Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-26T02:12:43.311Z Has data issue: false hasContentIssue false
  • English
  • Français

Relative abundance of pluripotency-associated candidate genes in immature oocytes and in vitro-produced buffalo embryos (Bubalus bubalis)

Published online by Cambridge University Press:  05 April 2021

Satish Kumar Open the ORCID record for Satish Kumar [Opens in a new window]  and
Manmohan Singh Chauhan
Satish Kumar*
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal132001, Haryana, India
Manmohan Singh Chauhan
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal132001, Haryana, India
*
Author for correspondence: Satish Kumar, Animal Biotechnology Centre, National Dairy Research Institute, Karnal132001, Haryana, India. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The present study was undertaken to analyze the relative abundance (RA) of pluripotency-associated genes (NANOG, OCT4, SOX2, c-MYC, and FOXD3) in different grades of immature oocytes and various stages of in vitro-produced buffalo embryos using RT-qPCR. Results showed that the RA of NANOG, OCT4, and FOXD3 transcripts was significantly higher (P < 0.05) in A grade oocytes compared with the other grades of oocytes. The RA of the c-MYC transcript was significantly higher (P < 0.05) in A grade compared with the C and D grades of oocytes, but the values did not differ significantly from the B grade of oocytes. The RA of the SOX2 transcript was almost similar in all grades of the oocytes. The expression levels of NANOG (P > 0.05), OCT4 (P > 0.05), c-MYC (P > 0.05) and SOX2 (P < 0.05) were higher in the blastocysts compared with the other stages of the embryos. Markedly, FOXD3 expression was significantly higher (P < 0.05) in 8–16-cell embryos compared with the 2-cell and 4-cell embryos and blastocyst, but did not differ significantly from the morula stage of the embryos. In the study, the majority of pluripotency-associated genes showed higher expression in A grade immature oocytes. Therefore, it is concluded that the A grade oocytes appeared to be more developmental competent and are suitable candidates for nuclear cloning research in buffalo. In buffalo, NANOG, OCT4, SOX2, and c-MYC are highly expressed in blastocysts compared with the other stages of embryos.

Keywords

BuffaloEmbryosGene expressionOocytesPluripotency genes
Type
Research Article
Information
Zygote , Volume 29 , Issue 6 , December 2021 , pp. 459 - 467
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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

Bebbere, D, Bogliolo, L, Ariu, F, Fois, S, Leoni, GG, Succu, S, Berlinguer, F and Ledda, S (2010). Different temporal gene expression patterns for ovine preimplantation embryos produced by parthenogenesis or in vitro fertilization. Theriogenology 74, 712–23.CrossRefGoogle ScholarPubMed
Brevini, TA, Lonergan, P, Cillo, F, Francisci, C, Favetta, LA, Fair, T and Gandolfi, F (2002). Evolution of mRNA polyadenylation between oocyte maturation and first embryonic cleavage in cattle and its relation with developmental competence. Mol Reprod Dev 63, 510–7.CrossRefGoogle ScholarPubMed
Brevini, TAL, Cillo, F, Antonini, S and Gandolfi, F (2005). Expression pattern of NANOG gene in porcine tissue and parthenogenetic embryos. Reprod Dom Anim 40, 384.Google Scholar
Brevini-Gandolfi, TA, Favetta, LA, Mauri, L, Luciano, AM, Cillo, F and Gandolfi, F (1999). Changes in poly(A) tail length of maternal transcripts during in vitro maturation of bovine oocytes and their relation with developmental competence. Mol Reprod Dev 52, 427–33.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
Chauhan, MS, Singla, SK, Palta, P, Manik, RS and Madan, ML (1998). In vitro maturation and fertilization, and subsequent development of buffalo (Bubalus bubalis) embryos: effects of oocyte quality and type of serum. Reprod Fert Dev 10, 173–7.CrossRefGoogle ScholarPubMed
