ARID1A Is Essential for Endometrial Function during Early Pregnancy
Endometriosis afflicts about 10% of women of reproductive age and is a major cause of pain and infertility. We showed attenuation of endometrial ARID1A in women with endometriosis as compared to women without endometriosis, and thus hypothesized that ARID1A plays an important role in ensuring normal fertility in the uterus. To test this hypothesis, we generated uterine-specific Arid1a knock-out mice, which were infertile due to defective implantation and decidualization. The mutant mice demonstrated increased endometrial epithelial proliferation with enhanced estrogen signaling and attenuation of epithelial PGR. Microarray and ChIP analysis revealed that Arid1a suppresses epithelial proliferation with PGR by regulating Klf15 expression. These data suggest that Arid1a plays an important role in steroid hormone signaling in endometrial function and dysfunction. Further investigation of ARID1A will be important for understanding altered endometrial function in infertility and endometriosis and in developing therapies for these disorders.
Vyšlo v časopise:
ARID1A Is Essential for Endometrial Function during Early Pregnancy. PLoS Genet 11(9): e32767. doi:10.1371/journal.pgen.1005537
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1005537
Souhrn
Endometriosis afflicts about 10% of women of reproductive age and is a major cause of pain and infertility. We showed attenuation of endometrial ARID1A in women with endometriosis as compared to women without endometriosis, and thus hypothesized that ARID1A plays an important role in ensuring normal fertility in the uterus. To test this hypothesis, we generated uterine-specific Arid1a knock-out mice, which were infertile due to defective implantation and decidualization. The mutant mice demonstrated increased endometrial epithelial proliferation with enhanced estrogen signaling and attenuation of epithelial PGR. Microarray and ChIP analysis revealed that Arid1a suppresses epithelial proliferation with PGR by regulating Klf15 expression. These data suggest that Arid1a plays an important role in steroid hormone signaling in endometrial function and dysfunction. Further investigation of ARID1A will be important for understanding altered endometrial function in infertility and endometriosis and in developing therapies for these disorders.
Zdroje
1. Eskenazi B, Warner ML (1997) Epidemiology of endometriosis. Obstetrics and gynecology clinics of North America 24: 235–258. 9163765
2. Villa ML (1994) Endometriosis. The New England journal of medicine 330: 70.
3. Csapo AI, Pulkkinen M (1978) Indispensability of the human corpus luteum in the maintenance of early pregnancy. Luteectomy evidence. Obstetrical & gynecological survey 33: 69–81.
4. Prapas Y, Prapas N, Jones EE, Duleba AJ, Olive DL, et al. (1998) The window for embryo transfer in oocyte donation cycles depends on the duration of progesterone therapy. Hum Reprod 13: 720–723. 9572441
5. Lydon JP, DeMayo FJ, Funk CR, Mani SK, Hughes AR, et al. (1995) Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 9: 2266–2278. 7557380
6. Martin L, Finn CA, Trinder G (1973) Hypertrophy and hyperplasia in the mouse uterus after oestrogen treatment: an autoradiographic study. J Endocrinol 56: 133–144. 4683406
7. Huet-Hudson YM, Andrews GK, Dey SK (1989) Cell type-specific localization of c-myc protein in the mouse uterus: modulation by steroid hormones and analysis of the periimplantation period. Endocrinology 125: 1683–1690. 2667965
8. Martin L, Das RM, Finn CA (1973) The inhibition by progesterone of uterine epithelial proliferation in the mouse. J Endocrinol 57: 549–554. 4715727
9. Paria BC, Huet-Hudson YM, Dey SK (1993) Blastocyst's state of activity determines the "window" of implantation in the receptive mouse uterus. Proc Natl Acad Sci U S A 90: 10159–10162. 8234270
10. Clarke CL, Sutherland RL (1990) Progestin regulation of cellular proliferation. Endocr Rev 11: 266–301. 2114281
11. Franco HL, Rubel CA, Large MJ, Wetendorf M, Fernandez-Valdivia R, et al. (2012) Epithelial progesterone receptor exhibits pleiotropic roles in uterine development and function. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 26: 1218–1227.
