Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2017 (2017), Article ID 1502489, 14 pages
https://doi.org/10.1155/2017/1502489
Research Article

Oxidative Stress Alters the Profile of Transcription Factors Related to Early Development on In Vitro Produced Embryos

1Center of Natural and Human Sciences, Universidade Federal do ABC, Santo André, SP, Brazil
2Institute of Biomedical Sciences, Universidade de São Paulo, SP, Brazil
3Institute of Biosciences, Campus Botucatu, Department of Pharmacology, Universidade Estadual Paulista (UNESP), Botucatu, SP, Brazil
4School of Sciences and Languages, Campus Assis, Department of Biological Sciences, Universidade Estadual Paulista (UNESP), Assis, SP, Brazil

Correspondence should be addressed to Marcella Pecora Milazzotto

Received 18 April 2017; Revised 4 August 2017; Accepted 21 August 2017; Published 25 October 2017

Academic Editor: Serafina Perrone

Copyright © 2017 Roberta Ferreira Leite et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. Lonergan, D. Rizosa, A. Gutiérrez-Adánb, T. Faira, and M. P. Bolanda, “Effect of culture environment on embryo quality and gene expression – experience from animal studies,” Reproductive Biomedicine Online, vol. 7, pp. 657–663, 2003. View at Publisher · View at Google Scholar
  2. T. C. Mundim, A. F. Ramos, R. Sartori et al., “Changes in gene expression profiles of bovine embryos produced in vitro, by natural ovulation, or hormonal superstimulation,” Genetics and Molecular Research, vol. 8, pp. 1398–1407, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. G. L. Cagnone, I. Dufort, C. Vigneault, and M. A. Sirard, “Differential gene expression profile in bovine blastocysts resulting from hyperglycemia exposure during early cleavage stages,” Biology of Reproduction, vol. 86, pp. 1–12, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. G. L. Cagnone and M. A. Sirard, “Transcriptomic signature to oxidative stress exposure at the time of embryonic genome activation in bovine blastocysts,” Molecular Reproduction and Development, vol. 80, pp. 297–314, 2013. View at Publisher · View at Google Scholar · View at Scopus
  5. M. P. Milazzotto, M. D. Goissis, J. L. Chitwood et al., “Early cleavages influence the molecular and the metabolic pattern of individually cultured bovine blastocysts,” Molecular Reproduction and Development, vol. 83, pp. 324–336, 2016. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Clemente, I. Lopez-Vidriero, P. O'Gaora et al., “Transcriptome changes at the initiation of elongation in the bovine conceptus,” Biology of Reproduction, vol. 85, pp. 285–295, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. D. Rizos, P. Lonergan, M. P. Boland et al., “Analysis of differential messenger RNA expression between bovine blastocysts produced in different culture systems: implications for blastocyst quality,” Biology of Reproduction, vol. 66, pp. 589–595, 2002. View at Publisher · View at Google Scholar
  8. V. A. Absalón-Medina, W. R. Butler, and R. O. Gilbert, “Preimplantation embryo metabolism and culture systems: experience from domestic animals and clinical implications,” Journal of Assisted Reproduction and Genetics, vol. 31, no. 4, pp. 393–409, 2014. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Gad, M. Hoelker, U. Besenfelder et al., “Molecular mechanisms and pathways involved in bovine embryonic genome activation and their regulation by alternative in vivo and in vitro culture conditions,” Biology of Reproduction, vol. 87, no. 4, pp. 1–13, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Amin, A. Gad, D. Salilew-Wondim et al., “Bovine embryo survival under oxidative-stress conditions is associated with activity of the NRF2-mediated oxidative-stress-response pathway,” Molecular Reproduction and Development, vol. 81, pp. 497–513, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. M. C. Simon and B. Keith, “The role of oxygen availability in embryonic development and stem cell function,” Nature Reviews-Molecular Cell Biology, vol. 9, p. 285, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. P. Guerin, S. Mouatassim, and Y. Menezo, “Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings,” Human Reproduction Update, vol. 7, pp. 175–189, 2001. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Gupta, L. Sekhon, and A. Agarwal, “The role of oxidative stress and antioxidants in assisted reproduction,” Current Women's Health Reviews, vol. 6, pp. 227–238, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. F. J. Martín-Romero, E. M. Miguel-Lasobras, J. A. Domínguez-Arroyo, E. González-Carrera, and I. S. Álvarez, “Contribution of culture media to oxidative stress and its effect on human oocytes,” Reproductive BioMedicine Online, vol. 17, pp. 652–661, 2008. View at Publisher · View at Google Scholar
