Nuclear receptor, coregulator signaling, and chromatin remodeling pathways suggest involvement of the epigenome in the steroid hormone response of endometrium and abnormalities in endometriosis

Reproductive Sciences

Volumn 19, Issue 2, 2012, Pages 152-162

  Zelenko, Z ^a   Aghajanova, L ^a   Irwin, J C ^a   Giudice, Linda C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

coregulators; DNA methylation; endometriosis; histone deacetylases; nuclear receptors

Indexed keywords

CELL NUCLEUS RECEPTOR; COMPLEMENTARY DNA; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; CYCLIN D1; ESTROGEN RECEPTOR; HISTONE DEACETYLASE 3; NOTCH2 RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROGESTERONE RECEPTOR; RETINOIC ACID INDUCIBLE PROTEIN I; STEROID HORMONE; THYROID HORMONE RECEPTOR; THYROID HORMONE RECEPTOR ALPHA; VITAMIN D RECEPTOR;

ADULT; APOPTOSIS; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DISEASE SEVERITY; DNA METHYLATION; DNA SYNTHESIS; EMBRYO DEVELOPMENT; ENDOMETRIOSIS; ENDOMETRIUM; EPIGENETICS; FEMALE; GENE ACTIVATION; GENOME ANALYSIS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MENSTRUAL CYCLE; MOLECULAR DYNAMICS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PURIFICATION; SCORING SYSTEM; SIGNAL TRANSDUCTION; STROMA CELL; TRANSCRIPTION REGULATION; UPREGULATION;

ADULT; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA METHYLATION; DRUG RESISTANCE; ENDOMETRIOSIS; ENDOMETRIUM; EPIGENESIS, GENETIC; ESTROGENS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; MENSTRUAL CYCLE; MIDDLE AGED; PROGESTINS; RECEPTORS, CALCITRIOL; RECEPTORS, THYROID HORMONE; SIGNAL TRANSDUCTION; YOUNG ADULT;

EID: 84859905212     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719111415546     Document Type: Article

References (49)

