Proper maturation of the mammalian oocyte is a compound processes determining successful monospermic fertilization, however the number of fully mature porcine oocytes is still unsatisfactory. Since oocytes' maturation and fertilization involve cellular adhesion and membranous contact, the aim was to investigate cell adhesion ontology group in porcine oocytes. The oocytes were collected from ovaries of 45 pubertal crossbred Landrace gilts and subjected to two BCB tests. After the first test, only granulosa cell-free BCB⁺ oocytes were directly exposed to microarray assays and RT-qPCR ("before IVM" group), or first in vitro matured and then if classified as BCB⁺ passed to molecular analyses ("after IVM" group). As a result, we have discovered substantial down-regulation of genes involved in adhesion processes, such as: organization of actin cytoskeleton, migration, proliferation, differentiation, apoptosis, survival or angiogenesis in porcine oocytes after IVM, compared to oocytes analyzed before IVM. In conclusion, we found that biological adhesion may be recognized as the process involved in porcine oocytes' successful IVM. Down-regulation of genes included in this ontology group in immature oocytes after IVM points to their unique function in oocyte's achievement of fully mature stages. Thus, results indicated new molecular markers involved in porcine oocyte IVM, displaying essential roles in biological adhesion processes.

Department of Anatomy Poznan University of Medical Sciences 60 781 Poznan Poland

Department of Biomaterials and Experimental Dentistry Poznan University of Medical Sciences 60 812 Poznan Poland

Department of Histology and Embryology Poznan University of Medical Sciences 60 781 Poznan Poland

Department of Histology and Embryology Wroclaw Medical University 50 368 Wroclaw Poland

Department of Obstetrics and Gynecology University Hospital and Masaryk University 602 00 Brno Czech Republic

Veterinary Center Nicolaus Copernicus University in Toruń 87 100 Torun Poland

Zobrazit více v PubMed

Uyar A., Torrealday S., Seli E. Cumulus and granulosa cell markers of oocyte and embryo quality. Fertil. Steril. 2013;99:979–997. doi: 10.1016/j.fertnstert.2013.01.129. PubMed DOI PMC

Orisaka M., Tajima K., Tsang B.K., Kotsuji F. Oocyte-granulosa-theca cell interactions during preantral follicular development. J. Ovarian Res. 2009;2 doi: 10.1186/1757-2215-2-9. PubMed DOI PMC

Eppig J.J. Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals. Reprod. Fertil. Dev. 1996;8:485–489. doi: 10.1071/RD9960485. PubMed DOI

Kranc W., Celichowski P., Budna J., Khozmi R., Bryja A., Ciesiółka S., Rybska M., Borys S., Jeseta M., Bukowska D., et al. Positive regulation of macromolecule metabolic process belongs to the main mechanisms crucial for porcine oocytes maturation. Adv. Cell Biol. 2017;5:15–32. doi: 10.1515/acb-2017-0002. DOI

Jin J.X., Lee S., Khoirinaya C., Oh A., Kim G.A., Lee B.C. Supplementation with spermine during in vitro maturation of porcine oocytes improves early embryonic development after parthenogenetic activation and somatic cell nuclear transfer. J. Anim. Sci. 2016;94:963–970. doi: 10.2527/jas.2015-9761. PubMed DOI

Galeati G., Giaretta E., Zannoni A., Bucci D., Tamanini C., Forni M., Spinaci M. Embelin supplementation of in vitro maturation medium does not influence nuclear and cytoplasmic maturation of pig oocytes. J. Physiol. Pharmacol. 2016;67:513–519. PubMed

Wu J., Emery B.R., Carrell D.T. In vitro growth, maturation, fertilization, and embryonic development of oocytes from porcine preantral follicles. Biol. Reprod. 2001;64:375–381. doi: 10.1095/biolreprod64.1.375. PubMed DOI