  15. D. Feil, M. Lane, C. T. Roberts et al., “Effect of culturing mouse embryos under different oxygen concentrations on subsequent fetal and placental development,” The Journal of Physiology, vol. 572, no. 1, pp. 87–96, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Takahashi, K. Keicho, Z. H. Takahashi, H. Ogawa, R. M. Schultz, and A. Okano, “Effect of oxidative stress on development and DNA damage in-vitro cultured bovine embryos by comet assay,” Theriogenology, vol. 54, pp. 137–145, 2000. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. Fujitani, K. Kasai, S. Ohtani, K. Nishimura, M. Yamada, and K. Utsumi, “Effect of oxygen concentration and free radicals on in vitro development of in vitro-produced bovine embryos,” Journal of Animal Science, vol. 75, pp. 483–489, 1997. View at Publisher · View at Google Scholar
  18. N. W. Karja, P. Wongsrikeao, M. Murakami et al., “Effects of oxygen tension on the development and quality of porcine in vitro fertilized embryos,” Theriogenology, vol. 62, pp. 1585–1595, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Agarwal, T. M. Said, M. A. Bedaiwy, J. Banerjee, and J. G. Alvarez, “Oxidative stress in an assisted reproductive techniques setting,” Fertility and Sterility, vol. 86, pp. 503–512, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. C. A. Burroughs, G. L. Williamson, M. C. Golding, and C. R. Long, “Oxidative stress induced changes in epigenetic modifying gene mRNA in pre-implantation in vitro bovine embryos,” Reproduction, Fertility and Development, vol. 25, p. 149, 2012. View at Publisher · View at Google Scholar
  21. S. B. Yoon, S. A. Choi, B. W. Sim et al., “Developmental competence of bovine early embryos depends on the coupled response between oxidative and endoplasmic reticulum stress,” Biology of Reproduction, vol. 90, pp. 1–10, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. W. Li, K. Goossens, M. Van Poucke et al., “High oxygen tension increases global methylation in bovine 4-cell embryos and blastocysts but does not affect general retrotransposon expression,” Reproduction, Fertility and Development, vol. 28, no. 7, pp. 948–959, 2016. View at Publisher · View at Google Scholar · View at Scopus
  23. A. J. Harvey, “The role of oxygen in ruminant preimplantation embryo development and metabolism,” Animal Reproduction Science, vol. 98, pp. 113–128, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. T. Ushijima and K. Asada, “Aberrant DNA methylation in contrast with mutations,” Cancer Science, vol. 101, pp. 300–305, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. R. Urrego, N. Rodriguez-Osorio, and H. Niemann, “Epigenetic disorders and altered gene expression after use of assisted reproductive technologies in domestic cattle,” Epigenetics, vol. 9, pp. 803–815, 2014. View at Publisher · View at Google Scholar · View at Scopus
  26. J. J. Parrish, J. Susko-Parrish, M. A. Winer, and N. L. First, “Capacitation of bovine sperm by heparin,” Biology of Reproduction, vol. 38, pp. 1171–1180, 1988. View at Publisher · View at Google Scholar
  27. E. O. Pontes, J. I. Moss, and P. J. Hansen, Detection of Reactive Oxygen Species in Preimplantation Bovine Embryos, Department of Animal Sciences, University of Florida, FL, USA, 2008.
  28. C. L. Andersen, J. L. Jensen, and T. F. Orntoft, “Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization,” Cancer Research, vol. 64, pp. 5245–5250, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. J. D. Zhang, R. Biczok, and M. Ruschhaupt, “ddCt: The ddCt Algorithm for the Analysis of Quantitative Real-Time PCR (qRT-PCR),” R package version 1.32.0, 2015, https://www.bioconductor.org/packages/release/bioc/html/ddCt.html. View at Google Scholar
  30. J. Block, S. D. Fields, and P. J. Hansen, Simple Protocol for Differential Staining of Inner Cell Mass and Trophectoderm of Bovine Embryos, Department of Animal Sciences, University of Florida, FL, USA, 2009.
  31. G. A. Thouas, N. A. Korfiatis, A. J. French, G. M. Jones, and A. O. Trounson, “Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts,” Reproductive BioMedicine Online, vol. 3, pp. 25–29, 2001. View at Publisher · View at Google Scholar · View at Scopus
  32. N. L. Selokar, A. Saha, M. Saini, M. Muzaffer, M. S. Chauhan, and R. S. Manik, “A protocol for differential staining of inner cell mass and trophectoderm of embryos for evaluation of health status,” Current Science, vol. 102, pp. 1256-1257, 2012. View at Google Scholar