1. Auboeuf D, Dowhan DH, Dutertre M, Martin N, Berget SM, O'Malley BW. A subset of nuclear receptor coregulators act as coupling proteins during synthesis and maturation of RNA transcripts. Mol Cell Biol. 2005;25(13):5307- 5316. (Pubitemid 40853570)
2. Fitzpatrick DR, Wilson CB. Methylation and demethylation in the regulation of genes, cells, and responses in the immune system. Clin Immunol. 2003;109(1):37-45. (Pubitemid 37324740)
3. Fuks F. DNA methylation and histone modifications: teaming up to silence genes. Curr Opin Genet Dev. 2005;15(5):490-495. (Pubitemid 41262404)
4. Giudice LC.Clinical practice. Endometriosis. N Engl J Med. 2010;362(25):2389-2398.
5. Eskenazi B, Warner ML. Epidemiology of endometriosis. Obstet Gynecol Clin North Am. 1997;24(2):235-258. (Pubitemid 27225159)
6. Bulun SE. Endometriosis. N Engl J Med. 2009;360(3):268-279.
7. Aghajanova L, Velarde MC, Giudice LC. Altered gene expression profiling in endometrium: evidence for progesterone resistance. Semin Reprod Med. 2010;28(1):51-58.
8. Bain DL, Heneghan AF, Connaghan-Jones KD, Miura MT. Nuclear receptor structure: implications for function. Annu Rev Physiol. 2007;69:201-220. (Pubitemid 46457641)
9. Bulun SE, Cheng YH, Yin P, et al. Progesterone resistance in endometriosis: link to failure to metabolize estradiol. Mol Cell Endocrinol. 2006;248(1-2):94-103.
10. Wu Y, Strawn E, Basir Z, Halverson G, Guo SW. Promoter hypermethylation of progesterone receptor isoform B (PR-B) in endometriosis. Epigenetics. 2006;1(2):106-111.
11. Aghajanova L, Velarde MC, Giudice LC. The progesterone receptor coactivator Hic-5 is involved in the pathophysiology of endometriosis. Endocrinology. 2009;150(8): 3863-3870.
12. Burney RO, Talbi S, Hamilton AE, et al. Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis. Endocrinology. 2007;148(8):3814-3826. (Pubitemid 47105847)
13. Aghajanova L, Giudice LC. Molecular evidence for differences in endometrium in severe versus mild endometriosis. Reprod Sci. 2011;18(3):229-251.
14. Chuang HC, Chang CW, Chang GD, Yao TP, Chen H. Histone deacetylase 3 binds to and regulates the GCMa transcription factor. Nucleic Acids Res. 2006;34(5):1459-1469.
15. Nakai A, Seino S, Sakurai A, Szilak I, Bell GI, DeGroot LJ. Characterization of a thyroid hormone receptor expressed in human kidney and other tissues. Proc Natl Acad Sci U S A. 1988; 85(8):2781-2785.
16. Wang Q, Fujii H, Knipp GT. Expression of PPAR and RXR isoforms in the developing rat and human term placentas. Placenta. 2002;23(8-9):661-671. (Pubitemid 37184675)
17. Kurooka H, Honjo T. Functional interaction between the mouse notch1 intracellular region and histone acetyltransferases PCAF and GCN5. J Biol Chem. 2000;275(22):17211-17220. (Pubitemid 30398970)
18. Leo C, Chen JD. The SRC family of nuclear receptor coactivators. Gene. 2000;245(1):1-11. (Pubitemid 30125358)
19. Wilson BJ, Bates GJ, Nicol SM, Gregory DJ, Perkins ND, Fuller-Pace FV. The p68 and p72 DEAD box RNA helicases interact with HDAC1 and repress transcription in a promoter-specific manner. BMC Mol Biol. 2004;5:11.
20. Aghajanova L, Stavreus-Evers A, Lindeberg M, Landgren BM, Sparre LS, Hovatta O. Thyroid-stimulating hormone receptor and thyroid hormone receptors are involved in human endometrial physiology. Fertil Steril. 2011;95(1):230-237 e232.
21. Hess A, Nayak N, Giudice L. Oviduct and endometrium: cyclic changes in primate oviduct and endometrium. In: Knobil E, Neill J, eds. The Physiology of Reproduction. San Diego: Academic Press; 2005:337-381.
22. Vienonen A, Miettinen S, Blauer M, et al. Expression of nuclear receptors and cofactors in human endometrium and myometrium. J Soc Gynecol Investig. 2004;11(2):104-112. (Pubitemid 38229738)
23. Shiozawa T, Shih HC, Miyamoto T, et al. Cyclic changes in the expression of steroid receptor coactivators and corepressors in the normal human endometrium. J Clin Endocrinol Metab. 2003; 88(2):871-878. (Pubitemid 36207836)
24. Wieser F, Schneeberger C, Hudelist G, et al. Endometrial nuclear receptor co-factors SRC-1 and N-CoR are increased in human endometrium during menstruation. Mol Hum Reprod. 2002;8(7): 644-650. (Pubitemid 34752925)
25. Catalano RD, Critchley HO, Heikinheimo O, et al. Mifepristone induced progesterone withdrawal reveals novel regulatory pathways in human endometrium. Mol Hum Reprod. 2007; 13(9):641-654. (Pubitemid 47354912)
26. Liu XF, Bagchi MK. Recruitment of distinct chromatin-modifying complexes by tamoxifen-complexed estrogen receptor at natural target gene promoters in vivo. J Biol Chem. 2004;279(15): 15050-15058. (Pubitemid 38618898)
27. Hodges-Gallagher L, Valentine CD, Bader SE, Kushner PJ. Inhibition of histone deacetylase enhances the anti-proliferative action of antiestrogens on breast cancer cells and blocks tamoxifen-induced proliferation of uterine cells. Breast Cancer Res Treat. 2007;105(3):297-309. (Pubitemid 47596448)
