Histone acetylation during the in vitro maturation of bovine oocytes with different levels of competence
Thais P. Pontelo A , Sarah A. D. Rodrigues B , Taynan S. Kawamoto C , Ligiane O. Leme D , A. C. M. M. Gomes E , Marcio G. Zangeronimo A , Mauricio M. Franco E and Margot A. N. Dode E FA Department of Veterinary Medicine, Federal University of Lavras, Lavras, MG 32700-000, Brazil.
B Department of Animal Science, University of Brasilia, Brasilia, DF 70910-900, Brazil.
C Department of Veterinary Medicine, Federal University Uberlândia, Uberlândia, MG 38400-902, Brazil.
D Department of Animal Science, Federal University of Espírito Santo, Vitória, ES 29075-073, Brazil.
E Embrapa Genetic Resources and Biotechnology, Brasília, DF 70770-900, Brazil.
F Corresponding author. Email: margot.dode@embrapa.br
Reproduction, Fertility and Development 32(7) 690-696 https://doi.org/10.1071/RD19218
Submitted: 17 June 2019 Accepted: 6 December 2019 Published: 31 March 2020
Abstract
We aimed to analyse the histone acetylation status and expression profile of genes involved in histone acetylation (histone acetyltransferase 1 (HAT1), lysine acetyltransferase 2A (KAT2A), histone deacetylase 1 (HDAC1), HDAC2 and HDAC3) in bovine oocytes of different competences during in vitro maturation (IVM). Cumulus–oocyte complexes were recovered from two groups of follicles: minor follicles (1.0–3.0 mm in diameter), classified as low competence (LC) and large follicles (6.0–8.0 mm in diameter) classified as high competence (HC). Oocytes were submitted to IVM for 0, 8 and 24 h and stored for analysis. Acetylation status of histone H4 on lysine K5, K6, K12 and K16 was assessed by immunohistochemistry. For gene expression, mRNA levels were determined by real-time quantitative polymerase chain reaction. All oocytes, regardless of their competence, showed a gradual decrease (P < 0.05) in acetylation signals during IVM. From 0 to 8 h of maturation, an increase (P < 0.05) in the relative abundance of HAT1 mRNA was observed only in the HC oocytes. In this group, higher (P < 0.05) mRNA levels of HDAC1 at 8 h of maturation were also observed. In conclusion, in the present study, LC oocytes were shown to have adequate acetylation levels for the resumption and progression of meiosis; however, these oocytes do not have the capacity to synthesise RNA during IVM as the HC oocytes do.
Additional keywords: cumulus–oocyte complexes, gene expression, histone acetyltransferase, immunohistochemistry, epigenetic marks.
References
Abramoff, M. D., Magalhaes, P. J., and Ram, S. J. (2004). Image processing with ImageJ. Biophotonics Int. 11, 36–42.Akiyama, T., Kim, J. M., Nagata, M., and Aoki, F. (2004). Regulation of histone acetylation during meiotic maturation in mouse oocytes. Mol. Reprod. Dev. 69, 222–227.
| Regulation of histone acetylation during meiotic maturation in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 15293224PubMed |
Bessa, I. R., Nishimura, R. C., Franco, M. M., and Dode, M. A. (2013). Transcription profile of candidate genes for the acquisition of competence during oocyte growth in cattle. Reprod. Domest. Anim. 48, 781–789.
| Transcription profile of candidate genes for the acquisition of competence during oocyte growth in cattle.Crossref | GoogleScholarGoogle Scholar | 23574109PubMed |
Blondin, P., and Sirard, M. A. (1995). Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes. Mol. Reprod. Dev. 41, 54–62.
| Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 7619506PubMed |
Blondin, P., Coenen, K., Guilbault, L. A., and Sirard, M. A. (1997). In vitro production of bovine embryos: developmental competence is acquired before maturation. Theriogenology 47, 1061–1075.
| In vitro production of bovine embryos: developmental competence is acquired before maturation.Crossref | GoogleScholarGoogle Scholar | 16728056PubMed |
Blondin, P., Vigneault, C., Nivet, A., and Sirard, M. (2012). Improving oocyte quality in cows and heifers – what have we learned so far? Anim. Reprod. 9, 281–289.
