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Expression of mRNA encoding leukaemia inhibitory factor (LIF) and its receptor (LIFRβ) in buffalo preimplantation embryos produced in vitro: markers of successful embryo implantation

Published online by Cambridge University Press:  14 August 2012

S. Eswari ,
G. Sai Kumar  and
G. Taru Sharma
S. Eswari*
Affiliation:
Department of Veterinary Physiology, Madras Veterinary College, Tamil Nadu Veterinary and Animal Sciences University, Chennai, Tamil Nadu, 600007
G. Sai Kumar
Affiliation:
I/C Cytopathology Laboratory, Division of Pathology, Indian Veterinary Research Institute, Izat Nagar, Uttar Pradesh, India, 243 122
G. Taru Sharma
Affiliation:
Division of Physiology and Climatology, Indian Veterinary Research Institute, Izat Nagar, Uttar Pradesh, India, 243 122
*
All correspondence to: S. Eswari. Department of Veterinary Physiology, Madras Veterinary College, Tamil Nadu Veterinary and Animal Sciences University, Chennai, Tamil Nadu, 600007. Tel: 09840798305. e-mail: drseswari@gmail.com
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Summary

The objective of this study was to evaluate the effect of supplementation of recombinant leukaemia inhibitory factor (LIF) in culture media on blastocyst development, total cell number and blastocyst hatching rates and the reverse transcription-polymerase chain reaction analysis of preimplantation buffalo embryos to determine whether they contain the LIF-encoding mRNA and its beta receptor (LIFRβ) genes in different stages of preimplantation buffalo embryos. Cumulus–oocyte complexes retrieved from slaughterhouse buffalo ovaries were matured in vitro and fertilized using frozen buffalo semen. After 18 h of co-incubation with sperm, the presumptive zygotes were cultured in modified synthetic oviductal fluid without (control) or with rhLIF (100 ng/ml). There was no significant difference in the overall cleavage rate up to morula stage however the development of blastocysts, hatching rate and total cell numbers were significantly higher in the LIF-treated group than control. Transcripts for LIFRβ were detected from immature, in vitro-matured oocytes and in the embryos up to blastocyst stage, while transcripts for the LIF were detected from 8–16-cell stage up to blastocyst, which indicated that embryo-derived LIF can act in an autocrine manner on differentiation process and blastocyst formation. This study indicated that the addition of LIF to the embryo culture medium improved development of blastocysts, functional (hatching) and morphological (number of cells) quality of the blastocysts produced in vitro. The stage-specific expression pattern of LIF and LIFRβ mRNA transcripts in buffalo embryos indicated that LIF might play an important role in the preimplantation development and subsequent implantation of buffalo embryos.

Keywords

BuffaloEmbryoGene ExpressionLeukaemia inhibitory factorLeukaemia inhibitory factor receptor β
Type
Research Article
Information
Zygote , Volume 21 , Issue 2 , May 2013 , pp. 203 - 213
Copyright
Copyright © Cambridge University Press 2012

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References

Brisson, C., Ethier, J.F. & Lussier, J.G. (1996). Bovine leukemia inhibitory factor is expressed in reproductive tissues including endometrial cell lines. Biol. Reprod. 54 (Suppl.1), 297.Google Scholar