Coussens, PM and Nobis, W (2002). Bioinformatics and high throughput approach to create genomic resources for the study of bovine immunobiology. Vet Immunol Immunopathol 86(3–4), 229–44.CrossRefGoogle Scholar
Cui, XS, Xu, YN, Shen, XH, Zhang, LQ, Zhang, JB and Kim, NH (2011). Trichostatin A modulates apoptotic-related gene expression and improves embryo viability in cloned bovine embryos. Cell Reprogram 13, 179–89.CrossRefGoogle ScholarPubMed
Deng, Y, Liu, Q, Luo, C, Chen, S, Li, X, Wang, C, Liu, Z, Lei, X, Zhang, H, Sun, H, Lu, F, Jiang, J and Shi, D (2012). Generation of induced pluripotent stem cells from buffalo (Bubalus bubalis) fetal fibroblasts with buffalo defined factors. Stem Cell Dev 21, 2485–94.CrossRefGoogle ScholarPubMed
du Puy, L, Lopes, SM, Haagsman, HP and Roelen, BA (2011). Analysis of coexpression of OCT4, NANOG and SOX2 in pluripotent cells of the porcine embryo, in vivo and in vitro . Theriogenology 75, 513–26.CrossRefGoogle Scholar
Gendelman, M and Roth, Z (2012). In vivo vs. in vitro models for studying the effects of elevated temperature on the GV-stage oocyte, subsequent developmental competence and gene expression. Anim Reprod Sci 134(3–4), 125–34.CrossRefGoogle ScholarPubMed
Graf, A, Krebs, S, Heininen-Brown, M, Zakhartchenko, V, Blum, H and Wolf, E (2014). Genome activation in bovine embryos: review of the literature and new insights from RNA sequencing experiments. Anim Reprod Sci 149(1–2), 46–58.CrossRefGoogle ScholarPubMed
Gu, Q, Hao, J, Hai, T, Wang, J, Jia, Y, Kong, Q, Wang, J, Feng, C, Xue, B, Xie, B, Liu, S, Li, J, He, Y, Sun, J, Liu, L, Wang, L, Liu, Z and Zhou, Q (2014). Efficient generation of mouse ESCs-like pig induced pluripotent stem cells. Protein Cell 5, 338–42.CrossRefGoogle ScholarPubMed
Hanna, LA, Foreman, RK, Tarasenko, IA, Kessler, DS and Labosky, PA (2002). Requirement for Foxd3 in maintaining pluripotent cells of the early mouse embryo. Genes Dev 16, 2650–61.CrossRefGoogle ScholarPubMed
He, S, Pant, D, Schiffmacher, A, Bischoff, S, Melican, D, Gavin, W and Keefer, CL (2006). Developmental expression of pluripotency determining factors in caprine embryos: novel pattern of Nanog protein localization in the nucleolus. Mol Reprod Dev 73, 1512–22.CrossRefGoogle ScholarPubMed
Herrmann, D, Dahl, JA, Lucas-Hahn, A, Collas, P and Niemann, H (2013). Histone modifications and mRNA expression in the inner cell mass and trophectoderm of bovine blastocysts. Epigenetics 8, 281–9.CrossRefGoogle ScholarPubMed
HosseinNia, P, Hajian, M, Jafarpour, F, Hosseini, SM, Tahmoorespur, M and Nasr-Esfahani, MH (2019). Dynamics of the expression of pluripotency and lineage specific genes in the pre and peri-implantation goat embryo. Cell J 21, 194–203.Google ScholarPubMed
Kirchhof, N, Carnath, JW, Lemme, E, Anastassiadis, K, Scholar, H and Neimann, H (2000). Expression pattern of Oct-4 in preimplantation embryo of different species. Biol Reprod 63, 1698–705.CrossRefGoogle ScholarPubMed
Kumar, D, Anand, T, Vijayalakshmy, K, Sharma, P, Rajendran, R, Selokar, NL, Yadav, PS and Kumar, D (2019). Transposon mediated reprogramming of buffalo fetal fibroblasts to induced pluripotent stem cells in feeder free culture conditions. Res Vet Sci 123, 252–60.CrossRefGoogle ScholarPubMed
Kumar, S (2012). Cloning and expression analysis of Nanog in putative buffalo embryonic stem cells. PhD thesis submitted to NDRI Karnal, Haryana, India.Google Scholar
Knoepfler, PS (2007). Myc goes global: new tricks for an old oncogene. Cancer Res 67, 5061–3.CrossRefGoogle ScholarPubMed
Koh, S and Piedrahita, JA (2014). From “ES-like” cells to induced pluripotent stem cells: a historical perspective in domestic animals. Theriogenology 81, 103–11.CrossRefGoogle ScholarPubMed
Kurosaka, S, Eckardt, S and McLaughlin, KJ (2004). Pluripotent lineage definition in bovine embryos by Oct4 transcript localization. Biol Reprod 71, 1578–82.CrossRefGoogle ScholarPubMed
Li, L, Sun, L, Gao, F, Jiang, J, Yang, Y, Li, C, Gu, J, Wei, Z, Yang, A, Lu, R, Ma, Y, Tang, F, Kwon, SW, Zhao, Y, Li, J and Jin, Y (2010). Stk40 links the pluripotency factor Oct4 to the Erk/MAPK pathway and controls extraembryonic endoderm differentiation. Proc Natl Acad Sci USA 107, 1402–7.CrossRefGoogle ScholarPubMed