Caixeta, E. S., Ripamonte, P., Franco, M. M., Junior, J. B., and Dode, M. A. (2009). Effect of follicle size on mRNA expression in cumulus cells and oocytes of Bos indicus: an approach to identify marker genes for developmental competence. Reprod. Fertil. Dev. 21, 655–664.
| Effect of follicle size on mRNA expression in cumulus cells and oocytes of Bos indicus: an approach to identify marker genes for developmental competence.Crossref | GoogleScholarGoogle Scholar | 19486602PubMed |
Caixeta, F. M., Sousa, R. V., Guimaraes, A. L., Leme, L. O., Spricigo, J. F., Netto, S. B., Pivato, I., and Dode, M. A. (2017). Meiotic arrest as an alternative to increase the production of bovine embryos by somatic cell nuclear transfer. Zygote 25, 32–40.
| Meiotic arrest as an alternative to increase the production of bovine embryos by somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 27780485PubMed |
De La Fuente, R. (2006). Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes. Dev. Biol. 292, 1–12.
| Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes.Crossref | GoogleScholarGoogle Scholar | 16466710PubMed |
de Wit, A. A., Wurth, Y. A., and Kruip, T. A. (2000). Effect of ovarian phase and follicle quality on morphology and developmental capacity of the bovine cumulus–oocyte complex. J. Anim. Sci. 78, 1277–1283.
| Effect of ovarian phase and follicle quality on morphology and developmental capacity of the bovine cumulus–oocyte complex.Crossref | GoogleScholarGoogle Scholar | 10834583PubMed |
Ding, L., Pan, R., Huang, X., Wang, J. X., Shen, Y. T., Xu, L., Zhang, Y., Liu, Y., He, X. Q., Yang, X. J., Qi, Z. Q., and Wang, H. L. (2012). Changes in histone acetylation during oocyte meiotic maturation in the diabetic mouse. Theriogenology 78, 784–792.
| Changes in histone acetylation during oocyte meiotic maturation in the diabetic mouse.Crossref | GoogleScholarGoogle Scholar | 22541329PubMed |
Endo, T., Kano, K., and Naito, K. (2008). Nuclear histone deacetylases are not required for global histone deacetylation during meiotic maturation in porcine oocytes. Biol. Reprod. 78, 1073–1080.
| Nuclear histone deacetylases are not required for global histone deacetylation during meiotic maturation in porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 18305223PubMed |
Ge, Z.-J., Schatten, H., Zhang, C.-L., and Sun, Q.-Y. (2015). Oocyte ageing and epigenetics. Reproduction 149, R103–R114.
| Oocyte ageing and epigenetics.Crossref | GoogleScholarGoogle Scholar | 25391845PubMed |
Hales, B. F., Grenier, L., Lalancette, C., and Robaire, B. (2011). Epigenetic programming: from gametes to blastocyst. Birth Defects Res. A Clin. Mol. Teratol. 91, 652–665.
| Epigenetic programming: from gametes to blastocyst.Crossref | GoogleScholarGoogle Scholar | 21425433PubMed |
Huang, J., Li, T., Ding, C. H., Brosens, J., Zhou, C. Q., Wang, H. H., and Xu, Y. W. (2012). Insufficient histone-3 lysine-9 deacetylation in human oocytes matured in vitro is associated with aberrant meiosis. Fertil. Steril. 97, 178–184e3.
| Insufficient histone-3 lysine-9 deacetylation in human oocytes matured in vitro is associated with aberrant meiosis.Crossref | GoogleScholarGoogle Scholar | 22100169PubMed |
Kim, J.-M., Liu, H., Tazaki, M., Nagata, M., and Aoki, F. (2003). Changes in histone acetylation during mouse oocyte meiosis. J. Cell Biol. 162, 37–46.
| Changes in histone acetylation during mouse oocyte meiosis.Crossref | GoogleScholarGoogle Scholar | 12835313PubMed |
Lequarre, A. S., Vigneron, C., Ribaucour, F., Holm, P., Donnay, I., Dalbies-Tran, R., Callesen, H., and Mermillod, P. (2005). Influence of antral follicle size on oocyte characteristics and embryo development in the bovine. Theriogenology 63, 841–859.