Cai, L.Q., Cao, Y.J. & Duan, E.K. (2000). Effects of leukaemia inhibitory factor on embryo implantation in the mouse. Cytokine 12, 1676–82.CrossRefGoogle ScholarPubMed
Carnegie, J.A., Durnford, R., Algire, J. & Morgan, J. (1997). Evaluation of mitomycin treated Vero cells as a co-culture system for IVM/IVF derived bovine embryos. Theriogenology 48, 377–89.CrossRefGoogle ScholarPubMed
Carnegie, J.A., Morgan, J.J., McDiarmid, N. & Durnford, R. (1999). Influence of protein supplements on the secretion of leukemia inhibitory factor by mitomycin-pretreated Vero cells: possible application to the in vitro production of bovine blastocysts with high cryotolerance. J. Reprod. Fertil. 117, 41–8.CrossRefGoogle Scholar
Chen, H.F., Shew, J.Y., Ho, H.N., Hsu, W.L. & Yang, Y.S. (1999). Expression of leukemia inhibitory factor and its receptor in pre-implantation embryos. Fertil. Steril. 72, 713–9.CrossRefGoogle Scholar
Cheung, L.P., Leung, H.Y. & Bongso, A. (2003). Effect of supplementation of leukemia inhibitory factor and epidermal growth factor on murine embryonic development in vitro, implantation and outcome of offspring. Fertil. Steril. 80, 727–35.CrossRefGoogle ScholarPubMed
Cheng, J.G., Rodriguez, C.I & Stewart, C.L. (2002). Control of uterine receptivity and embryo implantation by steroid hormone regulation of LIF production and LIF receptor activity: towards a molecular understanding of ‘the window of implantation’. Rev. Endo. Metab. Dis. 3, 119–26.CrossRefGoogle ScholarPubMed
Chiappe, M.E., Lattanzi, M.L., Colman-Lerner, A.A., Baranao, J.L. & Saragueta, P. (2002). Expression of betahydroxysteroid dehydrogenase in early bovine embryo development. Mol. Reprod. Dev. 61, 135–41.CrossRefGoogle ScholarPubMed
Dunglison, G.F., Barlow, D.H. & Sargent, I.L. (1996). Leukaemia inhibitory factor significantly enhances the blastocyst formation rates of human embryos cultured in serum-free medium. Hum. Reprod. 11, 191–196CrossRefGoogle ScholarPubMed
Dusewska, A.M., Reklewski, Z., Piekowski, M., Karasiewicz, J. & Modlinski, J.A. (2000). Development of bovine embryos on Vero/ BRL cell monolayers (mixed co-culture). Theriogenology 54, 1239–47.CrossRefGoogle Scholar
Eckert, & Niemann, H. (1998). mRNA expression of leukaemia inhibitory factor and its receptor subunits glycoprotein 130 and LIF-receptor beta in bovine embryos derived in vitro or in vivo. Mol. Hum. Reprod. 4, 957–65.CrossRefGoogle ScholarPubMed
Fry, R.C., Batt, P.A., Fairclough, R.J. & Parr, R.A. (1992). Human leukemia inhibitory factor improves the viability of cultured ovine embryos. Biol. Reprod, 46, 470–4.CrossRefGoogle ScholarPubMed
Fu, H.C., Jin-Yuh, S., Hong-Nerng, H., Wei-Li, H. & Yu-Shih, Y. (1999). Expression of leukemia inhibitory factor and its receptor in preimplantation embryos. Fertil. Steril. 72, 713–9.Google Scholar
Fukui, Y. & Matsuyama, K. (1994). Development of in vitro matured and fertilized bovine embryos cultured in media containing human leukemia inhibitory factor. Theriogenology 42, 663–73.CrossRefGoogle ScholarPubMed
Gearing, D., Gough, N., King, J., Hilton, D., Nicola, N., Simpson, R., Nice, E., Kelso, A. & Metcalf, D. (1987). Molecular cloning and expression of cDNA encoding a murine myeloid leukaemia inhibitory factor (LIF). EMBO J. 10, 2839–48.CrossRefGoogle Scholar
