ERRα augments HIF-1 signalling by directly interacting with HIF-1 α in normoxic and hypoxic prostate cancer cells

Journal of Pathology

Volumn 233, Issue 1, 2014, Pages 61-73

  Zou, Chang ^a,d   Yu, Shan ^a   Xu, Zhenyu ^a   Wu, Dinglan ^a   Ng, Chi Fai ^b   Yao, Xiaoqiang ^a   Yew, David T ^a   Vanacker, Jean Marc ^c   Chan, Franky L ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b and Hong Kong Branch of CAS Center for Excellence in Animal Evolution and Genetics   (Hong Kong)

^c UNIVERSITÉ DE LYON   (France)

^d AFFILIATED HOSPITAL OF JIANGSU UNIVERSITY   (China)

Author keywords

HIF 1 ; hypoxia; oestrogen related receptor ; orphan nuclear receptor; prostate cancer

Indexed keywords

ESTROGEN RELATED RECEPTOR ALPHA; HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA;

ARTICLE; CANCER CELL; CANCER GROWTH; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPRECIPITATION; MALE; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN INTERACTION; UBIQUITINATION;

HIF-1Α; HYPOXIA; OESTROGEN-RELATED RECEPTOR-Α; ORPHAN NUCLEAR RECEPTOR; PROSTATE CANCER;

ANIMALS; CELL HYPOXIA; CELL LINE, TUMOR; CELL PROLIFERATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOPRECIPITATION; MALE; MICE; MICE, SCID; OXYGEN; PROSTATIC NEOPLASMS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; RECEPTORS, ESTROGEN; RNA INTERFERENCE; TIME FACTORS; TRANSFECTION; TUMOR MICROENVIRONMENT; UBIQUITINATED PROTEINS; UBIQUITINATION;

EID: 84898597890     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4329     Document Type: Article

References (49)