12. Tan J, Paria BC, Dey SK, Das SK (1999) Differential uterine expression of estrogen and progesterone receptors correlates with uterine preparation for implantation and decidualization in the mouse. Endocrinology 140: 5310–5321. 10537162
13. Kaunitz AM (1998) Injectable depot medroxyprogesterone acetate contraception: an update for U.S. clinicians. Int J Fertil Womens Med 43: 73–83. 9609206
14. Olive DL, Lindheim SR, Pritts EA (2004) New medical treatments for endometriosis. Best Pract Res Clin Obstet Gynaecol 18: 319–328. 15157645
15. Bulun SE, Cheng YH, Yin P, Imir G, Utsunomiya H, et al. (2006) Progesterone resistance in endometriosis: link to failure to metabolize estradiol. Mol Cell Endocrinol 248: 94–103. 16406281
16. Kao LC, Germeyer A, Tulac S, Lobo S, Yang JP, et al. (2003) Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology 144: 2870–2881. 12810542
17. Burney RO, Talbi S, Hamilton AE, Vo KC, Nyegaard M, et al. (2007) Gene Expression Analysis of Endometrium Reveals Progesterone Resistance and Candidate Susceptibility Genes in Women with Endometriosis. Endocrinology.
18. Jick SS (1993) Combined estrogen and progesterone use and endometrial cancer. Epidemiology 4: 384. 8347751
19. Ehrlich CE, Young PC, Stehman FB, Sutton GP, Alford WM (1988) Steroid receptors and clinical outcome in patients with adenocarcinoma of the endometrium. Am J Obstet Gynecol 158: 796–807. 2966586
20. Hahn HS, Yoon SG, Hong JS, Hong SR, Park SJ, et al. (2009) Conservative treatment with progestin and pregnancy outcomes in endometrial cancer. Int J Gynecol Cancer 19: 1068–1073. doi: 10.1111/IGC.0b013e3181aae1fb 19820370
21. Ramirez PT, Frumovitz M, Bodurka DC, Sun CC, Levenback C (2004) Hormonal therapy for the management of grade 1 endometrial adenocarcinoma: a literature review. Gynecol Oncol 95: 133–138. 15385122
22. Hoekstra AV, Kim JJ, Keh P, Schink JC (2008) Absence of progesterone receptors in a failed case of fertility-sparing treatment in early endometrial cancer: a case report. J Reprod Med 53: 869–873. 19097521
23. Kim JJ, Chapman-Davis E (2010) Role of progesterone in endometrial cancer. Semin Reprod Med 28: 81–90. doi: 10.1055/s-0029-1242998 20104432
24. Kaku T, Yoshikawa H, Tsuda H, Sakamoto A, Fukunaga M, et al. (2001) Conservative therapy for adenocarcinoma and atypical endometrial hyperplasia of the endometrium in young women: central pathologic review and treatment outcome. Cancer Lett 167: 39–48. 11323097
25. Ness RB (2003) Endometriosis and ovarian cancer: thoughts on shared pathophysiology. Am J Obstet Gynecol 189: 280–294. 12861175
26. Vigano P, Somigliana E, Chiodo I, Abbiati A, Vercellini P (2006) Molecular mechanisms and biological plausibility underlying the malignant transformation of endometriosis: a critical analysis. Human reproduction update 12: 77–89. 16172112
27. Bulun SE (2009) Endometriosis. The New England journal of medicine 360: 268–279. doi: 10.1056/NEJMra0804690 19144942
28. Wiegand KC, Shah SP, Al-Agha OM, Zhao Y, Tse K, et al. (2010) ARID1A mutations in endometriosis-associated ovarian carcinomas. N Engl J Med 363: 1532–1543. doi: 10.1056/NEJMoa1008433 20942669
29. Van Rechem C, Boulay G, Leprince D (2009) HIC1 interacts with a specific subunit of SWI/SNF complexes, ARID1A/BAF250A. Biochemical and biophysical research communications 385: 586–590. doi: 10.1016/j.bbrc.2009.05.115 19486893
30. Guan B, Wang TL, Shih Ie M (2011) ARID1A, a factor that promotes formation of SWI/SNF-mediated chromatin remodeling, is a tumor suppressor in gynecologic cancers. Cancer research 71: 6718–6727. doi: 10.1158/0008-5472.CAN-11-1562 21900401
31. Jones S, Li M, Parsons DW, Zhang X, Wesseling J, et al. (2012) Somatic mutations in the chromatin remodeling gene ARID1A occur in several tumor types. Human mutation 33: 100–103. doi: 10.1002/humu.21633 22009941
32. Huang J, Zhao YL, Li Y, Fletcher JA, Xiao S (2007) Genomic and functional evidence for an ARID1A tumor suppressor role. Genes, chromosomes & cancer 46: 745–750.