Gearing, D.P., Thut, C.J. & Vanden Bos, (1991). Leukaemia inhibitory factor receptor is structurally related to the IL- 6 signal transducer, gp130. EMBO J. 6, 3995–4002.CrossRefGoogle Scholar
Han, Y.M., Lee, E.S., Mogoe, T., Lee, K.K. & Fukui, Y. (1995). Effect of human leukemia inhibitory factor on in vitro development of IVF-derived bovine morulae and blastocysts. Theriogenology 44, 507–16.CrossRefGoogle ScholarPubMed
Haines, B.P., Voyle, R.B. & Rathjen, P.D. (2000). Intracellular and extracellular leukemia inhibitory factor proteins have different cellular activities that are mediated by distinct protein motifs. Mol. Biol. Cell 11, 1369–83.CrossRefGoogle ScholarPubMed
Heinrich, P.C., Behrmann, I., Haan, S., Hermanns, H.M., Muller-Newen, G. & Schaper, F. (2003). Principles of interleukin (IL)-6-type cytokine signaling and its regulation. Biochem. J. 374, 1–20.CrossRefGoogle ScholarPubMed
Hilton, D.J. (1992). LIF: lots of interesting functions. Trends Biochem Sci. 17, 72–6.CrossRefGoogle ScholarPubMed
Hsieh, Y.Y., Tsai, H.D., Chang, C.C., Hsu, L.W., Chang, S.C. & Lo, H.Y. (2000). Prolonged culture of human cryopreserved embryos with recombinant human leukemia inhibitory factor. J. Assist. Reprod. Genet. 17, 131–4.CrossRefGoogle ScholarPubMed
Jeon, I., Oh, E., Park, J., Kim, S., Roh, S. & Yoon, H. (2001). Effects of IGF-I, TGFα and LIF on apoptosis of blastomere and Oct4 gene expression in mouse preimplantation embryos. Fertil. Steril. 76, S268.CrossRefGoogle Scholar
Jurisicova, A., Ben-Chetrit, A., Varmuza, S.L. & Casper, R.F. (1995). Recombinant human leukemia inhibitory factor does not enhance in vitro human blastocyst formation. Fertil. Steril. 64, 999–1002.CrossRefGoogle Scholar
Kauma, S.W. & Matt, D.W. (1995). Co-culture cells that express leukemia inhibitory factor enhance mouse blastocyst development in vitro. J. Assist. Reprod. Genet. 12, 153–6.CrossRefGoogle Scholar
Lass, A., Weiser, W., Munafo, A. & Loumaye, E. (2001). Leukemia inhibitory factor in human reproduction. Fertil. Steril. 76, 1091–6.CrossRefGoogle ScholarPubMed
Lee, K.F., Chow, J.F.C., Xu, J.S., Chan, S.T.H., Ip, S.M. & Yeung, W.S.B. (2001). A comparative study of gene expression in murine embryos developed in vivo, cultured in vitro and co-cultured with human oviductal cells using messenger ribonucleic acid differential display. Biol. Reprod. 64, 910–7.CrossRefGoogle Scholar
Liu, C.Q., Yuan, Y., Wang, Z.X. & Lu, S.H. (1999). Mifepristone regulation of leukemia inhibitory factor and uterine receptivity in rabbits. Contraception 60, 309–12.CrossRefGoogle ScholarPubMed
Lei, T., Yang, Z., Xia, T., Gan, L., Chen, X.D., Yuan, J.H. & Zhu, Y. (2004). Stage-specific expression of leukaemia inhibitory factor and its receptor in rabbit pre-implantation embryo and uterine epithelium during early pregnancy. Reprod. Dom. Anim. 39, 13–8.CrossRefGoogle ScholarPubMed
Madan, M.L., Chauhan, M.S., Singla, S.K. & Manik, R.S. (1994). Pregnancies established from water buffalo (Bubalus Bubalis) blastocysts derived from in vitro matured, in vitro fertilized oocytes and co-cultured with cumulus and oviductal cells. Theriogenology 42, 591–600.CrossRefGoogle ScholarPubMed
Menck, M.C., Guyader-Joly, C., Peynot, N., Le Bourhis, D, Lobo, R.B., Renard, J.P. & Heyman, . (1997). Beneficial effects of Vero cells for developing ICD bovine eggs in two different co-culture systems. Reprod. Nutr. Dev. 37, 141–50.CrossRefGoogle Scholar