1. Marignol L, Coffey M, Lawler M, et al., Hypoxia in prostate cancer: a powerful shield against tumour destruction? Cancer Treat Rev 2008; 34: 313-327.
2. Semenza GL,. Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene 2010; 29: 625-634.
3. Semenza GL,. Regulation of oxygen homeostasis by hypoxia-inducible factor 1. Physiology (Bethesda) 2009; 24: 97-106.
4. Greschik H, Wurtz JM, Sanglier S, et al., Structural and functional evidence for ligand-independent transcriptional activation by the estrogen-related receptor 3. Mol Cell 2002; 9: 303-313. (Pubitemid 34195556)
5. Kallen J, Schlaeppi JM, Bitsch F, et al., Evidence for ligand-independent transcriptional activation of the human estrogen-related receptor-α (ERRα): crystal structure of ERRα ligand binding domain in complex with peroxisome proliferator-activated receptor coactivator-1α. J Biol Chem 2004; 279: 49330-49337. (Pubitemid 39625820)
6. Bookout AL, Jeong Y, Downes M, et al., Anatomical profiling of nuclear receptor expression reveals a hierarchical transcriptional network. Cell 2006; 126: 789-799. (Pubitemid 44233630)
7. Giguere V., Transcriptional control of energy homeostasis by the estrogen-related receptors. Endocr Rev 2008; 29: 677-696.
8. Ranhotra HS,. The estrogen-related receptor-α: the oldest, yet an energetic orphan with robust biological functions. J Recept Signal Transduct Res 2010; 30: 193-205.
9. Ariazi EA, Clark GM, Mertz JE,. Estrogen-related receptor-α and estrogen-related receptor-γ associate with unfavorable and favorable biomarkers, respectively, in human breast cancer. Cancer Res 2002; 62: 6510-6518. (Pubitemid 35364116)
10. Suzuki T, Miki Y, Moriya T, et al., Estrogen-related receptor-α in human breast carcinoma as a potent prognostic factor. Cancer Res 2004; 64: 4670-4676. (Pubitemid 38856942)
11. Fradet A, Sorel H, Bouazza L, et al., Dual function of ERRα in breast cancer and bone metastasis formation: implication of VEGF and osteoprotegerin. Cancer Res 2011; 71: 5728-5738.
12. Mori T, Sawada M, Kuroboshi H, et al., Estrogen-related receptor-α expression and function are associated with vascular endothelial growth factor in human cervical cancer. Int J Gynecol Cancer 2011; 21: 609-615.
13. Cavallini A, Notarnicola M, Giannini R, et al., Oestrogen receptor-related receptor-α (ERRα) and oestrogen receptors (ERα and ERβ) exhibit different gene expression in human colorectal tumour progression. Eur J Cancer 2005; 41: 1487-1494. (Pubitemid 40826474)
14. Watanabe A, Kinoshita Y, Hosokawa K, et al., Function of estrogen-related receptor-α in human endometrial cancer. J Clin Endocrinol Metab 2006; 91: 1573-1577.
15. Gao M, Sun P, Wang J, et al., Expression of estrogen receptor-related receptor isoforms and clinical significance in endometrial adenocarcinoma. Int J Gynecol Cancer 2006; 16: 827-833.
16. Fujimoto J, Sato E,. Clinical implication of estrogen-related receptor (ERR) expression in uterine endometrial cancers. J Steroid Biochem Mol Biol 2009; 116: 71-75.
17. Sun P, Sehouli J, Denkert C, et al., Expression of estrogen receptor-related receptors, a subfamily of orphan nuclear receptors, as new tumor biomarkers in ovarian cancer cells. J Mol Med (Berl) 2005; 83: 457-467. (Pubitemid 40922168)
18. Fujimoto J, Alam SM, Jahan I, et al., Clinical implication of estrogen-related receptor (ERR) expression in ovarian cancers. J Steroid Biochem Mol Biol 2007; 104: 301-304. (Pubitemid 46891819)
19. Cheung CP, Yu S, Wong KB, et al., Expression and functional study of estrogen receptor-related receptors in human prostatic cells and tissues. J Clin Endocrinol Metab 2005; 90: 1830-1844. (Pubitemid 40464058)
20. Fujimura T, Takahashi S, Urano T, et al., Increased expression of estrogen-related receptorα (ERRα) is a negative prognostic predictor in human prostate cancer. Int J Cancer 2007; 120: 2325-2330. (Pubitemid 46642117)
21. Yang C, Zhou D, Chen S,. Modulation of aromatase expression in the breast tissue by ERRα-1 orphan receptor. Cancer Res 1998; 58: 5695-5700. (Pubitemid 29006408)
22. Kraus RJ, Ariazi EA, Farrell ML, et al., Estrogen-related receptor-α1 actively antagonizes estrogen receptor-regulated transcription in MCF-7 mammary cells. J Biol Chem 2002; 277: 24826-24834. (Pubitemid 34952015)
23. Lu D, Kiriyama Y, Lee KY, et al., Transcriptional regulation of the estrogen-inducible pS2 breast cancer marker gene by the ERR family of orphan nuclear receptors. Cancer Res 2001; 61: 6755-6761. (Pubitemid 32898670)
24. Teyssier C, Bianco S, Lanvin O, et al., The orphan receptor ERRα interferes with steroid signaling. Nucleic Acids Res 2008; 36: 5350-5361.
25. Deblois G, Hall JA, Perry MC, et al., Genome-wide identification of direct target genes implicates estrogen-related receptor-α as a determinant of breast cancer heterogeneity. Cancer Res 2009; 69: 6149-6157.
