{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,20]],"date-time":"2026-06-20T14:51:21Z","timestamp":1781967081827,"version":"3.54.5"},"reference-count":81,"publisher":"Oxford University Press (OUP)","license":[{"start":{"date-parts":[[2022,6,28]],"date-time":"2022-06-28T00:00:00Z","timestamp":1656374400000},"content-version":"am","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["grant R01 HD088352"],"award-info":[{"award-number":["grant R01 HD088352"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>WNT signaling is important for regulation of embryonic development. The most abundant WNT gene expressed in the bovine endometrium during the preimplantation period is WNT5A. One objective was to determine whether WNT5A regulates competence of the bovine preimplantation embryo to become a blastocyst and alters the number of cells in the inner cell mass and trophectoderm. A second objective was to delineate features of the cell-signaling mechanisms involved in WNT5A actions. WNT5A caused a concentration-dependent increase in the proportion of embryos developing to the blastocyst stage and in the number of inner cell mass cells in the resultant blastocysts. A concentration of 200\u00a0ng\/mL was most effective, and a higher concentration of 400\u00a0ng\/mL was not stimulatory. Bovine serum albumin in culture reduced the magnitude of effects of WNT5A on development to the blastocyst stage. WNT5A affected expression of 173 genes at the morula stage; all were upregulated by WNT5A. Many of the upregulated genes were associated with cell signaling. Actions of WNT5A on development to the blastocyst stage were suppressed by a Rho-associated coiled-coil kinase (ROCK) signaling inhibitor, suggesting that WNT5A acts through Ras homology gene family member A (RhoA)\/ROCK signaling. Other experiments indicated that actions of WNT5A are independent of the canonical \u03b2-catenin signaling pathway and RAC1\/c-Jun N-terminal kinase (JNK) signaling. This is the first report outlining the actions of WNT5A to alter the development of the mammalian embryo. These findings provide insights into how embryokines regulate maternal\u2013embryonic communication.<\/jats:p>","DOI":"10.1093\/biolre\/ioac127","type":"journal-article","created":{"date-parts":[[2022,6,29]],"date-time":"2022-06-29T05:01:33Z","timestamp":1656478893000},"source":"Crossref","is-referenced-by-count":5,"title":["Actions of WNT family member 5A to regulate characteristics of development of the bovine preimplantation embryo"],"prefix":"10.1093","author":[{"given":"Surawich","family":"Jeensuk","sequence":"first","affiliation":[{"name":"Department of Animal Sciences , University of Florida, Gainesville, FL, USA"},{"name":"Department of Livestock Development , Bureau of Biotechnology in Livestock Production, Pathum Thani, Thailand"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M Sofia","family":"Ortega","sequence":"additional","affiliation":[{"name":"Division of Animal Sciences , University of Missouri, Columbia, MO, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Muhammad","family":"Saleem","sequence":"additional","affiliation":[{"name":"Department of Animal Sciences , University of Florida, Gainesville, FL, USA"},{"name":"Department of Theriogenology , Faculty of Veterinary Science, University of Veterinary and Animal Sciences, Lahore, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Briana","family":"Hawryluk","sequence":"additional","affiliation":[{"name":"Department of Animal Sciences , University of Florida, Gainesville, FL, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tracy L","family":"Scheffler","sequence":"additional","affiliation":[{"name":"Department of Animal Sciences , University of Florida, Gainesville, FL, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter J","family":"Hansen","sequence":"additional","affiliation":[{"name":"Department of Animal Sciences , University of Florida, Gainesville, FL, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2022,6,28]]},"reference":[{"key":"2022071901483667700_ref1","doi-asserted-by":"crossref","first-page":"781","DOI":"10.1146\/annurev.cellbio.20.010403.113126","article-title":"The Wnt signaling pathway in development and