Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-18T15:13:45.974Z Has data issue: false hasContentIssue false
  • English
  • Français

The effect of kinetic heat shock on bovine oocyte maturation and subsequent gene expression of targeted genes

Published online by Cambridge University Press:  08 June 2017

Krishna C. Pavani ,
António Rocha ,
Erica Baron ,
Joana Lourenço ,
Marwa Faheem  and
Fernando Moreira da Silva
Krishna C. Pavani
Affiliation:
Department of Agrarian Sciences, CITA-A (Research Centre for Agricultural and Environmental Sciences and Technology of the Azores), Animal Reproduction, University of the Azores, Angra do Heroísmo 9700-042, Portugal Department of Reproduction, Obstetrics and Herd Health, Faculty of Veterinary Medicine, University of Ghent, Salisburylaan 133, B-9820 Merelbeke, Belgium
António Rocha
Affiliation:
ICBAS, Abel Salazar Biomedical Institute, University of Porto, Campus Agrário de Vairão, Rua Padre Armando Quintas, 4485–661 Vairão, Porto, Portugal
Erica Baron
Affiliation:
Centro Universitário Monte Serrat, Rua Comendador Martins, 52 - Vila Matias, Santos – SP, 11015–530, Brazil
Joana Lourenço
Affiliation:
Department of Agrarian Sciences, CITA-A (Research Centre for Agricultural and Environmental Sciences and Technology of the Azores), Animal Reproduction, University of the Azores, Angra do Heroísmo 9700-042, Portugal
Marwa Faheem
Affiliation:
Department of Animal Production Science, Faculty of Agriculture, Cairo University, 12613 Giza, Egypt
Fernando Moreira da Silva*
Affiliation:
Departamento de Ciências Agrárias, Secção Reprodução, Campus de Angra do Heroísmo, Universidade dos Açores, Rua Capitão João D'Avila, 9700-042 Angra do Heroísmo, Portugal
*
All correspondence to: Fernando Moreira da Silva. Departamento de Ciências Agrárias, Secção Reprodução, Campus de Angra do Heroísmo, Universidade dos Açores, Rua Capitão João D'Avila, 9700-042 Angra do Heroísmo, Portugal, Tel.: +351 295 402200, Fax: +351 295 402209, Email: joaquim.fm.silva@uac.pt
Get access Rights & Permissions [Opens in a new window]

Summary

The exposure of oocytes to heat stress during the maturation process results in harmful effects to their internal organelles, low fertilization capability and higher embryonic losses. In the present experiment the effect of heat shock (HS) during the maturation process was assessed. In Assay 1, oocytes from winter (December–March; n = 100) and summer (June–September; n = 100) months were collected and matured to analyse their HS tolerance. Total RNA was extracted from matured oocytes and cDNA synthesis was performed, followed by qPCR for selected genes (Cx43, CDH1, DNMT1, HSPA14), compared with two reference genes (GAPDH and SDHA). In Assay 2, oocytes collected during the winter were subjected to kinetic HS by stressing them at 39.5°C for 6, 12, 18 or 24 h and were afterwards matured at control temperature (38.5°C), and subsequently subjected to the previously described gene analysis procedure. Results of Assay 1 show that summer-collected oocytes exhibited lower maturation rate than winter-collected oocytes, which may be due to the down-regulation of the HSPA 14 gene. Assay 2 showed that 6 h of HS had no effect on gene regulation. CDH1 and DNMT1 up-regulation was observed starting at 12 h, which may represent the effect of heat shock on oocyte development.

