Nuclear Receptor Coactivator-6 Attenuates Uterine Estrogen Sensitivity to Permit Embryo Implantation

Developmental Cell

Volumn 23, Issue 4, 2012, Pages 858-865

  Kawagoe, Jun ^a   Li, Qingtian ^a   Mussi, Paola ^a   Liao, Lan ^a   Lydon, John P ^a   DeMayo, Francesco J ^a   Xu, Jianming ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b SOUTHWEST MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MUCIN 1; NUCLEAR RECEPTOR COACTIVATOR; NUCLEAR RECEPTOR COACTIVATOR 6; PROGESTERONE; STEROID RECEPTOR COACTIVATOR 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CORPUS LUTEUM; DECIDUALIZATION; DOWN REGULATION; EMBRYO; ENDOMETRIUM CELL; FEMALE; FEMALE INFERTILITY; GENE DELETION; GENE EXPRESSION; HORMONAL REGULATION; HORMONE SENSITIVITY; MALE; MOUSE; NIDATION; NONHUMAN; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; STROMA CELL; UBIQUITINATION; UTERINE TUBE; UTERUS FUNCTION;

ANIMALS; EMBRYO IMPLANTATION; ESTRADIOL; FEMALE; MALE; MICE; MICE, KNOCKOUT; NUCLEAR RECEPTOR COACTIVATORS; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; UTERUS;

EID: 84867690248     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.09.002     Document Type: Article

References (33)