disease","volume":"20","author":"Logan","year":"2004","journal-title":"Annu Rev Cell Dev Biol"},{"key":"2022071901483667700_ref2","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1007\/978-1-60327-469-2_1","article-title":"Evolution of the Wnt pathways","volume":"469","author":"Croce","year":"2008","journal-title":"Methods Mol Biol"},{"key":"2022071901483667700_ref3","doi-asserted-by":"crossref","first-page":"767","DOI":"10.1038\/nrm3470","article-title":"The complex world of WNT receptor signalling","volume":"13","author":"Niehrs","year":"2012","journal-title":"Nat Rev Mol Cell Biol"},{"key":"2022071901483667700_ref4","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1016\/j.cellsig.2009.11.021","article-title":"Dishevelled: the hub of Wnt signaling","volume":"22","author":"Gao","year":"2010","journal-title":"Cell Signal"},{"key":"2022071901483667700_ref5","doi-asserted-by":"crossref","first-page":"3205","DOI":"10.1242\/dev.033910","article-title":"Towards an integrated view of Wnt signaling in development","volume":"136","author":"Amerongen","year":"2009","journal-title":"Development"},{"key":"2022071901483667700_ref6","doi-asserted-by":"crossref","first-page":"3529","DOI":"10.1242\/dev.121.11.3529","article-title":"Lack of beta-catenin affects mouse development at gastrulation","volume":"121","author":"Haegel","year":"1995","journal-title":"Development"},{"key":"2022071901483667700_ref7","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1242\/dev.015339","article-title":"Inactivation of nuclear Wnt-beta-catenin signaling limits blastocyst competency for implantation","volume":"135","author":"Xie","year":"2008","journal-title":"Development"},{"key":"2022071901483667700_ref8","doi-asserted-by":"crossref","first-page":"711","DOI":"10.1093\/molehr\/gav036","article-title":"WNT3 and membrane-associated \u03b2-catenin regulate trophectoderm lineage differentiation in human blastocysts","volume":"21","author":"Krivega","year":"2015","journal-title":"Mol Hum Reprod"},{"key":"2022071901483667700_ref9","doi-asserted-by":"crossref","first-page":"1266","DOI":"10.1038\/srep01266","article-title":"Canonical WNT signaling regulates development of bovine embryos to the blastocyst stage","volume":"3","author":"Denicol","year":"2013","journal-title":"Sci Rep"},{"key":"2022071901483667700_ref10","doi-asserted-by":"crossref","first-page":"1129","DOI":"10.1093\/biolre\/iox048","article-title":"Consequences of endogenous and exogenous WNT signaling for development of the preimplantation bovine embryo","volume":"96","author":"Tr\u00edbulo","year":"2017","journal-title":"Biol Reprod"},{"key":"2022071901483667700_ref11","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1093\/biolre\/ioab075","article-title":"Importance of WNT-dependent signaling for derivation and maintenance of primed pluripotent bovine embryonic stem cells","volume":"105","author":"Xiao","year":"2021","journal-title":"Biol Reprod"},{"key":"2022071901483667700_ref12","doi-asserted-by":"crossref","first-page":"3975","DOI":"10.1096\/fj.14-253112","article-title":"The WNT signaling antagonist Dickkopf-1 directs lineage commitment and promotes survival of the preimplantation embryo","volume":"28","author":"Denicol","year":"2014","journal-title":"FASEB J"},{"key":"2022071901483667700_ref13","doi-asserted-by":"crossref","first-page":"11816","DOI":"10.1038\/s41598-019-48374-z","article-title":"Dickkopf-related protein 1 is a progestomedin acting on the bovine embryo during the morula-to-blastocyst transition to program trophoblast elongation","volume":"9","author":"Tr\u00edbulo","year":"2019","journal-title":"Sci Rep"},{"key":"2022071901483667700_ref14","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1038\/nm979","article-title":"Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor","volume":"10","author":"Sato","year":"2004","journal-title":"Nat Med"},{"key":"2022071901483667700_ref15","doi-asserted-by":"crossref","first-page":"762","DOI":"10.1038\/ncb2283","article-title":"Opposing effects of Tcf3 and Tcf1 control Wnt stimulation of embryonic stem cell self-renewal","volume":"13","author":"Yi","year":"2011","journal-title":"Nat Cell