Wnt6 is essential for stromal cell proliferation during decidualization in mice

Biology of Reproduction

Volumn 88, Issue 1, 2013, Pages

  Wang, Qiang ^a,b   Lu, Jinhua ^a,b   Zhang, Shuang ^a,b   Wang, Shumin ^a   Wang, Weixiang ^a   Wang, Bingyan ^a   Wang, Fengchao ^a   Chen, Qi ^a   Duan, Enkui ^a   Leitges, Michael ^c   Kispert, Andreas ^d   Wang, Haibin ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c UNIVERSITY OF OSLO   (Norway)

^d HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Decidualization; Proliferation; Stromal cell; Wnt6

Indexed keywords

CYCLIN B1; WNT6 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLASTOCYST; CELL CULTURE; CELL CYCLE; CELL PROLIFERATION; CONTROLLED STUDY; DECIDUALIZATION; DOWN REGULATION; FEMALE; FIRST TRIMESTER PREGNANCY; MALE; MOUSE; NONHUMAN; POLYPLOIDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STROMA CELL; UPREGULATION; UTERUS;

ANIMALS; CELL CYCLE; CELL PROLIFERATION; EMBRYO IMPLANTATION; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICE, KNOCKOUT; POLYPLOIDY; PREGNANCY; PROTO-ONCOGENE PROTEINS; RNA, MESSENGER; STROMAL CELLS; UTERUS; WNT PROTEINS;

MUS;

EID: 84877026251     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.104687     Document Type: Article

References (44)

