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Oviductal and endometrial mRNA expression of implantation candidate biomarkers during early pregnancy in rabbit

Published online by Cambridge University Press:  29 November 2013

Ayman Moustafa Saeed ,
María de los Desamparados Saenz de Juano ,
Francisco Marco Jiménez  and
José Salvador Vicente
Ayman Moustafa Saeed
Affiliation:
Animal Production Research Institute, Animal Biotechnology Department. Giza, Egypt.
María de los Desamparados Saenz de Juano
Affiliation:
Instituto de Ciencia y Tecnología Animal, Universidad Politécnica de Valencia, 46022-Valencia, Spain.
Francisco Marco Jiménez
Affiliation:
Instituto de Ciencia y Tecnología Animal, Universidad Politécnica de Valencia, 46022-Valencia, Spain.
José Salvador Vicente*
Affiliation:
Reproduction Biotechnology Laboratory, Institute of Science and Animal Technology (ICTA) at the Polytechnic University of Valencia, C/Camino de Vera s/n, 46022 Valencia, Spain Instituto de Ciencia y Tecnología Animal, Universidad Politécnica de Valencia, 46022-Valencia, Spain.
*
All correspondence to: José Salvador Vicente. Reproduction Biotechnology Laboratory, Institute of Science and Animal Technology (ICTA) at the Polytechnic University of Valencia, C/Camino de Vera s/n, 46022 Valencia, Spain. Tel: +34 96 3879754. Fax: +34 96 3877439. e-mail address: [email protected]
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Summary

Prenatal losses are a complex problem. Pregnancy requires orchestrated communication between the embryo and the uterus that includes secretions from the embryo to signal pregnancy recognition and secretion and remodelling from the uterine epithelium. Most of these losses are characterized by asynchronization between embryo and uterus. To better understand possible causes, an analysis was conducted of gene expression of a set of transcripts related to maternal recognition and establishment of rabbit pregnancy (uteroglobin, SCGB1A1; integrin α1, ITGA1; interferon-γ, IFNG; vascular endothelial growth factor, VEGF) in oviduct and uterine tissue at 16, 72 or 144 h post-ovulation and insemination. In the oviduct tissue, a significant decrease in the level of SCGB1A1 mRNA expression was observed from 144 h post-ovulation. In the case of ITGA1, the transcript abundance was initially lower, but mRNA expression increased significantly at 72 and 144 h post-ovulation. For IFNG, a huge decrease was observed from 16 to 72 h post-ovulation. Finally, no significant differences were observed in the VEGF transcript. For the endometrium, the results showed a significant decline in the level of SCGB1A1 mRNA expression from 16 to 144 h post-ovulation induction. The highest levels of ITGA1 transcript were detected at 144 h, followed by the 16 h group and lower at 72 h post-ovulation. For IFNG there were no significant differences among post-ovulation induction times. Finally, it was possible to observe that VEGF mRNA abundance was present at low levels at 16 h post-ovulation and remained low at 72 h, but increased at 144 h. The functional significance of these observations may provide new insights into the maternal role in prenatal losses.