Biol"},{"key":"2022071901483667700_ref16","doi-asserted-by":"crossref","first-page":"690","DOI":"10.3168\/jds.2017-13221","article-title":"Identification of potential embryokines in the bovine reproductive tract","volume":"101","author":"Tr\u00edbulo","year":"2018","journal-title":"J Dairy Sci"},{"key":"2022071901483667700_ref17","doi-asserted-by":"crossref","first-page":"694","DOI":"10.1002\/mrd.23534","article-title":"Atlas of receptor genes expressed by the bovine morula and corresponding ligand-related genes expressed by uterine endometrium","volume":"88","author":"Sang","year":"2021","journal-title":"Mol Reprod Dev"},{"key":"2022071901483667700_ref18","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1186\/s12861-018-0176-2","article-title":"Effects of sex on response of the bovine preimplantation embryo to insulin-like growth factor 1, activin A, and WNT7A","volume":"18","author":"Tr\u00edbulo","year":"2018","journal-title":"BMC Dev Biol"},{"key":"2022071901483667700_ref19","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1530\/REP-16-0610","article-title":"WNT regulation of embryonic development likely involves pathways independent of nuclear CTNNB1","volume":"153","author":"Tr\u00edbulo","year":"2017","journal-title":"Reproduction"},{"key":"2022071901483667700_ref20","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1016\/bs.ircmb.2014.10.003","article-title":"Insight into the role of Wnt5a-induced signaling in normal and cancer cells","volume":"314","author":"Endo","year":"2015","journal-title":"Int Rev Cell Mol Biol"},{"key":"2022071901483667700_ref21","doi-asserted-by":"crossref","first-page":"79","DOI":"10.3390\/cancers8090079","article-title":"Wnt5a signaling in cancer","volume":"8","author":"Asem","year":"2016","journal-title":"Cancers (Basel)"},{"key":"2022071901483667700_ref22","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/j.ydbio.2012.06.020","article-title":"Wnt5a can both activate and repress Wnt\/\u03b2-catenin signaling during mouse embryonic development","volume":"369","author":"Amerongen","year":"2012","journal-title":"Dev Biol"},{"key":"2022071901483667700_ref23","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/j.mod.2003.12.002","article-title":"WNT5A signaling affects pituitary gland shape","volume":"121","author":"Cha","year":"2004","journal-title":"Mech Dev"},{"key":"2022071901483667700_ref24","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1016\/j.ydbio.2005.08.035","article-title":"Wnt5a regulates Shh and Fgf10 signaling during lung development","volume":"287","author":"Li","year":"2005","journal-title":"Dev Biol"},{"key":"2022071901483667700_ref25","doi-asserted-by":"crossref","first-page":"3096","DOI":"10.1128\/MCB.00491-14","article-title":"Role of Wnt5a-Ror2 signaling in morphogenesis of the metanephric mesenchyme during ureteric budding","volume":"34","author":"Nishita","year":"2014","journal-title":"Mol Cell Biol"},{"key":"2022071901483667700_ref26","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.yjmcc.2018.10.014","article-title":"NOTCH maintains developmental cardiac gene network through WNT5A","volume":"125","author":"Wang","year":"2018","journal-title":"J Mol Cell Cardiol"},{"key":"2022071901483667700_ref27","doi-asserted-by":"crossref","first-page":"5163","DOI":"10.1091\/mbc.e06-04-0320","article-title":"Wnt5a signaling induces proliferation and survival of endothelial cells in vitro and expression of MMP-1 and Tie-2","volume":"17","author":"Masckauch\u00e1n","year":"2006","journal-title":"Mol Biol Cell"},{"key":"2022071901483667700_ref28","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0003517","article-title":"Wnt5a regulates ventral midbrain morphogenesis and the development of A9-A10 dopaminergic cells in vivo","volume":"3","author":"Andersson","year":"2008","journal-title":"PLoS One"},{"key":"2022071901483667700_ref29","doi-asserted-by":"crossref","first-page":"7569","DOI":"10.1523\/JNEUROSCI.1445-09.2009","article-title":"Wnt5a mediates nerve growth factor-dependent axonal branching and growth in developing sympathetic neurons","volume":"29","author":"Bodmer","year":"2009","journal-title":"J Neurosci"},{"key":"2022071901483667700_ref30","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1002\/dneu.22102","article-title":"Wnt5a