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Co-culture of buffalo (Bubalus bubalis) preantral follicles with antral follicles: a comparative study of developmental competence of oocytes derived from in vivo developed and in vitro cultured antral follicles

Published online by Cambridge University Press:  18 January 2012

G. Taru Sharma ,
Pawan K. Dubey ,
Amar Nath  and
G. Saikumar
G. Taru Sharma*
Affiliation:
Reproductive Physiology Laboratory, Physiology and Climatology Division, Indian Veterinary Research Institute, Izatnagar-243122, India.
Pawan K. Dubey
Affiliation:
Reproductive Physiology Laboratory, Physiology and Climatology Division, Indian Veterinary Research Institute, Izatnagar-243122, India.
Amar Nath
Affiliation:
Reproductive Physiology Laboratory, Physiology and Climatology Division, Indian Veterinary Research Institute, Izatnagar-243122, India.
G. Saikumar
Affiliation:
Reproductive Physiology Laboratory, Physiology and Climatology Division, Indian Veterinary Research Institute, Izatnagar-243122, India. Cytopathology Laboratory, Division of Pathology, Indian Veterinary Research Institute, Izatnagar-243122, India.
*
All correspondence to: G. Taru Sharma. Reproductive Physiology Laboratory, Physiology and Climatology Division, Indian Veterinary Research Institute, Izatnagar-243122, India Tel: +91 941 2603840 (M). Telefax: +91 581 2301327 (O). e-mail: gts553@gmail.com
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Summary

The present study was undertaken to examine whether the presence of antral follicles (AFs) affects the survival, growth and steroidogenesis of preantral follicles (PFs) and compare the maturation and developmental competence of buffalo oocytes derived from in vivo developed and in vitro cultured AFs. Two experiments were carried out. In experiment I, PFs (200–250 μm) were isolated and cultured with or without AFs (3–5 mm) in TCM-199 medium that contained 10% fetal bovine serum (FBS), 1% insulin transferin selenium (ITS), 20 ng/ml epidermal growth factor (EGF), 0.5 μg/ml follicle-stimulating hormone (FSH) and 100 ng/ml insulin-like growth factor (IGF)-I. In experiment II, in vitro developmental competence was compared for the cumulus–oocyte complexes (COCs) recovered from in vivo developed and in vitro cultured AFs. Survival, growth, development of antrum, accumulation of estradiol and progesterone was (P < 0.05) higher when PFs were co-cultured with AFs. Developmental competence of both types of follicular oocytes did not differ significantly in terms of maturation and cleavage rate, but morula and blastocyst production rate were (P < 0.05) higher with in vivo developed AFs as compared with the in vitro cultured antral follicular oocytes. In conclusion, co-culture of PFs with AFs supports long-term survival and growth of buffalo PFs and this co-culture system plays a dual role for in vitro production of embryos as well as understanding the relationship between developing PFs and AFs.

Keywords

Antral folliclesBuffaloEmbryoOocytesPreantral follicles
Type
Research Article
Information
Zygote , Volume 21 , Issue 3 , August 2013 , pp. 286 - 294
Copyright
Copyright © Cambridge University Press 2012 

