{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,12]],"date-time":"2025-10-12T02:40:34Z","timestamp":1760236834115,"version":"build-2065373602"},"reference-count":88,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2021,12,29]],"date-time":"2021-12-29T00:00:00Z","timestamp":1640736000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Fundaci\u00f3n Ren\u00e9 Bar\u00f3n y Fundaci\u00f3n Williams","award":["No number available"],"award-info":[{"award-number":["No number available"]}]},{"DOI":"10.13039\/501100002923","name":"National Scientific and Technical Research Council","doi-asserted-by":"publisher","award":["PIP 887"],"award-info":[{"award-number":["PIP 887"]}],"id":[{"id":"10.13039\/501100002923","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>Successful mammalian fertilization requires a well-orchestrated sequence of molecular events leading to gamete fusion. Since this interaction involves Ca2+-dependent adhesion events, the participation of the Ca+2-dependent cell-cell adhesion proteins Epithelial (E-cad) and Neural (N-cad) cadherin is envisaged. We have previously reported the expression of E-cad and N-cad in human gametes and showed evidence of their involvement in sperm-oocyte adhesion events leading to fertilization. To overcome ethical limitations associated with the use of human gametes in fertilization-related studies, the mouse has been selected worldwide as the experimental model for over 4 decades. Herein, we report a detailed study aimed at characterizing the expression of E-cad and N-cad in murine gametes and their involvement in murine fertilization using specific antibodies and blocking peptides towards both adhesion proteins. E-cad and N-cad protein forms, as well as other members of the adhesion complex, specifically \u03b2-catenin and actin, were identified in spermatozoa, cumulus cells and oocytes protein extracts by means of Western immunoblotting. In addition, subcellular localization of these proteins was determined in whole cells using optical fluorescent microscopy. Gamete pre-incubation with anti-E-cad (ECCD-1) or N-cad (H-63) antibodies resulted in decreased (p &lt; 0.05) In Vitro Fertilization (IVF) rates, when using both cumulus-oocytes complexes and cumulus-free oocytes. Moreover, IVF assays done with denuded oocytes and either antibodies or blocking peptides against E-cad and N-cad led to lower (p &lt; 0.05) fertilization rates. When assessing each step, penetration of the cumulus mass was lower (p &lt; 0.05) when spermatozoa were pre-incubated with ECCD-1 or blocking peptides towards E-cad or towards both E- and N-cad. Moreover, sperm-oolemma binding was impaired (p &lt; 0.0005) after sperm pre-incubation with E-cad antibody or blocking peptide towards E-cad, N-cad or both proteins. Finally, sperm-oocyte fusion was lower (p &lt; 0.05) after sperm pre-incubation with either antibody or blocking peptide against E-cad or N-cad. Our studies demonstrate the expression of members of the adherent complex in the murine model, and the use of antibodies and specific peptides revealed E-cad and N-cad participation in mammalian fertilization.<\/jats:p>","DOI":"10.3390\/cells11010102","type":"journal-article","created":{"date-parts":[[2021,12,29]],"date-time":"2021-12-29T23:31:35Z","timestamp":1640820695000},"page":"102","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Epithelial and Neural Cadherin in Mammalian Fertilization: Studies in the Mouse Model"],"prefix":"10.3390","volume":"11","author":[{"given":"Gustavo Luis","family":"Ver\u00f3n","sequence":"first","affiliation":[{"name":"Laboratorio de Estudios de Interacci\u00f3n Celular en Reproducci\u00f3n y C\u00e1ncer, Instituto de Biolog\u00eda y Medicina Experimental (IBYME), Consejo Nacional de Investigaciones Cient\u00edficas y T\u00e9cnicas (CONICET), Fundaci\u00f3n IBYME (FIBYME), Buenos Aires C1428ADN, Argentina"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mar\u00eda Florencia","family":"Veiga","sequence":"additional","affiliation":[{"name":"Laboratorio de Estudios de Interacci\u00f3n Celular en Reproducci\u00f3n y C\u00e1ncer, Instituto de Biolog\u00eda y Medicina Experimental (IBYME), Consejo Nacional de Investigaciones Cient\u00edficas y T\u00e9cnicas (CONICET), Fundaci\u00f3n IBYME (FIBYME), Buenos Aires C1428ADN, Argentina"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"M\u00f3nica","family":"Cameo","sequence":"additional","affiliation":[{"name":"BioAplicada\u2014Laboratorio de Cultivos Celulares y Estudios Especiales, Buenos Aires C1430EYV, Argentina"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Clara Isabel","family":"Mar\u00edn-Briggiler","sequence":"additional","affiliation":[{"name":"Laboratorio de Estudios de Interacci\u00f3n Celular en Reproducci\u00f3n y C\u00e1ncer, Instituto de Biolog\u00eda y Medicina Experimental (IBYME), Consejo Nacional de Investigaciones Cient\u00edficas y T\u00e9cnicas (CONICET), Fundaci\u00f3n IBYME (FIBYME), Buenos Aires C1428ADN, Argentina"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"M\u00f3nica Hebe","family":"Vazquez-Levin","sequence":"additional","affiliation":[{"name":"Laboratorio de Estudios de Interacci\u00f3n Celular en Reproducci\u00f3n y C\u00e1ncer, Instituto de Biolog\u00eda y Medicina Experimental (IBYME), Consejo Nacional de Investigaciones Cient\u00edficas y T\u00e9cnicas (CONICET), Fundaci\u00f3n IBYME (FIBYME), Buenos Aires C1428ADN, Argentina"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,12,29]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"748","DOI":"10.1111\/andr.12633","article-title":"Revisiting structure\/functions of the human epididymis","volume":"7","author":"Sullivan","year":"2019","journal-title":"Andrology"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1111\/andr.12632","article-title":"Epithelial dynamics in the epididymis: Role in the maturation, protection, and storage of spermatozoa","volume":"7","author":"Breton","year":"2019","journal-title":"Andrology"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"R155","DOI":"10.1530\/REP-18-0589","article-title":"The impact of epididymal proteins on sperm function","volume":"158","year":"2019","journal-title":"Reproduction"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"James, E.R., Carrell, D.T., Aston, K.I., Jenkins, T.G., Yeste, M., and Salas-Huetos, A. (2020). The Role of the Epididymis and the Contribution of Epididymosomes to Mammalian Reproduction. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21155377"},{"key":"ref_5","first-page":"289","article-title":"Biological basis for human capacitation-revisited","volume":"23","year":"2017","journal-title":"Hum. Reprod. Update"},{"key":"ref_6","first-page":"6","article-title":"Molecular Basis of Human Sperm Capacitation","volume":"27","author":"Luque","year":"2018","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1262\/jrd.11-015","article-title":"Fertilization studies and assisted fertilization in mammals: Their development and future","volume":"58","author":"Yanagimachi","year":"2012","journal-title":"J. Reprod. Dev."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1146\/annurev-physiol-020911-153339","article-title":"Sperm-egg interaction","volume":"74","author":"Evans","year":"2012","journal-title":"Annu. Rev. Physiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"466","DOI":"10.1038\/nature13227","article-title":"Reproductive biology: Sperm protein finds its mate","volume":"508","author":"Wassarman","year":"2014","journal-title":"Nature"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1146\/annurev-genet-121415-121834","article-title":"Sperm Meets Egg: The Genetics of Mammalian Fertilization","volume":"50","author":"Bianchi","year":"2016","journal-title":"Annu. Rev. Genet."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"610","DOI":"10.1111\/andr.12638","article-title":"Relevance of CRISP proteins for epididymal physiology, fertilization, and fertility","volume":"7","author":"Carvajal","year":"2019","journal-title":"Andrology"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Piprek, R.P., Kloc, M., Mizia, P., and Kubiak, J.Z. (2020). The Central Role of Cadherins in Gonad Development, Reproduction, and Fertility. Int. J. Mol. Sci., 21.","DOI":"10.20944\/preprints202010.0037.v1"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1171","DOI":"10.1093\/biolre\/ioaa140","article-title":"The enigmatic sperm proteins in mammalian fertilization: An overview","volume":"103","author":"Gahlay","year":"2020","journal-title":"Biol. Reprod."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1146\/annurev-cellbio-120219-021751","article-title":"The Fertilization Enigma: How Sperm and Egg Fuse","volume":"37","author":"Deneke","year":"2021","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Bianchi, E., and Wright, G.J. (2020). Find and fuse: Unsolved mysteries in sperm-egg recognition. PLoS Biol., 18.","DOI":"10.1371\/journal.pbio.3000953"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1242\/jcs.114.4.629","article-title":"The cadherin superfamily: Diversity in form and function","volume":"114","author":"Angst","year":"2001","journal-title":"J. Cell Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"464","DOI":"10.1083\/jcb.75.2.464","article-title":"Functional correlation between cell adhesive properties and some cell surface proteins","volume":"75","author":"Takeichi","year":"1977","journal-title":"J. Cell Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"3756","DOI":"10.1007\/s00018-008-8281-1","article-title":"The cell-cell adhesion molecule E-cadherin","volume":"65","author":"Berx","year":"2008","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1679\/aohc.69.135","article-title":"Differential expression of N-cadherin and E-cadherin in normal human tissues","volume":"69","author":"Tsuchiya","year":"2006","journal-title":"Arch. Histol. Cytol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"622","DOI":"10.1038\/nrm1699","article-title":"Regulation of cadherin-mediated adhesion in morphogenesis","volume":"6","author":"Gumbiner","year":"2005","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1196\/annals.1294.016","article-title":"Cadherin switch in tumor progression","volume":"1014","author":"Hazan","year":"2004","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"3199","DOI":"10.1101\/gad.1486806","article-title":"Cadherins in development: Cell adhesion, sorting, and tissue morphogenesis","volume":"20","author":"Halbleib","year":"2006","journal-title":"Genes Dev."