33. Gao X, Tate P, Hu P, Tjian R, Skarnes WC, et al. (2008) ES cell pluripotency and germ-layer formation require the SWI/SNF chromatin remodeling component BAF250a. Proc Natl Acad Sci U S A 105: 6656–6661. doi: 10.1073/pnas.0801802105 18448678
34. Lee JH, Kim TH, Oh SJ, Yoo JY, Akira S, et al. (2013) Signal transducer and activator of transcription-3 (Stat3) plays a critical role in implantation via progesterone receptor in uterus. FASEB journal: official publication of the Federation of American Societies for Experimental Biology.
35. Finn CA (1971) The biology of decidual cells. Advances in reproductive physiology 5: 1–26. 4949999
36. Jayatilak PG, Glaser LA, Warshaw ML, Herz Z, Gruber JR, et al. (1984) Relationship between luteinizing hormone and decidual luteotropin in the maintenance of luteal steroidogenesis. Biology of reproduction 31: 556–564. 6487695
37. Lala PK, Graham CH (1990) Mechanisms of trophoblast invasiveness and their control: the role of proteases and protease inhibitors. Cancer metastasis reviews 9: 369–379. 2097085
38. Klemmt PA, Carver JG, Kennedy SH, Koninckx PR, Mardon HJ (2006) Stromal cells from endometriotic lesions and endometrium from women with endometriosis have reduced decidualization capacity. Fertility and sterility 85: 564–572. 16500320
39. Lee CH, Kim TH, Lee JH, Oh SJ, Yoo JY, et al. (2013) Extracellular signal-regulated kinase 1/2 signaling pathway is required for endometrial decidualization in mice and human. PLoS One 8: e75282. doi: 10.1371/journal.pone.0075282 24086495
40. Hewitt SC, Li L, Grimm SA, Winuthayanon W, Hamilton KJ, et al. (2014) Novel DNA motif binding activity observed in vivo with an estrogen receptor alpha mutant mouse. Mol Endocrinol 28: 899–911. doi: 10.1210/me.2014-1051 24713037
41. Ray S, Pollard JW (2012) KLF15 negatively regulates estrogen-induced epithelial cell proliferation by inhibition of DNA replication licensing. Proc Natl Acad Sci U S A 109: E1334–1343. doi: 10.1073/pnas.1118515109 22538816
42. Jones S, Wang TL, Kurman RJ, Nakayama K, Velculescu VE, et al. (2012) Low-grade serous carcinomas of the ovary contain very few point mutations. J Pathol 226: 413–420. doi: 10.1002/path.3967 22102435
43. Guan B, Mao TL, Panuganti PK, Kuhn E, Kurman RJ, et al. (2011) Mutation and loss of expression of ARID1A in uterine low-grade endometrioid carcinoma. The American journal of surgical pathology 35: 625–632. doi: 10.1097/PAS.0b013e318212782a 21412130
44. Jones S, Wang TL, Shih Ie M, Mao TL, Nakayama K, et al. (2010) Frequent mutations of chromatin remodeling gene ARID1A in ovarian clear cell carcinoma. Science 330: 228–231. doi: 10.1126/science.1196333 20826764
45. Kuhn E, Wu RC, Guan B, Wu G, Zhang J, et al. (2012) Identification of molecular pathway aberrations in uterine serous carcinoma by genome-wide analyses. Journal of the National Cancer Institute 104: 1503–1513. doi: 10.1093/jnci/djs345 22923510
46. Kuo KT, Mao TL, Chen X, Feng Y, Nakayama K, et al. (2010) DNA copy numbers profiles in affinity-purified ovarian clear cell carcinoma. Clinical cancer research: an official journal of the American Association for Cancer Research 16: 1997–2008.
