Skip to main content Accessibility help
×
Home

Impact of oocyte-secreted factors on its developmental competence in buffalo

  • Swati Gupta (a1), Sriti Pandey (a1), Mehtab S. Parmar (a1), Anjali Somal (a1), Avishek Paul (a1), Bibhudatta S. K. Panda (a1), Irfan A. Bhat (a1), Indu Baiju (a1), Mukesh K. Bharti (a1), G. Saikumar (a1), Mihir Sarkar (a1), Vikash Chandra (a1) and G. Taru Sharma (a1)...

Summary

Oocyte-secreted factors (OSFs) play an important role in the acquisition of oocyte developmental competence through bidirectional cross-talk between oocyte and cumulus cells via gap junctions. Thus, the present study was designed to investigate the effect of two OSFs, growth differentiation factor 9 (GDF9) and bone morphogenetic protein 15 (BMP15), on the developmental competence of buffalo oocytes derived from two different follicle sizes. Cumulus–oocyte complexes (COCs) from large follicles (LF, >6 mm) or small follicles (SF, <6 mm) were collected and matured in vitro either in the presence of GDF9 or BMP15, or both, or with the denuded oocytes (DOs) as a source of native OSFs. Cleavage and blastocyst rates were significantly (P < 0.05) higher in LF-derived than SF-derived oocytes. Cleavage and blastocyst rates were significantly higher (P < 0.05) in the DOs and the combination groups compared with the control, GDF9 alone and BMP15 alone groups, both in LF-derived and SF-derived oocytes, although the cleavage and blastocyst rates did not differ significantly (P > 0.05) between DOs and combination groups. Relative mRNA analysis revealed significantly higher (P > 0.05) expression of the cumulus cell marker genes EGFR, HAS2, and CD44 in LF-derived than SF-derived oocyte; the expression of these markers was significantly higher (P > 0.05) in DOs and combination groups, irrespective of the follicle size. These results suggested that LF-derived oocytes have a higher developmental competence than SF-derived oocytes and that supplementation of GDF9 and BMP15 modulates the developmental competence of buffalo oocytes by increasing the relative abundance of cumulus-enabling factors and thereby increasing cleavage and the quality of blastocyst production.

Copyright

Corresponding author

All correspondence to: G. Taru Sharma. Reproductive Physiology Laboratory, Division of Physiology and Climatology, ICAR-Indian Veterinary Research Institute, Izatnagar-243 122, Bareilly, UP, India. Tel:/Fax:: +91 0581 2301327/ +91 9412 603840. E-mail: gts553@gmail.com