evokes cortical axon outgrowth and repulsive guidance by tau mediated reorganization of dynamic microtubules","volume":"74","author":"Li","year":"2014","journal-title":"Dev Neurobiol"},{"key":"2022071901483667700_ref31","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1038\/nm.2653","article-title":"Wnt5a-Ror2 signaling between osteoblast-lineage cells and osteoclast precursors enhances osteoclastogenesis","volume":"18","author":"Maeda","year":"2012","journal-title":"Nat Med"},{"key":"2022071901483667700_ref32","doi-asserted-by":"crossref","DOI":"10.1126\/scisignal.aan0023","article-title":"Protein kinase N3 promotes bone resorption by osteoclasts in response to Wnt5a-Ror2 signaling","volume":"10","author":"Uehara","year":"2017","journal-title":"Sci Signal"},{"key":"2022071901483667700_ref33","doi-asserted-by":"crossref","first-page":"1752","DOI":"10.1002\/jcp.26086","article-title":"Wnt5a suppresses osteoblastic differentiation of human periodontal ligament stem cell-like cells via Ror2\/JNK signaling","volume":"233","author":"Hasegawa","year":"2018","journal-title":"J Cell Physiol"},{"key":"2022071901483667700_ref34","doi-asserted-by":"crossref","first-page":"382","DOI":"10.1016\/j.celrep.2014.06.027","article-title":"Appropriate crypt formation in the uterus for embryo homing and implantation requires Wnt5a-ROR signaling","volume":"8","author":"Cha","year":"2014","journal-title":"Cell Rep"},{"key":"2022071901483667700_ref35","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1016\/j.ydbio.2016.11.023","article-title":"Porcupine-dependent Wnt signaling controls stromal proliferation and endometrial gland maintenance through the action of distinct WNTs","volume":"422","author":"Farah","year":"2017","journal-title":"Dev Biol"},{"key":"2022071901483667700_ref36","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1093\/biolre\/ioy160","article-title":"Targeted ablation of Wnt4 and Wnt5a in M\u00fcllerian duct mesenchyme impedes endometrial gland development and causes partial M\u00fcllerian agenesis","volume":"100","author":"St-Jean","year":"2019","journal-title":"Biol Reprod"},{"key":"2022071901483667700_ref37","doi-asserted-by":"crossref","first-page":"1147","DOI":"10.1016\/0093-691X(93)90285-D","article-title":"Location and status of embryos in the genital tract of superovulated cows 4 to 6 days after insemination","volume":"40","author":"Hackett","year":"1993","journal-title":"Theriogenology"},{"key":"2022071901483667700_ref38","doi-asserted-by":"crossref","first-page":"787","DOI":"10.1071\/RD04026","article-title":"Embryonic disc development and subsequent viability of cattle embryos following culture in two media under two oxygen concentrations","volume":"16","author":"Fischer-Brown","year":"2004","journal-title":"Reprod Fertil Dev"},{"key":"2022071901483667700_ref39","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1016\/j.theriogenology.2007.04.045","article-title":"The effect of in vitro treatment of bovine embryos with IGF-1 on subsequent development in utero to day 14 of gestation","volume":"68","author":"Block","year":"2007","journal-title":"Theriogenology"},{"key":"2022071901483667700_ref40","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1530\/REP-10-0511","article-title":"Consequences of conceptus exposure to colony-stimulating factor 2 on survival, elongation, interferon-\u03c4 secretion, and gene expression","volume":"141","author":"Loureiro","year":"2011","journal-title":"Reproduction"},{"key":"2022071901483667700_ref41","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1007\/978-1-4939-9566-0_8","article-title":"Production and culture of the bovine embryo","volume":"2006","author":"Tr\u00edbulo","year":"2019","journal-title":"Methods Mol Biol"},{"key":"2022071901483667700_ref42","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1016\/j.preghy.2018.06.022","article-title":"Impaired Wnt5a signaling in extravillous trophoblasts: relevance to poor placentation in early gestation and subsequent preeclampsia","volume":"13","author":"Ujita","year":"2018","journal-title":"Pregnancy Hypertens"},{"key":"2022071901483667700_ref43","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1016\/j.theriogenology.2017.04.008","article-title":"Hepatoma-derived