Expression of retinoic acid-related orphan receptor alpha and its responsive genes in human endometrium regulated by cholesterol sulfate

Journal of Steroid Biochemistry and Molecular Biology

Volumn 128, Issue 1-2, 2012, Pages 21-28

  Zenri, Fumiko ^a   Hiroi, Hisahiko ^a   Momoeda, Mikio ^a,b   Tsutsumi, Ryo ^a   Hosokawa, Yumi ^a   Koizumi, Minako ^a   Nakae, Hanako ^a   Osuga, Yutaka ^a   Yano, Tetsu ^a   Taketani, Yuji ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b ST LUKE'S INTERNATIONAL HOSPITAL   (Japan)

Author keywords

Cholesterol sulfate; NR1D1; Retinoic acid related orphan receptor alpha (RORA)

Indexed keywords

CHOLESTEROL SULFATE; COMPLEMENTARY DNA; NUCLEAR RECEPTOR NR1D1; RETINOID RELATED ORPHAN RECEPTOR ALPHA;

ADULT; ARTICLE; DNA SYNTHESIS; ENDOMETRIUM; ENDOMETRIUM CELL; FEMALE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; PLASMID; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; STEROIDOGENESIS; SURFACE PLASMON RESONANCE;

ADULT; CELLS, CULTURED; CHOLESTEROL ESTERS; ENDOMETRIUM; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION; GENES, REPORTER; HUMANS; LUCIFERASES, RENILLA; MIDDLE AGED; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP D, MEMBER 1; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 1; PRIMARY CELL CULTURE; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECOMBINANT PROTEINS; STROMAL CELLS; TRANSCRIPTIONAL ACTIVATION;

ORYCTOLAGUS CUNICULUS;

EID: 82755197059     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2011.10.001     Document Type: Article

References (43)