Keywords

EndometriumImplantation biomarkersOviductRabbit
Type
Research Article
Information
Zygote , Volume 23 , Issue 2 , April 2015 , pp. 288 - 296
Copyright
Copyright © Cambridge University Press 2013 

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References

Aboagye-Mathiesen, G., Tóth, F.D., Zdravkovic, M. & Ebbesen, P. (1995). Human trophoblast interferons: production and possible roles in early pregnancy. Early Pregnancy 1, 41–53.Google ScholarPubMed
Adams, C.E. (1960). Prenatal mortality in the rabbit Oryctolagus cuniculus. J. Reprod. Fertil. 1, 36–44.Google Scholar
Artini, P.G., Valentino, V., Montleone, P., Simi, G., Parisen-Toldin, M.R., Critello, F., Cela, V. & Genazzani, A.R. (2008). Vascular endothelial growth factor level changes during human embryo development in culture medium. Gynecol. Endocrinol. 24, 184–7.Google Scholar
Aviles, M., Gutierrez-Adan, A. & Coy, P. (2010). Oviductal secretions: will they be key factors for the future ARTs? Mol. Hum. Reprod. 16, 896–906.CrossRefGoogle ScholarPubMed
Beier, H.M. (1968). Uteroglobin: a hormone-sensitive endometrial protein involved in blastocyst development. Biochim. Biophys. Acta 160, 289–91.CrossRefGoogle ScholarPubMed
Beier, H.M. (2000). The discovery of uteroglobin and its significance for reproductive biology and endocrinology. Ann. N Y Acad. Sci. 923, 9–24.Google Scholar
Bowen, J.A., Bazer, F.W. & Burghardt, R.C. (1996). Spatial and temporal analyses of integrin and Muc-1 expression in porcine uterine epithelium and trophectoderm in vivo. Biol. Reprod. 55, 1098–106.CrossRefGoogle ScholarPubMed
Burghardt, R.C., Johnson, G.A., Jaeger, L.A., Ka, H., Garlow, J.E., Spencer, T.E. & Bazer, F.W. (2002). Integrins and extracellular matrix proteins at the maternal–fetal interface in domestic animals. Cells Tissues Organs 171, 202–17.CrossRefGoogle Scholar
Carney, E.W., Tobback, C. & Foote, R.H. (1990). Co-culture of rabbit one-cell embryos with rabbit oviduct epithelial cells. In Vitro Cell Dev. Biol. 26, 629–35.Google Scholar
Chakraborty, I., Das, S.K. & Dey, S.K. (1995). Differential expression of vascular endothelial growth factor and its receptor mRNAs in the mouse uterus around the time of implantation. J. Endocrinol. 147, 339–52.Google Scholar
Chandra, T., Woo, S.L. & Bullock, D.W. (1980). Cloning of thc rabbit uteroglobin structural gene. Biochem. Biophys. Res. Commun. 95, 197–204.Google Scholar
Cross, J.C. & Roberts, R.M. (1989). Porcine conceptuses secrete an interferon during the preattachment period of early pregnancy. Biol. Reprod. 40, 1109–18.CrossRefGoogle ScholarPubMed
Das, S.K., Chakraborty, I., Wang, J., Dey, S.K. & Hoffman, L.H. (1997). Expression of vascular endothelial growth factor (VEGF) and VEGF-receptor messenger ribonucleic acids in the peri-implantation rabbit uterus. Biol. Reprod. 56, 1390–9.Google Scholar
Denker, H.W. (1977). Implantation: the role of proteinases and blockage of implantation by proteinase inhibitors. Adv. Anat. Embryol. Cell Biol. 53, 1–123.Google Scholar
Druckmann, R. & Druckmann, M.A. (2005). Progesterone and the immunology of pregnancy. J. Steroid Biochem. Mol. Biol. 97, 389–96.Google Scholar
Enders, A.C. (1994). Contributions of comparative studies to understanding mechanisms of implantation. In Endocrinology of Embryo-Endometrium Interactions (eds Glasser, S.R., Mulholland, J. & Psychoyos, A.) pp. 11–16. New York and London: Plenum Press.Google Scholar