growth factor: protein quantification in uterine fluid, gene expression in endometrial-cell culture and effects on in vitro embryo development, pregnancy and birth","volume":"96","author":"G\u00f3mez","year":"2017","journal-title":"Theriogenology"},{"key":"2022071901483667700_ref44","doi-asserted-by":"crossref","first-page":"V5","DOI":"10.1530\/REP-20-0107","article-title":"Culture conditions antagonize lineage-promoting signaling in the mouse blastocyst","volume":"160","author":"Frum","year":"2020","journal-title":"Reproduction"},{"key":"2022071901483667700_ref45","doi-asserted-by":"crossref","first-page":"7618","DOI":"10.1073\/pnas.0307512101","article-title":"Rational design and characterization of a Rac GTPase-specific small molecule inhibitor","volume":"101","author":"Gao","year":"2004","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2022071901483667700_ref46","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0177994","article-title":"A Rho-associated coiled-coil containing kinases (ROCK) inhibitor, Y-27632, enhances adhesion, viability and differentiation of human term placenta-derived trophoblasts in vitro","volume":"12","author":"Motomura","year":"2017","journal-title":"PLoS One"},{"key":"2022071901483667700_ref47","doi-asserted-by":"crossref","first-page":"374","DOI":"10.1002\/mrd.22976","article-title":"Role of ROCK signaling in formation of the trophectoderm of the bovine preimplantation embryo","volume":"85","author":"Negr\u00f3n-P\u00e9rez","year":"2018","journal-title":"Mol Reprod Dev"},{"key":"2022071901483667700_ref48","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/nmeth.3317","article-title":"HISAT: a fast spliced aligner with low memory requirements","volume":"12","author":"Kim","year":"2015","journal-title":"Nat Methods"},{"key":"2022071901483667700_ref49","doi-asserted-by":"crossref","first-page":"923","DOI":"10.1093\/bioinformatics\/btt656","article-title":"featureCounts: an efficient general purpose program for assigning sequence reads to genomic features","volume":"30","author":"Liao","year":"2014","journal-title":"Bioinformatics"},{"key":"2022071901483667700_ref50","doi-asserted-by":"crossref","DOI":"10.1093\/nar\/gku310","article-title":"Robustly detecting differential expression in RNA sequencing data using observation weights","volume":"42","author":"Zhou","year":"2014","journal-title":"Nucleic Acids Res"},{"key":"2022071901483667700_ref51","doi-asserted-by":"crossref","first-page":"15545","DOI":"10.1073\/pnas.0506580102","article-title":"Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles","volume":"102","author":"Subramanian","year":"2005","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2022071901483667700_ref52","doi-asserted-by":"crossref","DOI":"10.1242\/bio.058669","article-title":"Regulation of NANOG and SOX2 expression by activin A and a canonical WNT agonist in bovine embryonic stem cells and blastocysts","volume":"10","author":"Xiao","year":"2021","journal-title":"Biol Open"},{"key":"2022071901483667700_ref53","doi-asserted-by":"crossref","first-page":"1391","DOI":"10.1126\/science.1082808","article-title":"Dishevelled 2 recruits beta-arrestin 2 to mediate Wnt5A-stimulated endocytosis of Frizzled 4","volume":"301","author":"Chen","year":"2003","journal-title":"Science"},{"key":"2022071901483667700_ref54","doi-asserted-by":"crossref","first-page":"522","DOI":"10.1016\/j.molcel.2015.03.015","article-title":"Dishevelled promotes Wnt receptor degradation through recruitment of ZNRF3\/RNF43 E3 ubiquitin ligases","volume":"58","author":"Jiang","year":"2015","journal-title":"Mol Cell"},{"key":"2022071901483667700_ref55","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pbio.0040115","article-title":"Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context","volume":"4","author":"Mikels","year":"2006","journal-title":"PLoS Biol"},{"key":"2022071901483667700_ref56","doi-asserted-by":"crossref","first-page":"1652","DOI":"10.1126\/science.275.5306.1652","article-title":"A member of the frizzled protein family mediating axis induction by Wnt-5A","volume":"275","author":"He","year":"1997","journal-title":"Science"},{"key":"2022071901483667700_ref57","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1002\/stem.3317","article-title":"FZD5 