Budna J., Bryja A., Celichowski P., Kranc W., Ciesiolka S., Borys S., Rybska M., Kolecka-Bednarczyk A., Jeseta M., Bukowska D., et al. “Bone Development” Is an Ontology Group Upregulated in Porcine Oocytes before In Vitro Maturation: A Microarray Approach. DNA Cell Biol. 2017;36:638–646. doi: 10.1089/dna.2017.3677. PubMed DOI

Budna J., Bryja A., Celichowski P., Kahan R., Kranc W., Ciesiolka S., Rybska M., Borys S., Jeseta M., Bukowska D., et al. Genes of cellular components of morphogenesis in porcine oocytes before and after IVM. Reproduction. 2017;154:535–545. doi: 10.1530/REP-17-0367. PubMed DOI

Budna J., Rybska M., Ciesiolka S., Bryja A., Borys S., Kranc W., Wojtanowicz-Markiewicz K., Jeseta M., Sumelka E., Bukowska D., et al. Expression of genes associated with BMP signaling pathway in porcine oocytes before and after IVM—A microarray approach. Reprod. Biol. Endocrinol. 2017;15 doi: 10.1186/s12958-017-0261-6. PubMed DOI PMC

Kranc W., Budna J., Chachula A., Borys S., Bryja A., Rybska M., Ciesiolka S., Sumelka E., Jeseta M., Brussow K.P., et al. “Cell Migration” Is the Ontology Group Differentially Expressed in Porcine Oocytes Before and After In Vitro Maturation: A Microarray Approach. DNA Cell Biol. 2017;36:273–282. doi: 10.1089/dna.2016.3425. PubMed DOI

Budna J., Celichowski P., Karimi P., Kranc W., Bryja A., Ciesiółka S., Rybska M., Borys S., Jeseta M., Bukowska D., et al. Does Porcine oocytes maturation in vitro is regulated by genes involved in transforming growth factor beta receptor signaling pathway? Adv. Cell Biol. 2017;5:1–14. doi: 10.1515/acb-2017-0001. DOI

Cal S., Freije J.M., Lopez J.M., Takada Y., Lopez-Otin C. ADAM 23/MDC3, a human disintegrin that promotes cell adhesion via interaction with the alphavbeta3 integrin through an RGD-independent mechanism. Mol. Biol. Cell. 2000;11:1457–1469. doi: 10.1091/mbc.11.4.1457. PubMed DOI PMC

Tsanou E., Peschos D., Batistatou A., Charalabopoulos A., Charalabopoulos K. The E-cadherin adhesion molecule and colorectal cancer. A global literature approach. Anticancer Res. 2008;28:3815–3826. PubMed

Wang X., Tully O., Ngo B., Zitin M., Mullin J.M. Epithelial tight junctional changes in colorectal cancer tissues. Sci. World J. 2011;11:826–841. doi: 10.1100/tsw.2011.86. PubMed DOI PMC

Turksen K., Troy T.-C. Junctions gone bad: Claudins and loss of the barrier in cancer. Biochim. Biophys. Acta. 2011;1816:73–79. doi: 10.1016/j.bbcan.2011.04.001. PubMed DOI

Kanczuga-Koda L. Gap junctions and their role in physiology and pathology of the digestive tract. Postepy Hig. Med. Dosw. 2004;58:158–165. PubMed

Kempisty B., Ziolkowska A., Ciesiolka S., Piotrowska H., Antosik P., Bukowska D., Nowicki M., Brussow K.P., Zabel M. Study on connexin gene and protein expression and cellular distribution in relation to real-time proliferation of porcine granulosa cells. J. Biol. Regul. Homeost. Agents. 2014;28:625–635. PubMed

Tatone C., Carbone M.C. Possible involvement of integrin-mediated signalling in oocyte activation: Evidence that a cyclic RGD-containing peptide can stimulate protein kinase C and cortical granule exocytosis in mouse oocytes. Reprod. Biol. Endocrinol. 2006;4 doi: 10.1186/1477-7827-4-48. PubMed DOI PMC

Evans J.P., Schultz R.M., Kopf G.S. Identification and localization of integrin subunits in oocytes and eggs of the mouse. Mol. Reprod. Dev. 1995;40:211–220. doi: 10.1002/mrd.1080400210. PubMed DOI

