CXADR-like membrane protein (CLMP) in the rat ovary: stimulation by human chorionic gonadotrophin during the periovulatory period
Feixue Li A C , Xiaoping Miao A , Yonglong Chen A and Thomas E. CurryA Zhejiang Key Laboratory of Organ Development and Regeneration, Institute of Developmental and Regenerative Biology, College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 310036, People’s Republic of China.
B Department of Obstetrics and Gynecology, Chandler Medical Center, 800 Rose Street, University of Kentucky, Lexington, KY 40536, USA.
C Corresponding author. Email: lifx@hznu.edu.cn
Reproduction, Fertility and Development 28(6) 742-749 https://doi.org/10.1071/RD14201
Submitted: 11 June 2014 Accepted: 17 September 2014 Published: 17 November 2014
Abstract
CXADR-like membrane protein (CLMP) is a novel cell–cell adhesion molecule. The present study investigated the spatiotemporal expression pattern of CLMP and its regulation in the rat ovary during the periovulatory period. Real-time polymerase chain reaction analysis revealed that Clmp mRNA was rapidly stimulated in intact ovaries by 4 h after human chorionic gonadotrophin (hCG) treatment. In situ hybridisation analysis demonstrated that Clmp mRNA expression was stimulated in theca cells at 4 h after hCG and remained elevated until 12 h. Clmp mRNA was also upregulated in granulosa cells and was present in forming corpora lutea. Our data indicate that the protein kinase A but not the protein kinase C pathway regulates the expression of Clmp mRNA in granulosa cells. Phosphatidylinositol 3 kinase and p38 kinase are also involved in regulating Clmp mRNA expression. The stimulation of Clmp mRNA by hCG requires new protein synthesis. Furthermore, inhibition of epidermal growth factor receptor activation significantly inhibited Clmp mRNA expression, whereas inhibition of prostaglandin synthesis or progesterone action had no effect. The stimulation of CLMP in the rat ovary may be important in cell adhesion events during ovulation and luteal formation such as maintaining the structure and communication of ovarian follicular and luteal cells.
Additional keywords: adhesion molecule, corpus luteum, ovary, ovulation.
References
Ashkenazi, H., Cao, X., Motola, S., Popliker, M., Conti, M., and Tsafriri, A. (2005). Epidermal growth factor family members: endogenous mediators of the ovulatory response. Endocrinology 146, 77–84.| Epidermal growth factor family members: endogenous mediators of the ovulatory response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFGmt7jP&md5=66aecdc72196de20ef326abd17791de0CAS | 15459120PubMed |
Bazzoni, G., and Dejana, E. (2004). Endothelial cell-to-cell junctions: molecular organisation and role in vascular homeostasis. Physiol. Rev. 84, 869–901.
| Endothelial cell-to-cell junctions: molecular organisation and role in vascular homeostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtlCnu78%3D&md5=f01aecfadb478395313bbc4ae972152cCAS | 15269339PubMed |
Carvalho, C. R., Carvalheira, J. B., Lima, M. H., Zimmerman, S. F., Caperuto, L. C., Amanso, A., Gasparetti, A. L., Meneghetti, V., Zimmerman, L. F., Velloso, L. A., and Saad, M. J. (2003). Novel signal transduction pathway for luteinising hormone and its interaction with insulin: activation of Janus kinase/signal transducer and activator of transcription and phosphoinositol 3-kinase/Akt pathways. Endocrinology 144, 638–647.
| Novel signal transduction pathway for luteinising hormone and its interaction with insulin: activation of Janus kinase/signal transducer and activator of transcription and phosphoinositol 3-kinase/Akt pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtVWltLo%3D&md5=895389a8dc218d93aba0558fabafdfe4CAS | 12538627PubMed |
Conti, M., Hsieh, M., Park, J. Y., and Su, Y. Q. (2006). Role of the epidermal growth factor network in ovarian follicles. Mol. Endocrinol. 20, 715–723.
| Role of the epidermal growth factor network in ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xkt1Oqu78%3D&md5=3f3d9846fc3d15258f0b973862c74d87CAS | 16051667PubMed |
Eguchi, J., Wada, J., Hida, K., Zhang, H., Matsuoka, T., Baba, M., Hashimoto, I., Shikata, K., Ogawa, N., and Makino, H. (2005). Identification of adipocyte adhesion molecule (ACAM), a novel CTX gene family, implicated in adipocyte maturation and development of obesity. Biochem. J. 387, 343–353.