Li, Y, Cang, M, Lee, AS, Zhang, K and Liu, D (2011). Reprogramming of sheep fibroblasts into pluripotency under a drug-inducible expression of mouse-derived defined factors. PLoS One 6, e15947.CrossRefGoogle Scholar
Livak, KJ and Schmittgen, TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2–DDCT method. Methods 25, 402–8.CrossRefGoogle Scholar
Madan, ML, Das, SK and Palta, P (1996). Application of reproductive technology to buffalo. Anim Reprod Sci 42, 299–306.CrossRefGoogle Scholar
Madeja, ZE, Sosnowski, J, Hryniewicz, K, Warzych, E, Pawlak, P, Rozwadowska, N, Plusa, B and Lechniak, D (2013). Changes in sub-cellular localisation of trophoblast and inner cell mass specific transcription factors during bovine preimplantation development. BMC Dev Biol 13, 32.CrossRefGoogle ScholarPubMed
Magnani, L and Cabot, RA (2008). In vitro and in vivo derived porcine embryos possess similar, but not identical, patterns of Oct4, Nanog, and Sox2 mRNA expression during cleavage development. Mol Reprod Dev 75, 1726–35.CrossRefGoogle Scholar
Mahesh, YU, Gibence, HR, Shivaji, S and Rao, BS (2017). Effect of different cryo-devices on in vitro maturation and development of vitrified-warmed immature buffalo oocytes. Cryobiology 75, 106–16.CrossRefGoogle ScholarPubMed
Niemann, H and Wrenzycki, C (2000). Alterations of expression of developmentally important genes in pre-implantation bovine embryos by in vitro culture conditions: implications for subsequent development. Theriogenology 53, 21–34.CrossRefGoogle Scholar
Ozawa, M, Sakatani, M, Yao, J, Shanker, S, Yu, F, Yamashita, R, Wakabayashi, S, Nakai, K, Dobbs, KB, Sudano, MJ, Farmerie, WG and Hansen, PJ (2012). Global gene expression of the inner cell mass and trophectoderm of the bovine blastocyst. BMC Dev Biol 12, 33.CrossRefGoogle ScholarPubMed
Pant, D and Keefer, CL (2009). Expression of pluripotency-related genes during bovine inner cell mass explant culture. Cloning Stem Cells 11, 355–65.CrossRefGoogle ScholarPubMed
Pesce, M, Gross, MK and Scholer, HR (1998). In line with our ancestors: Oct-4 and the mammalian germ. Bio-essays 20, 722–32.Google ScholarPubMed
Plank, JL, Suflita, MT, Galindo, CL and Labosky, PA (2014) Transcriptional targets of Foxd3 in murine ES cells. Stem Cell Res 12, 233–40.CrossRefGoogle ScholarPubMed
Pessôa, LVF, Bressan, FF and Freude, KK (2019). Induced pluripotent stem cells throughout the animal kingdom: availability and applications. World J Stem Cells 11, 491–505.CrossRefGoogle ScholarPubMed
Rodríguez-Alvarez, L, Cox, J, Navarrete, F, Valdés, C, Zamorano, T, Einspanier, R and Castro, FO (2009). Elongation and gene expression in bovine cloned embryos transferred to temporary recipients. Zygote 17, 353–65.CrossRefGoogle ScholarPubMed
Rodríguez-Alvarez, L, Cox, J, Tovar, H, Einspanier, R and Castro, FO (2010). Changes in the expression of pluripotency-associated genes during preimplantation and periimplantation stages in bovine cloned and in vitro produced embryos. Zygote 18, 269–79.CrossRefGoogle Scholar
Sadeesh, EM, Sikka, P, Balhara, AK and Balhara, S (2016). Developmental competence and expression profile of genes in buffalo (Bubalus bubalis) oocytes and embryos collected under different environmental stress. Cytotechnology 68, 2271–85.CrossRefGoogle ScholarPubMed
Sanna, D, Sanna, A, Mara, L, Pilichi, S, Mastinu, A, Chessa, F, Pani, L and Dattena, M (2009). Oct4 expression in in-vitro-produced sheep blastocysts and embryonic stem-like cells. Cell Biol Internat 34, 53–60.Google ScholarPubMed
Shah, SM, Saini, N, Ashraf, S, Singh, MK, Manik, R, Singla, SK, Palta, P and Chauhan, MS (2015). Development of buffalo (Bubalus bubalis) embryonic stem cell lines from somatic cell nuclear transferred blastocysts. Stem Cell Res 15, 633–9.CrossRefGoogle ScholarPubMed
Shahid, B, Jalalib, S, Khanc, MI, and Shamid, SA (2014). Different methods of oocytes recovery for in vitro maturation in Nili Ravi buffalo’s oocytes. APCBEE Procedia 8, 359–63.CrossRefGoogle Scholar