Yuan Y., Krisher R.L. In vitro maturation (IVM) of porcine oocytes. Methods Mol. Biol. 2012;825:183–198. PubMed

Dunning K.R., Lane M., Brown H.M., Yeo C., Robker R.L., Russell D.L. Altered composition of the cumulus-oocyte complex matrix during in vitro maturation of oocytes. Hum. Reprod. 2007;22:2842–2850. doi: 10.1093/humrep/dem277. PubMed DOI

Budna J., Chachula A., Kazmierczak D., Rybska M., Ciesiolka S., Bryja A., Kranc W., Borys S., Zok A., Bukowska D., et al. Morphogenesis-related gene-expression profile in porcine oocytes before and after in vitro maturation. Zygote. 2017;25:331–340. doi: 10.1017/S096719941700020X. PubMed DOI

Arias-Alvarez M., Garcia-Garcia R.M., Lopez-Tello J., Rebollar P.G., Gutierrez-Adan A., Lorenzo P.L. In vivo and in vitro maturation of rabbit oocytes differently affects the gene expression profile, mitochondrial distribution, apoptosis and early embryo development. Reprod. Fertil. Dev. 2017;29:1667–1679. doi: 10.1071/RD15553. PubMed DOI

Yerushalmi G.M., Maman E., Yung Y., Kedem A., Hourvitz A. Molecular characterization of the human ovulatory cascade-lesson from the IVF/IVM model. J. Assist. Reprod. Genet. 2011;28:509–515. doi: 10.1007/s10815-011-9594-9. PubMed DOI PMC

Huang X., Hao C., Shen X., Zhang Y., Liu X. RUNX2, GPX3 and PTX3 gene expression profiling in cumulus cells are reflective oocyte/embryo competence and potentially reliable predictors of embryo developmental competence in PCOS patients. Reprod. Biol. Endocrinol. 2013;11 doi: 10.1186/1477-7827-11-109. PubMed DOI PMC

Dieci C., Lodde V., Labreque R., Dufort I., Tessaro I., Sirard M.-A., Luciano A.M. Differences in cumulus cell gene expression indicate the benefit of a pre-maturation step to improve in-vitro bovine embryo production. Mol. Hum. Reprod. 2016;22:882–897. PubMed

Kempisty B., Ziolkowska A., Piotrowska H., Ciesiolka S., Antosik P., Bukowska D., Zawierucha P., Wozna M., Jaskowski J.M., Brussow K.P., et al. Short-term cultivation of porcine cumulus cells influences the cyclin-dependent kinase 4 (Cdk4) and connexin 43 (Cx43) protein expression—A real-time cell proliferation approach. J. Reprod. Dev. 2013;59:339–345. doi: 10.1262/jrd.2012-162. PubMed DOI PMC

Kempisty B., Ziolkowska A., Piotrowska H., Zawierucha P., Antosik P., Bukowska D., Ciesiolka S., Jaskowski J.M., Brussow K.P., Nowicki M., et al. Real-time proliferation of porcine cumulus cells is related to the protein levels and cellular distribution of Cdk4 and Cx43. Theriogenology. 2013;80:411–420. doi: 10.1016/j.theriogenology.2013.05.016. PubMed DOI

Anderson E., Albertini D.F. Gap junctions between the oocyte and companion follicle cells in the mammalian ovary. J. Cell Biol. 1976;71:680–686. doi: 10.1083/jcb.71.2.680. PubMed DOI PMC

Guasch R.M., Scambler P., Jones G.E., Ridley A.J. RhoE regulates actin cytoskeleton organization and cell migration. Mol. Cell Biol. 1998;18:4761–4771. doi: 10.1128/MCB.18.8.4761. PubMed DOI PMC

Cox D., Brennan M., Moran N. Integrins as therapeutic targets: Lessons and opportunities. Nat. Rev. Drug Discov. 2010;9:804–820. doi: 10.1038/nrd3266. PubMed DOI

