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Does heat stress provoke the loss of a continuous layer of cortical granules beneath the plasma membrane during oocyte maturation?

Published online by Cambridge University Press:  24 March 2010

C. Andreu-Vázquez ,
F. López-Gatius ,
I. García-Ispierto ,
M.J. Maya-Soriano ,
R.H.F. Hunter  and
M. López-Béjar
C. Andreu-Vázquez*
Affiliation:
Department of Animal Heath and Anatomy, Faculty of Veterinary, Autonomous University of Barcelona, Edifici V, Campus UAB, 08193 Barcelona, Spain.
F. López-Gatius
Affiliation:
Department of Animal Production, University of Lleida, Lleida, Spain.
I. García-Ispierto
Affiliation:
Department of Animal Production, University of Lleida, Lleida, Spain.
M.J. Maya-Soriano
Affiliation:
Department of Animal Health and Anatomy, Autonomous University of Barcelona, Barcelona, Spain.
R.H.F. Hunter
Affiliation:
Institute of Reproductive Medicine, Hannover Veterinary University, Germany.
M. López-Béjar
Affiliation:
Department of Animal Health and Anatomy, Autonomous University of Barcelona, Barcelona, Spain.
*
All correspondence to: C. Andreu-Vázquez. Department of Animal Heath and Anatomy, Faculty of Veterinary, Autonomous University of Barcelona, Edifici V, Campus UAB, 08193 Barcelona, Spain. Tel.: +34 93 5814615. Fax: +34 93 5812006. e-mail: cristina.andreu.vazquez@uab.cat
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Summary

The objective of the present study was to evaluate the influence of heat stress on bovine oocyte maturation. Both nuclear stage and distribution of cortical granules (CG) were simultaneously evaluated in each oocyte. Oocyte overmaturation under standard conditions of culture was also evaluated. For this purpose, logistic regression procedures were used to evaluate possible effects of factors such as heat stress, overmaturation, replicate, CG distribution and metaphase II (MII) morphology on oocyte maturation. Based on the odds ratio, oocytes on heat stressed (HSO) and overmaturated (OMO) oocyte group were, respectively, 14.5 and 5.4 times more likely to show anomalous MII morphology than those matured under control conditions (CO). The likelihood for an oocyte of showing the CG distribution pattern IV (aging oocyte) was 6.3 and 9.3 times higher for HSO and OMO groups, respectively, than for the CO group. The risk of undergoing anomalous oocyte maturation, considering both nuclear stage and distribution of CG was 17.1 and 18 times greater in oocytes cultured in HSO and OMO groups, respectively, than those in the CO group. In conclusion, heat stress proved to be valuable in aging oocytes. Heat stress advanced age for nuclear and cytoplasmic processes in a similar form to that of oocyte overmaturation.

Keywords

AgingCortical granulesHeat stressOocyte maturationOvermaturation
Type
Research Article
Information
Zygote , Volume 18 , Issue 4 , November 2010 , pp. 293 - 299
Copyright
Copyright © Cambridge University Press 2010

