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IGF-I slightly improves nuclear maturation and cleavage rate of bovine oocytes exposed to acute heat shock in vitro

Published online by Cambridge University Press:  29 May 2014

Qi Meiyu ,
Di Liu  and
Zvi Roth
Qi Meiyu
Affiliation:
Heilongjiang Academy of Agricultural Sciences, Harbin, China.
Di Liu
Affiliation:
Heilongjiang Academy of Agricultural Sciences, Harbin, China.
Zvi Roth*
Affiliation:
Department of Animal Sciences, Robert H. Smith Faculty of Agriculture, Food and Environment, the Hebrew University, Rehovot 76100, Israel.
*
All correspondence to: Zvi Roth. Department of Animal Sciences, Robert H. Smith Faculty of Agriculture, Food and Environment, the Hebrew University, Rehovot 76100, Israel. Tel: + 972 8 9489103. Fax: + 972 8 9498552. e-mail: roth@agri.huji.ac.il
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Summary

An in vitro model of embryo production was used to examine the effects of insulin-like growth factor (IGF)-I on maturation and developmental competence of oocytes exposed to heat shock. Cumulus–oocyte complexes were matured at 38.5°C or exposed to acute heat shock (HS; 41.5°C), with or without 100 ng/ml IGF-I, for 22 h through in vitro maturation. The experimental groups were control (C), C + IGF-I, HS, and HS + IGF-I. Oocytes were fertilized at the end of maturation, and the proportion of cleaved embryos was recorded 44 h later. HS during maturation increased the proportion of TUNEL-positive oocytes (P < 0.05). HS did not have any effect on cortical granule translocation but impaired resumption of meiosis, expressed as a decreased proportion of oocytes with nuclei in metaphase I (P < 0.05) and metaphase II (MII; P < 0.05). HS decreased the proportion of oocytes that cleaved (P < 0.05), in particular those oocytes that further developed to 4-cell-stage embryos (P < 0.05). IGF-I alleviated, to some extent, the deleterious effects of HS on the oocytes as reflected by a reduced proportion of TUNEL-positive oocytes (P < 0.03). While not significant, IGF-I tended to increase the proportion of MII-stage oocytes (P < 0.08) and 4-cell-stage cleaved embryos (P < 0.06). Further examination is required to explore whether IGF-I also affects the developmental competence of oocytes exposed to HS.

Keywords

BovineCleavage rateHeat shockIGF-IOocyte maturation
Type
Research Article
Information
Zygote , Volume 23 , Issue 4 , August 2015 , pp. 514 - 524
Copyright
Copyright © Cambridge University Press 2014 

