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Parthenogenetic activation of buffalo (Bubalus bubalis) oocytes: comparison of different activation reagents and different media on their developmental competence and quantitative expression of developmentally regulated genes

Published online by Cambridge University Press:  02 October 2020

K.P. Singh ,
S.K. Mohapatra Open the ORCID record for S.K. Mohapatra [Opens in a new window] ,
R. Kaushik ,
M.K. Singh ,
P. Palta ,
S.K. Singla ,
R.S. Manik  and
M.S. Chauhan
K.P. Singh
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal, Haryana, India
S.K. Mohapatra
Affiliation:
Department of Animal Biotechnology, College of Veterinary Science and A.H. Sardarkrushinagar Dantiwada Agricultural University, Sardarkrushinagar, Gujarat, India.
R. Kaushik
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal, Haryana, India
M.K. Singh
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal, Haryana, India
P. Palta
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal, Haryana, India
S.K. Singla
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal, Haryana, India
R.S. Manik
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal, Haryana, India
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Summary

This study was carried out to compare the efficacy of different methods to activate buffalo A + B and C + D quality oocytes parthenogenetically and to study the in vitro developmental competence of oocytes and expression of some important genes at the different developmental stages of parthenotes. The percentage of A + B oocytes (62.16 ± 5.06%, range 53.8–71.3%) was significantly higher (P < 0.001) compared with that of C + D oocytes (37.8 ± 5.00%, range 28.6–46.1%) retrieved from slaughterhouse buffalo ovaries. Among all combinations, ethanol activation followed by culture in research vitro cleave medium gave the highest cleavage and blastocyst yields for both A + B and C + D grade oocytes. Total cell numbers, inner cell mass/trophectoderm ratio and apoptotic index of A + B group blastocysts were significantly different (P < 0.05) from their C + D counterpart. To determine the status of expression patterns of developmentally regulated genes, the expression of cumulus–oocyte complexes, fertilization, developmental competence and apoptotic-related genes were also studied in parthenogenetically produced buffalo embryos at different stages, and indicated that the differential expression patterns of the above genes had a role in early embryonic development.

Keywords

BlastocystBuffaloEmbryoOocyteParthenogenetic activation
Type
Research Article
Information
Zygote , Volume 29 , Issue 1 , February 2021 , pp. 49 - 58
Copyright
© The Author(s), 2020. Published by Cambridge University Press

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Footnotes

*

Present address: Director, ICAR-National Dairy Research Institute, Karnal, Haryana, India.