References

Hide All
Bhardwaj, R., Ansari, M.M., Pandey, S., Parmar, M.S., Chandra, V., Kumar, G. S. & Sharma, G.T. (2016a). GREM1, EGFR and HAS2; the oocyte competence markers for improved buffalo embryo production in vitro . Theriogenology 86, 2004–11.
Bhardwaj, R., Ansari, M.M., Parmar, M.S., Chandra, V. & Sharma, G.T. (2016b). Stem cell conditioned media contains important growth factors and improves in vitro buffalo embryo production. Anim. Biotech. 27, 118–25.
Campbell, S., Swann, H.R., Aplin, J. D. & Seif, M. W. (1995). CD44 is expressed throughout pre-implantation human embryo development. Hum. Reprod. 10, 425–30.
Cillo, F., Brevini, T.A., Antonini, S., Paffoni, A., Ragni, G. & Gandolfi, F. (2007). Association between human oocyte developmental competence and expression levels of some cumulus genes. Reproduction 134, 645–50.
Conti, M., Hsieh, M., Park, J. Y. & Su, Y. Q. (2006). Role of the epidermal growth factor network in ovarian follicles. Mol. Endocrinol. 20, 715723.
Crawford, J.L. & McNatty, K.P. (2012). The ratio of growth differentiation factor 9: bone morphogenetic protein 15 mRNA expression is tightly co-regulated and differs between species over a wide range of ovulation rates. Mol. Cell. Endocrinol. 348, 339–43.
Dey, S.R., Deb, G.K., Ha, A.N., Lee, J.I., Bang, J.I., Lee, K.L. & Kong, I.K. (2012). Coculturing denuded oocytes during the in vitro maturation of bovine cumulus oocyte complexes exerts a synergistic effect on embryo development. Theriogenology 77, 1064–77.
Dixit, H., Rao, L.K., Padmalatha, V., Kanakavalli, M., Deenadayal, M., Gupta, N., Chakravarty, B. & Singh, L. (2005). Mutational screening of the coding region of growth differentiation factor 9 gene in Indian women with ovarian failure. Menopause 12, 749–54.
Eshkar, S.L., Ronen, D., Levartovsky, D., Elkayam, O., Caspi, D., Aamar, S., Amital, H., Rubinow, A., Golan, I., Naor, D. & Zick, Y. (2007). The involvement of CD44 and its novel ligand galectin-8 in apoptotic regulation of autoimmune inflammation. J. Immunol. 179, 1225–35.
Fatehi, A.N., van den Hurk, R., Colenbrander, B., Daemen, A.J.J.M., van Tol, H.T.A., Monteiro, R.M., Roelen, B.A.J. & Bevers, M.M. (2005). Expression of bone morphogenetic protein2 (BMP2), BMP4 and BMP receptors in the bovine ovary but absence of effects of BMP2 and BMP4 during IVM on bovine oocyte nuclear maturation and subsequent embryo development. Theriogenology 63, 872–89.
Furnus, C.C., Valcarcel, A., Dulout, F.N. & Errecalde, A.L. (2003). The hyaluronic acid receptor (CD44) is expressed in bovine oocytes and early stage embryos. Theriogenology 60, 1633–44.
Galloway, S.M., McNatty, K.P., Cambridge, L.M., Laitinen, M.P., Juengel, J.L., Jokiranta, T.S., McLaren, R.J., Luiro, K., Dodds, K.G., Montgomery, G.W., Beattie, A.E., Davis, G.H. & Ritvos, O. (2000). Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat. Genet. 25, 279–83.
Gilchrist, R.B., Lane, M. & Thompson, J. G. (2008). Oocyte-secreted factors: regulators of CC function and oocyte quality. Hum. Reprod. Update 14, 159–77.
Gomez, M.N., Kang, J.T., Koo, O.J., Kim, S.J., Kwon, D.K., Park, S.J., Atikuzzaman, M., Hong, S.G., Jang, G. & Lee, B.C. (2012). Effect of oocyte-secreted factors on porcine in vitro maturation, cumulus expansion and developmental competence of parthenogenic oocyte. Zygote 20, 135–45.
Hagemann, L.J. (1999). Influence of the dominant follicle on oocytes from subordinate follicles. Theriogenology 51, 449–59.
Hanrahan, J.P., Gregan, S.M., Mulsant, P., Mullen, M., Davis, G.H., Powell, R. & Galloway, S.M. (2004). Mutations in the genes for oocyte-derived growth factors GDF9 and BMP15 are associated with both increased ovulation rate and sterility in Cambridge and Belclare sheep (Ovis aries). Biol. Reprod. 70, 900–9.
Hussein, T.S., Froiland, D.A., Amato, F., Thompson, J.G. & Gilchrist, R. B. (2005). Oocytes prevent CC apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J. Cell Sci. 118, 5257–68.
Hussein, T.S., Sutton-McDowall, M.L., Gilchrist, R. B. & Thompson, J.G. (2011). Temporal effects of exogenous oocyte-secreted factors on bovine oocyte developmental competence during IVM. Reprod. Fertil. Dev. 23, 576–84.
Hussein, T.S., Thompson, J.G., Gilchrist, R.B. (2006). Oocyte-secreted factors enhance oocyte developmental competence. Dev. Biol. 296, 514–21.
Krisher, R.L. (2004). The effect of oocyte quality on development. J. Anim. Sci. 82, E14–23.