1. M. Momoeda, Y. Taketani, M. Mizuno, M. Iwamori, and Y. Nagai Characteristic expression of cholesterol sulfate in rabbit endometrium during the implantation period Biochem. Biophys. Res. Commun. 178 1991 145 150
2. K. Kubushiro, K. Kojima, M. Mikami, S. Nozawa, R. Iizuka, M. Iwamori, and Y. Nagai Menstrual cycle-associated alteration of sulfogalactosylceramide in human uterine endometrium: possible induction of glycolipid sulfation by sex steroid hormones Arch. Biochem. Biophys. 268 1989 129 136 (Pubitemid 19038245)
3. M. Momoeda, Y. Cui, Y. Sawada, Y. Taketani, M. Mizuno, and M. Iwamori Pseudopregnancy-dependent accumulation of cholesterol sulfate due to up-regulation of cholesterol sulfotransferase and concurrent down-regulation of cholesterol sulfate sulfatase in the uterine endometria of rabbits J. Biochem. 116 1994 657 662 (Pubitemid 24294798)
4. M. Koizumi, M. Momoeda, H. Hiroi, Y. Hosokawa, R. Tsutsumi, Y. Osuga, T. Yano, and Y. Taketani Expression and regulation of cholesterol sulfotransferase (SULT2B1b) in human endometrium Fertil. Steril. 93 2010 1538 1544
5. C.A. Strott, and Y. Higashi Cholesterol sulfate in human physiology: what's it all about? J. Lipid Res. 44 2003 1268 1278 (Pubitemid 37279607)
6. T. Sugawara, E. Nomura, and N. Hoshi Cholesterol sulphate affects production of steroid hormones by reducing steroidogenic acute regulatory protein level in adrenocortical cells J. Endocrinol. 195 2007 451 458
7. R. Tsutsumi, H. Hiroi, M. Momoeda, Y. Hosokawa, F. Nakazawa, M. Koizumi, T. Yano, O. Tsutsumi, and Y. Taketani Inhibitory effects of cholesterol sulfate on progesterone production in human granulosa-like tumor cell line, KGN Endocr. J. 55 2008 575 581 (Pubitemid 351949755)
8. M. Koizumi, M. Momoeda, H. Hiroi, F. Nakazawa, H. Nakae, T. Ohno, T. Yano, and Y. Taketani Inhibition of proteases involved in embryo implantation by cholesterol sulfate Hum. Reprod. 25 2010 192 197
9. H. Nakae, H. Hiroi, M. Momoeda, M. Koizumi, M. Iwamori, and Y. Taketani Inhibition of cell invasion and protease activity by cholesterol sulfate Fertil. Steril. 94 2010 2455 2457
10. F. Bitsch, R. Aichholz, J. Kallen, S. Geisse, B. Fournier, and J.M. Schlaeppi Identification of natural ligands of retinoic acid receptor-related orphan receptor alpha ligand-binding domain expressed in Sf9 cells - a mass spectrometry approach Anal. Biochem. 323 2003 139 149 (Pubitemid 37393367)
11. J. Kallen, J.M. Schlaeppi, F. Bitsch, I. Delhon, and B. Fournier Crystal structure of the human RORalpha Ligand binding domain in complex with cholesterol sulfate at 2.2 A J. Biol. Chem. 279 2004 14033 14038 (Pubitemid 38468938)
12. A.M. Jetten, S. Kurebayashi, and E. Ueda The ROR nuclear orphan receptor subfamily: critical regulators of multiple biological processes Prog. Nucleic Acid Res. Mol. Biol. 69 2001 205 247 (Pubitemid 33804679)
13. V. Gigure, M. Tini, G. Flock, E. Ong, R.M. Evans, and G. Otulakowski Isoform-specific amino-terminal domains dictate DNA-binding properties of ROR alpha, a novel family of orphan hormone nuclear receptors Genes Dev. 8 1994 538 553
14. C. Carlberg, R. Hooft van Huijsduijnen, J.K. Staple, J.F. DeLamarter, and M. Becker-André RZRs, a new family of retinoid-related orphan receptors that function as both monomers and homodimers Mol. Endocrinol. 8 1994 757 770 (Pubitemid 24179668)
15. C.I. Jarvis, B. Staels, B. Brugg, Y. Lemaigre-Dubreuil, A. Tedgui, and J. Mariani Age-related phenotypes in the staggerer mouse expand the RORalpha nuclear receptor's role beyond the cerebellum Mol. Cell. Endocrinol. 186 2002 1 5 (Pubitemid 34189773)
16. M. Akashi, and T. Takumi The orphan nuclear receptor RORalpha regulates circadian transcription of the mammalian core-clock Bmal1 Nat. Struct. Mol. Biol. 12 2005 441 448 (Pubitemid 43085905)
17. E.J. Kim, Y.G. Yoo, W.K. Yang, Y.S. Lim, T.Y. Na, I.K. Lee, and M.O. Lee Transcriptional activation of HIF-1 by RORalpha and its role in hypoxia signaling Arterioscler. Thromb. Vasc. Biol. 28 2008 1796 1802
18. R.D. Koos, A.A. Kazi, M.S. Roberson, and J.M. Jones New insight into the transcriptional regulation of vascular endothelial growth factor expression in the endometrium by estrogen and relaxin Ann. N. Y. Acad. Sci. 1041 2005 233 247 (Pubitemid 41132254)
19. B.M. Forman, J. Chen, B. Blumberg, S.A. Kliewer, R. Henshaw, E.S. Ong, and R.M. Evans Cross-talk among ROR alpha 1 and the Rev-erb family of orphan nuclear receptors Mol. Endocrinol. 8 1994 1253 1261
20. E. Rasp, G. Mautino, C. Duval, C. Fontaine, H. Duez, O. Barbier, D. Monte, J. Fruchart, J.C. Fruchart, and B. Staels Transcriptional regulation of human Rev-erbalpha gene expression by the orphan nuclear receptor retinoic acid-related orphan receptor alpha J. Biol. Chem. 277 2002 49275 49281 (Pubitemid 36014356)
21. P. Gervois, S. Chopin-Delannoy, A. Fadel, G. Dubois, V. Kosykh, J.C. Fruchart, J. Najïb, V. Laudet, and B. Staels Fibrates increase human REV-ERBalpha expression in liver via a novel peroxisome proliferator-activated receptor response element Mol. Endocrinol. 13 1999 400 409 (Pubitemid 29113872)
22. M. Downes, A.J. Carozzi, and G.E. Muscat Constitutive expression of the orphan receptor, Rev-erbA alpha, inhibits muscle differentiation and abrogates the expression of the myoD gene family Mol. Endocrinol. 9 1995 1666 1678
