Appropriate Crypt Formation in the Uterus for Embryo Homing and Implantation Requires Wnt5a-ROR Signaling

Cell Reports

Volumn 8, Issue 2, 2014, Pages 382-392

  Cha, Jeeyeon ^a   Bartos, Amanda ^a   Park, Craig ^a   Sun, Xiaofei ^a   Li, Yingju ^a   Cha, Sang Wook ^a   Ajima, Rieko ^b,c   Ho, Hsin YiHenry ^d,e   Yamaguchi, Terry P ^b   Dey, Sudhansu K ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c NATIONAL INSTITUTE OF GENETICS   (Japan)

^d HARVARD MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; PROTEIN ROR; UNCLASSIFIED DRUG; WNT5A PROTEIN; RECEPTOR TYROSINE KINASE LIKE ORPHAN RECEPTOR; ROR1 PROTEIN, MOUSE; ROR2 PROTEIN, MOUSE; WNT PROTEIN; WNT5A PROTEIN, MOUSE; BONE MORPHOGENETIC PROTEIN 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLASTOCYST; CELL HOMING; CONTROLLED STUDY; DECIDUALIZATION; DISEASE SEVERITY; EMBRYO DEVELOPMENT; EMBRYO HOMING; FEMALE; FEMALE INFERTILITY; FEMALE SUBFERTILITY; GAIN OF FUNCTION MUTATION; GENE; GENE CONTROL; GENE FUNCTION; GENE INACTIVATION; GENE INTERACTION; LOSS OF FUNCTION MUTATION; MOUSE; MOUSE MODEL; MUTATIONAL ANALYSIS; NIDATION; NONHUMAN; OVARY INSUFFICIENCY; PREGNANCY OUTCOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; REPRODUCTION; ROR GENE; ROR1 GENE; ROR2 GENE; SIGNAL TRANSDUCTION; THIRD TRIMESTER PREGNANCY; UTERUS CRYPT FORMATION; UTERUS FUNCTION; WNT5A GENE; ANIMAL; CYTOLOGY; DECIDUA; EPITHELIUM CELL; GENETICS; METABOLISM; PHYSIOLOGY; WNT SIGNALING PATHWAY; CELL POLARITY; ELECTRON MICROSCOPY; EMBRYO; LITTER SIZE; PROTEIN FUNCTION; UTERUS; UTERUS CAVITY;

MUS;

ANIMALS; DECIDUA; EMBRYO IMPLANTATION; EPITHELIAL CELLS; FEMALE; MICE; RECEPTOR TYROSINE KINASE-LIKE ORPHAN RECEPTORS; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84904816257     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.06.027     Document Type: Article

References (41)