28. Krusche CA, Vloet AJ, Classen-Linke I, von Rango U, Beier HM, Alfer J. Class I histone deacetylase expression in the human cyclic endometrium and endometrial adenocarcinomas. Hum Reprod. 2007;22(11):2956-2966. (Pubitemid 351696801)
29. Talbi S, Hamilton AE, Vo KC, et al. Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women. Endocrinology. 2006;147(3):1097-1121. (Pubitemid 43244341)
30. Munro SK, Farquhar CM, Mitchell MD, Ponnampalam AP. Epigenetic regulation of endometrium during the menstrual cycle. Mol Hum Reprod. 2010;16(5):297-310.
31. Suzuki A, Horiuchi A, Oka K, Miyamoto T, Kashima H, Shiozawa T. Immunohistochemical detection of steroid receptor cofactors in ovarian endometriosis: involvement of downregulated SRC-1 expression in the limited growth activity of the endometriotic epithelium. Virchows Arch. 2010;456(4):433-441.
32. Uchikawa J, Shiozawa T, Shih HC, et al. Expression of steroid receptor coactivators and corepressors in human endometrial hyperplasia and carcinoma with relevance to steroid receptors and Ki-67 expression. Cancer. 2003;98(10):2207-2213. (Pubitemid 37392425)
33. Jackson TA, Richer JK, Bain DL, Takimoto GS, Tung L, Horwitz KB. The partial agonist activity of antagonist-occupied steroid receptors is controlled by a novel hinge domain-binding coactivator L7/SPA and the corepressors N-CoR or SMRT. Mol Endocrinol. 1997;11(6):693-705. (Pubitemid 27225297)
34. Li H, Leo C, Schroen DJ, Chen JD. Characterization of receptor interaction and transcriptional repression by the corepressor SMRT. Mol Endocrinol. 1997;11(13):2025-2037. (Pubitemid 27524885)
35. Smith CL, Nawaz Z, O'Malley BW. Coactivator and corepressor regulation of the agonist/antagonist activity of the mixed antiestrogen, 4-hydroxytamoxifen. Mol Endocrinol. 1997;11(6): 657-666. (Pubitemid 27225293)
36. Jackson KS, Brudney A, Hastings JM, Mavrogianis PA, Kim JJ, Fazleabas AT. The altered distribution of the steroid hormone receptors and the chaperone immunophilin FKBP52 in a baboon model of endometriosis is associated with progesterone resistance during the window of uterine receptivity. Reprod Sci. 2007;14(2): 137-150. (Pubitemid 351168833)
37. DeMayo FJ, Zhao B, Takamoto N, Tsai SY. Mechanisms of action of estrogen and progesterone. Ann N Y Acad Sci. 2002; 955:48-59; discussion 86-48, 396-406.
38. Xu J, Qiu Y, DeMayo FJ, Tsai SY, Tsai MJ, O'Malley BW. Partial hormone resistance in mice with disruption of the steroid receptor coactivator-1 (SRC-1) gene. Science. 1998;279(5358): 1922-1925. (Pubitemid 28168645)
39. Garcia-Silva S, Aranda A. The thyroid hormone receptor is a suppressor of ras-mediated transcription, proliferation, and transformation. Mol Cell Biol. 2004;24(17):7514-7523. (Pubitemid 39121479)
40. Velarde MC, Aghajanova L, Nezhat CR, Giudice LC. Increased mitogen-activated protein kinase kinase/extracellularly regulated kinase activity in human endometrial stromal fibroblasts of women with endometriosis reduces 3′,5′-cyclic adenosine 5′-monophosphate inhibition of cyclin D1. Endocrinology. 2009;150(10):4701-4712.
41. Jacobs AM, Nicol SM, Hislop RG, Jaffray EG, Hay RT, Fuller-Pace FV. SUMO modification of the DEAD box protein p68 modulates its transcriptional activity and promotes its interaction with HDAC1. Oncogene. 2007;26(40):5866-5876.
42. Fuller-Pace FV. DExD/H box RNA helicases: multifunctional proteins with important roles in transcriptional regulation. Nucleic Acids Res. 2006;34(15):4206-4215. (Pubitemid 44542200)
43. Endoh H, Maruyama K, Masuhiro Y, et al. Purification and identification of p68 RNA helicase acting as a transcriptional coactivator specific for the activation function 1 of human estrogen receptor alpha. Mol Cell Biol. 1999;19(8):5363-5372. (Pubitemid 29339895)
44. Clark EL, Coulson A, Dalgliesh C, et al. The RNA helicase p68 is a novel androgen receptor coactivator involved in splicing and is overexpressed in prostate cancer. Cancer Res. 2008;68(19): 7938-7946.
45. Carter CL, Lin C, Liu CY, Yang L, Liu ZR. Phosphorylated p68 RNA helicase activates Snail1 transcription by promoting HDAC1 dissociation from the Snail1 promoter. Oncogene. 2010;29(39):5427-5436.
46. Santos-Rosa H, Caldas C. Chromatin modifier enzymes, the histone code and cancer. Eur J Cancer. 2005;41(16):2381-2402. (Pubitemid 41540617)
47. Yoo EJ, Chung JJ, Choe SS, Kim KH, Kim JB. Down-regulation of histone deacetylases stimulates adipocyte differentiation. J Biol Chem. 2006;281(10):6608-6615.
48. Guo SW. Epigenetics of endometriosis. Mol Hum Reprod. 2009; 15(10):587-607.
49. Taylor HS, Arici A, Olive D, Igarashi P. HOXA10 is expressed in response to sex steroids at the time of implantation in the human endometrium. J Clin Invest. 1998;101(7):1379-1384. (Pubitemid 28166835)