Menezo, Y., Hazout, , Dumont, A., Herbaut, M. & Nicollet, B. (1992). Co-culture of embryos on Vero cells and transfer of blastocysts in humans. Hum. Reprod. 7, 101–6.CrossRefGoogle Scholar
Mitchell, M.H., Swanson, R.J. & Oehninger, S. (2002). In vivo effect of leukemia inhibitory factor (LIF) and an anti-LIF polyclonal antibody on murine embryo and fetal development following exposure at the time of transcervical blastocyst transfer. Biol. Reprod. 67, 460–4.CrossRefGoogle Scholar
Niemann, H., Wrenzycki, C., Lucas-Hahn, A., Brambrink, T., Kues, W.A. & Carnwath, J.W. (2002). Gene expression pattern in bovine in vitro produced and nuclear transfer derived embryos and their implication for early development. Cloning Stem Cells 4, 29–38.CrossRefGoogle ScholarPubMed
Niemann, H. & Wrenzycki, C. (2000). Alteration of expression of developmentally important genes in preimplantation bovine embryos by in vitro culture conditions: implications for subsequent development. Theriogenology 53, 21–34.CrossRefGoogle ScholarPubMed
Nichols, J., Davidson, D., Taga, T., Yoshida, K., Chambers, I. & Smith, A. (1996). Complementary tissue specific expression of LIF and LIF-receptor mRNAs in early mouse embryogenesis. Mech. Dev. 57, 123–31.CrossRefGoogle ScholarPubMed
Pegoraro, L.M.C., Thuard, J.M., Delalleau, N., Guerin, B., Deschamps, J.C., Marquant-Le Guienne, B. & Humblot, P. (1998). Comparison of sex ratio and cell number of IVM- IVF bovine blastocysts co-cultured with bovine oviduct epithelial cells or with Vero cells. Theriogenology 49, 1579–90.CrossRefGoogle ScholarPubMed
Ptak, G., Lopes, F., Matsukawa, K., Tishner, M. & Loi, P. (2006). Leukemia inhibitory factor enhances sheep fertilization in vitro via an influence on the oocyte. Theriogenology 65, 1891–9.CrossRefGoogle ScholarPubMed
Pursel, V.G., Wall, R.J., Rexroad, C.E., Hammer, R.E. & Brinster, R.L. (1985). A rapid whole-mount staining procedure for nuclei of mammalian embryo. Theriogenology 24, 687–91.CrossRefGoogle Scholar
Reinhart, K.C., Dubey, R.K., Mummery, C.L., van Rooijen, M., Keller, P.J. & Marinella, R. (1998). Synthesis and regulation of leukaemia inhibitory factor in cultured bovine oviduct cells by hormones. Mol. Hum. Reprod. 4, 301–8.CrossRefGoogle ScholarPubMed
Rizos, D., Ward, F., Duffy, P., Boland, M.P. & Lonergan, P. (2002). Consequences of bovine oocyte maturation fertilization or early embryo development in vitro versus in vivo: implication for blastocyst yield and blastocyst quality. Mol. Reprod. Dev. 61, 234–48.CrossRefGoogle ScholarPubMed
Rizos, D., Gutierrez-Adan, A., Perez-Garnelo, J., De La Fuente, J., Boland, M.P. & Lonergan, P. (2003). Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance, and messenger RNA expression. Biol. Reprod. 68, 236–43.CrossRefGoogle ScholarPubMed
Robb, L., Dimitriadis, E., Li, R. & Salamonsen, L.A. (2002). Leukemia inhibitory factor and interleukin-11: cytokines with key roles in implantation. J. Reprod. Immunol. 57, 129–41.CrossRefGoogle ScholarPubMed
Rodriquez, A., DeFrutos, C., Diez, C., Caamano, J.N., Facal, N., Duque, P., Garcia-Ochoa, C. & Gomez, E. (2007). Effects of human versus mouse leukemia inhibitory factor on the in vitro development of bovine embryos. Theriogenology 67, 1092–5.CrossRefGoogle Scholar
Sambrook, J. (1989). Molecular Cloning. A Laboratory Manual. Cold Spring Harbor Laboratory Press.Google Scholar
