Endometrial stromal beta-catenin is required for steroid-dependent mesenchymal-epithelial cross talk and decidualization

Reproductive Biology and Endocrinology

Volumn 10, Issue , 2012, Pages

  Zhang, Ling ^a   Patterson, Amanda L ^b   Zhang, Lihua ^a   Teixeira, Jose M ^a   Pru, James K ^b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Beta catenin; Decidualization; Endometrium; Implantation; Pregnancy; Progesterone; Uterus

Indexed keywords

BETA CATENIN; ESTROGEN; PROGESTERONE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DECIDUALIZATION; EPITHELIUM CELL; FEMALE; GENE DELETION; GENE EXPRESSION; INFERTILITY; MITOSIS; MOUSE; NONHUMAN; PREGNANCY; PSEUDOPREGNANCY; SIGNAL TRANSDUCTION; UTERUS;

ANIMALS; BETA CATENIN; CELL TRANSDIFFERENTIATION; DECIDUA; ENDOMETRIUM; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; ESTROGENS; ESTROUS CYCLE; FEMALE; MICE; MICE, INBRED ICR; MICE, MUTANT STRAINS; MICE, TRANSGENIC; MYOMETRIUM; PLACENTATION; PREGNANCY; PROGESTERONE; PSEUDOPREGNANCY; RANDOM ALLOCATION; SIGNAL TRANSDUCTION; STROMAL CELLS;

MUS;

EID: 84865812003     PISSN: None     EISSN: 14777827     Source Type: Journal    
DOI: 10.1186/1477-7827-10-75     Document Type: Article

References (39)

1. Kurita T, Cooke PS, Cunha GR. Epithelial-stromal tissue interaction in paramesonephric (Mullerian) epithelial differentiation. Dev Biol 2001, 240:194-211. 10.1006/dbio.2001.0458, 11784056.
2. Abrahamsohn PA, Zorn TM. Implantation and decidualization in rodents. J Exp Zool 1993, 266:603-628. 10.1002/jez.1402660610, 8371101.
3. Hewitt SC, Harrell JC, Korach KS. Lessons in estrogen biology from knockout and transgenic animals. Annu Rev Physiol 2005, 67:285-308. 10.1146/annurev.physiol.67.040403.115914, 15709960.
4. O'Brien JE, Peterson TJ, Tong MH, Lee EJ, Pfaff LE, Hewitt SC, Korach KS, Weiss J, Jameson JL. Estrogen-induced proliferation of uterine epithelial cells is independent of estrogen receptor alpha binding to classical estrogen response elements. J Biol Chem 2006, 281:26683-26692. 10.1074/jbc.M601522200, 16847062.
5. Hou X, Tan Y, Li M, Dey SK, Das SK. Canonical Wnt signaling is critical to estrogen-mediated uterine growth. Mol Endocrinol 2004, 18:3035-3049. 10.1210/me.2004-0259, 15358837.
6. Ray S, Xu F, Wang H, Das SK. Cooperative control via lymphoid enhancer factor 1/T cell factor 3 and estrogen receptor-alpha for uterine gene regulation by estrogen. Mol Endocrinol 2008, 22:1125-1140. 10.1210/me.2007-0445, 2366180, 18202148.
7. Grigoryan T, Wend P, Klaus A, Birchmeier W. Deciphering the function of canonical Wnt signals in development and disease: conditional loss- and gain-of-function mutations of beta-catenin in mice. Genes Dev 2008, 22:2308-2341. 10.1101/gad.1686208, 2749675, 18765787.
8. Mikels AJ, Nusse R. Wnts as ligands: processing, secretion and reception. Oncogene 2006, 25:7461-7468. 10.1038/sj.onc.1210053, 17143290.
9. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 2001, 1:4. 10.1186/1471-213X-1-4, 31338, 11299042.
10. Brault V, Moore R, Kutsch S, Ishibashi M, Rowitch DH, McMahon AP, Sommer L, Boussadia O, Kemler R. Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 2001, 128:1253-1264.
11. Kashiwagi A, DiGirolamo CM, Kanda Y, Niikura Y, Esmon CT, Hansen TR, Shioda T, Pru JK. The postimplantation embryo differentially regulates endometrial gene expression and decidualization. Endocrinology 2007, 148:4173-4184. 10.1210/en.2007-0268, 17510242.
12. Szotek PP, Chang HL, Zhang L, Preffer F, Dombkowski D, Donahoe PK, Teixeira J. Adult mouse myometrial label-retaining cells divide in response to gonadotropin stimulation. Stem Cells 2007, 25:1317-1325. 10.1634/stemcells.2006-0204, 17289934.
13. Gavert N, Ben-Ze'ev A. Beta-catenin signaling in biological control and cancer. J Cell Biochem 2007, 102:820-828. 10.1002/jcb.21505, 17854061.
14. Herington JL, Bi J, Martin JD, Bany BM. Beta-catenin (CTNNB1) in the mouse uterus during decidualization and the potential role of two pathways in regulating its degradation. J Histochem Cytochem 2007, 55:963-974. 10.1369/jhc.7A7199.2007, 17533218.
15. Rider V, Isuzugawa K, Twarog M, Jones S, Cameron B, Imakawa K, Fang J. Progesterone initiates Wnt-beta-catenin signaling but estradiol is required for nuclear activation and synchronous proliferation of rat uterine stromal cells. J Endocrinol 2006, 191:537-548. 10.1677/joe.1.07030, 17170212.
16. Haegel H, Larue L, Ohsugi M, Fedorov L, Herrenknecht K, Kemler R. Lack of beta-catenin affects mouse development at gastrulation. Development 1995, 121:3529-3537.
17. Jamin SP, Arango NA, Mishina Y, Hanks MC, Behringer RR. Requirement of Bmpr1a for Mullerian duct regression during male sexual development. Nat Genet 2002, 32:408-410. 10.1038/ng1003, 12368913.
18. Arango NA, Szotek PP, Manganaro TF, Oliva E, Donahoe PK, Teixeira J. Conditional deletion of beta-catenin in the mesenchyme of the developing mouse uterus results in a switch to adipogenesis in the myometrium. Dev Biol 2005, 288:276-283. 10.1016/j.ydbio.2005.09.045, 16256976.
19. Deutscher E, Hung-Chang Yao H. Essential roles of mesenchyme-derived beta-catenin in mouse Mullerian duct morphogenesis. Dev Biol 2007, 307:227-236. 10.1016/j.ydbio.2007.04.036, 2020447, 17532316.
20. Martin L, Finn CA. Duration of progesterone treatment required for a stromal response to oestradiol-17-beta in the uterus of the mouse. J Endocrinol 1969, 44:279-280. 10.1677/joe.0.0440279, 5794264.
21. Jeong JW, Lee HS, Franco HL, Broaddus RR, Taketo MM, Tsai SY, Lydon JP, Demayo FJ. Beta-catenin mediates glandular formation and dysregulation of beta-catenin induces hyperplasia formation in the murine uterus. Oncogene 2009, 28:31-40. 10.1038/onc.2008.363, 2646831, 18806829.
