Hostname: page-component-745bb68f8f-lrblm Total loading time: 0 Render date: 2025-01-10T19:34:32.725Z Has data issue: false hasContentIssue false
  • English
  • Français

Gene expression, oocyte nuclear maturation and developmental competence of bovine oocytes and embryos produced after in vivo and in vitro heat shock

Published online by Cambridge University Press:  28 March 2016

Krishna C. Pavani ,
Erica Baron ,
Pedro Correia ,
Joana Lourenço ,
Bruno Filipe Bettencourt ,
Madalena Sousa  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.
Erica Baron
Affiliation:
Centro Universitário Monte Serrat, Rua Comendador Martins, 52 – Vila Matias, Santos – SP, 11015–530, Brazil.
Pedro Correia
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.
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.
Bruno Filipe Bettencourt
Affiliation:
Instituto de Investigação e Inovação em Saúde, Institute for Molecular and Cell Biology (IBMC), University of Porto, Porto, Portugal. Hospital de Santo Espírito da Ilha Terceira, SEEBMO, Angra do Heroísmo, Portugal.
Madalena Sousa
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.
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. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Three assays were performed. In assay 1, oocytes harvested during the winter months were subjected to kinetic heat shock by stressing the oocytes at 39.5°C (HS1) or at 40.5°C (HS2) for either 6, 12, 18 or 24 h and then matured at control temperature (38.5°C). The nuclear maturation rates (NMR) of all oocytes were recorded after 24 h. In assay 2, oocytes collected year-round maturated, were implanted via in vitro fertilization (IVF) and developed for 9 days. Gene expression analysis was performed on target genes (Cx43, CDH1, DNMT1, HSPA14) with reference to the two housekeeping genes (GAPDH and SDHA) in embryos. Similarly, in assay 3, genetic analysis was performed on the embryos produced from heat-stressed oocytes (from HS1 and HS2). In assay 1, the duration of heat stress resulted in a significant decline in NMR (P < 0.05) with HS1 for maturated oocytes at 86.4 ± 4.3; 65.5 ± 0.7; 51.3 ± 0.9; 38.1 ± 1.9 and 36.3 ± 0.9, for control, 6 h, 12 h, 18 h and 24 h, respectively. For assays 2 and 3, results demonstrated that DNMT1, Cx43 and HSPA14 were down-regulated in the embryos produced in the warm with respect to the cold months (P < 0.05). A constant up- and down-regulation of DNMT1 and HSPA14 genes were observed in both HS-treated samples. Also, an inconsistent pattern of gene expression was observed in Cx43 and CDH1 genes (P < 0.05). Targeted gene expression was aberrant in embryo development, which can provide evidence on early embryo arrest and slowed embryo development.

Keywords

ApoptosisGene quantificationKinetic heat shockMaternal heat stressNuclear maturation
Type
Research Article
Information
Zygote , Volume 24 , Issue 5 , October 2016 , pp. 748 - 759
Copyright
Copyright © Cambridge University Press 2016 

