Update of Wnt signaling in implantation and decidualization

Abstract

Embryonic development into an implantation-competent blastocyst, synchronized uterine transformation into a receptive stage, and an intimate cross-talk between the activated blastocyst and the receptive uterus are essential for successful implantation, and therefore for subsequent pregnancy outcome. Evidence accumulating during recent years has underlined the importance of the Wnt signaling pathway in mammalian implantation and decidualization. Herein, this review focuses on the current state of knowledge regarding Wnt signaling in multiple implantation and decidualization events: pre-implantation embryo development, blastocyst activation for implantation, uterine development, and decidualization.

References Nusse R, Varmus HE. Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell, 1982, 31, 99–109 10.1016/0092-8674(82)90409-3 Rijsewijk F, Schuermann M, Wagenaar E, Parren P, Weigel D, Nusse R. The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell, 1987, 50, 649–657 10.1016/0092-8674(87)90038-9 Nusse R, Brown A, Papkoff J, Scambler P, Shackleford G, McMahon A et al. A new nomenclature for int-1 and related genes: the Wnt gene family. Cell, 1991, 64, 231 10.1016/0092-8674(91)90633-A Riggleman B, Schedl P, Wieschaus E. Spatial expression of the Drosophila segment polarity gene armadillo is posttranscriptionally regulated by wingless. Cell, 1990, 63, 549–560 10.1016/0092-8674(90)90451-J Klingensmith J, Nusse R, Perrimon N. The Drosophila segment polarity gene dishevelled encodes a novel protein required for response to the wingless signal. Genes Dev, 1994, 8, 118–130 10.1101/gad.8.1.118 Peifer M, Pai LM, Casey M. Phosphorylation of the Drosophila adherens junction protein Armadillo: roles for wingless signal and zeste-white 3 kinase. Dev Biol, 1994, 166, 543–556 10.1006/dbio.1994.1336 McMahon AP, Moon RT. Ectopic expression of the proto-oncogene int-1 in Xenopus embryos leads to duplication of the embryonic axis. Cell., 1989, 58, 1075–1084 10.1016/0092-8674(89)90506-0 Clevers H. Wnt/β-catenin signaling in development and disease. Cell, 2006, 127, 469–480 10.1016/j.cell.2006.10.018 Chien AJ, Conrad WH, Moon RT. A Wnt survival guide: from flies to human disease. J Invest Dermatol, 2009, 129, 1614–1627 10.1038/jid.2008.4453125088 Amerongen R, Nusse R. Towards an integrated view of Wnt signaling in development. Development, 2009, 136, 3205–3214 10.1242/dev.033910 Clevers H, Nusse R. Wnt/β-catenin signaling and disease. Cell, 2012, 149, 1192–1205 10.1016/j.cell.2012.05.012 Maruotti N, Corrado A, Neve A, Cantatore FP. Systemic effects of Wnt signaling. J Cell Physiol, 2013, 228, 1428–1432 10.1002/jcp.24326 Wodarz A, Nusse R. Mechanisms of Wnt signaling in development. Annu Rev Cell Dev Biol, 1998, 14, 59–88 10.1146/annurev.cellbio.14.1.59 Teo JL, Kahn M. The Wnt signaling pathway in cellular proliferation and differentiation: a tale of two coactivators. Adv Drug Deliv Rev, 2010, 62, 1149–1155 10.1016/j.addr.2010.09.012 Gordon MD, Nusse R. Wnt signaling: multiple pathways, multiple receptors, and multiple transcription factors. J Biol Chem, 2006, 281, 22429–22433 10.1074/jbc.R600015200 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 10.1016/B978-0-12-386035-4.00002-1 Revel