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References

Baker, T.G. & Neal, P. (1972). Gonadotrophin-induced maturation of mouse Graafian follicles in organ culture. In Oogenesis (eds. Biggers, I.D. & Schuetz, A.W.), pp. 377–96. Baltimore: University Park Press.Google Scholar
Baker, T.G. & Neal, P. (1974). Organ culture of cortical fragments and Graafian follicles from human ovaries. J. Anat. 117, 361–71.Google ScholarPubMed
Bhojwani, M., Rudolph, E., Kanitz, W., Zuehlke, H., Schneider, F. & Tomek, W. (2006). Molecular analysis of maturation processes by protein and phosphoprotein profiling during in vitro maturation of bovine oocytes: a proteomic approach. Cloning Stem Cells 8, 259–74.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
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., 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
Eppig, J.J. (1996). Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals. Reprod. Fert. Dev. 8, 485–9.CrossRefGoogle ScholarPubMed
Evsikov, A.V. & Marin de Evsikova, C. (2009). Gene expression during the oocyte-to-embryo transition in mammals. Mol. Reprod. Dev. 76, 805–18.CrossRefGoogle ScholarPubMed
Fair, T., Carter, F., Park, S., Evans, A.C. & Lonergan, P. (2007). Global gene expression analysis during bovine oocyte in vitro maturation. Theriogenology 68, 91–7.CrossRefGoogle ScholarPubMed
Ferreira, E.M., Vireque, A.A., Adona, P.R., Meirelles, F.V., Ferriani, R.A. & Navarro, P.A. (2009). Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence. Theriogenology 71, 836–48.CrossRefGoogle ScholarPubMed
Flechon, J.E. (1970). Glycoprotein nature of cortical granules of rabbit egg: presentation by comparative use of ultrastructural cytochemical technics. J. Microsc. 9, 221–42.Google Scholar
Garcia-Ispierto, I., Lopez-Gatius, F., Bech-Sabat, G., Santolaria, P., Yaniz, J.L., Nogareda, C., De Rensis, F. & Lopez-Bejar, M. (2007). Climate factors affecting conception rate of high producing dairy cows in northeastern Spain. Theriogenology 67, 1379–85.CrossRefGoogle ScholarPubMed
Greve, T., Grondahl, C., Schmidt, M. et al. (1996). Bovine preovulatory follicular temperature: implications for in vitro production of embryos. Arch. Tierzuch. 39, 7–14.Google Scholar
Grinsted, J., Blendstrup, K., Andreasen, M.P. & Byskov, A.G. (1980). Temperature measurements of rabbit antral follicles. J. Reprod. Fert. 60, 149–55.CrossRefGoogle ScholarPubMed
Grinsted, J., Kjer, J.J., Blendstrup, K. & Pedersen, J.F. (1985). Is low temperature of follicular fluid prior to ovulation necessary for normal oocyte development? Fertil. Steril. 43, 34–9.CrossRefGoogle ScholarPubMed
Hosmer, D.W. & Lemeshow, S. (1987). Applied Logistic Regression. Wiley. New York.Google Scholar
Hosoe, M. & Shioya, Y. (1997). Distribution of cortical granules in bovine oocytes classified by cumulus complex. Zygote 5, 371–6.CrossRefGoogle ScholarPubMed
Hunter, R.H., Grondahl, C., Greve, T. & Schmidt, M. (1997). Graafian follicles are cooler than neighbouring ovarian tissues and deep rectal temperatures. Hum. Reprod. 12, 95–100.CrossRefGoogle ScholarPubMed
Hunter, R.H., Bogh, I.B., Einer-Jensen, N., Muller, S. & Greve, T. (2000). Pre-ovulatory graafian follicles are cooler than neighbouring stroma in pig ovaries. Hum. Reprod. 15, 273–83.CrossRefGoogle ScholarPubMed
Hunter, R.H., Einer-Jensen, N. & Greve, T. (2006). Presence and significance of temperature gradients among different ovarian tissues. Microsc. Res. Tech. 69, 501–7.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
Lawrence, J.L., Payton, R.R., Godkin, J.D., Saxton, A.M., Schrick, F.N. & Edwards, J.L. (2004). Retinol improves development of bovine oocytes compromised by heat stress during maturation. J. Dairy Sci. 87, 2449–54.CrossRefGoogle ScholarPubMed