References

Adams, JM and Cory, S (1998). The Bcl-2 protein family: arbiters of cell survival. Science 281, 1322–6.10.1126/science.281.5381.1322CrossRefGoogle ScholarPubMed
Alberio, R, Zakhartchenko, V, Motlik, J and Wolf, E (2001). Mammalian oocyte activation: lessons from the sperm and implications for nuclear transfer. Int J Dev Biol 45, 797–809.Google ScholarPubMed
Balasubramanian, S, Son, WJ, Kumar, BM, Ock, SA, Yoo, JG, Im, GS, Choe, SY and Rho, GJ (2007). Expression pattern of oxygen and stress-responsive gene transcripts at various developmental stages of in vitro and in vivo preimplantation bovine embryos. Theriogenology 68, 265–75.10.1016/j.theriogenology.2007.05.044CrossRefGoogle ScholarPubMed
Brevini, TA, Cillo, F, Colleoni, S, Lazzari, G, Galli, C and Gandolfi, F (2004). Expression pattern of the maternal factor zygote arrest 1 (Zar1) in bovine tissues, oocytes, and embryos. Mol Reprod Dev 69, 375–80.10.1002/mrd.20140CrossRefGoogle ScholarPubMed
Brinster, RL (1965). Studies on the development of mouse embryos in vitro . J Reprod Fertil 10, 227–40.10.1530/jrf.0.0100227CrossRefGoogle ScholarPubMed
Cheek, TR, McGuinness, OM, Vincent, C, Moreton, RB, Berridge, MJ and Johnson, MH (1993). Fertilisation and thimerosal stimulate similar calcium spiking patterns in mouse oocytes but by separate mechanisms. Development 119, 179–89.Google ScholarPubMed
Christians, E, Davis, AA, Thomas, ST and Benjamin, IJ (2000). Maternal effect of Hsf1 on reproductive success. Nature 407, 693–94.10.1038/35037669CrossRefGoogle ScholarPubMed
De La Fuente, R and King, WA (1998). Developmental consequences of karyokinesis without cytokinesis during the first mitotic cell cycle of bovine parthenotes. Biol Reprod 58, 952–62.10.1095/biolreprod58.4.952CrossRefGoogle ScholarPubMed
Dong, J, Albertini, DF, Nishimori, K, Kumar, TR, Lu, N and Matzuk, MM (1996). Growth differentiation factor-9 is required early ovarian folliculogenesis. Nature 383, 531–5.10.1038/383531a0CrossRefGoogle ScholarPubMed
Donnison, M and Pfeffer, PL (2004). Isolation of genes associated with developmentally competent bovine oocytes and quantitation of their levels during development. Biol Reprod 71, 1813–21.10.1095/biolreprod.104.032367CrossRefGoogle ScholarPubMed
Elamaran, G, Singh, KP, Singh, MK, Singla, SK, Chauhan, MS, Manik, RS and Palta, P (2012). Oxygen concentration and cysteamine supplementation during in vitro production of buffalo (Bubalus bubalis) embryos affect mRNA expression of BCL-2, BCL-XL, MCL-1, BAX and BID . Reprod Domest Anim 47, 1027–36.10.1111/j.1439-0531.2012.02009.xCrossRefGoogle ScholarPubMed
Eunju, K, Guangming, W, Hong, M, Ying, L, Rebecca, TH, Masahito, T, Michelle, S, Don, PW, Hans, RS and Shoukhrat, M (2014). Nuclear reprogramming by interphase cytoplasm of two-cell mouse embryos. Nature 509, 101–4.Google Scholar
Fumei, C, Qiang, F, Liping, P, Zhen, H, Zhuangzhuang, X, Pengfei, Z, Tingxian, D, Chunying, P, Xianwei, L, Yangqing, L and Ming, Z (2020). Maternal transcription profiles at different stages for the development of early embryo in buffalo. Reprod Domest Anim 55, 503–14.Google Scholar
Galloway, SM, McNatty, KP, Cambridge, LM, Laitinen, MP, Juenge, JL, Jokiranta, TS, McLaren, RJ, Luiro, K, Dodds, KG, Montgomery, GW, Beattie, AE, Davis, GH and Ritvos, O (2000). Mutation in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat Genet 25, 279–83.10.1038/77033CrossRefGoogle Scholar