47. Wilson BG, Roberts CW (2011) SWI/SNF nucleosome remodellers and cancer. Nature reviews Cancer 11: 481–492. doi: 10.1038/nrc3068 21654818
48. Lowery WJ, Schildkraut JM, Akushevich L, Bentley R, Marks JR, et al. (2012) Loss of ARID1A-associated protein expression is a frequent event in clear cell and endometrioid ovarian cancers. Int J Gynecol Cancer 22: 9–14. doi: 10.1097/IGC.0b013e318231f140 22193641
49. Wang DD, Chen YB, Pan K, Wang W, Chen SP, et al. (2012) Decreased expression of the ARID1A gene is associated with poor prognosis in primary gastric cancer. PLoS One 7: e40364. doi: 10.1371/journal.pone.0040364 22808142
50. Samartzis EP, Noske A, Dedes KJ, Fink D, Imesch P (2013) ARID1A mutations and PI3K/AKT pathway alterations in endometriosis and endometriosis-associated ovarian carcinomas. Int J Mol Sci 14: 18824–18849. doi: 10.3390/ijms140918824 24036443
51. Cancer Genome Atlas Research N, Kandoth C, Schultz N, Cherniack AD, Akbani R, et al. (2013) Integrated genomic characterization of endometrial carcinoma. Nature 497: 67–73. doi: 10.1038/nature12113 23636398
52. Rahman M, Nakayama K, Rahman MT, Katagiri H, Katagiri A, et al. (2013) Clinicopathologic analysis of loss of AT-rich interactive domain 1A expression in endometrial cancer. Human pathology 44: 103–109. doi: 10.1016/j.humpath.2012.04.021 22939958
53. Wiegand KC, Lee AF, Al-Agha OM, Chow C, Kalloger SE, et al. (2011) Loss of BAF250a (ARID1A) is frequent in high-grade endometrial carcinomas. J Pathol 224: 328–333. doi: 10.1002/path.2911 21590771
54. Bulun SE (2009) Endometriosis. The New England journal of medicine 360: 268–279. doi: 10.1056/NEJMra0804690 19144942
55. Soyal SM, Mukherjee A, Lee KY, Li J, Li H, et al. (2005) Cre-mediated recombination in cell lineages that express the progesterone receptor. Genesis 41: 58–66. 15682389
56. Tibbetts TA, Mendoza-Meneses M, O'Malley BW, Conneely OM (1998) Mutual and intercompartmental regulation of estrogen receptor and progesterone receptor expression in the mouse uterus. Biol Reprod 59: 1143–1152. 9780321
57. Lee K, Jeong J, Kwak I, Yu CT, Lanske B, et al. (2006) Indian hedgehog is a major mediator of progesterone signaling in the mouse uterus. Nature genetics 38: 1204–1209. 16951680
58. Kurihara I, Lee DK, Petit FG, Jeong J, Lee K, et al. (2007) COUP-TFII mediates progesterone regulation of uterine implantation by controlling ER activity. PLoS genetics 3: e102. 17590085
59. Braga VM, Gendler SJ (1993) Modulation of Muc-1 mucin expression in the mouse uterus during the estrus cycle, early pregnancy and placentation. Journal of cell science 105 (Pt 2): 397–405. 7691839
60. Jeong JW, Lee KY, Lydon JP, DeMayo FJ (2006) Steroid hormone regulation of Clca3 expression in the murine uterus. The Journal of endocrinology 189: 473–484. 16731779