| Influence of antral follicle size on oocyte characteristics and embryo development in the bovine.Crossref | GoogleScholarGoogle Scholar | 15629802PubMed |
Lin, J., Chen, F., Sun, M. J., Zhu, J., Li, Y. W., Pan, L. Z., Zhang, J., and Tan, J. H. (2016). The relationship between apoptosis, chromatin configuration, histone modification and competence of oocytes: a study using the mouse ovary-holding stress model. Sci. Rep. 6, 28347.
| The relationship between apoptosis, chromatin configuration, histone modification and competence of oocytes: a study using the mouse ovary-holding stress model.Crossref | GoogleScholarGoogle Scholar | 27321442PubMed |
Lodde, V., Modina, S., Galbusera, C., Franciosi, F., and Luciano, A. M. (2007). Large-scale chromatin remodeling in germinal vesicle bovine oocytes: interplay with gap junction functionality and developmental competence. Mol. Reprod. Dev. 74, 740–749.
| Large-scale chromatin remodeling in germinal vesicle bovine oocytes: interplay with gap junction functionality and developmental competence.Crossref | GoogleScholarGoogle Scholar | 17075796PubMed |
Lodde, V., Luciano, A., Franciosi, F., Labrecque, R., and Sirard, M. (2017). Accumulation of chromatin remodelling enzyme and histone transcripts in bovine oocytes. Results Probl. Cell. Differ. 63, 223–255.
| Accumulation of chromatin remodelling enzyme and histone transcripts in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 28779321PubMed |
Lonergan, P., Monaghan, P., Rizos, D., Boland, M. P., and Gordon, I. (1994). Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro. Mol. Reprod. Dev. 37, 48–53.
| Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro.Crossref | GoogleScholarGoogle Scholar | 8129930PubMed |
Lonergan, P., Rizos, D., Gutierrez-Adan, A., Fair, T., and Boland, M. P. (2003). Oocyte and embryo quality: effect of origin, culture conditions and gene expression patterns. Reprod. Domest. Anim. 38, 259–267.
| Oocyte and embryo quality: effect of origin, culture conditions and gene expression patterns.Crossref | GoogleScholarGoogle Scholar | 12887565PubMed |
Lowther, K. M., and Mehlmann, L. M. (2015). Embryonic poly(A)-binding protein is required during early stages of mouse oocyte development for chromatin organization, transcriptional silencing, and meiotic competence. Biol. Reprod. 93, 43.
| Embryonic poly(A)-binding protein is required during early stages of mouse oocyte development for chromatin organization, transcriptional silencing, and meiotic competence.Crossref | GoogleScholarGoogle Scholar | 26134869PubMed |
Luciano, A. M., Lodde, V., Franciosi, F., Tessaro, I., Corbani, D., and Modina, S. (2012). Large-scale chromatin morpho-functional changes during mammalian oocyte growth and differentiation. Eur. J. Histochem. 56, e37.
| Large-scale chromatin morpho-functional changes during mammalian oocyte growth and differentiation.Crossref | GoogleScholarGoogle Scholar | 23027353PubMed |
Ma, P., and Schultz, R. M. (2013). Histone deacetylase 2 (HDAC2) regulates chromosome segregation and kinetochore function via H4K16 deacetylation during oocyte maturation in mouse. PLoS Genet. 9, e1003377.
| Histone deacetylase 2 (HDAC2) regulates chromosome segregation and kinetochore function via H4K16 deacetylation during oocyte maturation in mouse.Crossref | GoogleScholarGoogle Scholar | 23516383PubMed |
Ma, P., and Schultz, R. M. (2016). HDAC1 and HDAC2 in mouse oocytes and preimplantation embryos: specificity versus compensation. Cell Death Differ. 23, 1119–1127.
| HDAC1 and HDAC2 in mouse oocytes and preimplantation embryos: specificity versus compensation.Crossref | GoogleScholarGoogle Scholar | 27082454PubMed |
Maalouf, W. E., Alberio, R., and Campbell, K. H. (2008). Differential acetylation of histone H4 lysine during development of in vitro-fertilized, cloned and parthenogenetically activated bovine embryos. Epigenetics 3, 199–209.