Keywords

ApoptosisGene quantificationKinetic heat shockMaternal heat stress
Type
Short Communication
Information
Zygote , Volume 25 , Issue 3 , June 2017 , pp. 383 - 389
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arechiga, C.F., Ealy, A.D. & Hansen, P.J. (1995). Evidence that glutathione is involved in thermotolerance of preimplantation murine embryos. Biol. Reprod. 52, 1296–301.Google Scholar
Badinga, L., Collier, R.J., Thatcher, W.W. & Wilcox, C.J. (1985). Effects of climatic and management factors on conception rate of dairy cattle in subtropical environment. J. Dairy Sci. 68, 78–85.Google Scholar
Cirio, M.C., Ratnam, S. & Ding, F. (2008). Preimplantation expression of the somatic form of Dnmt1 suggests a role in the inheritance of genomic imprints. BMC Dev. Biol. 8, 9–22.Google Scholar
Craig, E.A. & Gross, C.A. (1991). Is hsp70 the cellular thermometer? Trend. Biochem. Sci. 16,135–40.Google Scholar
Denomme, M.M. & Mann, M.R. (2012). Genomic imprints as a model for the analysis of epigenetic stability during assisted reproductive technologies. Reproduction 144, 393–409.Google Scholar
Edwards, J.L. & Hansen, P.J. (1997). Differential responses of bovine oocytes and preimplantation embryos to heat shock. Mol. Reprod. Dev. 46, 138–45.3.0.CO;2-R>CrossRefGoogle ScholarPubMed
Eguren, M., Porlan, E., Manchado, E., García-Higuera, I., Cañamero, M., Fariñas, I. & Malumbres, M. (2013). The APC/C cofactor Cdh1 prevents replicative stress and p53-dependent cell death in neural progenitors. Nat. Commun. 4, 2880.Google Scholar
Faheem, M.S., Baron, E., Carvalhais, I., Chaveiro, A., Pavani, K. & Moreira da Silva, F. (2014). The effect of vitrification of immature bovine oocytes to the subsequent in vitro development and gene expression. Zygote 26, 1–10.Google Scholar
Gallicano, G.I. (2001). Composition, regulation, and function of the cytoskeleton in mammalian eggs and embryos. Front. Biosci. 6, 1089–108.Google Scholar
Gendelman, M., Aroyo, A., Yavin, S. & Roth, Z. (2010). Seasonal effects on gene expression, cleavage timing, developmental competence of bovine preimplantation embryos. Reproduction 140, 73–82.CrossRefGoogle ScholarPubMed
Georgopoulos, C. & Welch, W.J. (1993). Role of the major heat shock proteins as molecular chaperones. Annu. Rev. Cell. Biol. 9, 601–34.Google Scholar
Golding, M.C. & Westhusin, M.E. (2003). Analysis of DNA (cytosine 5). methyltransferase mRNA sequence and expression in bovine preimplantation embryos, fetal and adult tissues. Gene. Expr. Patterns. 3, 551–8.Google Scholar
Hansen, P.J. (2009). Effects of heat stress on mammalian reproduction. Philos. Trans. Roy. Soc. B. 364, 3341–50.CrossRefGoogle ScholarPubMed
Hirasawa, R., Chiba, H. & Kaneda, M. (2008). Maternal and zygotic Dnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation development. Genes. Dev. 22, 1607–16.Google Scholar
Kang, P.J., Ostermann, J., Shilling, J., Neupert, W., Craig, E.A. & Pfanner, N. (1990). Requirement for Hsp70 in the mitochondrial matrix for translocation and folding of precursor protein. Nature 348, 137–43.Google Scholar
Kurihara, Y., Kawamura, Y., Uchijima, Y., Amamo, T., Kobayashi, H., Asano, T., & Kurihara, H. Maintenance of genomic methylation patterns during preimplantation development requires the somatic form of DNA methyltransferase 1. Dev. Biol. 313, 335–46.Google Scholar
Palii, S.S., Van Emburgh, B.O., Sankpal, U.T., Brown, K.D. & Robertson, K.D. (2008). DNA methylation inhibitor 5-Aza-2´-deoxycytidine induces reversible genome-wide DNA damage that is distinctly influenced by DNA methyltransferases 1 and 3B. Mol. Cell. Biol. 28, 752–71.Google Scholar
Pavani, K., Carvalhais, I., Faheem, M., Chaveiro, A., Reis, F.V. & Moreira da Silva, F. (2015b). Reproductive performance of Holstein dairy cows grazing in dry-summer subtropical climatic conditions: Effect of heat stress and heat shock on meiotic competence and in vitro fertilization. Asian Australas. J. Anim. Sci. 28, 334–42.CrossRefGoogle ScholarPubMed
Pavani, K.C., Baron, E.E., Faheem, M., Chaveiro, A. & Moreira da Silva, F. (2015a). Optimization of total RNA extraction from bovine oocytes and embryos for gene expression studies and effects of cryoprotectants on total RNA extraction. Cytology and Genetics 49, 2339.Google Scholar
Pavani, K.C., Baron, E., Correia, P., Lourenço, J., Bettencourt, B.F., Sousa, M. & Moreira da Silva, F. (2016). Gene expression, oocyte nuclear maturation and developmental competence of bovine oocytes and embryos produced after in vivo and in vitro heat shock. Zygote 28,1–12.Google Scholar
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
Pfeiffer, M.J., Slatkowski, M., Paudel, Y., Balbach, S.T., Baeumer, N., Crosetto, N., Drexler, H.C., Fuellen, G. & Boiani, M. (2011). Proteomic analysis of mouse oocytes reveals 28 candidate factors of the “Reprogrammome”. J. Proteome. Res. 10, 2140–53.CrossRefGoogle ScholarPubMed
Putney, D.J, Mullins, S., Thatcher, W.W., Drost, M. & Gross, T.S. (1989). Embryonic development in superovulated dairy cattle exposed to elevated ambient temperatures between the onset of estrus and insemination. Anim. Reprod. Sci. 19, 37–51.Google Scholar
Rivera, R.M., Kelley, K.L., Erdos, G.W. & Hansen, P.J. (2004). Reorganization of microfilaments and microtubules by thermal stress in two-cell bovine embryos. Biol. Reprod. 70, 1852–62.Google Scholar
Roth, Z., Inbar, G. & Arav, A. (2008). Comparison of oocyte developmental competence and follicular steroid content of nulliparous heifers and cows at different stages of lactation. Theriogenology 69, 932–9.Google Scholar
Russell, D.L. & Robker, R.L. (2007). Molecular mechanisms of ovulation: co-ordination through the cumulus complex. Hum. Reprod. Update. 13, 289–312.Google Scholar
Ryan, D.P., Blakewood, E.G., Lynn, J.W., Munyakazi, L. & Godke, R.A. (1992). Effect of heat-stress in bovine embryo development in vitro . J. Anim. Sci. 70, 3490–7.Google Scholar
Shin, M.R. & Kim, N.H. (2003). Maternal gamma (gamma)-tubulin is involved in microtubule reorganization during bovine fertilization and parthenogenesis. Mol. Reprod. Dev. 64, 438–45.Google Scholar
Sudo, T., Ota, Y., Kotani, S., Nakao, M., Takami, Y., Takeda, S. & Saya, H. (2001). Activation of Cdh1-dependent APC is required for G1 cell cycle arrest and DNA damage-induced G2 checkpoint in vertebrate cells. EMBO J. 20, 6499–508.Google Scholar
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.Google Scholar
Zhang, B., Peñagaricano, F., Driver, A., Chen, H. & Khatib, H. (2011). Differential expression of heat shock protein genes and their splice variants in bovine preimplantation embryos. J. Dairy Sci. 94, 4174–82.Google Scholar