Identification of NR0B1 as a novel androgen receptor co-repressor in mouse Sertoli cells

International Journal of Molecular Medicine

Volumn 38, Issue 3, 2016, Pages 853-860

  Li, Yu Chi ^a,b   Luo, Man Ling ^a,b   Guo, Huan ^a,c   Wang, Tian Tian ^a   Lin, Shou Ren ^a   Chen, Jian Bo ^a,d   Ma, Qian ^a   Gu, Yan Li ^a   Jiang, Zhi Mao ^a   Gui, Yao Ting ^a  

^a PEKING UNIVERSITY SHENZHEN HOSPITAL   (China)

^b SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

^c GUANGZHOU MEDICAL UNIVERSITY   (China)

^d ANHUI MEDICAL UNIVERSITY   (China)

Author keywords

Androgen receptor; Co repressor; NR0B1; Sertoli cells; Transcription

Indexed keywords

ANDROGEN RECEPTOR; NUCLEAR RECEPTOR DAX 1; PROTEIN TYROSINE PHOSPHATASE SHP; ANDROGEN; COREPRESSOR PROTEIN; NR0B1 PROTEIN, MOUSE; PROTEIN BINDING;

ADULT; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; IN VITRO STUDY; LONG TERMINAL REPEAT; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; SERTOLI CELL; TESTIS DEVELOPMENT; TRANSCRIPTION INITIATION; AGE; ANIMAL; CELL LINE; CONFOCAL MICROSCOPY; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEK293 CELL LINE; HUMAN; METABOLISM; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TESTIS; WESTERN BLOTTING;

AGE FACTORS; ANDROGENS; ANIMALS; BLOTTING, WESTERN; CELL LINE; CO-REPRESSOR PROTEINS; DAX-1 ORPHAN NUCLEAR RECEPTOR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEK293 CELLS; HUMANS; MALE; MICE; MICROSCOPY, CONFOCAL; PROTEIN BINDING; RECEPTORS, ANDROGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SERTOLI CELLS; TESTIS;

EID: 84979885665     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm.2016.2672     Document Type: Article

References (53)