Gasparrini, B, Boccia, L, Rosa, AD, Palo, R D, Campanile, G and Zicarelli, L (2004). Chemical activation of buffalo (Bubalus bubalis) oocytes by different methods: effects of aging on post-parthenogenetic development. Theriogenology 62, 1627–37.10.1016/j.theriogenology.2004.03.005CrossRefGoogle ScholarPubMed
George, A, Shah, RA, Sharma, R, Palta, P, Singla, SK, Manik, RS and Chauhan, MS (2011). Activation of zona-free buffalo (Bubalus bubalis) oocytes by chemical or electrical stimulation, and subsequent parthenogenetic embryo development. Reprod Domest Anim 46, 444–7.10.1111/j.1439-0531.2010.01687.xCrossRefGoogle ScholarPubMed
Gilbert, AS, Mark, BH, Andrew, JW, Mayi, YAP, Karen, J and Mark, EW (1996). Regulation of early embryonic development by growth factors: growth factor gene expression in cloned bovine embryos. J Anim Sci 74, 50–7.Google Scholar
Gómez, E, Gutiérrez-Adán, A, Díez, C, Bermejo-Alvarez, P, Muñoz, M, Rodriguez, A, Otero, J, Alvarez-Viejo, M, Martín, D, Carrocera, S and Caamaño, JN (2009). Biological differences between in vitro produced bovine embryos and parthenotes. Reproduction 137, 285–95.10.1530/REP-08-0220CrossRefGoogle ScholarPubMed
Granot, I and Dekel, N (2002). The ovarian gap junction protein connexin43: regulation by gonadotropins. Trends Endrocrinol Metab 13, 310–13.10.1016/S1043-2760(02)00623-9CrossRefGoogle ScholarPubMed
Hogan, A, Heyner, S, Charron, MJ, Copeland, NG, Gilbert, DJ, Jenkins, NA, Thorens, B and Schultz, GA (1991). Glucose transporter gene expression in early mouse embryos. Development 113, 363–72.Google ScholarPubMed
Holm, P, Booth, PJ and Callesen, H (2003). Developmental kinetics of bovine nuclear transfer and parthenogenetic embryos. Cloning Stem Cells 5, 133–42.CrossRefGoogle ScholarPubMed
Kidder, GM and Mhawi, AA (2002). Gap junctions and ovarian folliculogenesis. Reproduction 123, 613–20.10.1530/rep.0.1230613CrossRefGoogle ScholarPubMed
Kline, D and Kline, JT (1992). Repetitive calcium transients and the role of calcium in exocytosis and cell cycle activation in the mouse egg. Dev Biol 149, 80–9.10.1016/0012-1606(92)90265-ICrossRefGoogle ScholarPubMed
Kumar, P, Verma, A, Kumar, M, De, S, Kumar, R and Datta, TK (2015). Expression pattern of glucose metabolism genes correlate with development rate of buffalo oocytes and embryos in vitro under low oxygen condition. J Assist Reprod Genet 32, 471–8.CrossRefGoogle ScholarPubMed
Larson, RC, Ignotz, GG and Currie, WB (1992). Transforming growth factor β and basic fibroblast growth factor synergistically promote early bovine embryo development during the fourth cell cycle. Mol Reprod Dev 33, 432–5.10.1002/mrd.1080330409CrossRefGoogle ScholarPubMed
Loi, P, Ledda, S, Fulka, J, Cappai, P and Moor, RM (1998). Development of parthenogenetic and cloned ovine embryos: effect of activation protocols. Biol Reprod 58, 1177–87.10.1095/biolreprod58.5.1177CrossRefGoogle ScholarPubMed
McGrath, SA, Aurora, F, Esquela, and Lee, SJ (1995). Oocyte-specific expression of growth differentiation factor-9. Mol Endocrinol 9, 131–6.Google ScholarPubMed
Metchat, A, Malin, Å, Christiane, B, Virginie, D, Lea, S, Henri, A and Elisabeth, SC (2009). Mammalian heat shock factor1 is essential for oocyte meiosis and directly regulates Hsp90 expression. J Biol Chem 284, 9521–8.10.1074/jbc.M808819200CrossRefGoogle Scholar