1. Lim HJ, Wang H. Uterine disorders and pregnancy complications: insights from mouse models. J Clin Invest 2010; 120:1004-1015.
2. Wang H, Dey SK. Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet 2006; 7:185-199.
3. Das SK, Wang XN, Paria BC, Damm D, Abraham JA, Klagsbrun M, Andrews GK, Dey SK. Heparin-binding EGF-like growth factor gene is induced in the mouse uterus temporally by the blastocyst solely at the site of its apposition: a possible ligand for interaction with blastocyst EGF-receptor in implantation. Development 1994; 120:1071-1083.
4. van Amerongen R, Nusse R. Towards an integrated view of Wnt signaling in development. Development 2009; 136:3205-3214.
5. Wang J, Sinha T, Wynshaw-Boris A. Wnt signaling in mammalian development: lessons from mouse genetics. Cold Spring Harb Perspect Biol 2012; 4:1-16.
6. Chen Q, Zhang Y, Lu J, Wang Q, Wang S, Cao Y, Wang H, Duan E. Embryo-uterine cross-talk during implantation: the role of Wnt signaling. Mol Hum Reprod 2009; 15:215-221.
7. Sonderegger S, Pollheimer J, Knofler M. Wnt signalling in implantation, decidualisation and placental differentiation-review. Placenta 2010; 31:839-847.
8. Daikoku T, Song H, Guo Y, Riesewijk A, Mosselman S, Das SK, Dey SK. Uterine Msx-1 and Wnt4 signaling becomes aberrant in mice with the loss of leukemia inhibitory factor or Hoxa-10: evidence for a novel cytokine-homeobox-Wnt signaling in implantation. Mol Endocrinol 2004; 18:1238-1250.
9. Hayashi K, Erikson DW, Tilford SA, Bany BM, Maclean JA II, Rucker EB III, Johnson GA, Spencer TE. Wnt genes in the mouse uterus: potential regulation of implantation. Biol Reprod 2009; 80:989-1000.
10. 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 U S A 2005; 102:8579-8584.
11. Paria BC, Ma W, Tan J, Raja S, Das SK, Dey SK, Hogan BL. Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors. Proc Natl Acad Sci U S A 2001; 98:1047-1052.
12. Xie H, Tranguch S, Jia X, Zhang H, Das SK, Dey SK, Kuo CJ, Wang H. Inactivation of nuclear Wnt-beta-catenin signaling limits blastocyst competency for implantation. Development 2008; 135:717-727.
13. 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.
14. Franco HL, Dai D, Lee KY, Rubel CA, Roop D, Boerboom D, Jeong JW, Lydon JP, Bagchi IC, Bagchi MK, DeMayo FJ. WNT4 is a key regulator of normal postnatal uterine development and progesterone signaling during embryo implantation and decidualization in the mouse. FASEB J 2011; 25:1176-1187.
15. Macdonald LJ, Sales KJ, Grant V, Brown P, Jabbour HN, Catalano RD. Prokineticin 1 induces Dickkopf 1 expression and regulates cell proliferation and decidualization in the human endometrium. Mol Hum Reprod 2011; 17:626-636.
16. Tulac S, Overgaard MT, Hamilton AE, Jumbe NL, Suchanek E, Giudice LC. Dickkopf-1, an inhibitor of Wnt signaling, is regulated by progesterone in human endometrial stromal cells. J Clin Endocrinol Metab 2006; 91:1453-1461.
17. Liu Y, Kodithuwakku SP, Ng PY, Chai J, Ng EH, Yeung WS, Ho PC, Lee KF. Excessive ovarian stimulation up-regulates the Wnt-signaling molecule DKK1 in human endometrium and may affect implantation: an in vitro co-culture study. Hum Reprod 2010; 25:479-490.
18. Koler M, Achache H, Tsafrir A, Smith Y, Revel A, Reich R. Disrupted gene pattern in patients with repeated in vitro fertilization (IVF) failure. Hum Reprod 2009; 24:2541-2548.
19. Matsuoka A, Kizuka F, Lee L, Tamura I, Taniguchi K, Asada H, Taketani T, Tamura H, Sugino N. Progesterone increases manganese superoxide dismutase expression via a cAMP-dependent signaling mediated by noncanonical Wnt5a pathway in human endometrial stromal cells. J Clin Endocrinol Metab 2010; 95:E291-E299.
20. Hooper M, Hardy K, Handyside A, Hunter S, Monk M. HPRT-deficient (Lesch-Nyhan) mouse embryos derived from germline colonization by cultured cells. Nature 1987; 326:292-295.
21. Paria BC, Huet-Hudson YM, Dey SK. Blastocyst's state of activity determines the "window" of implantation in the receptive mouse uterus. Proc Natl Acad Sci U S A 1993; 90:10159-10162.
22. Lim H, Paria BC, Das SK, Dinchuk JE, Langenbach R, Trzaskos JM, Dey SK. Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 1997; 91:197-208.