Shamsuddin, M., Larsson, B., Gustafsson, H. & Rodriguez-Martinez, H. (1993). In vitro development upto hatching of bovine in vitro matured and fertilized oocytes with or with out support from somatic cells. Theriogenology 39, 1067–79.CrossRefGoogle Scholar
Shim, C., Lee, S.G. & Song, W.K. (1997). Laminin chain specific gene expression during mouse oocyte maturation. Mol. Reprod. Dev. 48, 185–93.3.0.CO;2-O>CrossRefGoogle ScholarPubMed
Snedecor, G.W. & Cochran, W.G. (1989). Statistical Methods. 9th edn.The Iowa State University Press. Ames, Iowa.Google Scholar
Sirisathien, S., Herandez,-Fonseca, H.J. & Brackett, B.G. (2003). Influence of epidermal growth factor and insulin-like growth factor-I on bovine blastocyst development in vitro. Anim. Reprod. Sci. 77 (1–2), 21–32.CrossRefGoogle ScholarPubMed
Stewart, C.L., Kaspar, P., Brunet, L.J., Bhatt, H., Gadi, I. & Kontgen, F. (1992). Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359, 76–9.CrossRefGoogle ScholarPubMed
Tsai, H.D., Chang, C.C., Hsieh, Y.Y., Hsu, L.W., Chang, S.C. & Lo, H.Y. (2000). Effect of different concentration of recombinant leukemia inhibitory factor on different development stage of mouse embryo in vitro. J. Assist. Reprod. Genet. 17, 352–5.CrossRefGoogle ScholarPubMed
Tsai, H.D., Hang, C.C., Hsieh, Y.Y., Lo, H.Y., Hsu, L.W. & Chang, S.C. (1999). Recombinant human leukemia inhibitory factor enhances the development of preimplantation mouse embryo in vitro. Fertil. Steril. 71, 722–5.CrossRefGoogle ScholarPubMed
Van Ejik, M.J.T., Mandelbaum, J., Salat-Baroux, J., Belaisch-Allart, J., Plahcot, M., Junca, A.M. & Mummery, C.L. (1996). Expression of leukemia inhibitory factor receptor subunits LIFRß and gp130 in human oocytes and pre-implantation embryos. Mol. Hum. Reprod. 2, 355–60.CrossRefGoogle Scholar
Vogiagis, D., Fry, R.C., Sandeman, R.M. & Salamonsen, L.A. (1997). Leukaemia inhibitory factor in endometrium during the oestrous cycle, early pregnancy and in ovariectomized steroid-treated ewes. J. Reprod. Fertil. 109, 279–88.CrossRefGoogle ScholarPubMed
Vogiagis, D. & Salamonsen, L.A. (1999). The role of leukemia inhibitory factor in the establishment of pregnancy. J. Endocrinol. 160, 181–90.CrossRefGoogle ScholarPubMed
Wrenzycki, C., Hermann, D., Carnewath, J.W., & Neimann, H. (1999). Alterations in relative abundance of gene transcripts in preimplantation bovine embryos cultured in medium supplemented with either serum or PVA. Mol. Reprod. Dev. 53, 8–18.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Wrenzycki, C., Herrmann, D., Keskintepe, L., Martins, J.R. & Sirisathien, S. (2001). Effect of culture and protein supplementation on mRNA expression in preimplantation bovine embryos. Hum. Reprod. 16, 893–901.CrossRefGoogle Scholar
Yadav, P.S., Anil Saini, A., Kumar, G.C. & Jain, . (1998). Effect of oviductal cell co-culture on cleavage and development of goat IVF embryos. Anim. Reprod. Sci. 51, 301–6.CrossRefGoogle ScholarPubMed
Yamanaka, M., Kudo, T., Kimura, N., Amano, T. & Itagaki, Y. (1999). Effect of bovine leukemia inhibitory factor on hatching and numbers of inner cell mass and trophectoderm of bovine intact and biopsied blastocysts. Anim Sci J. 70, 444–50.Google Scholar
Yamanaka, M., Amano, T. & Kudo, T. (2001). Effect of the presence period of bovine leukemia inhibitory factor in culture medium on the development of in vitro fertilized bovine embryos. Anim. Sci. J. 72, 285–90.Google Scholar