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1016\/j.devcel.2011.06.002","article-title":"Self-organization of animal tissues: Cadherin-mediated processes","volume":"21","author":"Takeichi","year":"2011","journal-title":"Dev. Cell"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"4182","DOI":"10.1016\/j.bpj.2021.03.025","article-title":"Holding it together: When cadherin meets cadherin","volume":"120","author":"Arslan","year":"2021","journal-title":"Biophys. J."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"56","DOI":"10.12703\/r\/10-56","article-title":"How adherens junctions move cells during collective migration","volume":"10","author":"Gupta","year":"2021","journal-title":"Fac. Rev."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Kaszak, I., Witkowska-Pi\u0142aszewicz, O., Niewiadomska, Z., Dworecka-Kaszak, B., Ngosa Toka, F., and Jurka, P. (2020). Role of Cadherins in Cancer-A Review. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21207624"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1038\/ncb3478","article-title":"A mechanically active heterotypic E-cadherin\/N-cadherin adhesion enables fibroblasts to drive cancer cell invasion","volume":"19","author":"Labernadie","year":"2017","journal-title":"Nat. Cell Biol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"110953","DOI":"10.1016\/j.mce.2020.110953","article-title":"Ca2+ signaling in mammalian spermatozoa","volume":"516","author":"Finkelstein","year":"2020","journal-title":"Mol. Cell Endocrinol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1093\/molehr\/gan053","article-title":"Expression of epithelial cadherin in the human male reproductive tract and gametes and evidence of its participation in fertilization","volume":"14","author":"Veiga","year":"2008","journal-title":"Mol. Hum. Reprod."},{"key":"ref_30","first-page":"e228","article-title":"Neural cadherin is expressed in human gametes and participates in sperm-oocyte interaction events","volume":"33","author":"Lapyckyj","year":"2010","journal-title":"Int. J. Androl."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.ydbio.2014.12.029","article-title":"Epithelial and neural cadherin expression in the mammalian reproductive tract and gametes and their participation in fertilization-related events","volume":"401","author":"Caballero","year":"2015","journal-title":"Dev. Biol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"F758","DOI":"10.1152\/ajprenal.2000.278.5.F758","article-title":"Mouse proximal tubular cell-cell adhesion inhibits apoptosis by a cadherin-dependent mechanism","volume":"278","author":"Bergin","year":"2000","journal-title":"Am. J. Physiol. Renal. Physiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1853","DOI":"10.1016\/j.peptides.2008.06.025","article-title":"Identification of a novel N-cadherin antagonist","volume":"29","author":"Devemy","year":"2008","journal-title":"Peptides"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1539","DOI":"10.1016\/j.peptides.2009.05.010","article-title":"Identification of a novel dual E- and N-cadherin antagonist","volume":"30","author":"Devemy","year":"2009","journal-title":"Peptides"},{"key":"ref_35","unstructured":"National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals (2011). Guide for the Care and Use of Laboratory Animals, National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals. [8th ed.]."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1256","DOI":"10.1016\/j.fertnstert.2008.01.082","article-title":"Antiacrosin antibodies and infertility. II. Gene immunization with human proacrosin to assess the effect of immunity toward proacrosin\/acrosin upon protein activities and animal fertility","volume":"91","author":"Veaute","year":"2009","journal-title":"Fertil. Steril."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1095\/biolreprod13.5.513","article-title":"The relationship between sperm concentration and fertilization in vitro of mouse eggs","volume":"13","author":"Fraser","year":"1975","journal-title":"Biol. Reprod."