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

Ahlskog, J.K., Björk, J.K, Elsing, A.N., Aspelin, C., Kallio, M., Roos-Mattjus, P. & Sistonen, L., (2010). Anaphase-promoting complex/cyclosome participates in the acute response to protein-damaging stress. Mol. Cell. Biol. 30, 5608–20.Google Scholar
Armstrong, D.V. (1994). Heat stress interaction with shade and cooling. J. Dairy Sci. 77, 2044–50.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.CrossRefGoogle ScholarPubMed
Beaman, G.M. (2012). Effects of heat shock, hypoxia, post-mortem interval and glioma disease state on heat shock gene HSPA expression. PhD thesis, University of Central Lancashire, Preston, England, http://clok.uclan.ac.uk/6584/ Google Scholar
Betts, D.H. & King, W.A. (2001). Genetic regulation of embryo death and senescence. Theriogenology 55, 171–91.Google Scholar
Boni, R., Tosti, E., Roviello, S. & Dale, B. (1999). Intercellular communication in in vivo and in vitro-produced bovine embryos. Biol. Reprod. 61, 1050–5.CrossRefGoogle ScholarPubMed
Cho, J., Kang, S. & Lee, B.C. (2014). Identification of abnormal gene expression in bovine transgenic somatic cell nuclear transfer embryos. J. Vet. Sci. 15, 225–31.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
Dode, M.A., Dufort, I., Massicotte, L. & Sirard, M.A. (2006). Quantitative expression of candidate genes for developmental competence in bovine two-cell embryos. Mol. Reprod. Dev. 73, 288–97.CrossRefGoogle ScholarPubMed
Dunlap, S.E. & Vincent, C.K. (1971) Influence of post breeding thermal stress on conception rate in beef cattle. J. Anim. Sci. 32, 1216–8.Google Scholar
Ealy, A.D., Drost, M. & Hansen, P.J. (1993). Developmental changes in embryonic resistance to adverse effects of maternal heat stress in cows. J. Dairy Sci. 76, 2899–905.CrossRefGoogle ScholarPubMed
Edwards, J.L. & Hansen, P.J. (1997). Differential responses of bovine oocytes and preimplantation embryos to heat shock. Mol. Reprod. Dev. 46, 138–45.Google Scholar
Edwards, J.L., Bogart, A.N., Rispoli, L.A., Saxton, A.M. & Schrick, F.N. (2009). Developmental competence of bovine embryos from heat-stressed ova. J. Dairy Sci. 92, 563–70.Google Scholar
Eymery, A., Souchier, C., Vourc'h, C. & Jolly, C. (2010). Heat shock factor 1 binds to and transcribes satellite II and III sequences at several pericentromeric regions in heat-shocked cells. Exp. Cell. Res. 316, 1845–55.Google Scholar
Faheem, M.S., Carvalhais, I., Chaveiro, A. & Moreira da Silva, F. (2011). In vitro oocyte fertilization and subsequent embryonic development after cryopreservation of bovine tissue, using an effective approach for oocyte collection. Anim. Reprod. Sci. 125, 49–55.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
Gad, A., Besenfelder, U., Rings, F., Ghanem, N., Salilew-Wondim, D., Hossain, M.M., Tesfaye, D., Lonergan, P., Becker, A., Cinar, U., Schellander, K., Havlicek, V. & Hölker, M. (2011). Effect of reproductive tract environment following controlled ovarian hyper stimulation treatment on embryo development and global transcriptome profile of blastocysts: implications for animal breeding and human assisted reproduction. Hum. Reprod. 26, 1693–707.CrossRefGoogle Scholar
Gendelman, M. & Roth, Z. (2012). Seasonal effect on germinal vesicle-stage bovine oocytes is further expressed by alterations in transcript levels in the developing embryos associated with reduced developmental competence. Biol. Reprod. 86, 1–9.CrossRefGoogle ScholarPubMed
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.Google Scholar
Giraldo, A.M., DeCourcy, K., Ball, S.F., Hylan, D. & Ayares, D.L. (2013). Gene expression of Dnmt1 isoforms in porcine oocytes, embryos, and somatic cells. Cell Reprogram. 15, 309–21.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
Gómez, E., Caamaño, J.N., Bermejo-Alvarez, P., Díez, C., Muñoz, M., Martín, D., Carrocera, S. & Gutiérrez-Adán, A. (2009). Gene expression in early expanded parthenogenetic and in vitro fertilized bovine blastocysts. J. Reprod. Dev. 55, 607–14.Google Scholar
Gordon, I. (2003). Laboratory production of cattle embryos. Chapter 4: Maturing the oocytes. Cambridge: CABI Publishing, pp. 155–6.Google Scholar
Hiendleder, S., Mund, C. & Reichenbach, H.D. (2004). Tissue-specific elevated genomic cytosine methylation levels are associated with an overgrowth phenotype of bovine foetuses derived by in vitro techniques. Biol. Reprod. 71, 217–23.Google Scholar
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
Houghton, F.D. (2005). Role of gap junctions during early embryo development. Reproduction 129, 129–35.Google Scholar
Ju, J.C., Parks, J.E. & Yang, X. (1999). Thermo tolerance of IVM-derived bovine oocytes and embryos after short term heat shock. Mol. Reprod. Dev. 53, 336–40.Google Scholar
Levy, R.R., Cordonier, H., Czyba, J.C. & Goerin, J.F. (2001). Apoptosis in preimplantation mammalian embryo and genetics. Int. J. Anat. Embryol. 106, 101–8.Google ScholarPubMed
Lima, R.S. (2012). O papel do fator de crescimento semelhante a insulin-1 sobre os efeitos deleterious do choque térmico em oócitos bovinos no stadio de vesicular germinativa. Botucatu, Brasil: UNESP. Thesis. [The role of growth factors similar to insulin-1 on the deleterious effects of heat shock in bovine ooccytes at the germinal vesicle stage.]Google Scholar