Lau L.F. CCN1/CYR61: The very model of a modern matricellular protein. Cell Mol. Life Sci. 2011;68:3149–3163. doi: 10.1007/s00018-011-0778-3. PubMed DOI PMC

Park S.-W., Bae J.-S., Kim K.-S., Park S.-H., Lee B.-H., Choi J.-Y., Park J.-Y., Ha S.-W., Kim Y.-L., Kwon T.-H., et al. Beta ig-h3 promotes renal proximal tubular epithelial cell adhesion, migration and proliferation through the interaction with alpha3beta1 integrin. Exp. Mol. Med. 2004;36:211–219. doi: 10.1038/emm.2004.29. PubMed DOI

Thumkeo D., Watanabe S., Narumiya S. Physiological roles of Rho and Rho effectors in mammals. Eur. J. Cell Biol. 2013;92:303–315. doi: 10.1016/j.ejcb.2013.09.002. PubMed DOI

Villalonga P., Guasch R.M., Riento K., Ridley A.J. RhoE inhibits cell cycle progression and Ras-induced transformation. Mol. Cell Biol. 2004;24:7829–7840. doi: 10.1128/MCB.24.18.7829-7840.2004. PubMed DOI PMC

Nousbeck J., Sarig O., Avidan N., Indelman M., Bergman R., Ramon M., Enk C.D., Sprecher E. Insulin-like growth factor-binding protein 7 regulates keratinocyte proliferation, differentiation and apoptosis. J. Investig. Dermatol. 2010;130:378–387. doi: 10.1038/jid.2009.265. PubMed DOI

Park S.-Y., Jung M.-Y., Kim I.-S. Stabilin-2 mediates homophilic cell–cell interactions via its FAS1 domains. FEBS Lett. 2009;583:1375–1380. doi: 10.1016/j.febslet.2009.03.046. PubMed DOI

Zhurinsky J., Shtutman M., Ben-Ze’ev A. Plakoglobin and beta-catenin: Protein interactions, regulation and biological roles. J. Cell Sci. 2000;113:3127–3139. PubMed

Liebig T., Erasmus J., Kalaji R., Davies D., Loirand G., Ridley A., Braga V.M.M. RhoE Is required for keratinocyte differentiation and stratification. Mol. Biol. Cell. 2009;20:452–463. doi: 10.1091/mbc.E07-11-1197. PubMed DOI PMC

Bektic J., Pfeil K., Berger A.P., Ramoner R., Pelzer A., Schafer G., Kofler K., Bartsch G., Klocker H. Small G-protein RhoE is underexpressed in prostate cancer and induces cell cycle arrest and apoptosis. Prostate. 2005;64:332–340. doi: 10.1002/pros.20243. PubMed DOI

Wajapeyee N., Serra R.W., Zhu X., Mahalingam M., Green M.R. Oncogenic BRAF induces senescence and apoptosis through pathways mediated by the secreted protein IGFBP7. Cell. 2008;132:363–374. doi: 10.1016/j.cell.2007.12.032. PubMed DOI PMC

Tamura K., Yoshie M., Hashimoto K., Tachikawa E. Inhibitory effect of insulin-like growth factor-binding protein-7 (IGFBP7) on in vitro angiogenesis of vascular endothelial cells in the rat corpus luteum. J. Reprod. Dev. 2014;60:447–453. doi: 10.1262/jrd.2014-069. PubMed DOI PMC

Vishnyakova T.G., Kurlander R., Bocharov A.V., Baranova I.N., Chen Z., Abu-Asab M.S., Tsokos M., Malide D., Basso F., Remaley A., et al. CLA-1 and its splicing variant CLA-2 mediate bacterial adhesion and cytosolic bacterial invasion in mammalian cells. Proc. Natl. Acad. Sci. USA. 2006;103:16888–16893. doi: 10.1073/pnas.0602126103. PubMed DOI PMC

Fritz G., Brachetti C., Bahlmann F., Schmidt M., Kaina B. Rho GTPases in human breast tumours: Expression and mutation analyses and correlation with clinical parameters. Br. J. Cancer. 2002;87:635–644. doi: 10.1038/sj.bjc.6600510. PubMed DOI PMC