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/S0165-0378(01)00080-8","article-title":"Evaluation of the proacrosin\/acrosin system and its mechanism of activation in human sperm extracts","volume":"54","author":"Zahn","year":"2002","journal-title":"J. Reprod. Immunol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1038\/227680a0","article-title":"Cleavage of structural proteins during the assembly of the head of bacteriophage T4","volume":"227","author":"Laemmli","year":"1970","journal-title":"Nature"},{"key":"ref_40","first-page":"145","article-title":"Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. 1979","volume":"24","author":"Towbin","year":"1992","journal-title":"Biotechnology"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Barraud-Lange, V., Naud-Barriant, N., Saffar, L., Gattegno, L., Ducot, B., Drillet, A.S., Bomsel, M., Wolf, J.P., and Ziyyat, A. (2007). Alpha6beta1 integrin expressed by sperm is determinant in mouse fertilization. BMC Dev. Biol., 7.","DOI":"10.1186\/1471-213X-7-102"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1054","DOI":"10.1093\/molehr\/gau073","article-title":"Evidence for the involvement of proline-rich tyrosine kinase 2 in tyrosine phosphorylation downstream of protein kinase A activation during human sperm capacitation","volume":"20","author":"Battistone","year":"2014","journal-title":"Mol. Hum. Reprod."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1016\/j.ydbio.2005.05.008","article-title":"Mouse SLLP1, a sperm lysozyme-like protein involved in sperm-egg binding and fertilization","volume":"284","author":"Herrero","year":"2005","journal-title":"Dev. Biol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/0012-1606(84)90112-X","article-title":"Molecular nature of the calcium-dependent cell-cell adhesion system in mouse teratocarcinoma and embryonic cells studied with a monoclonal antibody","volume":"101","author":"Suzuki","year":"1984","journal-title":"Dev. Biol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1016\/0092-8674(83)90095-8","article-title":"The calcium-dependent cell-cell adhesion system regulates inner cell mass formation and cell surface polarization in early mouse development","volume":"35","author":"Shirayoshi","year":"1983","journal-title":"Cell"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"2013","DOI":"10.1091\/mbc.e06-04-0348","article-title":"E-cadherin homophilic ligation inhibits cell growth and epidermal growth factor receptor signaling independently of other cell interactions","volume":"18","author":"Perrais","year":"2007","journal-title":"Mol. Biol. Cell"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e1356900","DOI":"10.1080\/21688370.2017.1356900","article-title":"Cadherin-mediated cell-cell interactions in normal and cancer cells","volume":"5","author":"Gloushankova","year":"2017","journal-title":"Tissue Barriers"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"547","DOI":"10.1002\/mrd.10149","article-title":"Cadherins expression during gamete maturation and fertilization in the rat","volume":"62","author":"Ziv","year":"2002","journal-title":"Mol. Reprod. Dev."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"35","DOI":"10.3109\/01485018608986921","article-title":"Sperm-egg interactions observed by scanning electron microscopy","volume":"16","author":"Tsuiki","year":"1986","journal-title":"Arch. Androl."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"999","DOI":"10.1051\/rnd:19860607","article-title":"Ultrastructural study of the interactions and fusion of ram spermatozoa with zona-free hamster oocytes","volume":"26","author":"Pavlok","year":"1986","journal-title":"Reprod. Nutr. Dev."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1007\/BF00305012","article-title":"Scanning electron microscopy of in vitro fertilization in cattle","volume":"178","author":"Hyttel","year":"1988","journal-title":"Anat. Embryol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/0165-0378(95)00928-E","article-title":"Fertilization antigen (FA-1) completely blocks human sperm binding to human zona pellucida: FA-1 antigen may be a sperm receptor for zona pellucida in humans","volume":"29","author":"Kadam","year":"1995","journal-title":"J. Reprod. Immunol."},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Frolikova, M., Manaskova-Postlerova, P., Cerny, J., Jankovicova, J., Simonik, O., Pohlova, A., Secova, P., Antalikova, J., and Dvorakova-Hortova, K. (2018). CD9 and CD81 Interactions and Their Structural Modelling in Sperm Prior to Fertilization. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19041236"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"909","DOI":"10.1530\/REP-06-0228","article-title":"Detection of osteopontin on Holstein bull spermatozoa, in cauda epididymal fluid and testis homogenates, and its potential role in bovine fertilization","volume":"133","author":"Erikson","year":"2007","journal-title":"Reproduction"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1186\/1477-7827-8-10","article-title":"Endoplasmic reticulum protein 29 (ERp29), a protein related to sperm maturation is involved in sperm-oocyte fusion in mouse","volume":"8","author":"Ying","year":"2010","journal-title":"Reprod. Biol. Endocrinol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"28","DOI":"10.3389\/fcell.2020.00028","article-title":"Essential Role of Sperm-Specific PLC-Zeta in Egg Activation and Male Factor Infertility: An Update","volume":"8","author":"Saleh","year":"2020","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Gianzo, M., Urizar-Arenaza, I., Mu\u00f1oa-Hoyos, I., Larreategui, Z., Garrido, N., Irazusta, J., and Subir\u00e1n, N. (2021). (Pro)renin Receptor Is Present in Human Sperm and It Adversely Affects Sperm Fertility Ability. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22063215"},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Miro-Moran, A., Jardin, I., Ortega-Ferrusola, C., Salido, G.M., Pe\u00f1a, F.J., Tapia, J.A., and Aparicio, I.M. (2012). Identification and function of exchange proteins activated directly by cyclic AMP (Epac) in mammalian spermatozoa. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0037713"},{"key":"ref_59","first-page":"4985","article-title":"Visualization of the moment of mouse sperm-egg fusion and dynamic localization of IZUMO1","volume":"125","author":"Satouh","year":"2012","journal-title":"J. Cell Sci."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"750","DOI":"10.1093\/biolre\/ioz223","article-title":"Cleavage of SPACA1 regulates assembly of sperm-egg membrane fusion machinery in mature spermatozoa","volume":"102","author":"Yamatoya","year":"2020","journal-title":"Biol. Reprod."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"e53913","DOI":"10.7554\/eLife.53913","article-title":"TMEM95 is a sperm membrane protein essential for mammalian fertilization","volume":"9","author":"Hamze","year":"2020","journal-title":"eLife"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"9393","DOI":"10.1073\/pnas.1917060117","article-title":"Spermatozoa lacking Fertilization Influencing Membrane Protein (FIMP) fail to fuse with oocytes in mice","volume":"117","author":"Fujihara","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"11493","DOI":"10.1073\/pnas.1922650117","article-title":"Sperm proteins SOF1, TMEM95, and SPACA6 are required for sperm-oocyte fusion in mice","volume":"117","author":"Noda","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"8263","DOI":"10.1073\/pnas.91.17.8263","article-title":"E-cadherin null mutant embryos fail to form a trophectoderm epithelium","volume":"91","author":"Larue","year":"1994","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1006\/dbio.1996.8443","article-title":"Developmental defects in mouse embryos lacking N-cadherin","volume":"181","author":"Radice","year":"1997","journal-title":"Dev. Biol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"837","DOI":"10.1095\/biolreprod.102.009233","article-title":"Remodeling of the actin cytoskeleton during mammalian sperm capacitation and acrosome reaction","volume":"68","author":"Brener","year":"2003","journal-title":"Biol. Reprod."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1016\/j.bbrc.2017.11.001","article-title":"Actin cytoskeleton and sperm function","volume":"506","author":"Breitbart","year":"2018","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1183","DOI":"10.1002\/mrd.22878","article-title":"Effects of latrunculin A on the relocation of sperm IZUMO1 during gamete interaction in mouse","volume":"84","author":"Zhou","year":"2017","journal-title":"Mol. Reprod. Dev."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"522","DOI":"10.1016\/S0012-1606(03)00273-2","article-title":"Involvement of Rho family G protein in the cell signaling for sperm incorporation during fertilization of mouse eggs: Inhibition by Clostridium difficile toxin B","volume":"260","author":"Kumakiri","year":"2003","journal-title":"Dev. Biol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1007\/s00418-018-1691-8","article-title":"The regulation of junctional actin dynamics by cell adhesion receptors","volume":"150","author":"Steinbacher","year":"2018","journal-title":"Histochem. Cell Biol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1093\/molehr\/6.2.163","article-title":"Expression of cadherin adhesion molecules on human gametes","volume":"6","author":"Rufas","year":"2000","journal-title":"Mol. Hum. Reprod."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"2319","DOI":"10.1210\/en.2009-1489","article-title":"Expression of E-cadherin and N-cadherin in perinatal hamster ovary: Possible involvement in primordial follicle formation and regulation by follicle-stimulating hormone","volume":"151","author":"Wang","year":"2010","journal-title":"Endocrinology"},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Bertoldo, M.J., Guibert, E., Faure, M., Ram\u00e9, C., Foretz, M., Viollet, B., Dupont, J., and Froment, P. (2015). Specific deletion of AMP-activated protein kinase (\u03b11AMPK) in murine oocytes alters junctional protein expression and mitochondrial physiology. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0119680"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/0092-8674(90)90222-Z","article-title":"Localization of specificity determining sites in cadherin cell adhesion molecules","volume":"61","author":"Nose","year":"1990","journal-title":"Cell"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"C876","DOI":"10.1152\/ajpcell.00282.2018","article-title":"Integrin-\u03b17 signaling regulates connexin 43, M-cadherin, and myoblast fusion","volume":"316","author":"McClure","year":"2019","journal-title":"Am. J. Physiol. Cell Physiol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"E5711","DOI":"10.1073\/pnas.1604012113","article-title":"Molecular determinants of cadherin ideal bond formation: Conformation-dependent unbinding on a multidimensional landscape","volume":"113","author":"Manibog","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Miron, R.J., Hedbom, E., Ruggiero, S., Bosshardt, D.D., Zhang, Y., Mauth, C., Gemperli, A.C., Iizuka, T., Buser, D., and Sculean, A. (2011). Premature osteoblast clustering by enamel matrix proteins induces osteoblast differentiation through up-regulation of connexin 43 and N-cadherin. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0023375"},{"key":"ref_78","first-page":"359","article-title":"Calreticulin Regulates Syncytialization Through Control of the Synthesis and Transportation of E-Cadherin in BeWo Cells","volume":"160","author":"Iwahashi","year":"2019","journal-title":"Endocrinology"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1970","DOI":"10.1038\/cdd.2015.44","article-title":"ADAM12-directed ectodomain shedding of E-cadherin potentiates trophoblast fusion","volume":"22","author":"Aghababaei","year":"2015","journal-title":"Cell Death Differ."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"12977","DOI":"10.1073\/pnas.95.22.12977","article-title":"Increase of intracellular Ca2+ and relocation of E-cadherin during experimental decompaction of mouse embryos","volume":"95","author":"Pey","year":"1998","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"7080","DOI":"10.1038\/sj.onc.1203191","article-title":"Calcium influx triggers the sequential proteolysis of extracellular and cytoplasmic domains of E-cadherin, leading to loss of beta-catenin from cell-cell contacts","volume":"18","author":"Ito","year":"1999","journal-title":"Oncogene"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1022","DOI":"10.1016\/j.neuron.2015.08.008","article-title":"Mechanism of Activity-Dependent Cargo Loading via the Phosphorylation of KIF3A by PKA and CaMKIIa","volume":"87","author":"Ichinose","year":"2015","journal-title":"Neuron"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1038\/srep00068","article-title":"\u03b2-catenin is a molecular switch that regulates transition of cell-cell adhesion to fusion","volume":"1","author":"Takezawa","year":"2011","journal-title":"Sci Rep"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"442","DOI":"10.1038\/nrc822","article-title":"Epithelial-mesenchymal transitions in tumour progression","volume":"2","author":"Thiery","year":"2002","journal-title":"Nat. Rev. Cancer"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1016\/bs.ctdb.2014.11.021","article-title":"Epithelial-mesenchymal transitions: From cell plasticity to concept elasticity","volume":"112","author":"Savagner","year":"2015","journal-title":"Curr. Top. Dev. Biol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1038\/s41580-018-0080-4","article-title":"New insights into the mechanisms of epithelial-mesenchymal transition and implications for cancer","volume":"20","author":"Dongre","year":"2019","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"e108","DOI":"10.1038\/emm.2014.44","article-title":"Role of the epithelial\u2013mesenchymal transition and its effects on embryonic stem cells","volume":"46","author":"Kim","year":"2014","journal-title":"Exp. Mol. Med."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"639244","DOI":"10.3389\/fcell.2021.639244","article-title":"Epithelial-Mesenchymal Transition Drives Three-Dimensional Morphogenesis in Mammalian Early Development","volume":"9","author":"Ismagulov","year":"2021","journal-title":"Front. Cell Dev. Biol."}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/11\/1\/102\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:55:37Z","timestamp":1760169337000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/11\/1\/102"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,12,29]]},"references-count":88,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2022,1]]}},"alternative-id":["cells11010102"],"URL":"https:\/\/doi.org\/10.3390\/cells11010102","relation":{},"ISSN":["2073-4409"],"issn-type":[{"type":"electronic","value":"2073-4409"}],"subject":[],"published":{"date-parts":[[2021,12,29]]}}}