regulates cellular senescence in human mesenchymal stem\/stromal cells","volume":"39","author":"Harada","year":"2021","journal-title":"Stem Cells"},{"key":"2022071901483667700_ref58","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1046\/j.1365-2443.2003.00662.x","article-title":"The receptor tyrosine kinase Ror2 is involved in non-canonical Wnt5a\/JNK signalling pathway","volume":"8","author":"Oishi","year":"2003","journal-title":"Genes Cells"},{"key":"2022071901483667700_ref59","doi-asserted-by":"crossref","first-page":"2498","DOI":"10.1016\/j.cellsig.2007.07.023","article-title":"Wnt5a promotes adhesion of human dermal fibroblasts by triggering a phosphatidylinositol-3 kinase\/Akt signal","volume":"19","author":"Kawasaki","year":"2007","journal-title":"Cell Signal"},{"key":"2022071901483667700_ref60","doi-asserted-by":"crossref","first-page":"1631","DOI":"10.1096\/fj.12-217539","article-title":"Noncanonical WNT-5A signaling regulates TGF-\u03b2-induced extracellular matrix production by airway smooth muscle cells","volume":"27","author":"Kumawat","year":"2013","journal-title":"FASEB J"},{"key":"2022071901483667700_ref61","doi-asserted-by":"crossref","first-page":"780","DOI":"10.1016\/j.cell.2015.07.013","article-title":"Alternative Wnt signaling activates YAP\/TAZ","volume":"162","author":"Park","year":"2015","journal-title":"Cell"},{"key":"2022071901483667700_ref62","doi-asserted-by":"crossref","first-page":"1943","DOI":"10.1016\/j.cellsig.2014.05.012","article-title":"Assessment of Frizzled 6 membrane mobility by FRAP supports G protein coupling and reveals WNT-Frizzled selectivity","volume":"26","author":"Kilander","year":"2014","journal-title":"Cell Signal"},{"key":"2022071901483667700_ref63","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/j.mce.2015.01.017","article-title":"Non-canonical WNT5A is a potential regulator of granulosa cell function in cattle","volume":"403","author":"Abedini","year":"2015","journal-title":"Mol Cell Endocrinol"},{"key":"2022071901483667700_ref64","doi-asserted-by":"crossref","first-page":"15436","DOI":"10.1073\/pnas.0704747104","article-title":"Wnt5a inhibits canonical Wnt signaling in hematopoietic stem cells and enhances repopulation","volume":"104","author":"Nemeth","year":"2007","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2022071901483667700_ref65","doi-asserted-by":"crossref","first-page":"2357","DOI":"10.1242\/jcs.080903","article-title":"Wnt5a is a cell-extrinsic factor that supports self-renewal of mouse spermatogonial stem cells","volume":"124","author":"Yeh","year":"2011","journal-title":"J Cell Sci"},{"key":"2022071901483667700_ref66","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1038\/emboj.2009.322","article-title":"Wnt5a regulates distinct signalling pathways by binding to Frizzled2","volume":"29","author":"Sato","year":"2010","journal-title":"EMBO J"},{"key":"2022071901483667700_ref67","doi-asserted-by":"crossref","DOI":"10.1126\/sciadv.aaw3896","article-title":"Synthetic presentation of noncanonical Wnt5a motif promotes mechanosensing-dependent differentiation of stem cells and regeneration","volume":"5","author":"Li","year":"2019","journal-title":"Sci Adv"},{"key":"2022071901483667700_ref68","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1093\/jb\/mvv124","article-title":"Regulation of bone metabolism by Wnt signals","volume":"159","author":"Kobayashi","year":"2016","journal-title":"J Biochem"},{"key":"2022071901483667700_ref69","doi-asserted-by":"crossref","DOI":"10.3389\/fimmu.2020.555245","article-title":"Non-canonical WNT5A signaling through RYK contributes to aggressive phenotype of the rheumatoid fibroblast-like synoviocytes","volume":"11","author":"Rodriguez-Trillo","year":"2020","journal-title":"Front Immunol"},{"key":"2022071901483667700_ref70","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1016\/j.jsbmb.2015.04.002","article-title":"A review of 1\u03b1,25(OH)2D3 dependent Pdia3 receptor complex components in Wnt5a non-canonical pathway signaling","volume":"152","author":"Doroudi","year":"2015","journal-title":"J Steroid Biochem Mol