A, Achache H, Stevens J, Smith Y, Reich R. MicroRNAs are associated with human embryo implantation defects. Hum Reprod, 2011, 26, 2830–2840 10.1093/humrep/der255 Saito-Diaz K, Chen TW, Wang X, Thorne CA, Wallace HA, Page-McCaw A et al. The way Wnt works: components and mechanism. Growth Factors, 2013, 31, 1–31 10.3109/08977194.2012.7527373697919 Astudillo P, Larraín J. Wnt signaling and cell-matrix adhesion. Curr Mol Med, 2014, 14, 209–220 10.2174/1566524014666140128105352 Aberle H, Bauer A, Stappert J, Kispert A, Kemler R. β-Catenin is a target for the ubiquitin-proteasome pathway. EMBO J, 1997, 16, 3797–3804 10.1093/emboj/16.13.37971170003 Ikeda S, Kishida S, Yamamoto H, Murai H, Koyama S, Kikuchi A. Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3β and β-catenin and promotes GSK-3β-dependent phosphorylation of β-catenin. EMBO J, 1998, 17, 1371–1384 10.1093/emboj/17.5.13711170485 Liu C, Li Y, Semenov M, Han C, Baeg GH, Tan Y et al. Control of β-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell, 2002, 108, 837–847 10.1016/S0092-8674(02)00685-2 Hurlstone A, Clevers H. T cell factors: turn-ons and turn-offs. EMBO J, 2002, 21, 2303–2311 10.1093/emboj/21.10.2303126013 Bilic J, Huang YL, Davidson G, Zimmermann T, Cruciat CM, Bienz M et al. Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science, 2007, 316, 1619–1622 10.1126/science.1137065 Daniels DL, Weis WI. β-Catenin directly displaces Groucho/TLE repressors from Tcf/Lef in Wnt-mediated transcription activation. Nat Struct Mol Biol, 2005, 12, 364–371 10.1038/nsmb912 Sonderegger S, Pollheimer J, Knöfler M. Wnt signalling in implantation, decidualisation and placental differentiation—review. Placenta, 2010, 31, 839–847 10.1016/j.placenta.2010.07.0112963059 Rao TP, Kühl M. An updated overview on Wnt signaling pathways: a prelude for more. Circ Res, 2010, 106, 1798–1806 10.1161/CIRCRESAHA.110.219840 Rattner A, Hsieh JC, Smallwood PM, Gilbert DJ, Copeland NG, Jenkins NA et al. A family of secreted proteins contains homology to the cysteine-rich ligand-binding domain of Frizzled receptors. Proc Natl Acad Sci USA, 1997, 94, 2859–2863 10.1073/pnas.94.7.285920287 Glinka A, Wu W, Delius H, Monaghan AP, Blumenstock C, Niehrs C. Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature, 1998, 391, 357–362 10.1038/34848 Bafico A, Liu G, Yaniv A, Gazit A, Aaronson SA. Novel mechanism of Wnt signalling inhibition mediated by Dickkopf-1 interaction with LRP6/Arrow. Nat Cell Biol, 2001, 3, 683–686 10.1038/35083081 Mao B, Wu W, Li Y, Hoppe D, Stannek P, Glinka A et al. LDL-receptor-related protein 6 is a receptor for Dickkopf proteins. Nature, 2001, 411, 321–325 10.1038/35077108 Dijksterhuis JP, Petersen J, Schulte G. WNT/Frizzled signalling: receptor-ligand selectivity with focus on FZD-G protein signalling and its physiological relevance: IUPHAR review 3. Br J Pharmacol, 2014, 171, 1195–1209 10.1111/bph.123643952798 Semenov MV, Habas R, Macdonald BT, He X. Snapshot: noncanonical Wnt signaling pathways. Cell, 2007, 131, 1378 10.1016/j.cell.2007.12.011 Topol L, Jiang X, Choi H, Garrett-Beal L, Carolan PJ, Yang Y. Wnt5a inhibits the canonical Wnt pathway by promoting GSK-3-independent β-catenin degradation. J Cell Biol, 2003, 162, 899–908 10.1083/jcb.2003031582172823 Weidinger G, Moon RT. When Wnts antagonize Wnts. J Cell Biol, 2003, 162, 753–755 10.1083/jcb.2003071812172824 Stoick-Cooper CL, Weidinger G, Riehle KJ, Hubbert C, Major MB, Fausto N et al. Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Development, 2007, 134, 479–489 10.1242/dev.001123 Komiya Y, Habas R. Wnt signal transduction pathways. Organogenesis, 2008, 4, 68–75 10.4161/org.4.2.58512634250 Niehrs C. The complex world of Wnt receptor signalling. Nat Rev Mol Cell Biol, 2012, 13, 767–779 10.1038/nrm3470 Wang Y. Wnt/Planar cell polarity signaling: a new paradigm for cancer therapy. Mol Cancer Ther, 2009, 8, 2103–2109 10.1158/1535-7163.MCT-09-0282 Slusarski DC, Corces VG, Moon RT. Interaction of Wnt and a Frizzled homologue triggers G-protein-linked phosphatidylinositol signalling. Nature, 1997, 390, 410–413 10.1038/37138 Hendrickx M, Leyns L. Non-conventional Frizzled ligands and Wnt receptors. Dev Growth Differ, 2008, 50, 229–243 10.1111/j.1440-169X.2008.01016.x Wang H, Dey SK. Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet, 2006, 7, 185–199 10.1038/nrg1808 Chen Q, Zhang Y, Lu J, Wang Q, Wang S, Cao Y et al. Embryo-uterine cross-talk during implantation: the role of Wnt signaling. Mol Hum Reprod, 2009, 15, 215–221 10.1093/molehr/gap009 Harwood BN, Cross SK, Radford EE, Haac BE, Vries WN. Members of the Wnt signaling pathways are widely expressed in mouse ovaries, oocytes, and cleavage stage embryos. Dev Dyn, 2008, 237, 1099–1111 10.1002/dvdy.21491 Lloyd S, Fleming TP, Collins JE. Expression of Wnt genes during mouse preimplantation development. Gene Expr Patterns, 2003, 3, 309–312 10.1016/S1567-133X(03)00046-2 Mohamed OA, Dufort D, Clarke HJ. Expression and estradiol regulation of Wnt genes in the mouse blastocyst identify a candidate pathway for embryo-maternal signaling at implantation. Biol Reprod, 2004, 71, 417–424 10.1095/biolreprod.103.025692 Kemp C, Willems E, Abdo S, Lambiv L, Leyns L. Expression of all Wnt genes and their secreted antagonists during mouse blastocyst and postimplantation development. Dev Dyn, 2005, 233, 1064–1075 10.1002/dvdy.20408 Wang QT, Piotrowska K, Ciemerych MA, Milenkovic L, Scott MP, Davis RW et al. A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. Dev Cell, 2004, 6, 133–144 10.1016/S1534-5807(03)00404-0 Xie H, Tranguch S, Jia X, Zhang H, Das SK, Dey SK et al. Inactivation of nuclear Wnt/β-catenin signaling limits blastocyst competency for implantation. Development, 2008, 135, 717–727 10.1242/dev.0153392829274 Haegel H, Larue L, Ohsugi M, Fedorov L, Herrenknecht K, Kemler R. Lack of β-catenin affects mouse development at gastrulation. Development, 1995, 121, 3529–3537 Huelsken J, Vogel R, Brinkmann V, Erdmann B, Birchmeier C, Birchmeier W. Requirement for β-catenin in anterior-posterior axis formation in mice. J Cell Biol, 2000, 148, 567–578 10.1083/jcb.148.3.5672174807 Vries WN, Evsikov AV, Haac BE, Fancher KS, Holbrook AE, Kemler R et al. Maternal β-catenin and E-cadherin in mouse development. Development, 2004, 131, 4435–4445 10.1242/dev.01316 Landeira D, Bagci H, Malinowski AR, Brown KE, Soza-Ried J, Feytout A et al. Jarid2 coordinates nanog expression and PCP/Wnt signaling required for efficient ESC differentiation and early embryo development. Cell Rep., 2015, 12, 573–586 10.1016/j.celrep.2015.06.0604534826 Gao C, Chen YG. Dishevelled: the hub of Wnt signaling. Cell Signal, 2010, 22, 717–727 10.1016/j.cellsig.2009.11.021 Na J, Lykke-Andersen K, Torres Padilla ME, Zernicka-Goetz M. Dishevelled proteins regulate cell adhesion in mouse blastocyst and serve to monitor changes in Wnt signaling. Dev Biol, 2007, 302, 40–49 10.1016/j.ydbio.2006.08.0363353122 Wansleeben C, Meijlink F. The planar cell polarity pathway in vertebrate development. Dev Dyn, 2011, 240, 616–626 10.1002/dvdy.22564 Horst PH, Wang Y, Zee M, Burger CW, Blok LJ. Interaction between sex hormones and Wnt/β-catenin signal transduction in endometrial physiology and disease. Mol Cell Endocrinol, 2012, 358, 176–184 10.1016/j.mce.2011.06.010 Cooke PS, Spencer TE, Bartol FF, Hayashi K. Uterine glands: development, function and experimental model systems. Mol Hum Reprod, 2013, 19, 547–558 10.1093/molehr/gat0313749806 Hayashi K, Yoshioka S, Reardon SN, Rucker EB, Spencer TE, DeMayo FJ et al. WNTs in the neonatal mouse uterus: potential regulation of endometrial gland development. Biol Reprod, 2011, 84, 308–319 10.1095/biolreprod.110.0881613071266 Wetendorf M, DeMayo FJ. The progesterone receptor regulates implantation, decidualization, and glandular development via a complex paracrine signaling network. Mol Cell Endocrinol, 2012, 357, 108–118 10.1016/j.mce.2011.10.0283443857 Vainio S, Heikkilä M, Kispert A, Chin N, McMahon AP. Female development in mammals is regulated by Wnt4 signalling. Nature, 1999, 397, 405–409 10.1038/17068 Franco HL, Dai D, Lee KY, Rubel CA, Roop D, Boerboom D et al. 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 10.1096/fj.10-1753493058697 Miller C, Sassoon DA. Wnt7a maintains appropriate uterine patterning during the development of the mouse female reproductive tract. Development, 1998, 125, 3201–3211 Dunlap KA, Filant J, Hayashi K, Rucker EB, Song G, Deng JM et al. Postnatal deletion of Wnt7a inhibits uterine gland morphogenesis and compromises adult fertility in mice. Biol Reprod, 2011, 85, 386–396 10.1095/biolreprod.111.0917693142262 Mericskay M, Kitajewski J, Sassoon D. Wnt5a is required for proper epithelial-mesenchymal interactions in the uterus. Development, 2004, 131, 2061–2072 10.1242/dev.01090 Jeong JW, Lee HS, Franco HL, Broaddus RR, Taketo MM, Tsai SY et al. β-Catenin mediates glandular formation and dysregulation of β-catenin induces hyperplasia formation in the murine uterus. Oncogene, 2009, 28, 31–40 10.1038/onc.2008.3632646831 Arango NA, Szotek PP, Manganaro TF, Oliva E, Donahoe PK, Teixeira J. Conditional deletion of β-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 Deutscher E, Hung-Chang Yao H. Essential roles of mesenchyme-derived β-catenin in mouse Müllerian duct morphogenesis. Dev Biol, 2007, 307, 227–236 10.1016/j.ydbio.2007.04.0362020447 Das SK. Cell cycle regulatory control for uterine stromal cell decidualization in implantation. Reproduction, 2009, 137, 889–899 10.1530/REP-08-0539 Gellersen B, Brosens JJ. Cyclic decidualization of the human endometrium in reproductive health and failure. Endocr Rev, 2014, 35, 851–905 10.1210/er.2014-1045 Hayashi K, Erikson DW, Tilford SA, Bany BM, Maclean JA, Rucker EB et al. Wnt genes in the mouse uterus: potential regulation of implantation. Biol Reprod, 2009, 80, 989–1000 10.1095/biolreprod.108.0754162804842 Wang Q, Lu