61. Sundstrom SA, Komm BS, Ponce-de-Leon H, Yi Z, Teuscher C, et al. (1989) Estrogen regulation of tissue-specific expression of complement C3. The Journal of biological chemistry 264: 16941–16947. 2674144
62. Surveyor GA, Gendler SJ, Pemberton L, Das SK, Chakraborty I, et al. (1995) Expression and steroid hormonal control of Muc-1 in the mouse uterus. Endocrinology 136: 3639–3647. 7628404
63. Ward PP, Mendoza-Meneses M, Mulac-Jericevic B, Cunningham GA, Saucedo-Cardenas O, et al. (1999) Restricted spatiotemporal expression of lactoferrin during murine embryonic development. Endocrinology 140: 1852–1860. 10098524
64. Davis RB, Curtis CD, Griffin CT (2013) BRG1 promotes COUP-TFII expression and venous specification during embryonic vascular development. Development 140: 1272–1281. doi: 10.1242/dev.087379 23406903
65. Franco HL, Jeong JW, Tsai SY, Lydon JP, DeMayo FJ (2008) In vivo analysis of progesterone receptor action in the uterus during embryo implantation. Semin Cell Dev Biol 19: 178–186. doi: 10.1016/j.semcdb.2007.12.001 18280760
66. Lee KY, DeMayo FJ (2004) Animal models of implantation. Reproduction 128: 679–695. 15579585
67. Jeong JW, Lee KY, Kwak I, White LD, Hilsenbeck SG, et al. (2005) Identification of murine uterine genes regulated in a ligand-dependent manner by the progesterone receptor. Endocrinology 146: 3490–3505. 15845616
68. Das SK, Chakraborty I, Paria BC, Wang XN, Plowman G, et al. (1995) Amphiregulin is an implantation-specific and progesterone-regulated gene in the mouse uterus. Mol Endocrinol 9: 691–705. 8592515
69. Rubel CA, Franco HL, Jeong JW, Lydon JP, DeMayo FJ (2012) GATA2 is expressed at critical times in the mouse uterus during pregnancy. Gene expression patterns: GEP 12: 196–203. doi: 10.1016/j.gep.2012.03.004 22476030
70. Oh SJ, Kim TH, Lim JM, Jeong JW (2013) Progesterone induces expression of Lrp2 in the murine uterus. Biochemical and biophysical research communications 441: 175–179. doi: 10.1016/j.bbrc.2013.10.037 24140060
71. Li Q, Kannan A, DeMayo FJ, Lydon JP, Cooke PS, et al. (2011) The antiproliferative action of progesterone in uterine epithelium is mediated by Hand2. Science 331: 912–916. doi: 10.1126/science.1197454 21330545
72. Daikoku T, Ogawa Y, Terakawa J, Ogawa A, DeFalco T, et al. (2014) Lactoferrin-iCre: a new mouse line to study uterine epithelial gene function. Endocrinology 155: 2718–2724. doi: 10.1210/en.2014-1265 24823394
73. Contreras CM, Akbay EA, Gallardo TD, Haynie JM, Sharma S, et al. (2010) Lkb1 inactivation is sufficient to drive endometrial cancers that are aggressive yet highly responsive to mTOR inhibitor monotherapy. Disease models & mechanisms 3: 181–193.