Enders, A.C. & Schlafke, S. (1971). Penetration of the uterus epithelium during implantation in the rabbit. Am. J. Anat. 132, 219–30.Google Scholar
Fazleabas, A.T.F., Donnelly, K.M., Hild-Petito, S., Hausermann, H.M. & Verhage, H.G. (1997). Secretory proteins of the baboon (Papio anubis) endometrium: regulation during the menstrual cycle and early pregnancy. Hum. Reprod. 3, 553–9.Google Scholar
Ferrara, N. & Davis-Smyth, T. (1997). The biology of vascular endothelial growth factor. Endocr. Rev. 18, 4–25.Google Scholar
Fleming, T.P., Kwong, W.Y., Porter, R., Ursell, E., Fesenko, I., Wilkins, A., Miller, D.J., Watkins, A.J. & Eckert, J.J. (2004). The embryo and its future. Biol. Reprod. 71, 1046–54.CrossRefGoogle ScholarPubMed
Fukuda, M.N., Sato, T., Nakayama, J., Klier, G., Mikami, M., Aoki, D. & Nozawa, S. (1995). Trophinin and tastin, a novel cell adhesion molecule complex with potential involvement in embryo implantation. Genes Dev. 9, 1199–210.Google Scholar
Godornes, C., Leader, B.T., Molini, B.J., Centurion-Lara, A. & Lukehart, S.A. (2007). Quantitation of rabbit cytokine mRNA by real-time RT-PCR. Cytokine 38, 1–7.Google Scholar
Grippo, A.A., S. H. Anderson, S.H., Chapman, D.A., Henault, M.A. & Killian, G.J. (1994). Cholesterol, phospholipid and phospholipase activity of ampullary and isthmic fluid from the bovine oviduct. J. Reprod. Fertil. 102, 87–93.Google Scholar
Henault, M.A. & Killian, G.J. (1993). Synthesis and secretion of lipids by bovine oviduct mucosal explants. J. Reprod. Fertil. 98, 431–43.Google Scholar
Hoffman, L.H., Olson, G.E., Carson, D.D. & Chilton, B.S. (1998). Progesterone and implanting blastocysts regulate Muc1 expression in rabbit uterine epithelium. Endocrinology 139, 266–71.Google Scholar
Illera, M.J., Lorenzo, P.L., Gui, L.T., Beyler, S.A., Apparao, K.B.C. & Lessey, B.A. (2003). A role for αVβ3 integrin during implantation in the rabbit model. Biol. Reprod. 68, 766–71.Google Scholar
Kay, E. & Feigelson, M. (1972). An estrogen modulated protein in rabbit oviductal fluid. Biochim. Biophys. Acta 271, 436–41.CrossRefGoogle Scholar
Killian, G.J. (2004). Evidence for the role of oviduct secretions in sperm function, fertilization and embryo development. Anim. Reprod. Sci. 82–83, 141–53.Google Scholar
Krishnan, R. S. & Daniel, J.C. (1967). Blastokinin: inducer and regulator of blastocyst development in the rabbit uterus. Science 158, 490–2.Google Scholar
Kopu, H.T., Hemminki, S.M., Torkkeli, T.K. & Janne, O.A. (1979). Hormonal control of uteroglobin secretion in rabbit uterus: inhibition of uteroglobin synthesis and messenger ribonucleic acid accumulation by oestrogen and anti-oestrogen administration. Biochem. J. 180, 491–500.Google Scholar
Krusche, C.A., Vloet, T.D., Herrler, A., Black, S. & Beier, H.M. (2002). Functional and structural regression of the rabbit corpus luteum is associated with altered luteal immune cell phenotypes and cytokine expression patterns. Histochem. Cell. Biol. 118, 479–89.Google Scholar
Lai, Y.M., Wang, H.S., Lee, C.L., Lee, J.D., Huang, H.Y., Chang, F.H., Lee, J.F. & Soong, Y.K. (1996). Insulin-like growth factor-binding proteins produced by Vero cells, human oviductal cells and human endometrial cells, and the role of insulin-like growth factor-binding protein-3 in mouse embryo co-culture systems. Hum. Reprod. 11, 1281–6.CrossRefGoogle ScholarPubMed
