of CXCR4, a coreceptor for HIV-1 entry. J. Immunol. 162:5986-5992.
74. Nicolas G, et al. 2001. Lack of hepcidin gene expression and severe tissue iron overload in upstream stimulatory factor 2 (USF2) knockout mice. Proc. Natl. Acad. Sci. U. S. A. 98:8780-8785.
75. Nishi H, et al. 2004. Hypoxia-inducible factor 1 mediates upregulation of telomerase (hTERT). Mol. Cell. Biol. 24:6076-6083.
76. Nowak M, et al. 2005. Insulin-mediated down-regulation of apolipoprotein A5 gene expression through the phosphatidylinositol 3-kinase pathway: role of upstream stimulatory factor. Mol. Cell. Biol. 25:1537-1548.
77. Rahl PB, et al. 2010. c-Myc regulates transcriptional pause release. Cell 141:432-445.
78. Rankin EB, et al. 2007. Hypoxia-inducible factor-2 (HIF-2) regulates hepatic erythropoietin in vivo. J. Clin. Invest. 117:1068-1077.
79. Raval RR, et al. 2005. Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-associated renal cell carcinoma. Mol. Cell. Biol. 25:5675-5686.
80. Roy AL, Meisterernst M, Pognonec P, Roeder RG. 1991. Cooperative interaction of an initiator-binding transcription initiation factor and the helix-loop-helix activator USF. Nature 354:245-248.
81. Ruas JL, et al. Complex regulation of the transactivation function of hypoxia-inducible factor-1 alpha by direct interaction with two distinct domains of the CREB-binding protein/p300. J. Biol. Chem. 285:2601-2609.
82. Ruas JL, Poellinger L, Pereira T. 2002. Functional analysis of hypoxiainducible factor-1 alpha-mediated transactivation. Identification of amino acid residues critical for transcriptional activation and/or interaction with CREB-binding protein. J. Biol. Chem. 277:38723-38730.
83. Salero E, Gimenez C, Zafra F. 2003. Identification of a non-canonical E-box motif as a regulatory element in the proximal promoter region of the apolipoprotein E gene. Biochem. J. 370:979-986.
84. Samoylenko A, et al. 2008. Opposite expression of the antioxidant heme oxygenase-1 in primary cells and tumor cells: regulation by interaction of USF-2 and Fra-1. Antioxid. Redox Signal. 10:1163-1174.
85. Sanchez-Elsner T, et al. 2001. Synergistic cooperation between hypoxia and transforming growth factor-beta pathways on human vascular endothelial growth factor gene expression. J. Biol. Chem. 276:38527-38535.
86. Sanchez-Elsner T, Botella LM, Velasco B, Langa C, Bernabeu C. 2002. Endoglin expression is regulated by transcriptional cooperation between the hypoxia and transforming growth factor-beta pathways. J. Biol. Chem. 277:43799-43808.
87. Sang N, et al. 2003. MAPK signaling up-regulates the activity of hypoxiainducible factors by its effects on p300. J. Biol. Chem. 278:14013-14019.
88. Sato M, et al. 1989. Transcriptional control of the rat heme oxygenase gene by a nuclear protein that interacts with adenovirus 2 major late promoter. J. Biol. Chem. 264:10251-10260.
89. Sato M, Ishizawa S, Yoshida T, Shibahara S. 1990. Interaction of upstream stimulatory factor with the human heme oxygenase gene promoter. Eur. J. Biochem. 188:231-237.
90. Schioppa T, et al. 2003. Regulation of the chemokine receptor CXCR4 by hypoxia. J. Exp. Med. 198:1391-1402.
91. -/- mice. Nat. Genet. 35:331-340.
92. Scortegagna M, et al. 2005. HIF-2alpha regulates murine hematopoietic development in an erythropoietin-dependent manner. Blood 105:3133-3140.
93. Semenza GL. 2012. Hypoxia-inducible factors in physiology and medicine. Cell 148:399-408.
94. Sirito M, Lin Q, Maity T, Sawadogo M. 1994. Ubiquitous expression of the 43- and 44-kDa forms of transcription factor USF in mammalian cells. Nucleic Acids Res. 22:427-433.