74. Kim TH, Lee DK, Cho SN, Orvis GD, Behringer RR, et al. (2013) Critical tumor suppressor function mediated by epithelial Mig-6 in endometrial cancer. Cancer research 73: 5090–5099. doi: 10.1158/0008-5472.CAN-13-0241 23811943
75. Trotter KW, Archer TK (2008) The BRG1 transcriptional coregulator. Nuclear receptor signaling 6: e004. doi: 10.1621/nrs.06004 18301784
76. Inoue H, Giannakopoulos S, Parkhurst CN, Matsumura T, Kono EA, et al. (2011) Target genes of the largest human SWI/SNF complex subunit control cell growth. The Biochemical journal 434: 83–92. doi: 10.1042/BJ20101358 21118156
77. Nagl NG Jr., Wang X, Patsialou A, Van Scoy M, Moran E (2007) Distinct mammalian SWI/SNF chromatin remodeling complexes with opposing roles in cell-cycle control. The EMBO journal 26: 752–763. 17255939
78. Nagl NG Jr., Zweitzig DR, Thimmapaya B, Beck GR Jr., Moran E (2006) The c-myc gene is a direct target of mammalian SWI/SNF-related complexes during differentiation-associated cell cycle arrest. Cancer research 66: 1289–1293. 16452181
79. Tangen IL, Werner HM, Berg A, Halle MK, Kusonmano K, et al. (2014) Loss of progesterone receptor links to high proliferation and increases from primary to metastatic endometrial cancer lesions. European journal of cancer 50: 3003–3010. doi: 10.1016/j.ejca.2014.09.003 25281525
80. Wetendorf M, DeMayo FJ (2014) Progesterone receptor signaling in the initiation of pregnancy and preservation of a healthy uterus. The International journal of developmental biology 58: 95–106. doi: 10.1387/ijdb.140069mw 25023675
81. Lessey BA, Young SL (2014) Homeostasis imbalance in the endometrium of women with implantation defects: the role of estrogen and progesterone. Semin Reprod Med 32: 365–375. doi: 10.1055/s-0034-1376355 24959818
82. Winuthayanon W, Hewitt SC, Orvis GD, Behringer RR, Korach KS (2010) Uterine epithelial estrogen receptor alpha is dispensable for proliferation but essential for complete biological and biochemical responses. Proc Natl Acad Sci U S A 107: 19272–19277. doi: 10.1073/pnas.1013226107 20974921
83. Pan H, Deng Y, Pollard JW (2006) Progesterone blocks estrogen-induced DNA synthesis through the inhibition of replication licensing. Proc Natl Acad Sci U S A 103: 14021–14026. 16966611
84. Tong W, Pollard JW (1999) Progesterone inhibits estrogen-induced cyclin D1 and cdk4 nuclear translocation, cyclin E- and cyclin A-cdk2 kinase activation, and cell proliferation in uterine epithelial cells in mice. Mol Cell Biol 19: 2251–2264. 10022912
85. Pan H, Zhu L, Deng Y, Pollard JW (2006) Microarray analysis of uterine epithelial gene expression during the implantation window in the mouse. Endocrinology 147: 4904–4916. 16794013
86. Niklaus AL, Aubuchon M, Zapantis G, Li P, Qian H, et al. (2007) Assessment of the proliferative status of epithelial cell types in the endometrium of young and menopausal transition women. Human reproduction 22: 1778–1788. 17371803
87. Suske G, Bruford E, Philipsen S (2005) Mammalian SP/KLF transcription factors: bring in the family. Genomics 85: 551–556. 15820306
88. Simmen RC, Heard ME, Simmen AM, Montales MT, Marji M, et al. (2015) The Kruppel-like factors in female reproductive system pathologies. Journal of molecular endocrinology 54: R89–R101. doi: 10.1530/JME-14-0310 25654975
89. Heard ME, Simmons CD, Simmen FA, Simmen RC (2014) Kruppel-like factor 9 deficiency in uterine endometrial cells promotes ectopic lesion establishment associated with activated notch and hedgehog signaling in a mouse model of endometriosis. Endocrinology 155: 1532–1546. doi: 10.1210/en.2013-1947 24476135