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References

Arunakumari, G., Vagdevi, R., Rao, B.S., Naik, B.R., Naidu, K.S., Suresh, R.V. & Rao, V.H. (2006). Effect of hormones and growth factors on in vitro development of sheep preantral follicles. Small Rum. Res. 70, 93–100.CrossRefGoogle Scholar
Barkawi, A.H., Hafez, Y.M., Ibrahim, S.A., Ashour, G.E., Asheeri, A.K. & Ghanem, N. (2009). Characteristics of ovarian follicular dynamics throughout the estrous cycle of Egyptian buffaloes. Anim. Reprod. Sci. 110, 326–34.CrossRefGoogle ScholarPubMed
Blondin, P. & Sirard, M.A. (1995). Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes. Mol. Reprod. Dev. 41, 54–62.CrossRefGoogle ScholarPubMed
Byrne, A.T., Southgate, J., Brison, D.R. & Leese, H.J. (2002). Regulation of apoptosis in the bovine blastocyst by insulin and the insulin-like growth factor (IGF) superfamily. Mol. Reprod. Dev. 62, 489–95.CrossRefGoogle ScholarPubMed
Campbell, B.K., Scaramuzzi, R.J. & Webb, R. (1995). Control of antral follicle development and selection in sheep and cattle. J. Reprod. Fertil. 49, 335–50.Google ScholarPubMed
Fouladi Nashta, A.A., Waddington, D. & Campbell, I.Q. (1998). Maintenance of bovine oocytes in meiotic arrest and subsequent development in vitro: a comparative evaluation of antral follicle culture with other methods. Biol. Reprod. 59, 255–62.CrossRefGoogle ScholarPubMed
Ghosh, D. & Sengupta, J. (1998). Recent developments in endocrine and paracrinology of blastocyst implantation in the primate. Hum. Reprod. Update 4, 153–68.CrossRefGoogle ScholarPubMed
Gutierrez, C.G., Ralph, J.H., Telfer, E.E., Wilmut, I. & Webb, R. (2000). Growth and antrum formation of bovine preantral follicles in long-term culture in vitro. Biol. Reprod 62, 1322–8.CrossRefGoogle ScholarPubMed
Hagemann, L.J. (1999). Influence of the dominant follicle on oocytes from subordinate follicles. Theriogenology 51, 449–59.CrossRefGoogle ScholarPubMed
Harada, M., Miyano, T., Matsumura, K., Osaki, S., Miyake, M. & Kato, S. (1997). Bovine oocytes from early antral follicles grow to meiotic competence in vitro: effect of FSH and hypoxanthine. Theriogenology 48, 743–55.CrossRefGoogle ScholarPubMed
Hardy, K. & Spanos, S. (2002). Growth factor expression and function in the human and mouse preimplantation embryo. J. Endocrinol. 172, 221–36.CrossRefGoogle ScholarPubMed
Hemamalini, N.C., Rao, B.S., Tammilmani, G., Amarnath, D., Vagdevi, R., Naidu, K.S., Reddy, K.K. & Rao, V.H. (2003). Influence of transforming growth factor-α, insulin-like growth factor-II, epidermal growth factor or follicle stimulating hormone on in vitro development of preantral follicles in sheep. Small Rum. Res. 50, 11–22.CrossRefGoogle Scholar
Hendriksen, P.J., Vos, P.L., Steenweg, W.N., Bevers, M.M. & Dieleman, S.J. (2000). Bovine follicular development and its effect on the in vitro competence of oocytes. Theriogenology 53, 11–20.CrossRefGoogle ScholarPubMed
Ireland, J.L., Scheetz, D., Jimenez-Krassel, F., Themmen, A.P., Ward, F., Lonergan, P., Smith, G.W., Perez, G.I., Evans, A.C. & Ireland, J.J. (2008). Antral follicle count reliably predicts number of morphologically healthy oocytes and follicles in ovaries of young adult cattle. Biol. Reprod. 79, 1219–25.CrossRefGoogle ScholarPubMed
Kruip, T.A. & Dieleman, S.J. (1982). Macroscopic classification of bovine follicles and its validation by micromorphological and steroid biochemical procedures. Reprod. Nutr. Dev. 22, 465–73.CrossRefGoogle ScholarPubMed
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, 48–53.CrossRefGoogle ScholarPubMed
Machatkova, M.K., Krausova, E., Jokesova, M. & Tomanek, V. (2004). Developmental competence of bovine oocytes: effects of follicle size and the phase of follicular wave on in vitro embryo production Theriogenology 61, 329–35.CrossRefGoogle ScholarPubMed
Mao, J., Smith, M.F., Rucker, E.B., Wu, G.M., McCauley, T.C., Cantley, T.C., Prather, R.S., Didion, B.A. & Day, B.N. (2004). Effect of epidermal growth factor and insulin-like growth factor I on porcine preantral follicular growth, antrum formation, and stimulation of granulosal cell proliferation and suppression of apoptosis in vitro. J. Anim. Sci. 82, 1967–75.CrossRefGoogle ScholarPubMed
Matos, M.H., van den Hurk, R., Lima-Verde, I.B., Luque, M.C., Santos, K.D., Martins, F.S., Bao, S.N., Lucci, C.M. & Figueiredo, J.R. (2007). Effects of fibroblast growth factor-2 on the in vitro culture of caprine preantral follicles, Cells Tissues Organs 186, 112–20.CrossRefGoogle ScholarPubMed