Mishra, V, Misra, AK and Sharma, R (2008). A comparative study of parthenogenic activation and in vitro fertilization of bubaline oocytes. Anim Reprod Sci 103, 249–59.10.1016/j.anireprosci.2006.12.019CrossRefGoogle ScholarPubMed
Mohapatra, SK, Sandhu, A, Singh, KP, Singla, SK, Chauhan, MS, Manik, RS 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, e0129235.10.1371/journal.pone.0129235CrossRefGoogle Scholar
Mohapatra, SK, Sandhu, A, Neerukattu, VS, Singh, KP, Selokar, NL, Singla, SK, Chauhan, MS, Manik, RS and Palta, P (2015b). Buffalo embryos produced by hand-made 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. Cell Reprogram 17, 141–50.10.1089/cell.2014.0077CrossRefGoogle Scholar
Murlidharan, K, Eswari, S and Vijayarani, K (2015). Expression profile of growth differentiation factor 9 (GDF9) and bone morphogenetic protein 15 (BMP15) genes in buffalo oocytes. Anim Sci Rep 9, 10–15.Google Scholar
Nandedkar, P, Chohan, P, Patwardhan, A, Gaikwad, S, Bhartiya, D (2009). Parthenogenesis and somatic cell nuclear transfer in sheep oocytes using PolScope. Ind J Exp Biol 47, 550–8.Google ScholarPubMed
Nath, A, Sharma, V, Dubey, PK, Pratheesh, MD, Gade, NE, Saikumar, G and Sharma, GT (2013). Impact of gonadotropin supplementation on the expression of germ cell marker genes (MATER, ZAR1, GDF9 and BMP15) during in vitro maturation of buffalo (Bubalus bubalis) oocyte. In Vitro Cell Dev Biol Anim 49, 34–41.10.1007/s11626-012-9561-5CrossRefGoogle ScholarPubMed
Nemcova, L, Machatkova, M, Hanzalova, K, Horakova, J and Kanka, J (2006). Gene expression in bovine embryos derived from oocytes with different developmental competence collected at the defined follicular developmental stage. Theriogenology 65, 1254–64.10.1016/j.theriogenology.2005.08.006CrossRefGoogle ScholarPubMed
Nilsson, E, Parrott, JA and Skinner, MK (2001). Basic fibroblast growth factor induces primordial Follicle development and initiates folliculogenesis. Mol Cell Endocrinol 175, 123–30.10.1016/S0303-7207(01)00391-4CrossRefGoogle ScholarPubMed
Nishi, M, Kumar, NM and Gilula, NB (1991). Developmental regulation of gap junction gene expression during mouse embryonic development. Dev Biol 146, 117–30CrossRefGoogle ScholarPubMed
Pantaleon, M, Ryan, JP, Gil, M and Kaye, P (2001). An unusual subcellular localization of GLUT1 and link with metabolism in oocytes and preimplantation mouse embryos. Biol Reprod 64, 1247–54.10.1095/biolreprod64.4.1247CrossRefGoogle ScholarPubMed
Ross, PJ, Beyhan, Z, Lager, AE, Yoo, SY, Malcuit, C, Schellander, K, Fissore, RA and Cibelli, JB (2008). Parthenogenetic activation of bovine oocytes using bovine and murine phospholipase C zeta. BMC Dev Biol 19, 8–16.Google Scholar
Sadeesh, EM, Meena, K, Balhara, S and Yadav, PS (2014). Expression profile of developmentally important genes between hand-made cloned buffalo embryos produced from reprogramming of donor cell with oocytes extract and selection of recipients to blast through brilliant cresyl blue staining and in vitro fertilized embryos. J Assist Reprod Genet 31, 1541–52.Google Scholar
Saikhun, J, Kitiyanant, N, Songtaveesin, C, Pavasuthipaisit, K and Kitiyanant, Y (2004). Development of swamp buffalo (Bubalus bubalis) embryos after parthenogenetic activation and nuclear transfer using serum fed or starved fetal fibroblasts. Reprod Nutr Dev 44, 65–78.10.1051/rnd:2004017CrossRefGoogle ScholarPubMed