| Identification of adipocyte adhesion molecule (ACAM), a novel CTX gene family, implicated in adipocyte maturation and development of obesity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivFWls7g%3D&md5=691592bbf6b7a77d94ca22e9898699adCAS | 15563274PubMed |
Espey, L. L., and Richards, J. S. (2002). Temporal and spatial patterns of ovarian gene transcription following an ovulatory dose of gonadotrophin in the rat. Biol. Reprod. 67, 1662–1670.
| Temporal and spatial patterns of ovarian gene transcription following an ovulatory dose of gonadotrophin in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XptVels74%3D&md5=a3e75cc139fdd418e73feb21d8878f6bCAS | 12444039PubMed |
Espey, L. L., Ujioka, T., Russell, D. L., Skelsey, M., Vladu, B., Robker, R. L., Okamura, H., and Richards, J. S. (2000). Induction of early growth response protein-1 gene expression in the rat ovary in response to an ovulatory dose of human chorionic gonadotrophin. Endocrinology 141, 2385–2391.
| 1:CAS:528:DC%2BD3cXlt1Wmt7c%3D&md5=31737845d219489e06576176da43698cCAS | 10875238PubMed |
Fujiwara, H., Honda, T., Ueda, M., Nakamura, K., Yamada, S., Maeda, M., and Mori, T. (1997). Laminin suppresses progesterone production by human luteinising granulosa cells via interaction with integrin alpha 6 beta 1. J. Clin. Endocrinol. Metab. 82, 2122–2128.
| 1:CAS:528:DyaK2sXksVequ74%3D&md5=8942b64a181f0cb8877a9005b6ea22a3CAS | 9215282PubMed |
Fujiwara, H., Kataoka, N., Honda, T., Ueda, M., Yamada, S., Nakamura, K., Suginami, H., Mori, T., and Maeda, M. (1998). Physiological roles of integrin alpha 6 beta 1 in ovarian functions. Horm. Res. 50, 25–29.
| Physiological roles of integrin alpha 6 beta 1 in ovarian functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXltV2nt7Y%3D&md5=3a485fe845e0595d70f69fdcf7656096CAS | 9721588PubMed |
Khan-Dawood, F. S., Yang, J., and Dawood, M. Y. (1996). Localisation and expression of zonula occludens-1 tight junction-associated protein in baboon (Papio anubis) corpora lutea. Hum. Reprod. 11, 1262–1267.
| Localisation and expression of zonula occludens-1 tight junction-associated protein in baboon (Papio anubis) corpora lutea.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK28zisVKguw%3D%3D&md5=ea20db538b5c3c8bd15fe77904655c6bCAS | 8671437PubMed |
Kirkup, K. M., Mallin, A. M., and Bagnell, C. A. (2000). Inhibition of pig granulosa cell adhesion and growth in vitro by immunoneutralisation of epithelial cadherin. J. Reprod. Fertil. 120, 275–281.
| 1:CAS:528:DC%2BD3cXovVajuro%3D&md5=9064d3a21a3d71406d11b1bdefb95582CAS | 11058443PubMed |
Kõks, S., Velthut, A., Sarapik, A., Altmäe, S., Reinmaa, E., Schalkwyk, L. C., Fernandes, C., Lad, H. V., Soomets, U., Jaakma, Ü., and Salumets, A. (2010). The differential transcriptome and ontology profiles of floating and cumulus granulosa cells in stimulated human antral follicles. Mol. Hum. Reprod. 16, 229–240.
| The differential transcriptome and ontology profiles of floating and cumulus granulosa cells in stimulated human antral follicles.Crossref | GoogleScholarGoogle Scholar | 19933312PubMed |
Le Bellego, F., Pisselet, C., Huet, C., Monget, P., and Monniaux, D. (2002). Laminin–alpha6beta1 integrin interaction enhances survival and proliferation and modulates steroidogenesis of ovine granulosa cells. J. Endocrinol. 172, 45–59.
| Laminin–alpha6beta1 integrin interaction enhances survival and proliferation and modulates steroidogenesis of ovine granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpsFWlsQ%3D%3D&md5=8d889546772d8407bc56edbb2db547afCAS | 11786373PubMed |
Li, F., and Curry, T. E. (2009). Regulation and function of tissue inhibitor of metalloproteinase (TIMP) 1 and TIMP3 in periovulatory rat granulosa cells. Endocrinology 150, 3903–3912.
| Regulation and function of tissue inhibitor of metalloproteinase (TIMP) 1 and TIMP3 in periovulatory rat granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsV2qsrs%3D&md5=bf00db7d9561543c1c3c776d99c4315cCAS | 19389837PubMed |
Li, F., Liu, J., Jo, M., and Curry, T. E. (2011). A role for nuclear factor interleukin-3 (NFIL3), a critical transcriptional repressor, in down-regulation of periovulatory gene expression. Mol. Endocrinol. 25, 445–459.
| A role for nuclear factor interleukin-3 (NFIL3), a critical transcriptional repressor, in down-regulation of periovulatory gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvFamtL4%3D&md5=4c9090a86e15407e62dd3bbccc24e407CAS | 21212137PubMed |
Li, F., Jo, M., Curry, T. E., and Liu, J. (2012). Hormonal induction of polo-like kinases (Plks) and impact of Plk2 on cell cycle progression in the rat ovary. PLoS ONE 7, e41844.
| Hormonal induction of polo-like kinases (Plks) and impact of Plk2 on cell cycle progression in the rat ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFKht7%2FM&md5=f8d625a082846d79205e0af394974647CAS | 22870256PubMed |
Liang, T. W., Chiu, H. H., Gurney, A., Sidle, A., Tumas, D. B., Schow, P., Foster, J., Klassen, T., Dennis, K., DeMarco, R. A., Pham, T., Frantz, G., and Fong, S. (2002). Vascular endothelial-junctional adhesion molecule (VE-JAM)/JAM 2 interacts with T, NK and dendritic cells through JAM 3. J. Immunol. 168, 1618–1626.
| Vascular endothelial-junctional adhesion molecule (VE-JAM)/JAM 2 interacts with T, NK and dendritic cells through JAM 3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xht1Cgu74%3D&md5=423675351e235facf1282cd0fc34c1b8CAS | 11823489PubMed |
Liu, J., Maccalman, C. D., Wang, Y. L., and Leung, P. C. (2009a). Promotion of human trophoblast invasion by gonadotrophin-releasing hormone (GnRH) I and GnRH II via distinct signalling pathways. Mol. Endocrinol. 23, 1014–1021.
| Promotion of human trophoblast invasion by gonadotrophin-releasing hormone (GnRH) I and GnRH II via distinct signalling pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotlGjurc%3D&md5=d1866ed8d058fa913529c8cb417baeb9CAS | 19372239PubMed |
Liu, J., Park, E. S., and Jo, M. (2009b). Runt-related transcription factor 1 regulates luteinised hormone-induced prostaglandin-endoperoxide synthase 2 expression in rat periovulatory granulosa cells. Endocrinology 150, 3291–3300.
| Runt-related transcription factor 1 regulates luteinised hormone-induced prostaglandin-endoperoxide synthase 2 expression in rat periovulatory granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotlCrsLY%3D&md5=67a99cc3e95c2fad160f65f30af1feb8CAS | 19342459PubMed |
Liu, J., Yang, Y., Yang, Y., Zhang, Y., and Liu, W. (2011). Disrupting effects of bifenthrin on ovulatory gene expression and prostaglandin synthesis in rat ovarian granulosa cells. Toxicology 282, 47–55.
| Disrupting effects of bifenthrin on ovulatory gene expression and prostaglandin synthesis in rat ovarian granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXit1Gltrs%3D&md5=948baf3e6a53272f45ec1e51267ae706CAS | 21251947PubMed |
Liu, J., Zhao, M., Zhuang, S., Yang, Y., Yang, Y., and Liu, W. (2012). Low concentrations of o,p’-DDT inhibit gene expression and prostaglandin synthesis by oestrogen receptor-independent mechanism in rat ovarian cells. PLoS ONE 7, e49916.
| Low concentrations of o,p’-DDT inhibit gene expression and prostaglandin synthesis by oestrogen receptor-independent mechanism in rat ovarian cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVCnsbnN&md5=85f80df11d529ad38fde0a0e6b71a46fCAS | 23209616PubMed |
Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=224f15b9dfd00d92fda868e1cb065922CAS | 11846609PubMed |
Makrigiannakis, A., Coukos, G., Christofidou-Solomidou, M., Gour, B. J., Radice, G. L., Blaschuk, O., and Coutifaris, C. (1999). N-cadherin-mediated human granulosa cell adhesion prevents apoptosis: a role in follicular atresia and luteolysis? Am. J. Pathol. 154, 1391–1406.
| N-cadherin-mediated human granulosa cell adhesion prevents apoptosis: a role in follicular atresia and luteolysis?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjtl2iu7o%3D&md5=ac00dd628c02bab20f6712fc5ff7bee5CAS | 10329592PubMed |
Ostermann, G., Weber, K. S., Zernecke, A., Schroder, A., and Weber, C. (2002). JAM-1 is a ligand of the beta(2) integrin LFA-1 involved in transendothelial migration of leukocytes. Nat. Immunol. 3, 151–158.
| JAM-1 is a ligand of the beta(2) integrin LFA-1 involved in transendothelial migration of leukocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtVygur0%3D&md5=93acf41edd8ffc7fb21a8e3ec42afd36CAS | 11812992PubMed |
Raschperger, E., Engstrom, U., Pettersson, R. F., and Fuxe, J. (2004). CLMP, a novel member of the CTX family and a new component of epithelial tight junctions. J. Biol. Chem. 279, 796–804.
| CLMP, a novel member of the CTX family and a new component of epithelial tight junctions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtVSqtLzF&md5=0b3386aac15ca92cc9bf838c4b12f7b2CAS | 14573622PubMed |
Rozen, S., and Skaletsky, H. (2000). Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132, 365–386.
| 1:CAS:528:DyaK1MXmslKqsbo%3D&md5=c0a04cc2da37ce24293e88ef86ddb8e7CAS | 10547847PubMed |
Ryan, P. L., Valentine, A. F., and Bagnell, C. A. (1996). Expression of epithelial cadherin in the developing and adult pig ovary. Biol. Reprod. 55, 1091–1097.
| Expression of epithelial cadherin in the developing and adult pig ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmtlarsLo%3D&md5=7b6630417aa1bb71c5a2ae48e34726c4CAS | 8902222PubMed |
Salvador, L. M., Maizels, E., Hales, D. B., Miyamoto, E., Yamamoto, H., and Hunzicker-Dunn, M. (2002). Acute signalling by the LH receptor is independent of protein kinase C activation. Endocrinology 143, 2986–2994.
| Acute signalling by the LH receptor is independent of protein kinase C activation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xls1Sgt7o%3D&md5=56e56ee7e69d99ffb2f6433948d2ddf2CAS | 12130564PubMed |
Sayasith, K., Bouchard, N., Boerboom, D., Brown, K. A., Dore, M., and Sirois, J. (2005). Molecular characterisation of equine P-selectin (CD62P) and its regulation in ovarian follicles during the ovulatory process. Biol. Reprod. 72, 736–744.
| Molecular characterisation of equine P-selectin (CD62P) and its regulation in ovarian follicles during the ovulatory process.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvVeisbw%3D&md5=ae67c628b0026a213c1295361d239010CAS | 15564599PubMed |
Sze, K. L., Lee, W. M., and Lui, W. Y. (2008a). Expression of CLMP, a novel tight junction protein, is mediated via the interaction of GATA with the Kruppel family proteins, KLF4 and Sp1, in mouse TM4 Sertoli cells. J. Cell. Physiol. 214, 334–344.
| Expression of CLMP, a novel tight junction protein, is mediated via the interaction of GATA with the Kruppel family proteins, KLF4 and Sp1, in mouse TM4 Sertoli cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitlA%3D&md5=a5d6ee989f27dc17be6daa21e7dc6af9CAS | 17620326PubMed |
Sze, K. L., Lui, W. Y., and Lee, W. M. (2008b). Post-transcriptional regulation of CLMP mRNA is controlled by tristetraprolin in response to TNFalpha via c-Jun N-terminal kinase signalling. Biochem. J. 410, 575–583.
| Post-transcriptional regulation of CLMP mRNA is controlled by tristetraprolin in response to TNFalpha via c-Jun N-terminal kinase signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisVWgt7Y%3D&md5=9a06bb48bc1a4baeb04e63831324f733CAS | 18047469PubMed |
Van Der Werf, C. S., Wabbersen, T. D., Hsiao, N. H., Paredes, J., Etchevers, H. C., Kroisel, P. M., Tibboel, D., Babarit, C., Schreiber, R. A., Hoffenberg, E. J., Vekemans, M., Zeder, S. L., Ceccherini, I., Lyonnet, S., Ribeiro, A. S., Seruca, R., Te Meerman, G. J., van Ijzendoorn, S. C., Shepherd, I. T., Verheij, J. B., and Hofstra, R. M. (2012). CLMP is required for intestinal development, and loss-of-function mutations cause congenital short-bowel syndrome. Gastroenterology 142, 453–462.
| CLMP is required for intestinal development, and loss-of-function mutations cause congenital short-bowel syndrome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XivFyjs7s%3D&md5=42e523bae49944e6f2fce33e6db32c34CAS | 22155368PubMed |
Walz, A., Keck, C., Weber, H., Kissel, C., and Pietrowski, D. (2005). Effects of luteinising hormone and human chorionic gonadotrophin on corpus luteum cells in a spheroid cell culture system. Mol. Reprod. Dev. 72, 98–104.
| Effects of luteinising hormone and human chorionic gonadotrophin on corpus luteum cells in a spheroid cell culture system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXntlClsLw%3D&md5=d808ec6bb8cd4cbcb1a9f18578de8c8cCAS | 15948162PubMed |
Wang, C., and Roy, S. K. (2010). Expression of E-cadherin and N-cadherin in perinatal hamster ovary: possible involvement in primordial follicle formation and regulation by follicle-stimulating hormone. Endocrinology 151, 2319–2330.
| Expression of E-cadherin and N-cadherin in perinatal hamster ovary: possible involvement in primordial follicle formation and regulation by follicle-stimulating hormone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsFKgsLs%3D&md5=660ad3da32b95ce8ce9ba6453f71ef61CAS | 20219978PubMed |
Yasuda, K., Hagiwara, E., Takeuchi, A., Mukai, C., Matsui, C., Sakai, A., and Tamotsu, S. (2005). Changes in the distribution of tenascin and fibronectin in the mouse ovary during folliculogenesis, atresia, corpus luteum formation and luteolysis. Zoolog. Sci. 22, 237–245.
| Changes in the distribution of tenascin and fibronectin in the mouse ovary during folliculogenesis, atresia, corpus luteum formation and luteolysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvFSgtb0%3D&md5=ef6d8f0e8b2155103d8bfb149946aec4CAS | 15738644PubMed |
Zhao, M., Zhang, Y., Liu, W., Xu, C., Wang, L., and Gan, J. (2008). Oestrogenic activity of lambda-cyhalothrin in the MCF-7 human breast carcinoma cell line. Environ. Toxicol. Chem. 27, 1194–1200.
| Oestrogenic activity of lambda-cyhalothrin in the MCF-7 human breast carcinoma cell line.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXls1ajtL8%3D&md5=3211ce05b2375afa5de90fd0d25608aaCAS | 18419197PubMed |
Zhao, M., Zhang, Y., Wang, C., Fu, Z., Liu, W., and Gan, J. (2009). Induction of macrophage apoptosis by an organochlorine insecticide acetofenate. Chem. Res. Toxicol. 22, 504–510.
| Induction of macrophage apoptosis by an organochlorine insecticide acetofenate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsl2itQ%3D%3D&md5=24cc25d407c01af1a35912e4ad5747fcCAS | 19166338PubMed |
Zhao, M., Zhang, Y., Zhuang, S., Zhang, Q., Lu, C., and Liu, W. (2014). Disruption of the hormonal network and the enantioselectivity of bifenthrin in trophoblast: maternal–fetal health risk of chiral pesticides. Environ. Sci. Technol. 48, 8109–8116.
| Disruption of the hormonal network and the enantioselectivity of bifenthrin in trophoblast: maternal–fetal health risk of chiral pesticides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpvFCnurg%3D&md5=e036627db2a5519397ac30d4bda070dbCAS | 24938463PubMed |