26. Ao A, Wang H, Kamarajugadda S, et al., Involvement of estrogen-related receptors in transcriptional response to hypoxia and growth of solid tumors. Proc Natl Acad Sci USA 2008; 105: 7821-7826. (Pubitemid 351872722)
27. Arany Z, Foo SY, Ma Y, et al., HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1α. Nature 2008; 451: 1008-1012. (Pubitemid 351301733)
28. Stein RA, Gaillard S, McDonnell DP,. Estrogen-related receptor-α induces the expression of vascular endothelial growth factor in breast cancer cells. J Steroid Biochem Mol Biol 2009; 114: 106-112.
29. Deblois G, Chahrour G, Perry MC, et al., Transcriptional control of the ERBB2 amplicon by ERRα and PGC-1β promotes mammary gland tumorigenesis. Cancer Res 2010; 70: 10277-10287.
30. Dwyer MA, Joseph JD, Wade HE, et al., WNT11 expression is induced by estrogen-related receptorα and β-catenin and acts in an autocrine manner to increase cancer cell migration. Cancer Res 2010; 70: 9298-9308.
31. Fisher KW, Das B, Kortum RL, et al., Kinase suppressor of ras1 (KSR1) regulates PGC1α and estrogen-related receptor-α to promote oncogenic Ras-dependent anchorage-independent growth. Mol Cell Biol 2011; 31: 2453-2461.
32. Cai Q, Lin T, Kamarajugadda S, et al., Regulation of glycolysis and the Warburg effect by estrogen-related receptors. Oncogene 2013; 32: 2079-2086.
33. Yu S, Wong YC, Wang XH, et al., Orphan nuclear receptor estrogen-related receptor-β suppresses in vitro and in vivo growth of prostate cancer cells via p21(WAF1/CIP1) induction and as a potential therapeutic target in prostate cancer. Oncogene 2008; 27: 3313-3328. (Pubitemid 351733386)
34. Yu S, Wang MW, Yao X, et al., Establishment of a novel immortalized human prostatic epithelial cell line stably expressing androgen receptor and its application for the functional screening of androgen receptor modulators. Biochem Biophys Res Commun 2009; 382: 756-761.
35. Chu JH, Yu S, Hayward SW, et al., Development of a three-dimensional culture model of prostatic epithelial cells and its use for the study of epithelial-mesenchymal transition and inhibition of PI3K pathway in prostate cancer. Prostate 2009; 69: 428-442.
36. Yu S, Wang X, Ng CF, et al., ERRγ suppresses cell proliferation and tumor growth of androgen-sensitive and androgen-insensitive prostate cancer cells and its implication as a therapeutic target for prostate cancer. Cancer Res 2007; 67: 4904-4914. (Pubitemid 46915313)
37. Ma X, Nilius B, Wong JW, et al., Electrophysiological properties of heteromeric TRPV4-C1 channels. Biochim Biophys Acta 2011; 1808: 2789-2797.
38. Higgins LH, Withers HG, Garbens A, et al., Hypoxia and the metabolic phenotype of prostate cancer cells. Biochim Biophys Acta 2009; 1787: 1433-1443.
39. Deblois G, Giguere V,. Oestrogen-related receptors in breast cancer: control of cellular metabolism and beyond. Nat Rev Cancer 2013; 13: 27-36.
40. Bianco S, Sailland J, Vanacker JM,. ERRs and cancers: effects on metabolism and on proliferation and migration capacities. J Steroid Biochem Mol Biol 2012; 130: 180-185.
41. Huss JM, Kopp RP, Kelly DP,. Peroxisome proliferator-activated receptor coactivator-1α (PGC-1α) coactivates the cardiac-enriched nuclear receptors estrogen-related receptor-α and -γ. Identification of novel leucine-rich interaction motif within PGC-1α. J Biol Chem 2002; 277: 40265-40274. (Pubitemid 35215598)
42. Mootha VK, Handschin C, Arlow D, et al., Errα and Gabpa/b specify PGC-1α-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc Natl Acad Sci USA 2004; 101: 6570-6575. (Pubitemid 38586015)
43. Kumar P, Mendelson CR,. Estrogen-related receptor-γ (ERRγ) mediates oxygen-dependent induction of aromatase (CYP19) gene expression during human trophoblast differentiation. Mol Endocrinol 2011; 25: 1513-1526.
44. Lee JH, Kim EJ, Kim DK, et al., Hypoxia induces PDK4 gene expression through induction of the orphan nuclear receptor ERRγ. PLoS One 2012; 7: e46324.
45. Li Y, Padmanabha D, Gentile LB, et al., HIF- and non-HIF-regulated hypoxic responses require the estrogen-related receptor in Drosophila melanogaster. PLoS Genet 2013; 9: e1003230.
46. Bianco S, Lanvin O, Tribollet V, et al., Modulating estrogen receptor-related receptor-α activity inhibits cell proliferation. J Biol Chem 2009; 284: 23286-23292.
47. Gao M, Sun PM, Wang JL, et al., Different biological effect of estrogen receptor-related receptor-α in estrogen receptor-positive and -negative endometrial carcinoma. Mol Med Rep 2008; 1: 917-924.
48. Stein RA, Chang CY, Kazmin DA, et al., Estrogen-related receptor-α is critical for the growth of estrogen receptor-negative breast cancer. Cancer Res 2008; 68: 8805-8812.
49. Tiraby C, Hazen BC, Gantner ML, et al., Estrogen-related receptor-γ promotes mesenchymal-to-epithelial transition and suppresses breast tumor growth. Cancer Res 2011; 71: 2518-2528.