Adnane J., Muro-Cacho C., Mathews L., Sebti S.M., Munoz-Antonia T. Suppression of rho B expression in invasive carcinoma from head and neck cancer patients. Clin. Cancer Res. 2002;8:2225–2232. PubMed

Mazieres J., Antonia T., Daste G., Muro-Cacho C., Berchery D., Tillement V., Pradines A., Sebti S., Favre G. Loss of RhoB expression in human lung cancer progression. Clin. Cancer Res. 2004;10:2742–2750. doi: 10.1158/1078-0432.CCR-03-0149. PubMed DOI

Gambaro K., Quinn M.C.J., Caceres-Gorriti K.Y., Shapiro R.S., Provencher D., Rahimi K., Mes-Masson A.-M., Tonin P.N. Low levels of IGFBP7 expression in high-grade serous ovarian carcinoma is associated with patient outcome. BMC Cancer. 2015;15 doi: 10.1186/s12885-015-1138-8. PubMed DOI PMC

Christenson L.K., Gunewardena S., Hong X., Spitschak M., Baufeld A., Vanselow J. Research resource: Preovulatory LH surge effects on follicular theca and granulosa transcriptomes. Mol. Endocrinol. 2013;27:1153–1171. doi: 10.1210/me.2013-1093. PubMed DOI PMC

Burghardt R.C., Johnson G.A., Jaeger L.A., Ka H., Garlow J.E., Spencer T.E., Bazer F.W. Integrins and extracellular matrix proteins at the maternal-fetal interface in domestic animals. Cells Tissues Organs. 2002;172:202–217. doi: 10.1159/000066969. PubMed DOI

Goossens K., van Soom A., van Zeveren A., Favoreel H., Peelman L.J. Quantification of fibronectin 1 (FN1) splice variants, including two novel ones, and analysis of integrins as candidate FN1 receptors in bovine preimplantation embryos. BMC Dev. Biol. 2009;9 doi: 10.1186/1471-213X-9-1. PubMed DOI PMC

He X., Li B., Wang F., Tian C., Rong W., Liu Y. Identification of differentially expressed genes in Mongolian sheep ovaries by suppression subtractive hybridization. Anim. Reprod. Sci. 2012;133:86–92. doi: 10.1016/j.anireprosci.2012.06.005. PubMed DOI

Smith S.R., Fulton N., Collins C.S., Welsh M., Bayne R.A.L., Coutts S.M., Childs A.J., Anderson R.A. N- and E-cadherin expression in human ovarian and urogenital duct development. Fertil. Steril. 2010;93:2348–2353. doi: 10.1016/j.fertnstert.2009.01.113. PubMed DOI

Wang C., Roy S.K. Expression of E-cadherin and N-cadherin in perinatal hamster ovary: Possible involvement in primordial follicle formation and regulation by follicle-stimulating hormone. Endocrinology. 2010;151:2319–2330. doi: 10.1210/en.2009-1489. PubMed DOI PMC

Kodama T., Matsukado Y., Suzuki T., Tanaka S., Shimizu H. Stimulated formation of adenosine 3′,5′-monophosphate by desipramine in brain slices. Biochim. Biophys. Acta. 1971;252:165–170. doi: 10.1016/0304-4165(71)90105-X. PubMed DOI

Mora J.M., Fenwick M.A., Castle L., Baithun M., Ryder T.A., Mobberley M., Carzaniga R., Franks S., Hardy K. Characterization and significance of adhesion and junction-related proteins in mouse ovarian follicles. Biol. Reprod. 2012;86:1–14. doi: 10.1095/biolreprod.111.096156. PubMed DOI

Kumar V., Maurya V.K., Joshi A., Meeran S.M., Jha R.K. Integrin beta 8 (ITGB8) regulates embryo implantation potentially via controlling the activity of TGF-B1 in mice. Biol. Reprod. 2015;92 doi: 10.1095/biolreprod.114.122838. PubMed DOI