23. I.P. Torra, V. Tsibulsky, F. Delaunay, R. Saladin, V. Laudet, J.C. Fruchart, V. Kosykh, and B. Staels Circadian and glucocorticoid regulation of Rev-erbalpha expression in liver Endocrinology 141 2000 3799 3806
24. G. Triqueneaux, S. Thenot, T. Kakizawa, M.P. Antoch, R. Safi, J.S. Takahashi, F. Delaunay, and V. Laudet The orphan receptor Rev-erbalpha gene is a target of the circadian clock pacemaker J. Mol. Endocrinol. 33 2004 585 608 (Pubitemid 40057557)
25. G. Adelmant, A. Bgue, D. Stéhelin, and V. Laudet A functional Rev-erb alpha responsive element located in the human Rev-erb alpha promoter mediates a repressing activity Proc. Natl. Acad. Sci. U. S. A. 93 1996 3553 3558
26. R.W. Noyes, A.T. Hertig, and J. Rock Dating the endometrial biopsy Am. J. Obstet. Gynecol. 122 1975 262 263
27. Y. Osuga, H. Toyoshima, N. Mitsuhashi, and Y. Taketani The presence of platelet-derived endothelial cell growth factor in human endometrium and its characteristic expression during the menstrual cycle and early gestational period Hum. Reprod. 10 1995 989 993
28. K. Koga, Y. Osuga, O. Tsutsumi, T. Yano, O. Yoshino, Y. Takai, H. Matsumi, H. Hiroi, K. Kugu, M. Momoeda, T. Fujiwara, and Y. Taketani Demonstration of angiogenin in human endometrium and its enhanced expression in endometrial tissues in the secretory phase and the decidua J. Clin. Endocrinol. Metab. 86 2001 5609 5614 (Pubitemid 33070295)
29. Y. Hirota, Y. Osuga, T. Hirata, O. Yoshino, K. Koga, M. Harada, C. Morimoto, E. Nose, T. Yano, O. Tsutsumi, and Y. Taketani Possible involvement of thrombin/protease-activated receptor 1 system in the pathogenesis of endometriosis J. Clin. Endocrinol. Metab. 90 2005 3673 3679 (Pubitemid 41014342)
30. K. Hanley, L. Wood, D.C. Ng, S.S. He, P. Lau, A. Moser, P.M. Elias, D.D. Bikle, M.L. Williams, and K.R. Feingold Cholesterol sulfate stimulates involucrin transcription in keratinocytes by increasing Fra-1, Fra-2, and Jun D J. Lipid Res. 42 2001 390 398 (Pubitemid 32270063)
31. C. Chauvet, B. Bois-Joyeux, and J.L. Danan Retinoic acid receptor-related orphan receptor (ROR) alpha4 is the predominant isoform of the nuclear receptor RORalpha in the liver and is up-regulated by hypoxia in HepG2 human hepatoma cells Biochem. J. 364 2002 449 456 (Pubitemid 34620805)
32. T. Hirata, Y. Osuga, K. Hamasaki, Y. Hirota, E. Nose, C. Morimoto, M. Harada, Y. Takemura, K. Koga, O. Yoshino, T. Tajima, A. Hasegawa, T. Yano, and Y. Taketani Expression of toll-like receptors 2, 3, 4, and 9 genes in the human endometrium during the menstrual cycle J. Reprod. Immunol. 74 2007 53 60 (Pubitemid 46679066)
33. M. Becker-André, E. André, and J.F. DeLamarter Identification of nuclear receptor mRNAs by RT-PCR amplification of conserved zinc-finger motif sequences Biochem. Biophys. Res. Commun. 194 1993 1371 1379 (Pubitemid 23255034)
34. P. Lau, Bailey, D.H. Dowhan, and G.E. Muscat Exogenous expression of a dominant negative RORalpha1 vector in muscle cells impairs differentiation: RORalpha1 directly interacts with p300 and myoD Nucleic Acids Res. 27 1999 411 420 (Pubitemid 29210002)
35. E. Raspé, H. Duez, P. Gervois, C. Fiévet, J.C. Fruchart, S. Besnard, J. Mariani, A. Tedgui, and B. Staels Transcriptional regulation of apolipoprotein C-III gene expression by the orphan nuclear receptor RORalpha J. Biol. Chem. 276 2001 2865 2871
36. N. Vu-Dac, P. Gervois, T. Grötzinger, P. De Vos, K. Schoonjans, J.C. Fruchart, J. Auwerx, J. Mariani, A. Tedgui, and B. Staels Transcriptional regulation of apolipoprotein A-I gene expression by the nuclear receptor RORalpha J. Biol. Chem. 272 1997 22401 22404 (Pubitemid 27386046)
37. P. Delerive, D. Monté, G. Dubois, F. Trottein, J. Fruchart-Najib, J. Mariani, J.C. Fruchart, and B. Staels The orphan nuclear receptor ROR alpha is a negative regulator of the inflammatory response EMBO Rep. 2 2001 42 48 (Pubitemid 32229720)
38. B. Kopmels, J. Mariani, V. Taupin, N. Delhaye-Bouchaud, and E.E. Wollman Differential IL-6 mRNA expression by stimulated peripheral macrophages of Staggerer and Lurcher cerebellar mutant mice Eur. Cytokine Netw. 2 1991 345 353
39. S. Besnard, J.S. Silvestre, M. Duriez, J. Bakouche, Y. Lemaigre-Dubreuil, J. Mariani, B.I. Levy, and A. Tedgui Increased ischemia-induced angiogenesis in the staggerer mouse, a mutant of the nuclear receptor Roralpha Circ. Res. 89 2001 1209 1215 (Pubitemid 34627880)
40. J. Wang, L. Yin, and M.A. Lazar The orphan nuclear receptor Rev-erb alpha regulates circadian expression of plasminogen activator inhibitor type 1 J. Biol. Chem. 281 2006 33842 33848 (Pubitemid 46036596)
41. D.J. Kennaway, T.J. Varcoe, and V.J. Mau Rhythmic expression of clock and clock-controlled genes in the rat oviduct Mol. Hum. Reprod. 9 2003 503 507 (Pubitemid 37220808)
42. J.A. Kallen, J.M. Schlaeppi, F. Bitsch, S. Geisse, M. Geiser, I. Delhon, and B. Fournier X-ray structure of the hRORalpha LBD at 1.63 A: structural and functional data that cholesterol or a cholesterol derivative is the natural ligand of RORalpha Structure 10 2002 1697 1707 (Pubitemid 35452576)
43. S. Balasubramaniam, A. Szanto, and P.D. Roach Circadian rhythm in hepatic low-density-lipoprotein (LDL)-receptor expression and plasma LDL levels Biochem. J. 298 1994 39 43 (Pubitemid 24061539)