Lee, K.Y. & DeMayo, F.J. (2004). Animal models of implantation. Reproduction 128, 679–95.Google Scholar
Leese, H.J. (1988). The formation and function of oviduct fluid. J. Reprod. Fertil. 82, 843–56.Google Scholar
Lessey, B.A. (1998). Endometrial integrins and the establishment of uterine receptivity. Hum. Reprod. 13, 247–58.Google Scholar
Lessey, B.A., Ilesanmi, A.O., Sun, J., Lessey, M.A., Harris, J. & Chwalisz, K. (1996). Luminal and glandular endometrial epithelium express integrins differentially throughout the menstrual cycle: implications for implantation, contraception, and infertility. Am. J. Reprod. Immunol. 35, 195–204.Google Scholar
Llobat, L., Marco-Jiménez, F., Peñaranda, D.S., Thieme, R., Navarrete-Santos, A. & Vicente, J.S. (2012a). mRNA expression in rabbit blastocyst and endometrial tissue of candidate gene involved in gestational losses. Reprod. Domest. Anim. 47, 281–7.Google Scholar
Llobat, L., Marco-Jiménez, F., Peñaranda, D.S., Saenz-de-Juano, M.D. & Vicente, J.S. (2012b). Effect of embryonic genotype on reference gene selection for RT-qPCR normalization. Reprod. Domest. Anim. 47, 629–34.CrossRefGoogle ScholarPubMed
Lloyd, R.E., Romar, R., Matas, C., Gutierrez-Adan, A., Holt, W.V. & Coy, P. (2009). Effects of oviductal fluid on the development, quality, and gene expression of porcine blastocysts produced in vitro. Reproduction 137, 679–87.Google Scholar
Lonergan, P., Rizos, D., Kanka, J., Nemcova, L., Mbaye, A.M., Kingston, M., Wade, M., Duffy, P. & Boland, M.P. (2003). Temporal sensitivity of bovine embryos to culture environment after fertilization and the implications for blastocyst quality. Reproduction 126, 337–46.Google Scholar
Mamo, S., Gal, A.B., Polgar, Z. & Dinnyes, A. (2008). Expression profiles of the pluripotency marker gene POU5f1 and validation of reference genes in rabbit oocytes and preimplantation stage embryos. BMC Mol. Biol. 9, 67.Google Scholar
Marco-Jiménez, F., Vicente, J.S., Lavara, R., Balasch, S. & Viudes-de-Castro, M.P. (2010). Poor prediction value of sperm head morphometry for fertility and litter size in rabbit. Reprod. Domest. Anim. 45, 118–23.Google Scholar
McLaren, A. & Michie, D. (1954). Studies on the transfer of fertilized mouse eggs to uterine foster-mothers. J. Exp. Biol. 33, 394–416.Google Scholar
Minami, N., Kato, H., Inoue, Y., Yamada, M., Utsumi, K. & Iritani, A. (1994). Nonspecies-specific effects of mouse oviducts on the development of bovine IVM/IVF embryos by a serum free co-culture. Theriogenology 41, 1435–45.Google Scholar
Mocé, M.L., Santacreu, M.A. & Climent, A. (2002). The effect of divergent selection for uterine capacity on progesterone, estradiol and cholesterol levels around implantation time in rabbits. World Rabbit Sci. 10, 89–97.Google Scholar
Mukherjee, A.B., Zhang, Z. & Chilton, B.S. (2007). Uteroglobin: a steroid-inducible immunomodulatory protein that founded the secretoglobin superfamily. Endocr. Rev. 28, 707–25.CrossRefGoogle ScholarPubMed
Muller, H. & Beato, M. (1980). RNA synthesis in rabbit endometrial nuclei. Hormonal regulation of transcription of the uteroglobin gene. Eur. J. Biochem. 112, 235–41.Google Scholar