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References

Arav, A., Aroyo, A., Yavin, S. & Roth, Z. (2008). Prediction of embryonic developmental competence by time-lapse observation and ‘shortest-half’ analysis. Reprod. Biomed. Online 17, 669–75.CrossRefGoogle ScholarPubMed
Carneiro, F.G., Liu, I.K.M., Hyde, D., Lorenzo, P.L. & Ball, B.A. (2002). Quantification and distribution of equine oocyte cortical granules during meiotic maturation and after activation. Mol. Reprod. Dev. 63, 451–8.CrossRefGoogle ScholarPubMed
Damiani, P., Fissore, R.A., Cibelli, J.B., Long, C.R., Balise, J.J., Robl, J.M. & Duby, R.T. (1996). Evaluation of developmental competence, nuclear and ooplasmic maturation of calf oocytes. Mol. Reprod. Dev. 45, 521–34.3.0.CO;2-Z>CrossRefGoogle ScholarPubMed
de Castro e Paula, L.A. & Hansen, P.J. (2007). Interactions between oxygen tension and glucose concentration that modulate actions of heat shock on bovine oocytes during in vitro maturation. Theriogenology 68, 763–70.CrossRefGoogle ScholarPubMed
de Rensis, F. & Scaramuzzi, R.J. (2003). Heat stress and seasonal effects on reproduction in the dairy cow – a review. Theriogenology 60, 1139–51.CrossRefGoogle ScholarPubMed
de S. Torres-Júnior, J.R., de F.A. Pires, M., de Sá, W.F., de M. Ferreira, A., Viana, J.H.M., Camargo, L.S.A, Ramos, A.A., Folhadella, I.M., Polisseni, J., de Freitas, C., Clemente, C.A.A., de Sá Filho, M.F., Paula-Lopes, F.F. & Baruselli, P.S. (2008). Effect of maternal heat-stress on follicular growth and oocyte competence in Bos indicus cattle. Theriogenology 69, 155–66.CrossRefGoogle ScholarPubMed
Demeestere, I., Gervy, C., Centner, J., Deverker, F., Englert, Y. & Delbaere, A. (2004). Effect of insulin-like growth factor during preantral follicular culture on embryo development in mice. Biol. Reprod. 70, 1664–9.CrossRefGoogle ScholarPubMed
Dinnyés, A., Lonergan, P., Fair, T., Boland, M.P. & Yang, X. (1999). Timing of the first cleavage post-insemination affects cryosurvival of in vitro-produced bovine blastocysts. Mol. Reprod. Dev. 53, 318–24.3.0.CO;2-O>CrossRefGoogle ScholarPubMed
Ducibella, T. & Buetow, J. (1994). Competence to undergo normal, fertilization-induced cortical activation develops after metaphase I of meiosis in mouse oocytes. Dev. Biol. 165, 95–104.CrossRefGoogle ScholarPubMed
Edwards, J.L. & Hansen, P.J. (1996). Elevated temperature increases heat shock protein 70 synthesis in bovine two-cell embryos and compromises function of maturing oocytes. Biol. Reprod. 55, 340–6.CrossRefGoogle ScholarPubMed
Edwards, J.L., Saxton, A.M., Lawrence, J.L., Payton, R.R. & Dunlap, J.R. (2005). Exposure to a physiologically relevant elevated temperature hastens in vitro maturation in bovine oocytes. J. Dairy Sci. 88, 4326–33.CrossRefGoogle ScholarPubMed
Fabian, D., Il’ková, G., Rehák, P., Czikková, S., Baran, V. & Koppel, J. (2004). Inhibitory effect of IGF-I on induced apoptosis in mouse preimplantation embryos cultured in vitro. Theriogenology 61, 745–55.CrossRefGoogle ScholarPubMed
Gendelman, M., Aroyo, A., Yavin, S. & Roth, Z. (2010). Seasonal effects on gene expression, cleavage timing, and developmental competence of bovine preimplantation embryos. Reproduction 140, 73–82.CrossRefGoogle ScholarPubMed
Gomez, E., Tarin, J.J. & Pellicer, A. (1993). Oocyte maturation in humans: the role of gonadotropins and growth factors. Fertil. Steril. 60, 40–6.CrossRefGoogle ScholarPubMed
Guler, A., Poulin, N., Mermillod, M., Terqui, M. & Cognié, Y. (2000). Effect of growth factors, EGF and IGF-I, and estradiol on in vitro maturation of sheep oocytes. Theriogenology 54, 209–18.CrossRefGoogle ScholarPubMed
Hainaut, P., Gioregetti, S., Kowlaski, A., Ballotti, R. & Van Obberghen, E. (1991). Antibodies to phosphotyrosine injected into Xenopus laevis oocytes modulate maturation induced by insulin/IGF-I. Exp. Cell Res. 195, 129–36.CrossRefGoogle ScholarPubMed
Hasler, J.F., Henderson, W.B., Hurtgen, P.J., Jin, Z.Q., McCauley, A.D., Mower, S.A., Neely, B., Shuey, L.S., Stokes, J.E. & Trimmer, S.A. (1995). Production, freezing and transfer of bovine IVF embryos and subsequent calving results. Theriogenology 43, 141–52.CrossRefGoogle Scholar