Shah, RA, George, A, Singh, MK, Kumar, D, Chauhan, MS, Manik, R, Palta, P and Singla, SK (2008). Hand-made cloned buffalo (Bubalus bubalis) embryos: comparison of different media and culture systems. Cloning Stem Cells 10, 435–42.10.1089/clo.2008.0033CrossRefGoogle ScholarPubMed
Shi, D, Lu, F, Wei, Y, Cui, K, Yang, S, Wei, J and Liu, Q (2007). Buffalos (Bubalus bubalis) cloned by nuclear transfer of somatic cells. Biol Reprod 77, 285–91.10.1095/biolreprod.107.060210CrossRefGoogle ScholarPubMed
Singh, KP, Kaushik, R, Garg, V, Sharma, R, George, A, Singh, MK, Manik, RS, Palta, P, Singla, SK and Chauhan, MS (2012). Expression pattern of pluripotent markers in different embryonic developmental stages of buffalo (Bubalus bubalis) embryos and putative embryonic stem cells generated by parthenogenetic activation. Cell Reprogram 14, 530–8.CrossRefGoogle ScholarPubMed
Singh, KP, Kaushik, R, Mohapatra, SK, Garg, V, Ameshbabu, KR, Singh, MK, Palta, P, Manik, RS, Singla, SK and Chauhan, MS (2014). Quantitative expression of pluripotency-related genes in parthenogenetically produced buffalo (Bubalus bubalis) embryos and in putative embryonic stem cells derived from them. Gene Exp Patterns 16, 23–30.10.1016/j.gep.2014.06.004CrossRefGoogle Scholar
Swann, K (1991). Thimerosal causes calcium oscillations and sensitizes calcium induced calcium release in unfertilized hamster eggs. FEBS Lett 278, 175–8.10.1016/0014-5793(91)80110-OCrossRefGoogle ScholarPubMed
Swann, K and Ozil, JP (1994). Dynamics of the calcium signal that triggers mammalian egg activation. Int Rev Cytol 152, 183–222.CrossRefGoogle ScholarPubMed
Telford, NA, Watson, AJ and Schultz, GA (1990). Transition of maternal to embryonic control in early mammalian development: a comparison of several species. Mol Reprod Dev 26, 90–100.10.1002/mrd.1080260113CrossRefGoogle ScholarPubMed
Thouas, GA, Korfiatis, NA, French, AJ, Jones, GM and Trounson, AO (2001). Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts. Reprod Biomed Online 3, 25–9.10.1016/S1472-6483(10)61960-8CrossRefGoogle ScholarPubMed
Uzbekova, S, Roy-Sabau, M, Dalbiès-Tran, R, Perreau, C, Pappillier, P, Mompart, F, Thelie, A, Pennetier, S, Cognie, J, Cadoret, V, Royere, D, Monget, P and Mermillod, P (2006). Zygote arrest 1 gene in pig, cattle and human: evidence of different transcript variants in male and female germ cells. Reprod Biol Endocrinol 4, 12.10.1186/1477-7827-4-12CrossRefGoogle ScholarPubMed
Wrenzycki, C, Herrmann, D, Carnwath, JW and Niemann, H (1996). Expression of the gap junction gene connex in 43 (Cx43) in preimplantation bovine embryos derived in vitro or in vivo . J Reprod Fertil 108, 17–24.10.1530/jrf.0.1080017CrossRefGoogle ScholarPubMed
Wrenzycki, C, Herrmann, D, Carnwath, JW and Niemann, H (1998). Expression of RNA from developmentally important genes in preimplantation bovine embryos produced in TCM supplemented with BSA. J Reprod Fertil 112, 387–98.10.1530/jrf.0.1120387CrossRefGoogle ScholarPubMed
Wu, B, Ignotz, G, Currie, B and Yang, X (1997). Dynamics of maturation-promoting factor and its constituent proteins during in vitro maturation of bovine oocytes. Biol Reprod 56, 253–9.10.1095/biolreprod56.1.253CrossRefGoogle ScholarPubMed
Wu, X, Viveiros, MM, Eppig, JJ, Bai, Y, Fitzpatrick, S and Matzuk, MM (2003). Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat Genet 33, 187–91.10.1038/ng1079CrossRefGoogle ScholarPubMed
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