Biol"},{"key":"2022071901483667700_ref71","doi-asserted-by":"crossref","first-page":"4935","DOI":"10.1093\/emboj\/20.17.4935","article-title":"The chromatin remodelling factor Brg-1 interacts with beta-catenin to promote target gene activation","volume":"20","author":"Barker","year":"2001","journal-title":"EMBO J"},{"key":"2022071901483667700_ref72","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1038\/nature08137","article-title":"Telomerase modulates Wnt signalling by association with target gene chromatin","volume":"460","author":"Park","year":"2009","journal-title":"Nature"},{"key":"2022071901483667700_ref73","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1096\/fj.201800197R","article-title":"Brahma related gene 1 (Brg1) contributes to liver regeneration by epigenetically activating the Wnt\/\u03b2-catenin pathway in mice","volume":"33","author":"Li","year":"2019","journal-title":"FASEB J"},{"key":"2022071901483667700_ref74","doi-asserted-by":"crossref","first-page":"5546","DOI":"10.1158\/1078-0432.CCR-12-0977","article-title":"c-Myc and cancer metabolism","volume":"18","author":"Miller","year":"2012","journal-title":"Clin Cancer Res"},{"key":"2022071901483667700_ref75","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1016\/j.cels.2015.12.004","article-title":"The molecular signatures database (MSigDB) hallmark gene set collection","volume":"1","author":"Liberzon","year":"2015","journal-title":"Cell Syst"},{"key":"2022071901483667700_ref76","doi-asserted-by":"crossref","first-page":"2104","DOI":"10.1002\/ar.22592","article-title":"Wnt\/\u03b2-catenin signaling pathway upregulates c-Myc expression to promote cell proliferation of P19 teratocarcinoma cells","volume":"295","author":"Zhang","year":"2012","journal-title":"Anat Rec (Hoboken)"},{"key":"2022071901483667700_ref77","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1186\/s12964-019-0444-1","article-title":"Induction of LEF1 by MYC activates the WNT pathway and maintains cell proliferation","volume":"17","author":"Hao","year":"2019","journal-title":"Cell Commun Signal"},{"key":"2022071901483667700_ref78","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1186\/1476-4598-9-55","article-title":"Wnt-11 promotes neuroendocrine-like differentiation, survival and migration of prostate cancer cells","volume":"9","author":"Uysal-Onganer","year":"2010","journal-title":"Mol Cancer"},{"key":"2022071901483667700_ref79","doi-asserted-by":"crossref","first-page":"6479","DOI":"10.1111\/jcmm.16663","article-title":"The complex role of Wnt ligands in type 2 diabetes mellitus and related complications","volume":"25","author":"Nie","year":"2021","journal-title":"J Cell Mol Med"},{"key":"2022071901483667700_ref80","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1016\/0093-691X(96)84684-X","article-title":"Evaluation of bovine embryos produced in vitro vs. in vivo by differential staining of inner cell mass and trophectoderm cells","volume":"45","author":"Du","year":"1996","journal-title":"Theriogenology"},{"key":"2022071901483667700_ref81","doi-asserted-by":"crossref","first-page":"1041","DOI":"10.1095\/biolreprod57.5.1041","article-title":"Timing of compaction and inner cell allocation in bovine embryos produced in vivo after superovulation","volume":"57","author":"Van Soom","year":"1997","journal-title":"Biol Reprod"}],"container-title":["Biology of Reproduction"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/biolreprod\/advance-article-pdf\/doi\/10.1093\/biolre\/ioac127\/45021214\/ioac127.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/biolreprod\/advance-article-pdf\/doi\/10.1093\/biolre\/ioac127\/45021214\/ioac127.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,7,19]],"date-time":"2022-07-19T01:49:54Z","timestamp":1658195394000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/biolreprod\/advance-article\/doi\/10.1093\/biolre\/ioac127\/6619149"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,6,28]]},"references-count":81,"URL":"https:\/\/doi.org\/10.1093\/biolre\/ioac127","relation":{},"ISSN":["0006-3363","1529-7268"],"issn-type":[{"value":"0006-3363","type":"print"},{"value":"1529-7268","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,6,28]]},"article-number":"ioac127"}}