Lee, K.B., Bettegowda, A., Wee, G., Ireland, J.J. & Smith, G.W. (2009). Molecular determinants of oocyte competence: potential functional role for maternal (oocyte-derived) follistatin in promoting bovine early embryogenesis. Endocrinology 150, 2463–71.
Lesley, J., Gal, I., Mahoney, D.J., Cordell, M.R., Rugg, M.S., Hyman, R., Day, A.J. & Mikecz, K. (2004). TSG-6 modulates the interaction between hyaluronan and cell surface CD44. J. Biol. Chem. 279, 25745–54.
Li, R., Norman, R.J., Armstrong, D.T. & Gilchrist, R.B. (2000). Oocyte-secreted factors determine functional differences between bovine mural granulosa cells and CCs. Biol. Reprod. 63, 839–45.
Li, Y., Li, R.Q., Ou, S.B., Zhang, N.F., Ren, L., Wei, L.N., Zhang, Q.X. & Yang, D.Z. (2014). Increased GDF9 and BMP15 mRNA levels in cumulus granulosa cells correlate with oocyte maturation, fertilization, and embryo quality in humans. Reprod. Biol. Endocrinol. 12, 81.
Lonergan, P., Monaghan, P., Rizos, D., Boland, M.P. & Gordon, I. (1994). Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro. Mol . Reprod. Dev. 37, 4853.
Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, 45.
Rossi, R.O.D.S., Portela, A.M.L.R., Passos, J.R.S., Cunha, E.V., Silva, A.W.B., Costa, J.J.N., Saraiva, M.V.A., Donato, M.A.M., Peixoto, C.A., Van Den Hurk, R. & Silva, J.R.V. (2015). Effects of BMP-4 and FSH on growth, morphology and mRNA expression of oocyte-secreted factors in cultured bovine secondary follicles. Anim. Reprod. 12, 910–9.
Romaguera, R., Morato, R., Jimenez-Macedo, A.R., Catala, M., Roura, M., Paramio, M.T., Palomo, M.J., Mogas, T. & Izquierdo, D. (2010). Oocyte secreted factors improve embryo developmental competence of COCs from small follicles in prepubertal goats. Theriogenology 74, 1050–9.
Schoenfelder, M. & Einspanier, R. (2003). Expression of hyaluronan synthases and corresponding hyaluronan receptors is differentially regulated during oocyte maturation in cattle. Biol. Reprod. 69, 269–77.
Sudiman, J., Ritter, L.J., Feil, D.K., Wang, X., Chan, K., Mottershead, D.G., Robertson, D.M., Thompson, J.G. & Gilchrist, R.B. (2014). Effects of differing oocyte-secreted factors during mouse in vitro maturation on subsequent embryo and fetal development. J. Assist. Reprod. Genet. 31, 295306.
Sutton-McDowall, M.L., Mottershead, D.G., Gardner, D.K., Gilchrist, R.B. & Thompson, J.G. (2012). Metabolic differences in bovine cumulus–oocyte complexes matured in vitro in the presence or absence of follicle-stimulating hormone and bone morphogenetic protein 15. Biol. Reprod. 87, 8.
Sutton-Mcdowall, M.L., Purdey, M., Hannah, M., Brown, A.D.A., Mottershead, D.G., Cetica, P.D., Dalvit, G.C., Goldys, E.M., Gilchrist, R.B., Gardner, D.K. & Thompson, J.G. (2015). Redox and anti-oxidant state within cattle oocytes following in vitro maturation with bone morphogenetic protein 15 and follicle stimulating hormone. Biol. Reprod. 82, 283–94.
Toyokawa, K., Harayama, H. & Miyake, M. (2005). Exogenous hyaluronic acid enhances porcine parthenogenetic embryo development in vitro possibly mediated by CD44. Theriogenology 64, 378–92.
Tunjung, W.A., Yokoo, M., Hoshino, Y., Miyake, Y., Kadowaki, A. & Sato, E. (2009). Effect of hyaluronan to inhibit caspase activation in porcine granulosa cells. Biochem. Biophys. Res. Commun. 382, 160–4.
Wang, B., Zhou, S., Wang, J., Liu, J., Ni, F., Zhang, X., Zhao, H., Ma, J., Chen, Z. J. (2010). Identification of novel missense mutations of GDF9 in Chinese women with polycystic ovary syndrome. Reprod. Biomed. Online 21, 344–8.
Wheatley, S.C., Isacke, C.M. & Crossley, P.H. (1993). Restricted expression of the hyaluronan receptor, CD44, during post implantation mouse embryogenesis suggests key roles in tissue formation and patterning. Development 119, 295306.
Yeo, C.X., Gilchrist, R.B., Thompson, J.G. & Lane, M. (2008). Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice. Hum. Reprod. 23, 6773.
Yokoo, M., Kimura, N. & Sato, E. (2010). Induction of oocyte maturation by hyaluronan–CD44 interaction in pigs. J. Reprod. Dev. 56, 15–9.

Keywords

Impact of oocyte-secreted factors on its developmental competence in buffalo

  • Swati Gupta (a1), Sriti Pandey (a1), Mehtab S. Parmar (a1), Anjali Somal (a1), Avishek Paul (a1), Bibhudatta S. K. Panda (a1), Irfan A. Bhat (a1), Indu Baiju (a1), Mukesh K. Bharti (a1), G. Saikumar (a1), Mihir Sarkar (a1), Vikash Chandra (a1) and G. Taru Sharma (a1)...

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed