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Effects of epigenetic modifier on the developmental competence and quantitative expression of genes in male and female buffalo (Bubalus bubalis) cloned embryos

Published online by Cambridge University Press:  09 January 2023

Anjit Sandhu*
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal 132001, Haryana, India
Sushil K. Mohapatra
Affiliation:
Department of Animal Biotechnology, College of Veterinary Science and AH, Kamdhenu University, Sardarkrushinagar, Gujarat, India
Manoj K. Singh
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal 132001, Haryana, India
Suresh K. Singla
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal 132001, Haryana, India
Manmohan S. Chauhan
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal 132001, Haryana, India
Radhey S. Manik
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal 132001, Haryana, India
*
Author for correspondence: Anjit Sandhu. Animal Biotechnology Centre, National Dairy Research Institute, Karnal 132001, Haryana, India. E-mail: anjitsandhu26@gmail.com

Summary

Adult male and female Murrah buffalo fibroblast cells were used as donors for the production of embryos using handmade cloning. Both donor cells and reconstructed embryos were treated with 50 nM trichostatin-A (TSA) and 7.5 nM 5-aza-2′-deoxycytidine (5-aza-dC). The blastocyst rate of both treated male (40.1% ± 2.05) and female (37.0% ± 0.83) embryos was significantly lower than in untreated control males (49.7% ± 3.80) and females (47.2% ± 2.44) but their apoptotic index was lower (male, control: 5.90 ± 0.48; treated: 4.96 ± 0.31): (female, control: 8.11 ± 0.67; treated: 6.65 ± 0.43) and epigenetic status in terms of global acetylation and methylation of histone was significantly improved. The expression level of hypoxanthine-guanine phosphoribosyltransferase (HPRT) was higher (P < 0.05) and that of PGK, G6PD, OCT 4, IFN-tau and CASPASE3 was significantly lower (P < 0.05) in treated male blastocyst than control and the expression levels of DNMT1, IGF1R and BCL-XL were not significantly different between the two groups. In the female embryos, the relative mRNA abundance of OCT4 was significantly higher (P < 0.05), and that of XIST and CASPASE3 was significantly lower (P < 0.05) in the epigenetic modifier-treated group compared with that of the control group, whereas the expression levels of HPRT, PGK, G6PD, DNMT1, IFN-tau, IGF1R and BCL-XL were not significantly different between the two groups. In both embryos, a similar effect of treatment was observed on genes related to growth and development, but the effect on the expression of X-linked genes varied. These results indicate that not all X-linked genes respond to TSA and 5-aza-dC treatment in the same manner.

Type
Research Article
Copyright
© National Dairy Research Institute, Karnal, India, 2023. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally to this work.

References

Bermejo-Alvarez, P., Rizos, D., Rath, D., Lonergan, P. and Gutierrez-Adan, A. (2010). Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts. Proceedings of the National Academy of Sciences of the United States of America, 107(8), 33943399. doi: 10.1073/pnas.0913843107 CrossRefGoogle ScholarPubMed
Boiani, M., Eckardt, S., Schöler, H. R. and McLaughlin, K. J. (2002). Oct4 distribution and level in mouse clones: Consequences for pluripotency. Genes and Development, 16(10), 12091219. doi: 10.1101/gad.966002 CrossRefGoogle ScholarPubMed
Bourc’his, D., Le Bourhis, D., Patin, D., Niveleau, A., Comizzoli, P., Renard, J. P. and Viegas-Péquignot, E. (2001). Delayed and incomplete reprogramming of chromosome methylation patterns in bovine cloned embryos. Current Biology, 11(19), 15421546. doi: 10.1016/s0960-9822(01)00480-8 CrossRefGoogle ScholarPubMed
Cervera, R. P., Martí-Gutiérrez, N., Escorihuela, E., Moreno, R. and Stojkovic, M. (2009). Trichostatin-A affects histone acetylation and gene expression in porcine somatic cell nucleus transfer embryos. Theriogenology, 72(8), 10971110. doi: 10.1016/j.theriogenology.2009.06.030 CrossRefGoogle ScholarPubMed
Cui, X. S., Xu, Y. N., Shen, X. H., Zhang, L. Q., Zhang, J. B. and Kim, N. H. (2011). Trichostatin-A modulates apoptotic-related gene expression and improves embryo viability in cloned bovine embryos. Cellular Reprogramming, 13(2), 179189. doi: 10.1089/cell.2010.0060 CrossRefGoogle ScholarPubMed
Ding, X., Wang, Y., Zhang, D., Wang, Y., Guo, Z. and Zhang, Y. (2008). Increased preimplantation development of cloned bovine embryos treated with 5-aza-2¢-deoxycytidine and trichostatin-A. Theriogenology, 70(4), 622630. doi: 10.1016/j.theriogenology.2008.04.042 CrossRefGoogle ScholarPubMed
Enright, B. P., Kubota, C., Yang, X. and Tian, X. C. (2003). Epigenetic characteristics and development of embryos cloned from donor cells treated by trichostatin-A or 5-aza-2¢-deoxycytidine. Biology of Reproduction, 69(3), 896901. doi: 10.1095/biolreprod.103.017954 CrossRefGoogle ScholarPubMed
Enright, B. P., Sung, L. Y., Chang, C. C., Yang, X. and Tian, X. C. (2005). Methylation and acetylation characteristics of cloned bovine embryos from donor cells treated with 5-aza-2¢-deoxycytidine. Biology of Reproduction, 72(4), 944948. doi: 10.1095/biolreprod.104.033225 CrossRefGoogle ScholarPubMed
Haaf, T., Ott, G. and Schimd, M. (1988) Inhibition of condensation in the late replicating X chromosome induced by 5 aza deoxy cytidine in human lymphocyte culture. Human Genetics,79, 1823. doi: 10.1007/BF00291703 CrossRefGoogle Scholar
Hattori, N., Nishino, K., Ko, Y. G., Hattori, N., Ohgane, J., Tanaka, S. and Shiota, K. (2004). Epigenetic control of mouse Oct-4 gene expression in embryonic stem cells and trophoblast stem cells. Journal of Biological Chemistry, 279(17), 1706317069. doi: 10.1074/jbc.M309002200 CrossRefGoogle ScholarPubMed
Heard, E., Rougeulle, C., Arnaud, D., Avner, P., Allis, C. D. and Spector, D. L. (2001). Methylation of histone H3 at Lys-9 is an early mark on the X chromosome during X-inactivation. Cell, 107(6), 727738. doi: 10.1016/s0092-8674(01)00598-0 CrossRefGoogle Scholar
Iager, A. E., Ragina, N. P., Ross, P. J., Beyhan, Z., Cunniff, K., Rodriguez, R. M. and Cibelli, J. B. (2008). Trichostatin-A improves histone acetylation in bovine somatic cell nuclear transfer early embryos. Cloning and Stem Cells, 10(3), 371379. doi: 10.1089/clo.2007.0002 CrossRefGoogle ScholarPubMed
Jeon, B. G., Coppola, G., Perrault, S. D., Rho, G. J., Betts, D. H. and King, W. A. (2008). S-adenosylhomocysteine treatment of adult female fibroblasts alters X-chromosome inactivation and improves in vitro embryo development after somatic cell nuclear transfer. Reproduction, 135(6), 815828. doi: 10.1530/REP-07-0442 CrossRefGoogle ScholarPubMed
Kang, Y. K., Koo, D. B., Park, J. S., Choi, Y. H., Chung, A. S., Lee, K. K. and Han, Y. M. (2001). Aberrant methylation of donor genome in cloned bovine embryos. Nature Genetics, 28(2), 173177. doi: 10.1038/88903 CrossRefGoogle ScholarPubMed
Kishigami, S., Mizutani, E., Ohta, H., Hikichi, T., Thuan, N. V., Wakayama, S., Bui, H. T. and Wakayama, T. (2006a). Significant improvement of mouse cloning technique by treatment with trichostatin-A after somatic nuclear transfer. Biochemical and Biophysical Research Communications, 340(1), 183189. doi: 10.1016/j.bbrc.2005.11.164 CrossRefGoogle ScholarPubMed
Kishigami, S., Van Thuan, N., Hikichi, T., Ohta, H., Wakayama, S., Mizutani, E. and Wakayama, T. (2006b). Epigenetic abnormalities of the mouse paternal zygotic genome associated with microinsemination of round spermatids. Developmental Biology, 289(1), 195205. doi: 10.1016/j.ydbio.2005.10.026 CrossRefGoogle ScholarPubMed
Lee, H. S., Park, M. H.., Yang, S. J., Jung, H. Y., Byun, S. S., Lee, D. S., Yoo, H. S., Yeom, Y. I. and Seo, S. B. (2004) Gene expression analysis in human gastric cancer cell line treated with trichostatin A and S-adenosyl-l-homocysteine using cDNA microarray. Biological & Pharmaceutical Bulletin, 27, 14971503. doi: 10.1248/bpb.27.1497 CrossRefGoogle ScholarPubMed
Li, X. P., Kato, Y., Tsuji, Y. and Tsunoda, Y. (2008). The effects of trichostatin-A on mRNA expression of chromatin structure-, DNA methylation-, and development-related genes in cloned mouse blastocyst. Cloning and Stem Cells, 10(1), 133142. doi: 10.1089/clo.2007.0066 CrossRefGoogle Scholar
Lyon, M. F. (1961). Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature, 190, 372373. doi: 10.1038/190372a0 CrossRefGoogle ScholarPubMed
Meng, Q.-G., Polgar, Z., Liu, J. and Dinnyes, A. (2009). Live birth of somatic cell-cloned rabbits following trichostatin-A treatment and cotransfer of parthenogenetic embryos. Cloning and Stem Cells, 11(1), 203208. doi: 10.1089/clo.2008.0072 CrossRefGoogle ScholarPubMed
Mermoud, J. E., Popova, B., Peters, A. H., Jenuwein, T. and Brockdorff, N. (2002). Histone H3 lysine 9 methylation occurs rapidly at the onset of random X chromosome inactivation. Current Biology, 12(3), 247251. doi: 10.1016/s0960-9822(02)00660-7 CrossRefGoogle ScholarPubMed
Mohapatra, S. K., Sandhu, A., Neerukattu, V. S., Singh, K. P., Selokar, N. L., Singla, S. K., Chauhan, M. S., Manik, R. S. and Palta, P. (2015b). Buffalo embryos produced by handmade cloning from oocytes selected using brilliant cresyl blue staining have better developmental competence and quality and are closer to embryos produced by in vitro fertilization in terms of their epigenetic status and gene expression pattern. Cellular Reprogramming, 17(2), 141150. doi: 10.1089/cell.2014.0077 CrossRefGoogle ScholarPubMed
Mohapatra, S. K., Sandhu, A., Singh, K. P., Singla, S. K., Chauhan, M. S., Manik, R. S. and Palta, P. (2015a). Establishment of trophectoderm cell lines from buffalo (Bubalus bubalis) embryos of different sources and examination of in vitro developmental competence, quality, epigenetic status and gene expression in cloned embryos derived from them. PLOS ONE, 10(6), e0129235. doi: 10.1371/journal.pone.0129235 CrossRefGoogle Scholar
Nolen, L. D., Gao, S., Han, Z., Mann, M. R., Gie Chung, Y., Otte, A. P., Bartolomei, M. S. and Latham, K. E. (2005). X chromosome reactivation and regulation in cloned embryos. Developmental Biology, 279(2), 525540. doi: 10.1016/j.ydbio.2005.01.016 CrossRefGoogle ScholarPubMed
Ogawa, H., Ono, Y., Shimozawa, N., Sotomaru, Y., Katsuzawa, Y., Hiura, H., Ito, M. and Kono, T. (2003). Disruption of imprinting in cloned mouse fetuses from embryonic stem cells. Reproduction, 126(4), 549557. doi: 10.1530/rep.0.1260549 CrossRefGoogle ScholarPubMed
Panning, B. and Jaenisch, R. (1996). DNA hypomethylation can activate Xist expression and silence X-linked genes. Genes and Development, 10(16), 19912002. doi: 10.1101/gad.10.16.1991 CrossRefGoogle ScholarPubMed
Park, C. H., Jeong, Y. H., Jeong, Y. I., Lee, S. Y., Jeong, Y. W., Shin, T., Kim, N. H., Jeung, E. B., Hyun, S. H., Lee, C. K., Lee, E. and Hwang, W. S. (2012). X-linked gene transcription patterns in female and male in vivo, in vitro and cloned porcine individual blastocysts. PLOS ONE, 7(12), e51398. doi: 10.1371/journal.pone.0051398 CrossRefGoogle ScholarPubMed
Peters, A. H., Mermoud, J. E., O’Carroll, D., Pagani, M., Schweizer, D., Brockdorff, N. and Jenuwein, T. (2002). Histone H3 lysine 9 methylation is an epigenetic imprint of facultative heterochromatin. Nature Genetics, 30(1), 7780. doi: 10.1038/ng789 CrossRefGoogle ScholarPubMed
Saini, M., Selokar, N. L., Agrawal, H., Singla, S. K., Chauhan, M. S., Manik, R. S. and Palta, P. (2017). Treatment of donor cells and reconstructed embryos with a combination of trichostatin-A and 5-aza-2'-deoxycytidine improves the developmental competence and quality of buffalo embryos. Cellular Reprogramming, 19(3), 208215. doi: 10.1089/cell.2016.0061 CrossRefGoogle ScholarPubMed
Sandhu, A., Mohapatra, S. K., Agrawal, H., Singh, M. K., Palta, P., Singla, S. K., Chauhan, M. S. and Manik, R. S. (2016). Effect of sex of embryo on developmental competence, epigenetic status, and gene expression in buffalo (Bubalus bubalis) embryos produced by hand-made cloning. Cellular Reprogramming, 18(5), 356365. doi: 10.1089/cell.2015.0077 CrossRefGoogle ScholarPubMed
Sangalli, J. R., De Bem, T. H., Perecin, F., Chiaratti, M. R., Oliveira, Lde J., de Araújo, R. R., Valim Pimentel, J. R., Smith, L. C. and Meirelles, F. V. (2012). Treatment of nuclear-donor cells or cloned zygotes with chromatin-modifying agents increases histone acetylation but does not improve full-term development of cloned cattle. Cellular Reprogramming, 14(3), 235247. doi: 10.1089/cell.2011.0079 CrossRefGoogle Scholar
Sasaki, T., Hansen, R.S. and Gartler, S.M. (1992) Hemimethylation and hypersensitivity are early events in transcriptional reactivation of human inactive X-linked genes in a hamster x human somatic cell hybrid. Molecular Cell Biology, 12, 38193826 doi: 10.1128/mcb.12.9.3819 Google Scholar
Selokar, N. L., Shah, R. A., Saha, A. P., Muzaffar, M., Saini, M., Chauhan, M. S., Manik, R. S., Palta, P. and Singla, S. K. (2012). Effect of post-fusion holding time, orientation and position of somatic cell-cytoplasts during electrofusion on the development of handmade cloned embryos in buffalo (Bubalus bubalis). Theriogenology, 78(4), 930936. doi: 10.1016/j.theriogenology.2012.03.018 CrossRefGoogle ScholarPubMed
Sharma, R., George, A., Kamble, N. M., Singh, K. P., Chauhan, M. S., Singla, S. K., Manik, R. S. and Palta, P. (2011). Optimization of culture conditions to support long-term self-renewal of buffalo (Bubalus bubalis) embryonic stem cell-like cells. Cellular Reprogramming, 13(6), 539549. doi: 10.1089/cell.2011.0041 CrossRefGoogle ScholarPubMed
Singh, K. P., Mohapatra, S. K., Kaushik, R., Singh, M. K., Palta, P., Singla, S. K., Manik, R. S. and Chauhan, M. S. (2021). Parthenogenetic activation of buffalo (Bubalus bubalis) oocytes: Comparison of different activation reagents and different mediamedium on their developmental competence and quantitative expression of developmentally regulated genes. Zygote, 29(1), 4958. doi: 10.1017/S0967199420000519 CrossRefGoogle ScholarPubMed
Verma, G., Arora, J. S., Sethi, R. S., Mukhopadhyay, C. S. and Verma, R. (2015). Handmade cloning: Recent advances, potential and pitfalls. Journal of Animal Science and Biotechnology, 6, 43. doi: 10.1186/s40104-015-0043-y CrossRefGoogle ScholarPubMed
Wang, Y., Su, J., Wang, L., Xu, W., Quan, F., Liu, J. and Zhang, Y. (2011a). The effects of 5-aza-2'-deoxycytidine and trichostatin-A on gene expression and DNA methylation status in cloned bovine blastocysts. Cellular Reprogramming, 13(4), 297306. doi: 10.1089/cell.2010.0098 CrossRefGoogle ScholarPubMed
Wang, Y. S., Xiong, X. R., An, Z. X., Wang, L. J., Liu, J., Quan, F. S., Hua, S. and Zhang, Y. (2011b). Production of cloned calves by combination treatment of both donor cells and early cloned embryos with 5-aza-2'-deoxycytidine and trichostatin-A. Theriogenology, 75(5), 819825. doi: 10.1016/j.theriogenology.2010.10.022 CrossRefGoogle ScholarPubMed
Xiong, Y. N., Dowdy, S. C., Podratz, K. C., Jin, F., Attewell, J. R., Eberhardt, N. L. and Jiang, S. W. (2005). Histone deacetylase inhibitors decrease DNA methyltransferase-3B messenger RNA stability and down-regulate de novo DNA methyltransferase activity in human endometrial cells. Cancer Research, 65(7), 26842689. doi: 10.1158/0008-5472.CAN-04-2843 CrossRefGoogle ScholarPubMed
Xue, F., Tian, X. C., Du, F., Kubota, C., Taneja, M., Dinnyes, A., Dai, Y., Levine, H., Pereira, L. V. and Yang, X. (2002). Aberrant patterns of X chromosome inactivation in bovine clones. Nature Genetics, 31(2), 216220. doi: 10.1038/ng900 CrossRefGoogle ScholarPubMed
Yoshida, M., Kijima, M., Akita, M. and Beppu, T. (1990). Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin-A. Journal of Biological Chemistry, 265(28), 1717417179. doi: 10.1016/S0021-9258(17)44885-X CrossRefGoogle ScholarPubMed
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