22. Zhu L, Pollard JW. Estradiol-17beta regulates mouse uterine epithelial cell proliferation through insulin-like growth factor 1 signaling. Proc Natl Acad Sci 2007, 104:15847-15851. 10.1073/pnas.0705749104, 2000402, 17895382.
23. Chen B, Pan H, Zhu L, Deng Y, Pollard JW. Progesterone inhibits the estrogen-induced phosphoinositide 3-kinase->AKT->GSK-3beta->cyclin D1->pRB pathway to block uterine epithelial cell proliferation. Mol Endocrinol 2005, 19:1978-1990. 10.1210/me.2004-0274, 15845746.
24. Winuthayanon W, Hewitt SC, Orvis GD, Behringer RR, Korach KS. Uterine epithelial estrogen receptor alpha is dispensable for proliferation but essential for complete biological and biochemical responses. Proc Natl Acad Sci 2010, 107:19272-19275. 10.1073/pnas.1013226107, 2984169, 20974921.
25. Martin L, Finn CA. Hormonal regulation of cell division in epithelial and connective tissues of the mouse uterus. J Endocrinol 1968, 41:363-371. 10.1677/joe.0.0410363, 5711112.
26. Franco HL, Dai D, Lee KY, Rubel CA, Roop D, Boerboom D, Jeong JW, Lyson JP, Bagchi IC, Bagchi MK, Demayo FJ. WNT4 is a key regulator of normal postnatal uterine development and progesterone signaling during embryo implanation and decidualization in the mouse. FASEB J 2011, 25:1176-1187. 10.1096/fj.10-175349, 3058697, 21163860.
27. Cloke B, Huhtinen K, Fusi L, Kajihara T, Yliheikkilä M, Ho KK, Teklenburg G, Lavery S, Jones MC, Trew G, Kim JJ, Lam EW, Cartwright JE, Poutanen M, Brosens JJ. The androgen and progesterone receptors regulate distinct gene networks and cellular functions in decidualizing endometrium. Endocrinology 2008, 149:4462-4474. 10.1210/en.2008-0356, 18511503.
28. Simon L, Speiwak KA, Ekman GC, Kim J, Lydon JP, Bagchi MK, Bagchi IC, DeMayo FJ, Cooke PS. Stromal progesterone receptors mediate induction of Indian Hedgehog (IHH) in uterine epithelium and its downstream targets in uterine stroma. Endocrinology 2009, 150:3871-3876. 10.1210/en.2008-1691, 2717869, 19372202.
29. Tan J, Paria BC, Dey SK, Das SK. Differential uterine expression of estrogen and progesterone receptors correlates with uterine preparation for implantation and decidualization in the mouse. Endocrinology 1999, 140:5310-5321. 10.1210/en.140.11.5310, 10537162.
30. Bazer FW, Slayden OD. Progesterone-induced gene expression in uterine epithelia; a myth perpetuated by conventional wisdom. Biol Reprod 2008, 79:1008-1009. 10.1095/biolreprod.108.072702, 18953018.
31. Li Q, Kannan A, DeMayo FJ, Lyson JP, Cooke PS, Yamagishi H, Srivastava D, Bagchi MK, Bagchi IC. The antiproliferative action of progesterone in uterine epithelium is mediated by Hand2. Science 2011, 331:912-916. 10.1126/science.1197454, 3320855, 21330545.
32. Franco HL, Jeong JW, Tsai SY, Lydon JP, DeMayo FJ. In vivo analysis of progesterone receptor action in the uterus during embryo implantation. Semin Cell Dev Biol 2008, 19:178-186. 10.1016/j.semcdb.2007.12.001, 18280760.
33. Khatua A, Wang X, Ding T, Zhang Q, Reese J, DeMayo FJ, Paria BC. Indian hedgehog, but not histidine decarboxylase or amphiregulin, is a progesterone-regulated uterine gene in hamsters. Endocrinology 2006, 147:4079-4092. 10.1210/en.2006-0231, 16794005.
34. Lee K, Jeong J, Kwak I, Yu CT, Lanske B, Soegiarto DW, Toftgard R, Tsai MJ, Tsai S, Lydon JP, DeMayo FJ. Indian hedgehog is a major mediator of progesterone signaling in the mouse uterus. Nat Genet 2006, 38:1204-1209. 10.1038/ng1874, 16951680.
35. Matsumoto H, Zhao X, Das SK, Hogan BL, Dey SK. Indian hedgehog as a progesterone-responsive factor meditating epithelial-mesenchymal interactions in the mouse uterus. Dev Biol 2002, 245:280-290. 10.1006/dbio.2002.0645, 11977981.
36. Jeong JW, Lee KY, Han SJ, Aronow BJ, Lydon JP, O'Malley BW, DeMayo FJ. 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. 10.1210/en.2007-0122, 17556502.
37. Cheon YP, Li Q, Xu X, DeMayo FJ, Bagchi IC, Bagchi MK. A genomic approach to identify novel progesterone receptor regulated pathways in the uterus during implantation. Mol Endocrinol 2002, 16:2853-2871. 10.1210/me.2002-0270, 12456805.
38. Mohamed OA, Jonnaert M, Labelle-Dumais C, Kuroda K, Clarke HJ, Dufort D. Uterine Wnt/beta-catenin signaling is required for implantation. Proc Natl Acad Sci 2005, 102:8579-8584. 10.1073/pnas.0500612102, 1150820, 15930138.
39. Tanwar PS, Zhang L, Roberts DJ, Teixeira JM. Stromal deletion of the APC tumor suppressor in mice triggers development of endometrial cancer. Cancer Res 2011, 71:1-13.