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Osteopontin is expressed in the oviduct and promotes fertilization and preimplantation embryo development of mouse

Published online by Cambridge University Press:  29 September 2014

Qian Liu ,
Qing-zhen Xie ,
Yun Zhou  and
Jing Yang
Qian Liu
Affiliation:
Center for Reproductive Medicine, Renmin Hospital of Wuhan University, 238 Jie Fang Road, Wuhan, China.
Qing-zhen Xie*
Affiliation:
Center for Reproductive Medicine, Renmin Hospital of Wuhan University, 238 Jie Fang Road, Wuhan, China.
Yun Zhou
Affiliation:
Center for Reproductive Medicine, Renmin Hospital of Wuhan University, 238 Jie Fang Road, Wuhan, China.
Jing Yang*
Affiliation:
Center for Reproductive Medicine, Renmin Hospital of Wuhan University, 238 Jie Fang Road, Wuhan, China.
*
All correspondence to: Qing-zhen Xie. Center for Reproductive Medicine, Renmin Hospital of Wuhan University, 238 Jie Fang Road, Wuhan, China. Tel: +86 13296500268. Fax: +86 27 88080749. e-mail: [email protected]
Center for Reproductive Medicine, Renmin Hospital of Wuhan University, 238 Jie Fang Road, Wuhan, China. Tel: +86 13507182023. Fax: +86 27 88080749. e-mail: [email protected].
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Summary

Osteopontin (OPN) is a multifunctional phosphoprotein that is detected in various tissues, including male and female reproductive tracts. In this study, we evaluated OPN expression in mouse oviducts during the estrus cycle, and at days 1–5 of pregnancy and pseudopregnancy by reverse transcription polymerase chain reaction (RT-PCR) and immunohistochemistry. The mice oocytes, sperm and embryos were treated with different concentrations of anti-OPN antibody in vitro to detect the function of OPN in fertilization and preimplantation embryo development. OPN mRNA and protein expression in mouse oviducts were cyclic dependent throughout the estrous cycle, which was highest at estrous and lowest at diestrous. Such a phenomenon was consistent with the change in estrogen level in mice. The expression levels of OPN in mice oviduct of normal pregnancy and pseudopregnancy were significantly different, which indicated that OPN expression in mouse oviducts was depend on estrogen and preimplantation embryo. Furthermore, anti-OPN antibody treatment could reduce the rates of fertilization, cleavage and blastocyst formation in vitro in a dose-dependent way. Overall, our results indicated that the expression of OPN in mouse oviducts during the estrous cycle and early pregnancy is likely regulated by estrogen and the embryo, and OPN may play a vital role in oocyte fertilization and preimplantation embryo development.

Keywords

FertilizationMouseOsteopontinOviductPreimplantation embryo development
Type
Research Article
Information
Zygote , Volume 23 , Issue 4 , August 2015 , pp. 622 - 630
Copyright
Copyright © Cambridge University Press 2014 