95. Sirito M, et al. 1992. Members of the USF family of helix-loop-helix proteins bind DNA as homo- as well as heterodimers. Gene Expr. 2:231-240.
96. Staller P, et al. 2003. Chemokine receptor CXCR4 downregulated by von Hippel-Lindau tumour suppressor pVHL. Nature 425:307-311.
97. Tabuchi A, Sakaya H, Kisukeda T, Fushiki H, Tsuda M. 2002. Involvement of an upstream stimulatory factor as well as cAMP-responsive element-binding protein in the activation of brain-derived neurotrophic factor gene promoter I. J. Biol. Chem. 277:35920-35931.
98. Takahashi Y, Takahashi S, Shiga Y, Yoshimi T, Miura T. 2000. Hypoxic induction of prolyl 4-hydroxylase alpha (I) in cultured cells. J. Biol. Chem. 275:14139-14146.
99. Tendler DS, et al. 2001. Intersection of interferon and hypoxia signal transduction pathways in nitric oxide-induced tumor apoptosis. Cancer Res. 61:3682-3688.
100. Thanos D, Maniatis T. 1995. Virus induction of human IFN beta gene expression requires the assembly of an enhanceosome. Cell 83:1091-1100.
101. Viollet B, et al. 1996. Immunochemical characterization and transacting properties of upstream stimulatory factor isoforms. J. Biol. Chem. 271: 1405-1415.
102. Virolle T, et al. 2002. Binding of USF to a non-canonical E-box following stress results in a cell-specific derepression of the lama3 gene. Nucleic Acids Res. 30:1789-1798.
103. Wang V, Davis DA, Haque M, Huang LE, Yarchoan R. 2005. Differential gene up-regulation by hypoxia-inducible factor-1alpha and hypoxia-inducible factor-2alpha in HEK293T cells. Cancer Res. 65:3299-3306.
104. Warnecke C, et al. 2004. Differentiating the functional role of hypoxiainducible factor (HIF)-1alpha and HIF-2alpha (EPAS-1) by the use of RNA interference: erythropoietin is a HIF-2alpha target gene in Hep3B and Kelly cells. FASEB J. 18:1462-1464.
105. Wenger RH, Stiehl DP, Camenisch G. 2005. Integration of oxygen signaling at the consensus HRE. Sci. STKE 2005:re12. doi:10.1126/ stke.3062005re12.
106. West AG, Huang S, Gaszner M, Litt MD, Felsenfeld G. 2004. Recruitment of histone modifications by USF proteins at a vertebrate barrier element. Mol. Cell 16:453-463.
107. Wickramasinghe NS, Banerjee K, Nagaraj NS, Vigneswaran N, Zacharias W. 2005. Hypoxia alters cathepsin B/inhibitor profiles in oral carcinoma cell lines. Anticancer Res. 25:2841-2849.
108. Xia X, et al. 2009. Integrative analysis of HIF binding and transactivation reveals its role in maintaining histone methylation homeostasis. Proc. Natl. Acad. Sci. U. S. A. 106:4260-4265.
109. Xiao Q, Kenessey A, Ojamaa K. 2002. Role of USF1 phosphorylation on cardiac alpha-myosin heavy chain promoter activity. Am. J. Physiol. Heart Circ. Physiol. 283:H213-H219.
110. Yago M, Ohki R, Hatakeyama S, Fujita T, Ishikawa F. 2002. Variant forms of upstream stimulatory factors (USFs) control the promoter activity of hTERT, the human gene encoding the catalytic subunit of telomerase. FEBS Lett. 520:40-46.
111. Yan S, Jane DT, Dufresne MJ, Sloane BF. 2003. Transcription of cathepsin B in glioma cells: regulation by an E-box adjacent to the transcription initiation site. Biol. Chem. 384:1421-1427.
112. Yang ZZ, Zou AP. 2001. Transcriptional regulation of heme oxygenases by HIF-1alpha in renal medullary interstitial cells. Am. J. Physiol. Renal Physiol. 281:F900-F908.
113. Yatabe N, et al. 2004. HIF-1-mediated activation of telomerase in cervical cancer cells. Oncogene 23:3708-3715.