1. Basir G.S., O W.S., Ng E.H., Ho P.C. Morphometric analysis of peri-implantation endometrium in patients having excessively high oestradiol concentrations after ovarian stimulation. Hum. Reprod. 2001, 16:435-440.
2. Caira F., Antonson P., Pelto-Huikko M., Treuter E., Gustafsson J.A. Cloning and characterization of RAP250, a novel nuclear receptor coactivator. J. Biol. Chem. 2000, 275:5308-5317.
3. Cakmak H., Taylor H.S. Implantation failure: molecular mechanisms and clinical treatment. Hum. Reprod. Update 2011, 17:242-253.
4. Cooke P.S., Buchanan D.L., Young P., Setiawan T., Brody J., Korach K.S., Taylor J., Lubahn D.B., Cunha G.R. Stromal estrogen receptors mediate mitogenic effects of estradiol on uterine epithelium. Proc. Natl. Acad. Sci. USA 1997, 94:6535-6540.
5. Ferdous A., Gonzalez F., Sun L., Kodadek T., Johnston S.A. The 19S regulatory particle of the proteasome is required for efficient transcription elongation by RNA polymerase II. Mol. Cell 2001, 7:981-991.
6. Gregory C.W., Wilson E.M., Apparao K.B., Lininger R.A., Meyer W.R., Kowalik A., Fritz M.A., Lessey B.A. Steroid receptor coactivator expression throughout the menstrual cycle in normal and abnormal endometrium. J. Clin. Endocrinol. Metab. 2002, 87:2960-2966.
7. Hama K., Aoki J., Bandoh K., Inoue A., Endo T., Amano T., Suzuki H., Arai H. Lysophosphatidic receptor, LPA3, is positively and negatively regulated by progesterone and estrogen in the mouse uterus. Life Sci. 2006, 79:1736-1740.
8. Hewitt S.C., Li Y., Li L., Korach K.S. Estrogen-mediated regulation of Igf1 transcription and uterine growth involves direct binding of estrogen receptor alpha to estrogen-responsive elements. J. Biol. Chem. 2010, 285:2676-2685.
9. Jeong J.W., Lee K.Y., Han S.J., Aronow B.J., Lydon J.P., O'Malley B.W., DeMayo F.J. The p160 steroid receptor coactivator 2, SRC-2, regulates murine endometrial function and regulates progesterone-independent and -dependent gene expression. Endocrinology 2007, 148:4238-4250.
10. Kennedy T.G. Intrauterine infusion of prostaglandins and decidualization in rats with uteri differentially sensitized for the decidual cell reaction. Biol. Reprod. 1986, 34:327-335.
11. Ko L., Cardona G.R., Chin W.W. Thyroid hormone receptor-binding protein, an LXXLL motif-containing protein, functions as a general coactivator. Proc. Natl. Acad. Sci. USA 2000, 97:6212-6217.
12. Kuang S.Q., Liao L., Zhang H., Pereira F.A., Yuan Y., DeMayo F.J., Ko L., Xu J. Deletion of the cancer-amplified coactivator AIB3 results in defective placentation and embryonic lethality. J. Biol. Chem. 2002, 277:45356-45360.
13. Kurihara I., Lee D.K., Petit F.G., Jeong J., Lee K., Lydon J.P., DeMayo F.J., Tsai M.J., Tsai S.Y. COUP-TFII mediates progesterone regulation of uterine implantation by controlling ER activity. PLoS Genet. 2007, 3:e102.
14. Large M.J., Demayo F.J. The regulation of embryo implantation and endometrial decidualization by progesterone receptor signaling. Mol. Cell. Endocrinol. 2011, 358:155-165.
15. Lee D.K., Kurihara I., Jeong J.W., Lydon J.P., DeMayo F.J., Tsai M.J., Tsai S.Y. Suppression of ERalpha activity by COUP-TFII is essential for successful implantation and decidualization. Mol. Endocrinol. 2010, 24:930-940.
16. Lee K., Jeong J., Kwak I., Yu C.T., Lanske B., Soegiarto D.W., Toftgard R., Tsai M.J., Tsai S., Lydon J.P., DeMayo F.J. Indian hedgehog is a major mediator of progesterone signaling in the mouse uterus. Nat. Genet. 2006, 38:1204-1209.
17. Lee S.K., Anzick S.L., Choi J.E., Bubendorf L., Guan X.Y., Jung Y.K., Kallioniemi O.P., Kononen J., Trent J.M., Azorsa D., et al. A nuclear factor, ASC-2, as a cancer-amplified transcriptional coactivator essential for ligand-dependent transactivation by nuclear receptors in vivo. J. Biol. Chem. 1999, 274:34283-34293.
18. Li Q., Xu J. Identification and characterization of the alternatively spliced nuclear receptor coactivator-6 isoforms. Int. J. Biol. Sci. 2011, 7:505-516.
19. Li Q., Kannan A., DeMayo F.J., Lydon J.P., Cooke P.S., Yamagishi H., Srivastava D., Bagchi M.K., Bagchi I.C. The antiproliferative action of progesterone in uterine epithelium is mediated by Hand2. Science 2011, 331:912-916.
20. Lonard D.M., Nawaz Z., Smith C.L., O'Malley B.W. The 26S proteasome is required for estrogen receptor-alpha and coactivator turnover and for efficient estrogen receptor-alpha transactivation. Mol. Cell 2000, 5:939-948.
21. Ma W.G., Song H., Das S.K., Paria B.C., Dey S.K. Estrogen is a critical determinant that specifies the duration of the window of uterine receptivity for implantation. Proc. Natl. Acad. Sci. USA 2003, 100:2963-2968.
22. Mahajan M.A., Samuels H.H. A new family of nuclear receptor coregulators that integrate nuclear receptor signaling through CREB-binding protein. Mol. Cell. Biol. 2000, 20:5048-5063.
23. Mahajan M.A., Samuels H.H. Nuclear hormone receptor coregulator: role in hormone action, metabolism, growth, and development. Endocr. Rev. 2005, 26:583-597.
24. Matsumoto H., Zhao X., Das S.K., Hogan B.L., Dey S.K. Indian hedgehog as a progesterone-responsive factor mediating epithelial-mesenchymal interactions in the mouse uterus. Dev. Biol. 2002, 245:280-290.
25. Mussi P., Yu C., O'Malley B.W., Xu J. Stimulation of steroid receptor coactivator-3 (SRC-3) gene overexpression by a positive regulatory loop of E2F1 and SRC-3. Mol. Endocrinol. 2006, 20:3105-3119.
26. Reid G., Hübner M.R., Métivier R., Brand H., Denger S., Manu D., Beaudouin J., Ellenberg J., Gannon F. Cyclic, proteasome-mediated turnover of unliganded and liganded ERalpha on responsive promoters is an integral feature of estrogen signaling. Mol. Cell 2003, 11:695-707.
27. Soyal S.M., Mukherjee A., Lee K.Y., Li J., Li H., DeMayo F.J., Lydon J.P. Cre-mediated recombination in cell lineages that express the progesterone receptor. Genesis 2005, 41:58-66.
28. Tibbetts T.A., Mendoza-Meneses M., O'Malley B.W., Conneely O.M. Mutual and intercompartmental regulation of estrogen receptor and progesterone receptor expression in the mouse uterus. Biol. Reprod. 1998, 59:1143-1152.
29. Valbuena D., Jasper M., Remohí J., Pellicer A., Simón C. Ovarian stimulation and endometrial receptivity. Hum. Reprod. 1999, 14(Suppl 2):107-111.
30. Wang H., Dey S.K. Roadmap to embryo implantation: clues from mouse models. Nat. Rev. Genet. 2006, 7:185-199.
31. Winuthayanon W., Hewitt S.C., Orvis G.D., Behringer R.R., Korach K.S. Uterine epithelial estrogen receptor α is dispensable for proliferation but essential for complete biological and biochemical responses. Proc. Natl. Acad. Sci. USA 2010, 107:19272-19277.
32. Xu J., Wu R.C., O'Malley B.W. Normal and cancer-related functions of the p160 steroid receptor co-activator (SRC) family. Nat. Rev. Cancer 2009, 9:615-630.
33. Zhang H., Liao L., Kuang S.Q., Xu J. Spatial distribution of the messenger ribonucleic acid and protein of the nuclear receptor coactivator, amplified in breast cancer-3, in mice. Endocrinology 2003, 144:1435-1443.