Lonergan, P., Rizos, D., Gutierrez-Adan, A., Moreira, P.M., Pintado, B., De la Fuente, J. & Boland, M.P. (2003). Temporal divergence in the pattern of messenger RNA expression in bovine embryos cultured from the zygote to blastocyst stage in vitro or in vivo . Biol. Reprod. 69, 1424–31.Google Scholar
Monica, C., Dorella, D.P., Enrica, T., Romina, G., Giovanni, G., Angela, D.A. & Franca, A. (2004). GAPDH as housekeeping gene at renal level. Kidney Int. 65, 1972–1973.Google Scholar
Nemcova, L., Machatkova, M., Hanzalova, K., Horakova, J. & Kanka, J. (2006). Gene expression in bovine embryos derived from oocytes with different developmental competence collected at the defined follicular developmental stage. Theriogenology 65, 1254–64.Google Scholar
Neuer, A., Spandorfer, S.D., Giraldo, P., Dieterle, S., Rosenwaks, Z. & Witkin, S.S. (2000). The role of heat shock proteins in reproduction. Hum. Reprod. Update 6, 149–59.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.CrossRefGoogle ScholarPubMed
Paula-Lopes, F.F., Milazzotto, M., Assumpcao, M.E.O.A. & Visintin, J.A. (2008). Heat shock-induced damage in bovine oocytes. Reprod. Fertil. Dev. 43, 208.Google Scholar
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, 232–239.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.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.Google Scholar
Payton, R.R., Rispoli, L.A., Saxton, A.M. & Edwards, J.L. (2011). Impact of heat stress exposure during meiotic maturation on oocyte, surrounding cumulus cell, and embryo RNA populations. J. Reprod. Dev. 57, 481–91.Google Scholar
Pfaffl, M.W., Horgan, G.W. & Dempfle, L. (2002). Relative Expression Software Tool (REST C) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, 1–10.Google Scholar
Riethmacher, D., Brinkmann, V. & Birchmeier, C. (1995). A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development. Proc. Natl. Acad. Sci. 92, 855–9.Google Scholar
Rivera, R.M. & Hansen, P.J. (2001). Development of cultured bovine embryos after exposure to high temperatures in the physiological range. Reproduction 121, 107–15.Google Scholar
Rizos, D., Gutierrez-Adan, A., Perez-Garnelo, S., De La Fuente, J., Boland, M.P. & Lonergan, P. (2003). Bovine embryo culture in the presence of serum: implication for blastocyst development, cryotolerance, and messenger RNA expression. Biol. Reprod. 68, 236–43.Google Scholar
Robertson, K.D. (2005). DNA methylation and human disease. Nat. Rev. Genet. 6, 597–610.Google Scholar
Roth, Z., Arav, A., Bor, A., Zeron, Y., Braw-Tal, R. & Wolfenson, D. (2001). Improvement of quality of oocytes collected in the autumn by enhanced removal of impaired follicles from previously heat-stressed cows. Reproduction 122, 737–44.Google Scholar
Roth, Z. & Hansen, P.J. (2004) Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation. Biol. Reprod. 71, 1898–906.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
Rozen, S. & Skaletsky, H. (2000). Primer3 on the WWW for general users and for biologist programmers methods. Mol. Biol. 132, 365–86.Google Scholar
Sartori, R., Sartor-Bergfelt, R., Mertens, S.A., Guenther, J.N., Parrish, J.J. & Wiltbank, M.C. (2002). Fertilization and early embryonic development in heifers and lactating cows in summer and lactating and dry cows in winter. J. Dairy Sci. 85, 2803–12.CrossRefGoogle ScholarPubMed
Sibley, C.P., Coan, P.M., Ferguson-Smith, A.C., Dean, W., Hughes, J., Smith, P., Reik, W., Burton, G.J., Fowden, A.L. & Constancia, M. (2004). Placental-specific insulin-like growth factor 2 (Igf2) regulates the diffusional exchange characteristics of the mouse placenta. Proc. Natl. Acad. Sci. USA 101, 8204–8.Google Scholar
Sirotkin, A.V. (2010). Effect of two types of stress (heat shock/high temperature and malnutrition/serum deprivation) on porcine ovarian cell functions and their response to hormones. J. Exp. Biol. 213, 2125–30.CrossRefGoogle ScholarPubMed
Sonna, L.A., Fujita, J., Gaffin, S.L. & Craig, M.L. (2002). Molecular biology of thermoregulation invited review: effects of heat and cold stress on mammalian gene expression. J. Appl. Physiol. 92, 1725–42.Google Scholar
Stancheva, I., El-Maarri, O., Walter, J., Niveleau, A. & Meehan, R.R. (2002). DNA methylation at promoter regions regulates the timing of gene activation in Xenopus laevis embryos. Dev. Biol. 243, 155–65.Google Scholar
Su, J., Wang, Y., Xing, X., Liu, J. & Zhang, Y. (2014). Genome-wide analysis of DNA methylation in bovine placentas. BMC Genomics 15, 12.Google Scholar
Suzuki, M.M. & Bird, A. (2008). DNA methylation landscapes: provocative insights from epigenomics. Nat. Rev. Genet. 9, 465–76.Google Scholar
Tilman, G., Arnoult, N., Lenglez, S., Van Beneden, A., Loriot, A., De Smet, C. & Decottignies, A. (2012). Cancer-linked satellite 2 DNA hypomethylation does not regulate Sat2 non-coding RNA expression and is initiated by heat shock pathway activation. Epigenetics 7, 903–13.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
Vestweber, D. & Kemler, R. (1984). Rabbit antiserum against a purified surface glycoprotein decompacts mouse preimplantation embryos and reacts with specific adult tissues. Exp. Cell. Res. 152, 169–78.Google Scholar
Wolfenson, D., Roth, Z. & Meidan, R. (2000). Impaired reproduction in heat-stressed cattle: basic and applied aspects. Anim. Reprod. Sci. 60–61, 535–47.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