Ispada, J., Lima, R.S., Risolia, P.H.B., Andrade, E.S., Assumpção, M.E.O.A., Visintin, J.A. & Paula-Lopes, F.F. (2010). The role of insulin-like growth factor-I on inhibition of heat-induced apoptosis in bovine oocytes. Anim. Reprod. 7, 333.Google Scholar
Ispada, J., Lima, R.S., Risolia, P.H.B., Assumpção, M.E.O.A., Visintin, J.A. & Paula-Lopes, F.F. (2011). Insulin-like growth factor-1 exerts a thermoprotective role on mitochondrial function of bovine oocytes exposed to heat shock. Reprod. Fertil. Dev. 24, 209.CrossRefGoogle Scholar
Izadyar, F., Hage, W.J., Colenbrander, B. & Bevers, M.M. (1998). The promotory effect of growth hormone on the developmental competence of in vitro matured bovine oocytes is due to improved cytoplasmic maturation. Mol. Reprod. Dev. 49, 444–53.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
Jousan, F.D. & Hansen, P.J. (2007). Insulin-like growth factor-I promotes resistance of bovine preimplantation embryos to heat shock through actions independent of its anti-apoptotic actions requiring PI3K signaling. Mol. Reprod. Dev. 74, 189–96.CrossRefGoogle ScholarPubMed
Jousan, F.D., Oliveira, L.J. & Hansen, P.J. (2008). Short-term culture of in vitro produced bovine preimplantation embryos with insulin-like growth factor-I prevents heat shock-induced apoptosis through activation of the phosphatidylinositol 3-kinase/Akt pathway. Mol. Reprod. Dev. 75, 681–8.CrossRefGoogle ScholarPubMed
Ju, J.C., Jiang, S., Tseng, J.K., Parks, J.E. & Yang, X. (2005) Heat shock reduces developmental competence and alters spindle configuration of bovine oocytes. Theriogenology 64, 1677–89.CrossRefGoogle ScholarPubMed
Kalo, D. & Roth, Z. (2011). Involvement of the sphingolipid ceramide in heat-shock-induced apoptosis of bovine oocytes. Reprod. Fertil. Dev. 23, 876–88.CrossRefGoogle ScholarPubMed
Lonergan, P., Khatir, H., Piumi, F., Rieger, D., Humblot, P. & Boland, M.P. (1999). Effect of time interval from insemination to first cleavage on the developmental characteristics, sex ratio and pregnancy rate after transfer of bovine embryos. J Reprod. Fertil. 117, 159–67.CrossRefGoogle ScholarPubMed
Lonergan, P., Gutierrez-Adan, A., Pintado, B., Fair, T., Ward, F., Fuente, J.D. & Boland, M. (2000). Relationship between time of the first cleavage and the expression of IGF-I growth factors, its receptor, and two housekeeping genes in bovine two-cell embryos and blastocysts produced in vitro. Mol. Reprod. Dev. 57, 146–52.3.0.CO;2-2>CrossRefGoogle Scholar
Lorenzo, P.L., Illera, M.J., Illera, J.C. & Illera, M. (1994). Enhancement of cumulus expansion and nuclear maturation during bovine oocyte maturation in vitro by the addition of epidermal growth factor and insulin-like growth factor I. J. Reprod. Fertil. 101, 697–701.CrossRefGoogle ScholarPubMed
Lorenzo, P.L., Rebollar, P.G., Illera, M.J., Illera, J.C., Illera, M. & Alvarino, J.M. (1996). Stimulatory effect of insulin-like growth factor I and epidermal growth factor on the maturation of rabbit oocyte in vitro. J. Reprod. Fertil. 107, 109–17.CrossRefGoogle Scholar
Makarevich, A.V. & Markkula, M. (2002). Apoptosis and cell proliferation potential of bovine embryos stimulated with insulin-like growth factor I during in vitro maturation and culture. Biol. Reprod. 66, 386–92.CrossRefGoogle ScholarPubMed
Paula-Lopes, F.F., Lima, R.S., Satrapa, R.A. & Barros, C.M. (2013). Physiology and Endocrinology Symposium: Influence of cattle genotype (Bos indicus vs. Bos taurus) on oocyte and preimplantation embryo resistance to increased temperature. J. Anim. Sci. 91, 1143–53.CrossRefGoogle ScholarPubMed
Pawshe, C.H., Rao, K.B. & Totey, S.M. (1998). Effect of insulin-like growth factor I and its interaction with gonadotropins on in vitro maturation and embryonic development, cell proliferation, and biosynthetic activity of cumulus–oocyte complexes and granulosa cells in buffalo. Mol. Reprod. Dev. 49, 277–85.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Payton, R.R., Romar, R., Coy, P., Saxton, A.M., Lawrence, J.L. & Edwards, J.L. (2004) Susceptibility of bovine germinal vesicle-stage oocytes from antral follicles to direct effects of heat stress in vitro. Biol. Reprod. 71, 1303–8.CrossRefGoogle ScholarPubMed