1. Goto M and Katsumata N: X-linked adrenal hypoplasia congenita caused by a novel intronic mutation of the DAX-1 gene. Horm Res 71: 120-124, 2009.
2. Ikeda Y, Takeda Y, Shikayama T, Mukai T, Hisano S and Morohashi KI: Comparative localization of Dax-1 and Ad4BP/SF-1 during development of the hypothalamicpituitarygonadal axis suggests their closely related and distinct functions. Dev Dyn 220: 363-376, 2001.
3. Bardoni B, Zanaria E, Guioli S, Floridia G, Worley KC, Tonini G, Ferrante E, Chiumello G, McCabe ER, Fraccaro M, et al: A dosage sensitive locus at chromosome Xp21 is involved in male to female sex reversal. Nat Genet 7: 497-501, 1994.
4. Achermann JC, Meeks JJ and Jameson JL: Phenotypic spectrum of mutations in DAX-1 and SF-1. Mol Cell Endocrinol 185: 17-25, 2001.
5. Yu RN, Ito M, Saunders TL, Camper SA and Jameson JL: Role of Ahch in gonadal development and gametogenesis. Nat Genet 20: 353-357, 1998.
6. Jeffs B, Meeks JJ, Ito M, Martinson FA, Matzuk MM, Jameson JL and Russell LD: Blockage of the rete testis and efferent ductules by ectopic Sertoli and Leydig cells causes infertility in Dax1deficient male mice. Endocrinology 142: 4486-4495, 2001.
7. Heemers HV and Tindall DJ: Androgen receptor (AR) coregulators: a diversity of functions converging on and regulating the AR transcriptional complex. Endocr Rev 28: 778-808, 2007.
8. Heinlein CA and Chang C: Androgen receptor (AR) coregulators: an overview. Endocr Rev 23: 175-200, 2002.
9. Patrão MT, Silva EJ and Avellar MC: Androgens and the male reproductive tract: an overview of classical roles and current perspectives. Arq Bras Endocrinol Metabol 53: 934-945, 2009.
10. De Gendt K, Swinnen JV, Saunders PT, Schoonjans L, Dewerchin M, Devos A, Tan K, Atanassova N, Claessens F, Lécureuil C, et al: A Sertoli cell-selective knockout of the androgen receptor causes spermatogenic arrest in meiosis. Proc Natl Acad Sci USA 101: 1327-1332, 2004.
11. Wang RS, Yeh S, Tzeng CR and Chang C: Androgen receptor roles in spermatogenesis and fertility: lessons from testicular cell-specific androgen receptor knockout mice. Endocr Rev 30: 119-132, 2009.
12. Yeh S, Tsai MY, Xu Q, Mu XM, Lardy H, Huang KE, Lin H, Yeh SD, Altuwaijri S, Zhou X, et al: Generation and characterization of androgen receptor knockout (ARKO) mice: an in vivo model for the study of androgen functions in selective tissues. Proc Natl Acad Sci USA 99: 13498-13503, 2002.
13. Quigley CA, De Bellis A, Marschke KB, el-Awady MK, Wilson EM and French FS: Androgen receptor defects: historical, clinical, and molecular perspectives. Endocr Rev 16: 271-321, 1995.
14. Yong EL, Ghadessy F, Wang Q, Mifsud A and Ng SC: Androgen receptor transactivation domain and control of spermatogenesis. Rev Reprod 3: 141-144, 1998.
15. Culig Z, Hobisch A, Bartsch G and Klocker H: Androgen receptor-an update of mechanisms of action in prostate cancer. Urol Res 28: 211-219, 2000.
16. Hughes IA: Minireview: sex differentiation. Endocrinology 142: 3281-3287, 2001.
17. Jänne OA, Moilanen AM, Poukka H, Rouleau N, Karvonen U, Kotaja N, Häkli M and Palvimo JJ: Androgen-receptor-interacting nuclear proteins. Biochem Soc Trans 28: 401-405, 2000.
18. Schmittgen TD and Livak KJ: Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108, 2008.
19. Meeks JJ, Crawford SE, Russell TA, Morohashi K, Weiss J and Jameson JL: Dax1 regulates testis cord organization during gonadal differentiation. Development 130: 1029-1036, 2003.
20. Hanley NA, Hagan DM, Clement-Jones M, Ball SG, Strachan T, Salas-Cortés L, McElreavey K, Lindsay S, Robson S, Bullen P, et al: SRY, SOX9, and DAX1 expression patterns during human sex determination and gonadal development. Mech Dev 91: 403-407, 2000.
21. Münsterberg A and Lovell-Badge R: Expression of the mouse anti-müllerian hormone gene suggests a role in both male and female sexual differentiation. Development 113: 613-624, 1991.
22. Kent J, Wheatley SC, Andrews JE, Sinclair AH and Koopman P: A male-specific role for SOX9 in vertebrate sex determination. Development 122: 2813-2822, 1996.
23. Morais da Silva S, Hacker A, Harley V, Goodfellow P, Swain A and Lovell-Badge R: Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nat Genet 14: 62-68, 1996.
24. Denolet E, De Gendt K, Allemeersch J, Engelen K, Marchal K, Van Hummelen P, Tan KA, Sharpe RM, Saunders PT, Swinnen JV and Verhoeven G: The effect of a Sertoli cell-selective knockout of the androgen receptor on testicular gene expression in prepubertal mice. Mol Endocrinol 20: 321-334, 2006.
25. De Gendt K, Denolet E, Willems A, Daniels VW, Clinckemalie L, Denayer S, Wilkinson MF, Claessens F, Swinnen JV and Verhoeven G: Expression of Tubb3, a beta-tubulin isotype, is regulated by androgens in mouse and rat Sertoli cells. Biol Reprod 85: 934-945, 2011.
26. Zhou W, Wang G, Small CL, Liu Z, Weng CC, Yang L, Griswold MD and Meistrich ML: Gene expression alterations by conditional knockout of androgen receptor in adult Sertoli cells of Utp14b jsd/jsd (jsd) mice. Biol Reprod 84: 400-408, 2011.
27. Zhang QX, Zhang XY, Zhang ZM, Lu W, Liu L, Li G, Cai ZM, Gui YT and Chang C: Identification of testosterone-/androgen receptor-regulated genes in mouse Sertoli cells. Asian J Androl 14: 294-300, 2012.