J, Zhang S, Wang S, Wang W, Wang B et al. Wnt6 is essential for stromal cell proliferation during decidualization in mice. Biol Reprod, 2013, 88, 5 10.1095/biolreprod.112.104687 Hatta K, Chen Z, Carter AL, Leno-Durán E, Zhang J, Ruiz-Ruiz C et al. Orphan receptor kinase ROR2 is expressed in the mouse uterus. Placenta, 2010, 31, 327–333 10.1016/j.placenta.2010.01.012 Herington JL, Bi J, Martin JD, Bany BM. β-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 Paria BC, Ma W, Tan J, Raja S, Das SK, Dey SK et al. 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 10.1073/pnas.98.3.104714706 Aoki K, Taketo MM. Tissue-specific transgenic, conditional knockout and knock-in mice of genes in the canonical Wnt signaling pathway. Methods Mol Biol, 2008, 468, 307–331 10.1007/978-1-59745-249-6_24 Zhang L, Patterson AL, Teixeira JM, Pru JK. Endometrial stromal β-catenin is required for steroid-dependent mesenchymal-epithelial cross talk and decidualization. Reprod Biol Endocrinol, 2012, 10, 75 10.1186/1477-7827-10-753462133 Li Q, Kannan A, Wang W, Demayo FJ, Taylor RN, Bagchi MK et al. 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 10.1074/jbc.M704723200 Lee KY, Jeong JW, Wang J, Ma L, Martin JF, Tsai SY et al. Bmp2 is critical for the murine uterine decidual response. Mol Cell Biol, 2007, 27, 5468–5478 10.1128/MCB.00342-071952078 Li Q, Kannan A, Das A, Demayo FJ, Hornsby PJ, Young SL et al. Wnt-4 acts downstream of Bmp2 and functions via β-catenin signaling pathway to regulate human endometrial stromal cell differentiation. Endocrinology, 2013, 154, 446–457 10.1210/en.2012-15853529366 Carson DD, Lagow E, Thathiah A, Al-Shami R, Farach-Carson MC, Vernon M et al. Changes in gene expression during the early to mid-luteal (receptive phase) transition in human endometrium detected by high-density microarray screening. Mol Hum Reprod, 2002, 8, 871–879 10.1093/molehr/8.9.871 Kao LC, Tulac S, Lobo S, Imani B, Yang JP, Germeyer A et al. Global gene profiling in human endometrium during the window of implantation. Endocrinology, 2002, 143, 2119–2138 10.1210/endo.143.6.8885 Duncan WC, Shaw JL, Burgess S, McDonald SE, Critchley HO, Horne AW. Ectopic pregnancy as a model to identify endometrial genes and signaling pathways important in decidualization and regulated by local trophoblast. PLoS One, 2011, 6, e23595 10.1371/journal.pone.00235953157392 Liu Y, Kodithuwakku SP, Ng PY, Chai J, Ng EH, Yeung WS et al. 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 10.1093/humrep/dep429 Timeva T, Shterev A, Kyurkchiev S. Recurrent implantation failure: the role of the endometrium. J Reprod Infertil., 2014, 15, 173–1834227974 Larsen EC, Christiansen OB, Kolte AM, Macklon N. New insights into mechanisms behind miscarriage. BMC Med, 2013, 11, 154 10.1186/1741-7015-11-1543699442 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 10.1093/humrep/dep193 Bao SH, Shuai W, Tong J, Wang L, Chen P, Duan T. Increased Dickkopf-1 expression in patients with unexplained recurrent spontaneous miscarriage. Clin Exp Immunol, 2013, 172, 437–443 10.1111/cei.120663646443 Li S, Li N, Zhu P, Wang Y, Tian Y, Wang X. Decreased β-catenin expression in first-trimester villi and decidua of patients with recurrent spontaneous abortion. J Obstet Gynaecol Res, 2015, 41, 904–911 10.1111/jog.12647