Miyano, T., Ozaki, S., Matsumura, K., Miyake, M., Kato, S., Yamamoto, K. (1998). In vitro growth, fertilization and development of bovine oocytes from early antral follicles. In: Lauria, A., Gandolfi, F., Enne, G., Gianaroli, L. (eds). Proceeding of the Serono Symp, Gametes: Development and Function. p. 575.Google Scholar
Monniaux, D., Monget, P., Besnard, N., Huet, C. & Pisselet, C. (1997). Growth factors and antral follicular development in domestic ruminants. Theriogenology 47, 3–12.CrossRefGoogle Scholar
O'Brien, M.J., Pendola, J.K. & Eppig, J.J. (2003). A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol. Reprod. 68, 1682–6.CrossRefGoogle ScholarPubMed
Pavlok, A., Lucas-Hahn, A. & Niemann, H. (1992). Fertilization and developmental competence of bovine oocytes derived from different categories of antral follicles. Mol. Reprod. Dev. 31, 63–7.CrossRefGoogle ScholarPubMed
Rajarajan, K., Rao, B.S., Vagdevi, R., Tammilmani, G., Arunakumari, G., Sreenu, M., Amarnath, D., Naik, B.R. & Rao, V.H. (2006). Influence of various growth factors on in vitro development of goat preantral follicles. Small Rum. Res. 63, 204–12.CrossRefGoogle Scholar
Rieger, D., Luciano, A.M., Modina, S., Pocar, P., Lauria, A. & Gandolfi, F. (1998). The effects of epidermal growth factor and insulin-like growth factor I on the metabolic activity, nuclear maturation and subsequent development of cattle oocytes in vitro. J. Reprod. Fertil. 112, 123–30.CrossRefGoogle ScholarPubMed
Sharma, G.T., & Loganathasamy, K. (2007). Effect of meiotic stages during in vitro maturation on the survival of vitrified-wormed buffalo oocytes. Vet. Res. Commun. 31, 881–93.CrossRefGoogle ScholarPubMed
Sharma, G.T., Pawan, K.D. & Meur, S.K. (2009a). Survival and developmental competence of buffalo preantral follicles using three dimensional collagen gel culture system. Anim. Reprod. Sci. 114, 115–24.CrossRefGoogle ScholarPubMed
Sharma, G.T., Pawan, K.D. & Meur, S.K. (2009b). Effect of different mechanical isolation techniques on developmental competence and survival of buffalo ovarian preantral follicles. Livest. Sci. 123, 300–5.CrossRefGoogle Scholar
Sinclair, K.D., Rooke, J.A. & McEvoy, T.G. (2003). Regulation of nutrient uptake and metabolism in pre-elongation ruminant embryos. Reproduction 61, 371–85.Google ScholarPubMed
Sirisathien, S., Hernandez-Fonseca, H.J. & Brackett, B.G. (2003). Influences of epidermal growth factor and insulin-like growth factor-I on bovine blastocyst development in vitro. Anim. Reprod. Sci. 77, 21–32.CrossRefGoogle ScholarPubMed
Spicer, L.J. & Aad, P.Y. (2007). Insulin-like growth factor (IGF) 2 stimulates steroidogenesis and mitosis of bovine granulosa cells through the IGF1 receptor: role of follicle-stimulating hormone and IGF2 receptor. Biol. Reprod. 77, 18–27.CrossRefGoogle ScholarPubMed
Sudo, N., Shimizu, T., Kawashima, C., Kaneko, E., Tetsuka, M. & Miyamoto, A. (2007). Insulin-like growth factor-I (IGF-I) system during follicle development in the bovine ovary: relationship among IGF-I, type 1 IGF receptor (IGFR-1) and pregnancy-associated plasma protein-A (PAPP-A). Mol. Cell Endocrinol. 264, 197–203.CrossRefGoogle ScholarPubMed
Torner, H., Kubelka, M., Heleil, B., Tomek, W., Aim, H., Kuzmina, T.et al. (2001). Dynamics of meiosis and protein kinase activities in bovine oocytes correlated to prolactin treatment and follicle size. Theriogenology 55, 885–99.CrossRefGoogle ScholarPubMed
Vikash, C., Kumar, G.S. & Sharma, G.T. (2011). Temporal expression pattern of insulin like growth factors (IGF-I & IGF-2) ligands and their receptors (IGF-IR & IGF-2R) in buffalo (Bubalus bubalis) embryos produced in vitro. Livestock Sci. 135, 225–30.Google Scholar
Wandji, S.A., Eppig, J.J. & Fortune, J.E. (1996). FSH and growth factors affect the growth and endocrine function in vitro of granulosa cells of bovine preantral follicles. Theriogenology 45, 817–32.CrossRefGoogle ScholarPubMed
Webb, R. & Campbell, B.K. (2007). Development of the dominant follicle: mechanisms of selection and maintenance of oocyte quality. Reprod. Dom. Rumin. VI Suppl. 64, 140–63.Google ScholarPubMed
Yang, M.Y. & Rajamahendran, R. (1998). Effects of gonadotropins and insulin-like growth factors-I and -II on in vitro steroid production by bovine granulosa cells. Can. J. Anim. Sci. 78, 587–97.CrossRefGoogle Scholar