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References

Bazer, F.W., Song, G., Kim, J., Erikson, D.W., Johnson, G.A., Burghardt, R.C., Gao, H., Carey Satterfield, M., Spencer, T.E. & Wu, G. (2012). Mechanistic mammalian target of rapamycin (MTOR) cell signaling: effects of select nutrients and secreted phosphoprotein 1 on development of mammalian conceptuses. Mol. Cell. Endocrinol. 354, 22–33.CrossRefGoogle ScholarPubMed
Bian, F., Mao, G., Guo, M., Mao, G., Wang, J., Li, J., Han, Y., Chen, X., Zhang, M. & Xia, G. (2012). Gradients of natriuretic peptide precursor A (NPPA) in oviduct and of natriuretic peptide receptor 1 (NPR1) in spermatozoon are involved in mouse sperm chemotaxis and fertilization. J. Cell. Physiol. 227, 2230–9.CrossRefGoogle ScholarPubMed
Botquin, V., Hess, H., Fuhrmann, G., Anastassiadis, C., Gross, M.K., Vriend, G., & Schöler, H.R. (1998). New POU dimer configuration mediates antagonistic control of an osteopontin preimplantation enhancer by Oct-4 and Sox-2. Genes Dev. 12, 2073–90.CrossRefGoogle ScholarPubMed
Briese, J., Oberndorfer, M., Patschenik, C., Schulte, H.M., Makrigiannakis, A., Löning, T., & Bamberger, A.M. (2005). Osteopontin is colocalized with the adhesion molecule CEACAM1 in the extravillous trophoblast of the human placenta and enhances invasion of CEACAM1-expressing placental cells. J. Clin. Endocrinol. Metab. 90, 5407–13.CrossRefGoogle ScholarPubMed
Brown, J.K., Shaw, J.L., Critchley, H.O. & Horne, A.W. (2012). Human fallopian tube epithelium constitutively expresses integrin endometrial receptivity markers: no evidence for a tubal implantation window. Mol. Hum. Reprod. 18, 111–20.CrossRefGoogle ScholarPubMed
Chabas, D., Baranzini, S. E., Mitchell, D., Bernard, C.C., Rittling, S.R., Denhardt, D.T., Sobel, R.A., Lock, C., Karpuj, M., Pedotti, R., Heller, R., Oksenberg, J.R, & Steinman, L. (2001). The influence of the proinflammatory cytokine, osteopontin, on autoimmune demyelinating disease. Science 294, 1731–5.CrossRefGoogle ScholarPubMed
Denhardt, D.T., Noda, M., O’Regan, A.W., Pavlin, D. & Berman, J.S. (2001). Osteopontin as a means to cope with environmental insults: regulation of inflammation, tissue remodeling, and cell survival. J. Clin. Invest. 107, 1055–61.CrossRefGoogle Scholar
Erikson, D.W., Way, A.L., Chapman, D.A. & Killian, G.J. (2007). Detection of osteopontin on Holstein bull spermatozoa, in cauda epididymal fluid and testis homogenates, and its potential role in bovine fertilization. Reproduction 133, 909–17.CrossRefGoogle ScholarPubMed
Gabler, C., Chapman, D.A. & Killian, G.J. (2003). Expression and presence of osteopontin and integrins in the bovine oviduct during the oestrous cycle. Reproduction 126, 721–9.CrossRefGoogle ScholarPubMed
Goncalves, R.F., Staros, A.L. & Killian, G.J. (2008). Oviductal fluid proteins associated with the bovine zona pellucida and the effect on in vitro sperm-egg binding, fertilization and embryo development. Reprod. Domest. Anim. 43, 720–9.CrossRefGoogle ScholarPubMed
Hag, A.M., Pedersen, S.F., Christoffersen, C., Binderup, T., Jensen, M.M., Jørgensen, J.T., Skovgaard, D., Ripa, R.S. & Kjaer, A. (2012). (18)F-FDG PET imaging of murine atherosclerosis: association with gene expression of key molecular markers. PLoS One 7, e50908.CrossRefGoogle ScholarPubMed
Hao, Y., Mathialagan, N., Walters, E., Mao, J., Lai, L., Becker, D., Li, W., Critser, J. & Prather, R.S. (2006). Osteopontin reduces polyspermy during in vitro fertilization of porcine oocytes. Biol. Reprod. 75, 726–33.CrossRefGoogle ScholarPubMed
Hao, Y., Murphy, C.N., Spate, L., Wax, D., Zhong, Z., Samuel, M., Mathialagan, N., Schatten, H., & Prather, R.S. (2008). Osteopontin improves in vitro development of porcine embryos and decreases apoptosis. Mol. Reprod. Dev. 75, 291–8.CrossRefGoogle ScholarPubMed
Lee, K.F., Yao, Y.Q., Kwok, K.L., Xu, J.S. & Yeung, W.S. (2002). Early developing embryos affect the gene expression patterns in the mouse oviduct. Biochem. Biophys. Res. Commun. 292, 564–70.CrossRefGoogle ScholarPubMed
Lee, K.F., Xu, J.S., Lee, Y.L. & Yeung, W.S. (2006). Demilune cell and parotid protein from murine oviductal epithelium stimulates preimplantation embryo development. Endocrinology 147, 79–87.CrossRefGoogle ScholarPubMed
Lim, W., Jeong, W., Kim, J., Ka, H., Bazer, F.W., Han, J.Y. & Song, G. (2012). Differential expression of secreted phosphoprotein 1 in response to estradiol-17beta and in ovarian tumors in chickens. Biochem. Biophys. Res. Commun. 422, 494–500.CrossRefGoogle ScholarPubMed
Lorenzen, J.M., Martino, F., Scheffner, I., Bröcker, V., Leitolf, H., Haller, H., & Gwinner, W. (2012). Fetuin, matrix-Gla protein and osteopontin in calcification of renal allografts. PLoS One 7, e52039.CrossRefGoogle ScholarPubMed
Makrigiannakis, A., Karamouti, M., Petsas, G., Makris, N., Nikas, G. & Antsaklis, A. (2009). The expression of receptivity markers in the fallopian tube epithelium. Histochem. Cell Biol. 132, 159–67.CrossRefGoogle ScholarPubMed
Oldberg, A., Franzen, A. & Heinegard, D. (1986). Cloning and sequence analysis of rat bone sialoprotein (osteopontin) cDNA reveals an Arg-Gly-Asp cell-binding sequence. Proc. Natl. Acad. Sci. USA 83, 8819–23.CrossRefGoogle ScholarPubMed
Qi, S., Huang, G., Pan, J., Li, J., Zhang, X., Fang, L., Liu, B., Meng, W., Zhang, Y. & Liu, X. (2010). Involvement of osteopontin as a core protein in 336 craniopharyngioma calcification formation. J. Neur. Oncol. l98, 21–30.Google Scholar
Souza, F.F., Chirinéa, V.H., Martins, M.I. & Lopes, M.D. (2009). Osteopontin in seminal plasma and sperm membrane of dogs. Reprod. Domest. Anim. 44 (Suppl. 2), 283–6.CrossRefGoogle ScholarPubMed
Wang, H. & Dey, S.K. (2006). Roadmap to embryo implantation: clues from mouse models. Nat. Rev. Genet. 7, 185–99.CrossRefGoogle ScholarPubMed
Wang, K.X. & Denhardt, D.T. (2008). Osteopontin: role in immune regulation and stress responses. Cytokine Growth Factor Rev. 19, 333–45.CrossRefGoogle ScholarPubMed
Xie, Q.Z, Qi, Q.R., Chen, Y.X, Xu, W.M, Liu, Q. & Yang, J. (2013). Uterine micro-environment and estrogen-dependent regulation of osteopontin expression in mouse blastocyst. Int. J. Mol. Sci. 14, 14504–7.CrossRefGoogle ScholarPubMed
Yamaga, M., Tsuji, K., Miyatake, K., Yamada, J., Abula, K., Ju, Y.J., Sekiya, I. & Muneta, T. (2012). Osteopontin level in synovial fluid is associated with the severity of joint pain and cartilage degradation after anterior cruciate ligament rupture. PLoS One 7, e49014.CrossRefGoogle ScholarPubMed
Yamaguchi, Y., Shao, Z., Sharif, S., Du, X.Y, Myles, T., Merchant, M., Harsh, G., Glantz, M., Recht, L., Morser, J. & Leung, L.L. (2013). Thrombin-cleaved fragments of osteopontin are overexpressed in malignant glial tumors and provide a molecular niche with survival advantage. J. Biol. Chem. 288, 3097–111.Google ScholarPubMed