Peruzzi, F., Prisco, M., Dews, M., Salomoni, P., Grassilli, E., Romano, G., Callabretta, B. & Baserga, R. (1999). Multiple signaling pathways of the insulin-like growth factor 1 receptor in protection from apoptosis. Mol. Cell. Biol. 19, 7203–15.CrossRefGoogle ScholarPubMed
Puteny, D.J., Drost, M. & Thatcher, W.W. (1988). Embryonic development in superovulated dairy cattle exposed to elevated ambient temperatures between days 1 to 7 post insemination. Theriogenology 30, 195–209.CrossRefGoogle Scholar
Reed, M.L., Estrada, J.L., Illera, M.J. & Petters, R.M. (1993). Effects of epidermal growth factor, insulin-like growth factor-I, and dialyzed porcine follicular fluid on porcine oocyte maturation in vitro. J. Exp. Zoo. 266, 74–8.CrossRefGoogle ScholarPubMed
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
Roth, Z. (2008). Heat stress, the follicle, and its enclosed oocyte: mechanisms and potential strategies to improve fertility in dairy cows. Reprod. Domest. Anim. 43, 238–44.CrossRefGoogle ScholarPubMed
Roth, Z. & Hansen, P.J. (2004a). Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation. Biol. Reprod. 71, 1898–906.CrossRefGoogle ScholarPubMed
Roth, Z. & Hansen, P.J. (2004b). Sphingosine 1-phosphate protects bovine oocytes from heat shock during maturation. Biol. Reprod. 71, 2072–8.CrossRefGoogle ScholarPubMed
Roth, Z. & Hansen, P.J. (2005). Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reproduction 129, 235–44.CrossRefGoogle ScholarPubMed
Sakkas, D., Shoukir, Y., Chardonnens, D., Bianchi, P.G. & Campana, A. (1998). Early cleavage of human embryos to the two-cell stage after intracytoplasmic sperm injection as an indicator of embryo viability. Hum. Reprod. 13, 182–7.CrossRefGoogle Scholar
Shoukir, Y., Campana, A., Farley, T. & Sakkas, D. (1997). Early cleavage of in-vitro fertilized human embryos to the 2-cell stage: a novel indicator of embryo quality and viability. Hum. Reprod. 12, 1531–6.CrossRefGoogle Scholar
Su, E.J., Cioffi, C.L., Stefansson, S., Mittereder, N., Garay, M., Hreniuk, D. & Lisu, G. (2003). Gene therapy vector-mediated expression of insulin-like growth factors protects cardiomyocytes from apoptosis and enhances neovascularization. Am. J. Phys. 284, H1429–40.Google ScholarPubMed
Thomas, F.H., Campbell, B.K., Armstrong, D.G. & Telfer, E.E. (2007). Effects of IGF-I bioavailability on bovine preantral follicular development in vitro. Reproduction 133, 1121–8.CrossRefGoogle ScholarPubMed
Van Montfoort, A.P., Dumoulin, J.C., Kester, A.D. & Evers, J.L. (2004) Early cleavage is a valuable addition to existing embryo selection parameters: a study using single embryo transfers. Hum. Reprod. 19, 2103–8.CrossRefGoogle ScholarPubMed
Velazquez, M.A., Hadeler, K.G., Herrmann, D., Kues, W.A., Ulbrich, S.E., Meyer, H.H., Rémy, B., Beckers, J.F. & Sauerwein, H. (2011). In vivo oocyte developmental competence is reduced in lean but not in obese superovulated dairy cows after intraovarian administration of IGF1. Reproduction 142, 41–52.CrossRefGoogle Scholar
Wasielak, M. & Bogacki, M. (2007). Apoptosis inhibition by insulin-like growth factor (IGF)-I during in vitro maturation of bovine oocytes. J. Reprod. Dev. 53, 419–26.CrossRefGoogle ScholarPubMed
Yoshida, Y., Miyamura, M., Hamano, S. & Yoshida, M. (1998). Expression of growth factor ligand and their receptor mRNAs in bovine ova during in vitro maturation and after fertilization in vitro. J. Vet. Med. Sci. 60, 549–54.CrossRefGoogle ScholarPubMed
Zhandi, M., Towhidi, A., Nasr-Esfahani, M.H., Eftekhari-Yazdi, P. & Zare-Shahneh, A. (2009). Unexpected detrimental effect of insulin like growth factor-1 on bovine oocyte developmental competence under heat stress. J. Assist. Reprod. Genet. 26, 605–11.CrossRefGoogle ScholarPubMed