Shen T.-L., Park A.Y.-J., Alcaraz A., Peng X., Jang I., Koni P., Flavell R.A., Gu H., Guan J.-L. Conditional knockout of focal adhesion kinase in endothelial cells reveals its role in angiogenesis and vascular development in late embryogenesis. J. Cell Biol. 2005;169:941–952. doi: 10.1083/jcb.200411155. PubMed DOI PMC

Ozawa A., Sato Y., Imabayashi T., Uemura T., Takagi J., Sekiguchi K. Molecular Basis of the Ligand Binding Specificity of alphavbeta8 Integrin. J. Biol. Chem. 2016;291:11551–11565. doi: 10.1074/jbc.M116.719138. PubMed DOI PMC

Thys M., Nauwynck H., Maes D., Hoogewijs M., Vercauteren D., Rijsselaere T., Favoreel H., van Soom A. Expression and putative function of fibronectin and its receptor (integrin alpha(5)beta(1)) in male and female gametes during bovine fertilization in vitro. Reproduction. 2009;138:471–482. doi: 10.1530/REP-09-0094. PubMed DOI

Tamura K., Matsushita M., Endo A., Kutsukake M., Kogo H. Effect of insulin-like growth factor-binding protein 7 on steroidogenesis in granulosa cells derived from equine chorionic gonadotropin-primed immature rat ovaries. Biol. Reprod. 2007;77:485–491. doi: 10.1095/biolreprod.106.058867. PubMed DOI

Wandji S.A., Gadsby J.E., Barber J.A., Hammond J.M. Messenger ribonucleic acids for MAC25 and connective tissue growth factor (CTGF) are inversely regulated during folliculogenesis and early luteogenesis. Endocrinology. 2000;141:2648–2657. doi: 10.1210/endo.141.7.7576. PubMed DOI

Casey O.M., Fitzpatrick R., McInerney J.O., Morris D.G., Powell R., Sreenan J.M. Analysis of gene expression in the bovine corpus luteum through generation and characterisation of 960 ESTs. Biochim. Biophys. Acta. 2004;1679:10–17. doi: 10.1016/j.bbaexp.2004.03.011. PubMed DOI

Zhang B., Tsang P.C.W., Pate J.L., Moses M.A. A role for cysteine-rich 61 in the angiogenic switch during the estrous cycle in cows: Regulation by prostaglandin F2alpha. Biol. Reprod. 2011;85:261–268. doi: 10.1095/biolreprod.110.086645. PubMed DOI PMC

Sampath D., Winneker R.C., Zhang Z. Cyr61, a member of the CCN family, is required for MCF-7 cell proliferation: Regulation by 17beta-estradiol and overexpression in human breast cancer. Endocrinology. 2001;142:2540–2548. doi: 10.1210/endo.142.6.8186. PubMed DOI

MacLaughlan S.D., Palomino W.A., Mo B., Lewis T.D., Lininger R.A., Lessey B.A. Endometrial expression of Cyr61: A marker of estrogenic activity in normal and abnormal endometrium. Obstet. Gynecol. 2007;110:146–154. doi: 10.1097/01.AOG.0000269047.46078.28. PubMed DOI

Borel F., Marzocca F., Delcros J.-G., Rama N., Mehlen P., Ferrer J.-L. Molecular characterization of Netrin-1 and APP receptor binding: New leads to block the progression of senile plaques in Alzheimer’s disease. Biochem. Biophys. Res. Commun. 2017;488:466–470. doi: 10.1016/j.bbrc.2017.05.056. PubMed DOI

Jackson S.W., Hoshi T., Wu Y., Sun X., Enjyoji K., Cszimadia E., Sundberg C., Robson S.C. Disordered purinergic signaling inhibits pathological angiogenesis in cd39/Entpd1-null mice. Am. J. Pathol. 2007;171:1395–1404. doi: 10.2353/ajpath.2007.070190. PubMed DOI PMC

Zou C., Huang W., Ying G., Wu Q. Sequence analysis and expression mapping of the rat clustered protocadherin gene repertoires. Neuroscience. 2007;144:579–603. doi: 10.1016/j.neuroscience.2006.10.011. PubMed DOI