Murata, T., Hori, M., Lee, S., Nakamura, A., Kohama, K., Karaki, H. & Ozaki, H. (2005). Vascular endothelium has a local anti-adenovirus vector system and glucocorticoid optimizes its gene transduction. Arterioscler. Thromb. Vasc. Biol. 25, 1796–803.Google Scholar
Muscettola, M., Massai, L., Lodi, L., Briganti, F., Fontani, G. & Lupo, C. (2003). IFN-gamma production in rabbits: behavioral and endocrine correlates. Life Sci. 72, 1331–43.CrossRefGoogle ScholarPubMed
Naturil-Alfonso, C., Vicente, J.S., Peñaranda, D.S. & Marco-Jiménez, F. (2013). Up-regulation of insulin-like growth factor I and uteroglobin in in vivo-developed parthenogenetic embryos. Reprod. Domest. Anim. 48, 126–30.Google Scholar
Navarrete-Santos, A., Ramin, N., Tonack, S. & Fischer, B. (2008). Cell lineage-specific signaling of insulin and insulin-like growth factor I in rabbit blastocysts. Endocrinology 149, 515–24.Google Scholar
Paria, B.C., Song, H. & Dey, S.K. (2001). Implantation: molecular basis of embryo–uterine dialogue. Int. J. Dev. Biol. 45, 597–606.Google ScholarPubMed
Peri, A., Dubin, N.H., Dhanireddy, R. & Mukherjee, A.B. (1995). Uteroglobin gene expression in the rabbit uterus throughout gestation and in the fetal lung. Relationship between uteroglobin and eicosanoid levels in the developing fetal lung. J. Clin. Invest. 96, 343–53.CrossRefGoogle ScholarPubMed
Platt, J.S. & Hunt, J.S. (1998). Interferon-gamma gene expression in cycling and pregnant mouse uterus: temporal aspects and cellular localization. J. Leukoc. Biol. 64, 393–400.Google Scholar
Pollard, J.W., Hunt, J.S., Wiktor-Jedrzejczak, W. & Stanley, E.R. (1991). A pregnancy defect in the osteopetrotic (op/op) mouse demonstrates the requirement for CSF-1 in female fertility. Dev. Biol. 148, 273–83.Google Scholar
Psychoyos, A. (1986). Uterine receptivity for nidation. Ann. N Y Acad. Sci. 476, 36–42.Google Scholar
Psychoyos, A. & Nikas, G. (1994). Uterine pinopodes as markers of uterine receptivity. Assisted Reprod. Rev. 4, 26–32.Google Scholar
Riffo, M., Diaz-Gonzalez, K. & Nieto, A., (2007). Uteroglobin induces the development and cellular proliferation of the mouse early embryo. J. Exp. Zool. 307, 28–34.Google Scholar
Rizos, D., Carter, F., Besenfelder, U., Havlicek, V. & Lonergan, P. (2010). Contribution of the female reproductive tract to low fertility in postpartum lactating dairy cows. J. Dairy Sci. 93, 1022–9.Google Scholar
Saenz-de-Juano, M.D., Peñaranda, D.S., Marco-Jiménez, F., Llobat, L. & Vicente, J.S. (2011). Differential mRNA expression in rabbit in vivo preimplantation embryos. Reprod. Dom. Anim. 46, 567–72.Google Scholar
Saenz-de-Juano, M.D., Marco-Jiménez, F., Peñaranda, D.S., Joly, T. & Vicente, J.S. (2012). Effects of slow freezing procedure on late blastocyst gene expression and survival rate in rabbit. Biol. Reprod. 87, 91.CrossRefGoogle ScholarPubMed
Salilew-Wondim, D., Schellander, K., Hoelker, M. & Tesfaye, D. (2012). Oviductal, endometrial and embryonic gene expression patterns as molecular clues for pregnancy establishment. Anim. Reprod. Sci. 134, 9–18.Google Scholar
Sharkey, A. (1998). Cytokines and implantation. Rev. Reprod. 3, 52–61.Google Scholar
Shen, X.Z., Tsai, M.J., Bullock, D.W. & Woo, S.L. (1983). Hormonal regulation of rabbit uteroglobin gene transcription. Endocrinology 112, 871–6.Google Scholar