28. Eacker SM, Shima JE, Connolly CM, Sharma M, Holdcraft RW, Griswold MD and Braun RE: Transcriptional profiling of androgen receptor (AR) mutants suggests instructive and permissive roles of AR signaling in germ cell development. Mol Endocrinol 21: 895-907, 2007.
29. Yang L, Wang Y, Zhang Q, Lai Y, Li C, Zhang Q, Huang W, Duan Y, Jiang Z, Li X, et al: Identification of Hsf1 as a novel androgen receptor-regulated gene in mouse Sertoli cells. Mol Reprod Dev 81: 514-523, 2014.
30. Mou L, Zhang Q, Wang Y, Zhang Q, Sun L, Li C, Huang W, Yuan Y, Duan Y, Diao R, et al: Identification of Ube2b as a novel target of androgen receptor in mouse sertoli cells. Biol Reprod 89: 32, 2013.
31. Burris TP, Guo W and McCabe ER: The gene responsible for adrenal hypoplasia congenita, DAX-1, encodes a nuclear hormone receptor that defines a new class within the superfamily. Recent Prog Horm Res 51: 241-260, 1996.
32. Giguère V: Orphan nuclear receptors: from gene to function. Endocr Rev 20: 689-725, 1999.
33. Iyer AK and McCabe ER: Molecular mechanisms of DAX1 action. Mol Genet Metab 83: 60-73, 2004.
34. Jeffs B, Ito M, Yu RN, Martinson FA, Wang ZJ, Doglio LT and Jameson JL: Sertoli cell-specific rescue of fertility, but not testicular pathology, in Dax1 (Ahch)-deficient male mice. Endocrinology 142: 2481-2488, 2001.
35. Kotaja N, Vihinen M, Palvimo JJ and Jänne OA: Androgen receptor-interacting protein 3 and other PIAS proteins cooperate with glucocorticoid receptor-interacting protein 1 in steroid receptor-dependent signaling. J Biol Chem 277: 17781-17788, 2002.
36. Yu X, Li P, Roeder RG and Wang Z: Inhibition of androgen receptor-mediated transcription by amino-terminal enhancer of split. Mol Cell Biol 21: 4614-4625, 2001.
37. Reutens AT, Fu M, Wang C, Albanese C, McPhaul MJ, Sun Z, Balk SP, Jänne OA, Palvimo JJ and Pestell RG: Cyclin D1 binds the androgen receptor and regulates hormone-dependent signaling in a p300/CBP-associated factor (P/CAF)-dependent manner. Mol Endocrinol 15: 797-811, 2001.
38. Hayes SA, Zarnegar M, Sharma M, Yang F, Peehl DM, ten Dijke P and Sun Z: SMAD3 represses androgen receptor-mediated transcription. Cancer Res 61: 2112-2118, 2001.
39. Lin HK, Yeh S, Kang HY and Chang C: Akt suppresses androgen-induced apoptosis by phosphorylating and inhibiting androgen receptor. Proc Natl Acad Sci USA 98: 7200-7205, 2001.
40. Yang F, Li X, Sharma M, Zarnegar M, Lim B and Sun Z: Androgen receptor specifically interacts with a novel p21-activated kinase, PAK6. J Biol Chem 276: 15345-15353, 2001.
41. Poukka H, Karvonen U, Janne OA and Palvimo JJ: Covalent modification of the androgen receptor by small ubiquitin-like modifier 1 (SUMO-1). Proc Natl Acad Sci USA 97: 14145-14150, 2000.
42. Zhang H, Thomsen JS, Johansson L, Gustafsson JA and Treuter E: DAX-1 functions as an LXXLL-containing corepressor for activated estrogen receptors. J Biol Chem 275: 39855-39859, 2000.
43. Ito M, Yu R and Jameson JL: DAX-1 inhibits SF-1-mediated transactivation via a carboxy-terminal domain that is deleted in adrenal hypoplasia congenita. Mol Cell Biol 17: 1476-1483, 1997.
44. Altincicek B, Tenbaum SP, Dressel U, Thormeyer D, Renkawitz R and Baniahmad A: Interaction of the corepressor Alien with DAX-1 is abrogated by mutations of DAX-1 involved in adrenal hypoplasia congenita. J Biol Chem 275: 7662-7667, 2000.
45. Crawford PA, Dorn C, Sadovsky Y and Milbrandt J: Nuclear receptor DAX-1 recruits nuclear receptor corepressor N-CoR to steroidogenic factor 1. Mol Cell Biol 18: 2949-2956, 1998.
46. Yong EL, Lim J, Qi W, Ong V and Mifsud A: Molecular basis of androgen receptor diseases. Ann Med 32: 15-22, 2000.
47. Thompson J, Saatcioglu F, Jänne OA and Palvimo JJ: Disrupted amino-and carboxyl-terminal interactions of the androgen receptor are linked to androgen insensitivity. Mol Endocrinol 15: 923-935, 2001.
48. Beilin J, Ball EM, Favaloro JM and Zajac JD: Effect of the androgen receptor CAG repeat polymorphism on transcriptional activity: Specificity in prostate and non-prostate cell lines. J Mol Endocrinol 25: 85-96, 2000.
49. Slagsvold T, Kraus I, Bentzen T, Palvimo J and Saatcioglu F: Mutational analysis of the androgen receptor AF-2 (activation function 2) core domain reveals functional and mechanistic differences of conserved residues compared with other nuclear receptors. Mol Endocrinol 14: 1603-1617, 2000.
50. Reutens AT, Achermann JC, Ito M, Ito M, Gu WX, Habiby RL, Donohoue PA, Pang S, Hindmarsh PC and Jameson JL: Clinical and functional effects of mutations in the DAX-1 gene in patients with adrenal hypoplasia congenita. J Clin Endocrinol Metab 84: 504-511, 1999.
51. Muscatelli F, Strom TM, Walker AP, Zanaria E, Récan D, Meindl A, Bardoni B, Guioli S, Zehetner G, Rabl W, et al: Mutations in the DAX-1 gene give rise to both X-linked adrenal hypoplasia congenita and hypogonadotropic hypogonadism. Nature 372: 672-676, 1994.
52. Lalli E, Bardoni B, Zazopoulos E, Wurtz JM, Strom TM, Moras D and Sassone-Corsi P: A transcriptional silencing domain in DAX-1 whose mutation causes adrenal hypoplasia congenita. Mol Endocrinol 11: 1950-1960, 1997.
53. Achermann JC and Jameson JL: Fertility and infertility: genetic contributions from the hypothalamic-pituitary-gonadal axis. Mol Endocrinol 13: 812-818, 1999.