Lopez-Gatius, F. (2003). Is fertility declining in dairy cattle? A retrospective study in northeastern Spain. Theriogenology 60, 89–99.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
Picton, H.M., Harris, S.E., Muruvi, W. & Chambers, E.L. (2008). The in vitro growth and maturation of follicles. Reproduction 136, 703–15.CrossRefGoogle ScholarPubMed
Putney, D.J., Drost, M. & Thatcher, W.W. (1989). Influence of summer heat stress on pregnancy rates of lactating dairy cattle following embryo transfer or artificial insemination. Theriogenology 31, 765–78.CrossRefGoogle ScholarPubMed
Rensis, F.D. & Scaramuzzi, R.J. (2003). Heat stress and seasonal effects on reproduction in the dairy cow: a review. Theriogenology 60, 1139–51.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
Roti, J.L. (2008). Cellular responses to hyperthermia (40–46°C): cell killing and molecular events. Int. J. Hyperthermia 24, 3–15.CrossRefGoogle Scholar
Schrock, G.E., Saxton, A.M., Schrick, F.N. & Edwards, J.L. (2007). Early in vitro fertilization improves development of bovine ova heat stressed during in vitro maturation. J. Dairy Sci. 90, 4297–303.CrossRefGoogle ScholarPubMed
Siemer, C., Smiljakovic, T., Bhojwani, M., Leiding, C., Kanitz, W., Kubelka, M. & Tomek, W. (2009). Analysis of mRNA associated factors during bovine oocyte maturation and early embryonic development. Mol. Reprod. Dev. 76, 1208–19.CrossRefGoogle ScholarPubMed
Sirard, M.A. (2001). Resumption of meiosis: mechanism involved in meiotic progression and its relation with developmental competence. Theriogenology 55, 1241–54.CrossRefGoogle ScholarPubMed
Szollosi, D. (1962). Cortical granules: a general feature of mammalian eggs? J. Reprod. Fert. 4, 223–4.Google Scholar
Szollosi, D. (1967). Development of cortical granules and the cortical reaction in rat and hamster eggs. Anat. Rec. 159, 431–46.CrossRefGoogle ScholarPubMed
Szollosi, D. (1971). Morphological changes in mouse eggs due to aging in the fallopian tube. Am. J. Anat. 130, 209–25.CrossRefGoogle ScholarPubMed
Szollosi, D. (1974). The spindle structure in mammalian eggs: the effect of ageing. Colloque: Les accidents chromosomiques de la reproduction. pp. 241–50.Google Scholar
Szollosi, D. (1975a). Mammalian eggs aging in the fallopian tubes. In Aging Gametes, Their Biology and Pathology. Proceedings of the International Symposium on Aging Gametes, 13–16 June 1973. pp. 98–121. Seattle: Washington, USA.Google Scholar
Szollosi, D. (1975b). Ultrastructural aspects of oocyte maturation and fertilization in mammals. La fecondation. Colloque de la Societe Nationale pour l'Etude de la Sterilite et de la Fecondite. pp. 13–35.Google Scholar
Szollosi, D., Gerard, M., Menezo, Y. & Thibault, C. (1978). Permeability of ovarian follicle: corona cell–oocyte relationship in mammals. Ann. Biol. Anim. Bioch. Biophys. 18, 511–21.CrossRefGoogle Scholar
Thibault, C., Szollosi, D. & Gerard, M. (1987). Mammalian oocyte maturation. Reprod. Nutr. Dev. 27, 865–96.CrossRefGoogle ScholarPubMed
Tseng, J.K., Chen, C.H., Chou, P.C., Yeh, S.P. & Ju, J.C. (2004). Influences of follicular size on parthenogenetic activation and in vitro heat shock on the cytoskeleton in cattle oocytes. Reprod. Domest. Anim. 39, 146–53.CrossRefGoogle ScholarPubMed
Wang, W., Hosoe, M., Li, R. & Shioya, Y. (1997). Development of the competence of bovine oocytes to release cortical granules and block polyspermy after meiotic maturation. Dev. Growth Differ. 39, 607–15.CrossRefGoogle ScholarPubMed
Wessel, G.M., Brooks, J.M., Green, E., Haley, S., Voronina, E., Wong, J., Zaydfudim, V. & Conner, S. (2001). The biology of cortical granules. Int. Rev. Cytol. 209, 117–206.CrossRefGoogle ScholarPubMed
Wessel, G.M., Conner, S.D. & Berg, L. (2002). Cortical granule translocation is microfilament mediated and linked to meiotic maturation in the sea urchin oocyte. Development 129, 4315–25.CrossRefGoogle ScholarPubMed