Snead, R., Day, L., Chandra, T., Mace, M. Jr, Bullock, D.W. & Woo, S.L. (1981). Mosaic structure and mRNA precursors of uteroglobin, a hormone regulated mammalian gene. J. Biol. Chem. 256, 11911–6.Google Scholar
Spencer, T.E., Burghardt, R.C., Johnson, G.A. & Bazer, F.W. (2004). Conceptus signals for establishment and maintenance of pregnancy. Anim. Reprod. Sci. 82–83, 537–50.Google Scholar
Stewart, C.L., Kaspar, P., Brunet, L.J., Bhatt, H., Gadi, I., Köntgen, F. & Abbondanzo, J.S. (1992). Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359, 76–9.Google Scholar
Sutherland, A.E., Calarco, P.G. & Damsky, C.H. (1993). Developmental regulation of integrin expression at the time of implantation in the mouse embryo. Development 119, 1175–86.Google Scholar
Szekeres-Bartho, J. (2002). Immunological relationship between the mother and the fetus. Int. Rev. Immunol. 21, 471–95.Google Scholar
Tesfaye, D., Salilew-Wondim, D. & Schellander, K. (2011). The role of endometrium in bovine pregnancy establishment. In 27th Annual Meeting AETE, Chester, England, 9–10 September 2011 (eds AETE) pp. 75–86. Chester, UK: AETE.Google Scholar
Torry, D.S., Leavenworth, J., Chang, M., Maheshwari, V., Groesch, K., Ball, E.R. & Torry, R.J. (2007). Angiogenesis in implantation. J. Assist. Reprod. Genet. 24, 303–15.Google Scholar
van Mourik, M.S.M., Macklon, N.S. & Heijnen, C.J. (2009). Embryonic implantation: cytokines, adhesion molecules, and immune cells in establishing an implantation environment. J. Leukoc. Biol. 85, 4–19.Google Scholar
Vecchio, D., Neglia, G., Di Palo, R., Campanile, G., Balestrieri, M., Giovane, A., Killian, G., Zicarelli, L. & Gasparrini, B. (2010). Ion, protein, phospholipid and energy substrate content of oviduct fluid during the oestrous cycle of buffalo (Bubalus bubalis). Reprod. Domest. Anim. 45, e32–9.Google Scholar
Viudes-De-Castro, M.P. & Vicente, J.S. (1997). Effect of sperm count on the fertility and prolificity rates of meat rabbits. Anim. Reprod. Sci. 46, 313–9.Google Scholar
Weitlauf, H.M. (1994). Biology of implantation. In The Physiology of Reproduction (eds Knobil, E. & Neill, J.D.) pp. 391–440. New York: Raven Press.Google Scholar
Weltzien, F.A., Pasqualini, C., Vernier, P. & Dufour, S. (2005). A quantitative real-time RT-PCR assay for European eel tyrosine hydroxylase. Gen. Comp. Endocrinol. 142, 134–42.Google Scholar
Wijayagunawardane, M.P., Kodithuwakku, S.P., Yamamoto, D. & Miyamoto, A. (2005). Vascular endothelial growth factor system in the cow oviduct: a possible involvement in the regulation of oviductal motility and embryo transport. Mol. Reprod. Dev. 72, 511–20.Google Scholar
Winterhager, E., Mulholland, J. & Glasser, S.R. (1994). Morphological and immunohistochemical differentiation patterns of rabbit uterine epithelium in vitro. Anat. Embryol. 189, 71–9.Google Scholar
Yadav, P.S., Saini, A., Kumar, A. & Jain, G.C. (1998). Effect of oviductal cell co-culture on cleavage and development of goat IVF embryos. Anim. Reprod. Sci. 51, 301–6.Google Scholar
Yang, X. & Foote, R. (1987). Production of identical twin rabbits by micromanipulation of embryos. Biol. Reprod. 37, 1007–14.CrossRefGoogle ScholarPubMed
Zhu, L.J., Bagchi, M.K. & Bagchi, I.C. (1998). Attenuation of calcitonin gene expression in pregnant rat uterus leads to a block in embryonic implantation. Endocrinology 139, 330–9.Google Scholar