Purohit A., Sadanandam A., Myneni P., Singh R.K. Semaphorin 5A mediated cellular navigation: Connecting nervous system and cancer. Biochim. Biophys. Acta. 2014;1846:485–493. doi: 10.1016/j.bbcan.2014.09.006. PubMed DOI PMC

Shimoda Y., Watanabe K. Contactins: Emerging key roles in the development and function of the nervous system. Cell Adhes. Migr. 2009;3:64–70. doi: 10.4161/cam.3.1.7764. PubMed DOI PMC

Kidd T., Brose K., Mitchell K.J., Fetter R.D., Tessier-Lavigne M., Goodman C.S., Tear G. Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell. 1998;92:205–215. doi: 10.1016/S0092-8674(00)80915-0. PubMed DOI

Vite A., Li J., Radice G.L. New functions for alpha-catenins in health and disease: From cancer to heart regeneration. Cell Tissue Res. 2015;360:773–783. doi: 10.1007/s00441-015-2123-x. PubMed DOI PMC

Sagane K., Ohya Y., Hasegawa Y., Tanaka I. Metalloproteinase-like, disintegrin-like, cysteine-rich proteins MDC2 and MDC3: Novel human cellular disintegrins highly expressed in the brain. Biochem. J. 1998;334:93–98. doi: 10.1042/bj3340093. PubMed DOI PMC

Goldsmith A.P., Gossage S.J., ffrench-Constant C. ADAM23 is a cell-surface glycoprotein expressed by central nervous system neurons. J. Neurosci. Res. 2004;78:647–658. doi: 10.1002/jnr.20320. PubMed DOI

Khan D.R., Landry D.A., Fournier E., Vigneault C., Blondin P., Sirard M.-A. Transcriptome meta-analysis of three follicular compartments and its correlation with ovarian follicle maturity and oocyte developmental competence in cows. Physiol. Genom. 2016;48:633–643. doi: 10.1152/physiolgenomics.00050.2016. PubMed DOI PMC

Yang J.J., Ye Y., Carroll A., Yang W., Lee H.W. Structural biology of the cell adhesion protein CD2: Alternatively folded states and structure-function relation. Curr. Protein Pept. Sci. 2001;2:1–17. doi: 10.2174/1389203013381251. PubMed DOI

Hattori N., Ueda M., Fujiwara H., Fukuoka M., Maeda M., Mori T. Human luteal cells express leukocyte functional antigen (LFA)-3. J. Clin. Endocrinol. Metab. 1995;80:78–84. PubMed

Soto-Pantoja D.R., Kaur S., Roberts D.D. CD47 signaling pathways controlling cellular differentiation and responses to stress. Crit. Rev. Biochem. Mol. Biol. 2015;50:212–230. doi: 10.3109/10409238.2015.1014024. PubMed DOI PMC

Gao A.G., Lindberg F.P., Finn M.B., Blystone S.D., Brown E.J., Frazier W.A. Integrin-associated protein is a receptor for the C-terminal domain of thrombospondin. J. Biol. Chem. 1996;271:21–24. doi: 10.1074/jbc.271.1.21. PubMed DOI

Bornstein P. Thrombospondins function as regulators of angiogenesis. J. Cell Commun. Signal. 2009;3:189–200. doi: 10.1007/s12079-009-0060-8. PubMed DOI PMC

Berisha B., Schams D., Rodler D., Sinowatz F., Pfaffl M.W. Expression and localization of members of the thrombospondin family during final follicle maturation and corpus luteum formation and function in the bovine ovary. J. Reprod. Dev. 2016;62:501–510. doi: 10.1262/jrd.2016-056. PubMed DOI PMC

Roca J., Martinez E., Vazquez J.M., Lucas X. Selection of immature pig oocytes for homologous in vitro penetration assays with the brilliant cresyl blue test. Reprod. Fertil. Dev. 1998;10:479–485. doi: 10.1071/RD98060. PubMed DOI