  33. D. W. Huang, B. T. Sherman, and R. A. Lempicki, “Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources,” Nature Protocols, vol. 4, pp. 44–57, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. S. E. Olson and G. E. Seidel, “Reduced oxygen tension and EDTA improve bovine zygote development in a chemically defined medium,” Journal of Animal Science, vol. 78, pp. 152–157, 2000. View at Publisher · View at Google Scholar
  35. NCBI, “GENES,” October 2016, http://www.ncbi.nlm.nih.gov/gene.
  36. A. J. Harvey, K. L. Kind, and J. G. Thompson, “REDOX regulation of early embryo development,” Reproduction, vol. 123, pp. 479–486, 2002. View at Publisher · View at Google Scholar
  37. B. Bavister, “Oxygen concentration and preimplantation development,” Reproductive BioMedicine Online, vol. 9, pp. 484–486, 2004. View at Publisher · View at Google Scholar
  38. A. Van Soom, Y. Q. Yuan, L. J. Peelman et al., “Prevalence of apoptosis and inner cell allocation in bovine embryos cultured under different oxygen tensions with or without cysteine addition,” Theriogenology, vol. 57, pp. 1453–1465, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. C. M. G. Silva, L. R. Faustino, M. V. A. Saraiva, R. Rossetto, and J. R. Figueiredo, “Influence of oxygen tension in oocyte maturation and in vitro culture of follicles and embryos,” Revista Brasileira de Reprodução Animal, vol. 34, pp. 233–242, 2010. View at Google Scholar
  40. M. Misirlioglu, G. P. Page, H. Sagirkaya et al., “Dynamics of global transcriptome in bovine matured oocytes and preimplantation embryos,” Proceedings of the National Academy of Sciences, vol. 103, pp. 18905–18910, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. V. Hall, K. Hinrichs, G. Lazzari, D. H. Betts, and P. Hyttel, “Early embryonic development, assisted reproductive technologies, and pluripotent stem cell biology in domestic mammals,” The Veterinary Journal, vol. 197, pp. 128–142, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. E. Hervouet, F. M. Vallette, and P.-F. Cartron, “Dnmt3/transcription factor interactions as crucial players in targeted DNA methylation,” Epigenetics, vol. 4, pp. 487–499, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. L. Liu, G. Jin, and X. Zhou, “Modeling the relationship of epigenetic modifications to transcription factor binding,” Nucleic Acids Research, vol. 43, pp. 3873–3885, 2015. View at Publisher · View at Google Scholar · View at Scopus
  44. A. J. Bannister and T. Kouzarides, “Regulation of chromatin by histone modifications,” Cell Research, vol. 21, pp. 381–395, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. D. Corcoran, T. Fair, and P. Lonergan, “Predicting embryo quality: mRNA expression and the preimplantation embryo,” Reprodicineiton Biomed Online, vol. 11, pp. 340–348, 2005. View at Publisher · View at Google Scholar
  46. A. M. Reimold, N. N. Iwakoshi, J. Manis et al., “Plasma cell differentiation requires the transcription factor XBP-1,” Nature, vol. 412, pp. 300–307, 2001. View at Publisher · View at Google Scholar · View at Scopus
  47. D. R. Khan, D. Dube, L. Gall et al., “Expression of pluripotency master regulators during two key developmental transitions: EGA and early lineage specification in the bovine embryo,” PLoS One, vol. 7, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. M. D. Goissis and J. B. Cibelli, “Functional characterization of SOX2 in bovine preimplantation embryos,” Biology of Reproduction, vol. 90, pp. 1–10, 2014. View at Publisher · View at Google Scholar · View at Scopus
  49. E. R. Gibney and C. M. Nolan, “Epigenetics and gene expression,” Heredity, vol. 105, pp. 4–13, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Mathieu, Z. Zhang, A. Nelson et al., “Hypoxia induces re-entry of committed cells into pluripotency,” Stem Cells, vol. 31, pp. 1737–1748, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. E. Waal, W. Mak, S. Calhoun et al., “In vitro culture increases the frequency of stochastic epigenetic errors at imprinted genes in placental tissues from mouse concepti produced through assisted reproductive technologies,” Biology of Reproduction, vol. 90, pp. 1–12, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. D. M. Messerschmidt, B. B. Knowles, and D. Solter, “DNA methylation dynamics during epigenetic reprogramming in the germline and preimplantation embryos,” Genes & Development, vol. 28, pp. 812–828, 2014. View at Publisher · View at Google Scholar · View at Scopus
  53. J. G. Thompson, A. C. Simpson, P. A. Pugh, P. E. Donnelley, and H. R. Tervit, “Effect of oxygen concentration on in-vitro development of preimplantation sheep and cattle embryos,” Journal of Reproduction and Fertility, vol. 89, pp. 573–578, 1990. View at Publisher · View at Google Scholar