90. Pabona JM, Simmen FA, Nikiforov MA, Zhuang D, Shankar K, et al. (2012) Kruppel-like factor 9 and progesterone receptor coregulation of decidualizing endometrial stromal cells: implications for the pathogenesis of endometriosis. The Journal of clinical endocrinology and metabolism 97: E376–392. doi: 10.1210/jc.2011-2562 22259059
91. Velarde MC, Geng Y, Eason RR, Simmen FA, Simmen RC (2005) Null mutation of Kruppel-like factor9/basic transcription element binding protein-1 alters peri-implantation uterine development in mice. Biology of reproduction 73: 472–481. 15917344
92. Lee KY, Jeong JW, Wang J, Ma L, Martin JF, et al. (2007) Bmp2 is critical for the murine uterine decidual response. Mol Cell Biol 27: 5468–5478. 17515606
93. Yang Z, Wolf IM, Chen H, Periyasamy S, Chen Z, et al. (2006) FK506-binding protein 52 is essential to uterine reproductive physiology controlled by the progesterone receptor A isoform. Molecular endocrinology 20: 2682–2694. 16873445
94. Tranguch S, Cheung-Flynn J, Daikoku T, Prapapanich V, Cox MB, et al. (2005) Cochaperone immunophilin FKBP52 is critical to uterine receptivity for embryo implantation. Proc Natl Acad Sci U S A 102: 14326–14331. 16176985
95. Kearns AE, Demay MB (2000) BMP-2 induces the expression of activin betaA and follistatin in vitro. Journal of cellular biochemistry 79: 80–88. 10906757
96. Korhonen MO, Symons JP, Hyde BM, Rowan JP, Wilborn WH (1997) Histologic classification and pathologic findings for endometrial biopsy specimens obtained from 2964 perimenopausal and postmenopausal women undergoing screening for continuous hormones as replacement therapy (CHART 2 Study). American journal of obstetrics and gynecology 176: 377–380. 9065185
97. Kim BG, Yoo JY, Kim TH, Shin JH, Langenheim JF, et al. (2015) Aberrant activation of signal transducer and activator of transcription-3 (STAT3) signaling in endometriosis. Hum Reprod 30: 1069–1078. doi: 10.1093/humrep/dev050 25750101
98. Yoo JY, Shin H, Kim TH, Choi WS, Ferguson SD, et al. (2014) CRISPLD2 is a target of progesterone receptor and its expression is decreased in women with endometriosis. PloS one 9: e100481. doi: 10.1371/journal.pone.0100481 24955763
99. Noyes RW, Hertig AT, Rock J (1975) Dating the endometrial biopsy. Am J Obstet Gynecol 122: 262–263. 1155504
100. Finn CA, Martin L (1972) Endocrine control of the timing of endometrial sensitivity to a decidual stimulus. Biology of reproduction 7: 82–86. 5050152
101. Ishibashi H, Suzuki T, Suzuki S, Moriya T, Kaneko C, et al. (2003) Sex steroid hormone receptors in human thymoma. The Journal of clinical endocrinology and metabolism 88: 2309–2317. 12727990
102. Mazur EC, Vasquez YM, Li X, Kommagani R, Jiang L, et al. (2015) Progesterone receptor transcriptome and cistrome in decidualized human endometrial stromal cells. Endocrinology 156: 2239–2253. doi: 10.1210/en.2014-1566 25781565
103. Kim TH, Yoo JY, Kim HI, Gilbert J, Ku BJ, et al. (2014) Mig-6 suppresses endometrial cancer associated with Pten deficiency and ERK activation. Cancer Res 74: 7371–7382. doi: 10.1158/0008-5472.CAN-14-0794 25377472
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2015 Číslo 9
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
Najčítanejšie v tomto čísle
- Arabidopsis AtPLC2 Is a Primary Phosphoinositide-Specific Phospholipase C in Phosphoinositide Metabolism and the Endoplasmic Reticulum Stress Response
- Bridges Meristem and Organ Primordia Boundaries through , , and during Flower Development in
- KLK5 Inactivation Reverses Cutaneous Hallmarks of Netherton Syndrome
- The Chromatin Protein DUET/MMD1 Controls Expression of the Meiotic Gene during Male Meiosis in