| Differential acetylation of histone H4 lysine during development of in vitro-fertilized, cloned and parthenogenetically activated bovine embryos.Crossref | GoogleScholarGoogle Scholar | 18698155PubMed |
Machatkova, M., Krausova, K., Jokesova, E., and Tomanek, M. (2004). Developmental competence of bovine oocytes: effects of follicle size and the phase of follicular wave on in vitro embryo production. Theriogenology 61, 329–335.
| Developmental competence of bovine oocytes: effects of follicle size and the phase of follicular wave on in vitro embryo production.Crossref | GoogleScholarGoogle Scholar | 14662132PubMed |
Pan, Z., Zhang, J., Li, Q., Li, Y., Shi, F., Xie, Z., and Liu, H. (2012). Current advances in epigenetic modification and alteration during mammalian ovarian folliculogenesis. J. Genet. Genomics 39, 111–123.
| Current advances in epigenetic modification and alteration during mammalian ovarian folliculogenesis.Crossref | GoogleScholarGoogle Scholar | 22464470PubMed |
Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
| A new mathematical model for relative quantification in real-time RT-PCR.Crossref | GoogleScholarGoogle Scholar | 11328886PubMed |
Racedo, S. E., Wrenzycki, C., Lepikhov, K., Salamone, D., Walter, J., and Niemann, H. (2009). Epigenetic modifications and related mRNA expression during bovine oocyte in vitro maturation. Reprod. Fertil. Dev. 21, 738–748.
| Epigenetic modifications and related mRNA expression during bovine oocyte in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 19567217PubMed |
Sirard, M. A. (2001). Resumption of meiosis: mechanism involved in meiotic progression and its relation with developmental competence. Theriogenology 55, 1241–1254.
| Resumption of meiosis: mechanism involved in meiotic progression and its relation with developmental competence.Crossref | GoogleScholarGoogle Scholar | 11327682PubMed |
Sirard, M. A., Richard, F., Blondin, P., and Robert, C. (2006). Contribution of the oocyte to embryo quality. Theriogenology 65, 126–136.
| Contribution of the oocyte to embryo quality.Crossref | GoogleScholarGoogle Scholar | 16256189PubMed |
Stojkovic, M., Machado, S. A., Stojkovic, P., Zakhartechenko, V., Hutzler, P., Gonçalves, P. B., and Wolf, E. (2001). Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol. Reprod. 64, 904–909.
| Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture.Crossref | GoogleScholarGoogle Scholar | 11207207PubMed |
Sun, H., Lu, F., Liu, X., Tian, M., Ruan, Z., Zhu, P., Ruan, Q., Jiang, J., and Shi, D. (2015). Effects of scriptaid on the histone acetylation of buffalo oocytes and their ability to support the development of somatic cell nuclear transfer embryos. Theriogenology 83, 1219–1225.
| Effects of scriptaid on the histone acetylation of buffalo oocytes and their ability to support the development of somatic cell nuclear transfer embryos.Crossref | GoogleScholarGoogle Scholar | 25640327PubMed |
van den Berg, I. M., Eleveld, C., van der Hoeven, M., Birnie, E., Steegers, E. A., Galjaard, R. J., Laven, J. S., and van Doorninck, J. H. (2011). Defective deacetylation of histone 4 K12 in human oocytes is associated with advanced maternal age and chromosome misalignment. Hum. Reprod. 26, 1181–1190.
| Defective deacetylation of histone 4 K12 in human oocytes is associated with advanced maternal age and chromosome misalignment.Crossref | GoogleScholarGoogle Scholar | 21349858PubMed |
Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, research0034.1.
| Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.Crossref | GoogleScholarGoogle Scholar | 12184808PubMed |
Wu, X. F., Yuan, H. J., Li, H., Gong, S., Lin, J., Miao, Y. L., Wang, T. Y., and Tan, J. H. (2015). Restraint stress on female mice diminishes the developmental potential of oocytes: roles of chromatin configuration and histone modification in germinal vesicle stage oocytes. Biol. Reprod. 92, 13.
| Restraint stress on female mice diminishes the developmental potential of oocytes: roles of chromatin configuration and histone modification in germinal vesicle stage oocytes.Crossref | GoogleScholarGoogle Scholar | 25411393PubMed |