23. Kover K, Liang L, Andrews GK, Dey SK. Differential expression and regulation of cytokine genes in the mouse uterus. Endocrinology 1995; 136:1666-1673.
24. Tan Y, Li M, Cox S, Davis MK, Tawfik O, Paria BC, Das SK. HB-EGF directs stromal cell polyploidy and decidualization via cyclin D3 during implantation. Dev Biol 2004; 265:181-195.
25. Mori M, Kitazume M, Ose R, Kurokawa J, Koga K, Osuga Y, Arai S, Miyazaki T. Death effector domain-containing protein (DEDD) is required for uterine decidualization during early pregnancy in mice. J Clin Invest 2011; 121:318-327.
26. Scherle PA, Ma W, Lim H, Dey SK, Trzaskos JM. Regulation of cyclooxygenase-2 induction in the mouse uterus during decidualization. An event of early pregnancy. J Biol Chem 2000; 275:37086-37092.
27. Das SK. Cell cycle regulatory control for uterine stromal cell decidualization in implantation. Reproduction 2009; 137:889-899.
28. Laws MJ, Taylor RN, Sidell N, DeMayo FJ, Lydon JP, Gutstein DE, Bagchi MK, Bagchi IC. Gap junction communication between uterine stromal cells plays a critical role in pregnancy-associated neovascularization and embryo survival. Development 2008; 135:2659-2668.
29. Li Q, Kannan A, Wang W, Demayo FJ, Taylor RN, Bagchi MK, Bagchi IC. Bone morphogenetic protein 2 functions via a conserved signaling pathway involving Wnt4 to regulate uterine decidualization in the mouse and the human. J Biol Chem 2007; 282:31725-31732.
30. Falk S, Wurdak H, Ittner LM, Ille F, Sumara G, Schmid MT, Draganova K, Lang KS, Paratore C, Leveen P, Suter U, Karlsson S, et al. Brain areaspecific effect of TGF-beta signaling on Wnt-dependent neural stem cell expansion. Cell Stem Cell 2008; 2:472-483.
31. Nowakowski RS, Lewin SB, Miller MW. Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J Neurocytol 1989; 18:311-318.
32. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006; 127:469-480.
33. Niehrs C, Acebron SP. Mitotic and mitogenic Wnt signalling. EMBO J 2012; 31:2705-2713.
34. van Amerongen R, Berns A. Knockout mouse models to study Wnt signal transduction. Trends Genet 2006; 22:678-689.
35. Geetha-Loganathan P, Nimmagadda S, Prols F, Patel K, Scaal M, Huang R, Christ B. Ectodermal Wnt-6 promotes Myf5-dependent avian limb myogenesis. Dev Biol 2005; 288:221-233.
36. Shtutman M, Zhurinsky J, Simcha I, Albanese C, D'Amico M, Pestell R, Ben-Ze'ev A. The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc Natl Acad Sci U S A 1999; 96:5522-5527.
37. Tetsu O, McCormick F. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 1999; 398:422-426.
38. Tan J, Raja S, Davis MK, Tawfik O, Dey SK, Das SK. Evidence for coordinated interaction of cyclin D3 with p21 and cdk6 in directing the development of uterine stromal cell decidualization and polyploidy during implantation. Mech Dev 2002; 111:99-113.
39. Ayyanan A, Civenni G, Ciarloni L, Morel C, Mueller N, Lefort K, Mandinova A, Raffoul W, Fiche M, Dotto GP, Brisken C. Increased Wnt signaling triggers oncogenic conversion of human breast epithelial cells by a Notch-dependent mechanism. Proc Natl Acad Sci U S A 2006; 103:3799-3804.
40. Tang L, Zhang Y, Pan H, Luo Q, Zhu XM, Dong MY, Leung PC, Sheng JZ, Huang HF. Involvement of cyclin B1 in progesterone-mediated cell growth inhibition, G2/M cell cycle arrest, and apoptosis in human endometrial cell. Reprod Biol Endocrinol 2009; 7:144.
41. Tang L, Wang TT, Wu YT, Zhou CY, Huang HF. High expression levels of cyclin B1 and Polo-like kinase 1 in ectopic endometrial cells associated with abnormal cell cycle regulation of endometriosis. Fertil Steril 2009; 91:979-987.
42. Vella LA, Yu M, Fuhrmann SR, El-Amine M, Epperson DE, Finn OJ. Healthy individuals have T-cell and antibody responses to the tumor antigen cyclin B1 that when elicited in mice protect from cancer. Proc Natl Acad Sci U S A 2009; 106:14010-14015.
43. Xie H, Wang H, Tranguch S, Iwamoto R, Mekada E, Demayo FJ, Lydon JP, Das SK, Dey SK. Maternal heparin-binding-EGF deficiency limits pregnancy success in mice. Proc Natl Acad Sci U S A 2007; 104:18315-18320.
44. Wang H, Ma WG, Tejada L, Zhang H, Morrow JD, Das SK, Dey SK. Rescue of female infertility from the loss of cyclooxygenase-2 by compensatory up-regulation of cyclooxygenase-1 is a function of genetic makeup. J Biol Chem 2004; 279:10649-10658.