1. Angers S., Moon R.T. Proximal events in Wnt signal transduction. Nat. Rev. Mol. Cell Biol. 2009, 10:468-477.
2. Bayly R., Axelrod J.D. Pointing in the right direction: new developments in the field of planar cell polarity. Nat. Rev. Genet. 2011, 12:385-391.
3. Cha J., Sun X., Dey S.K. Mechanisms of implantation: strategies for successful pregnancy. Nat. Med. 2012, 18:1754-1767.
4. Daikoku T., Cha J., Sun X., Tranguch S., Xie H., Fujita T., Hirota Y., Lydon J., DeMayo F., Maxson R., Dey S.K. Conditional deletion of Msx homeobox genes in the uterus inhibits blastocyst implantation by altering uterine receptivity. Dev. Cell 2011, 21:1014-1025.
5. Das S.K., Wang X.N., Paria B.C., Damm D., Abraham J.A., Klagsbrun M., Andrews G.K., Dey S.K. 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.
6. Dey S.K., Lim H., Das S.K., Reese J., Paria B.C., Daikoku T., Wang H. Molecular cues to implantation. Endocr. Rev. 2004, 25:341-373.
7. Dunlap K.A., Filant J., Hayashi K., Rucker E.B., Song G., Deng J.M., Behringer R.R., DeMayo F.J., Lydon J., Jeong J.W., Spencer T.E. Postnatal deletion of Wnt7a inhibits uterine gland morphogenesis and compromises adult fertility in mice. Biol. Reprod. 2011, 85:386-396.
8. Gao B., Song H., Bishop K., Elliot G., Garrett L., English M.A., Andre P., Robinson J., Sood R., Minami Y., et al. Wnt signaling gradients establish planar cell polarity by inducing Vangl2 phosphorylation through Ror2. Dev. Cell 2011, 20:163-176.
9. Green J.L., Kuntz S.G., Sternberg P.W. Ror receptor tyrosine kinases: orphans no more. Trends Cell Biol. 2008, 18:536-544.
10. Grumolato L., Liu G., Mong P., Mudbhary R., Biswas R., Arroyave R., Vijayakumar S., Economides A.N., Aaronson S.A. Canonical and noncanonical Wnts use a common mechanism to activate completely unrelated coreceptors. Genes Dev. 2010, 24:2517-2530.
11. Ho H.Y., Susman M.W., Bikoff J.B., Ryu Y.K., Jonas A.M., Hu L., Kuruvilla R., Greenberg M.E. Wnt5a-Ror-Dishevelled signaling constitutes a core developmental pathway that controls tissue morphogenesis. Proc. Natl. Acad. Sci. USA 2012, 109:4044-4051.
12. Kikuchi A., Yamamoto H., Sato A., Matsumoto S. New insights into the mechanism of Wnt signaling pathway activation. Int. Rev. Cell Mol. Biol. 2011, 291:21-71.
13. Kirby D.R.S. Blastocyst-Uterine Relationship before and during Implantation. The Biology of the Blastocyst 1971, 393-412. The University of Chicago Press, Chicago. R.J. Blandau (Ed.).
14. 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.
15. Lee K.Y., Jeong J.W., Wang J., Ma L., Martin J.F., Tsai S.Y., Lydon J.P., DeMayo F.J. Bmp2 is critical for the murine uterine decidual response. Mol. Cell. Biol. 2007, 27:5468-5478.
16. Lim H., Paria B.C., Das S.K., Dinchuk J.E., Langenbach R., Trzaskos J.M., Dey S.K. Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 1997, 91:197-208.
17. Lyashenko N., Weissenböck M., Sharir A., Erben R.G., Minami Y., Hartmann C. Mice lacking the orphan receptor ror1 have distinct skeletal abnormalities and are growth retarded. Dev. Dyn. 2010, 239:2266-2277.
18. MacDonald B.T., Tamai K., He X. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell 2009, 17:9-26.
19. Macheda M.L., Sun W.W., Kugathasan K., Hogan B.M., Bower N.I., Halford M.M., Zhang Y.F., Jacques B.E., Lieschke G.J., Dabdoub A., Stacker S.A. The Wnt receptor Ryk plays a role in mammalian planar cell polarity signaling. J.Biol. Chem. 2012, 287:29312-29323.
20. 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.
21. Mikels A., Minami Y., Nusse R. Ror2 receptor requires tyrosine kinase activity to mediate Wnt5A signaling. J.Biol. Chem. 2009, 284:30167-30176.
22. Minami Y., Oishi I., Endo M., Nishita M. Ror-family receptor tyrosine kinases in noncanonical Wnt signaling: their implications in developmental morphogenesis and human diseases. Dev. Dyn. 2010, 239:1-15.
23. Miyoshi H., Ajima R., Luo C.T., Yamaguchi T.P., Stappenbeck T.S. Wnt5a potentiates TGF-β signaling to promote colonic crypt regeneration after tissue injury. Science 2012, 338:108-113.
24. Niehrs C. The complex world of WNT receptor signalling. Nat. Rev. Mol. Cell Biol. 2012, 13:767-779.
25. Nomi M., Oishi I., Kani S., Suzuki H., Matsuda T., Yoda A., Kitamura M., Itoh K., Takeuchi S., Takeda K., et al. Loss of mRor1 enhances the heart and skeletal abnormalities in mRor2-deficient mice: redundant and pleiotropic functions of mRor1 and mRor2 receptor tyrosine kinases. Mol. Cell. Biol. 2001, 21:8329-8335.
26. Paria B.C., Das S.K., Andrews G.K., Dey S.K. Expression of the epidermal growth factor receptor gene is regulated in mouse blastocysts during delayed implantation. Proc. Natl. Acad. Sci. USA 1993, 90:55-59.
27. Paria B.C., Zhao X., Das S.K., Dey S.K., Yoshinaga K. Zonula occludens-1 and E-cadherin are coordinately expressed in the mouse uterus with the initiation of implantation and decidualization. Dev. Biol. 1999, 208:488-501.
28. Paria B.C., Ma W., Tan J., Raja S., Das S.K., Dey S.K., Hogan B.L. Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors. Proc. Natl. Acad. Sci. USA 2001, 98:1047-1052.
29. Psychoyos A. Endocrine control of egg implantation. Handbook of Physiology 1973, 187-215. American Physiology Society, Washington, D.C. E.G.A.R.O. Greep, S.R. Geiger (Eds.).
30. Schambony A., Wedlich D. Wnt-5A/Ror2 regulate expression of XPAPC through an alternative noncanonical signaling pathway. Dev. Cell 2007, 12:779-792.
31. Schlafke S., Enders A.C. Cellular basis of interaction between trophoblast and uterus at implantation. Biol. Reprod. 1975, 12:41-65.
32. Simmons D.G., Rawn S., Davies A., Hughes M., Cross J.C. Spatial and temporal expression of the 23 murine Prolactin/Placental Lactogen-related genes is not associated with their position in the locus. BMC Genomics 2008, 9:352.
33. Song H., Lim H., Das S.K., Paria B.C., Dey S.K. Dysregulation of EGF family of growth factors and COX-2 in the uterus during the preattachment and attachment reactions of the blastocyst with the luminal epithelium correlates with implantation failure in LIF-deficient mice. Mol. Endocrinol. 2000, 14:1147-1161.
34. Song H., Lim H., Paria B.C., Matsumoto H., Swift L.L., Morrow J., Bonventre J.V., Dey S.K. Cytosolic phospholipase A2alpha is crucial [correction of A2alpha deficiency is crucial] for 'on-time' embryo implantation that directs subsequent development. Development 2002, 129:2879-2889.
35. 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.
36. Stewart C.L., Kaspar P., Brunet L.J., Bhatt H., Gadi I., Köntgen F., Abbondanzo S.J. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 1992, 359:76-79.
37. Sun X., Zhang L., Xie H., Wan H., Magella B., Whitsett J.A., Dey S.K. Kruppel-like factor 5 (KLF5) is critical for conferring uterine receptivity to implantation. Proc. Natl. Acad. Sci. USA 2012, 109:1145-1150.
38. van Amerongen R., Nusse R. Towards an integrated view of Wnt signaling in development. Development 2009, 136:3205-3214.
39. Veeman M.T., Axelrod J.D., Moon R.T. A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev. Cell 2003, 5:367-377.
40. Yamaguchi T.P., Bradley A., McMahon A.P., Jones S. A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 1999, 126:1211-1223.
41. Ye X., Hama K., Contos J.J., Anliker B., Inoue A., Skinner M.K., Suzuki H., Amano T., Kennedy G., Arai H., et al. LPA3-mediated lysophosphatidic acid signalling in embryo implantation and spacing. Nature 2005, 435:104-108.