Silva, PGC, Moura, MT, Silva, RLO, Nascimento, PS, Silva, JB, Ferreira-Silva, JC, Cantanhede, LF, Chaves, MS, Benko-Iseppon, AM and Oliveira, MA (2018). Temporal expression of pluripotency-associated transcription factors in sheep and cattle preimplantation embryos. Zygote 26, 270–8.CrossRefGoogle ScholarPubMed
Singh, KP, Kaushik, R, Mohapatra, SK, Garg, V, Rameshbabu, K, 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 Expr Patterns 16, 23–30.CrossRefGoogle Scholar
Stuart, HT, van Oosten, AL, Radzisheuskaya, A, Martello, G, Miller, A, Dietmann, S, Nichols, J and Silva, JC (2014). NANOG amplifies STAT3 activation and they synergistically induce the naive pluripotent program. Curr Biol 24, 340–6.CrossRefGoogle ScholarPubMed
Sumer, H, Liu, J, Malaver-Ortega, LF, Lim, ML, Khodadadi, K and Verma, PJ (2011). NANOG is a key factor for induction of pluripotency in bovine adult fibroblasts. J Anim Sci 89, 2708–16.CrossRefGoogle ScholarPubMed
Suzuki, T, Abe, K, Inoue, A and Aoki, F (2009). Expression of c-MYC in nuclear speckles during mouse oocyte growth and preimplantation development. J Reprod Dev 55, 491–5.CrossRefGoogle ScholarPubMed
Takahashi, K and Yamanaka, S (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663–76.CrossRefGoogle ScholarPubMed
Takahashi, K, Tenabe, K, Ohnuki, M, Narita, M, Ichisaka, T, Tomoda, K and Yamanaka, S (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861–72.CrossRefGoogle ScholarPubMed
Tan, G, Ren, L, Huang, Y, Tang, X, Zhou, Y, Zhou, Y, Li, D, Song, H, Ouyang, H and Pang, D (2011). Isolation and culture of embryonic stem-like cells from pig nuclear transfer blastocysts of different days. Zygote 18, 1–6.Google Scholar
Titens, F, Kliem, A, Tscheudschilsuren, G, Navarrete Santos, A and Fischer, B (2000). Expression of proto-oncogenes in bovine preimplantation blastocysts. Anat Embryol (Berl) 201, 349–55.CrossRefGoogle Scholar
Vejlsted, M, Offenberg, H, Thorup, F and Maddox-Hyttel, P (2006). Confinement and clearance of Oct4 in the porcine embryo at stereo microscopically defined stages around gastrulation. Mol Reprod Dev 73, 709–18.CrossRefGoogle Scholar
Velásquez, AE, Veraguas, D, Cabezas, J, Manríquez, J, Castro, FO and Rodríguez-Alvarez, LL (2019). The expression level of Sox2 at the blastocyst stage regulates the developmental capacity of bovine embryos up to day-13 of in vitro culture. Zygote 27, 398–404.CrossRefGoogle Scholar
Wang, K, Beyhan, Z, Rodriguez, RM, Ross, PJ, Iager, AE, Kaiser, GG, Chen, Y and Cibelli, JB (2009). Bovine ooplasm partially remodels primate somatic nuclei following somatic cell nuclear transfer. Cloning Stem Cells 11, 187–202.CrossRefGoogle ScholarPubMed
Watson, AJ, Natale, DR and Barcroft, LC (2004). Molecular regulation of blastocyst formation. Anim Reprod Sci 82–83, 583–92.CrossRefGoogle ScholarPubMed
Wei, Q, Zhong, L, Mu, H, Xiang, J, Yue, L, Dai, Y and Han, J (2017). Bovine lineage specification revealed by single cell gene expression analysis from zygote to blastocyst. Biol Reprod 97, 5–17.CrossRefGoogle Scholar
Welstead, GG, Schorderet, P and Boyer, LA (2008). The reprogramming language of pluripotency. Curr Opin Genet Dev 18, 1–7.CrossRefGoogle ScholarPubMed
West, FD, Terlouw, SL, Kwon, DJ, Mumaw, JL, Dhara, SK, Hasneen, K, Dobrinsky, JR and Stice, SL (2010). Porcine induced pluripotent stem cells produce chimeric offspring. Stem Cells Dev 19, 1211–20.CrossRefGoogle ScholarPubMed
Wrenzycki, C, Herrmann, D, Keskintepe, L, Martins, A Jr, Sirisathien, S, Brackett, B and Niemann, H (2001). Effects of culture system and protein supplementation on mRNA expression in pre-implantation bovine embryos. Hum Reprod 16, 893–901.CrossRefGoogle ScholarPubMed
Wrenzycki, C, Herrmann, D, Lucas-Hahn, A, Lemme, E, Korsawe, K and Niemann, H (2004). Gene expression patterns in in vitro-produced and somatic nuclear transfer derived pre-implantation bovine embryos: relationship to the large offspring syndrome. Anim Reprod Sci 82–83, 593–603.CrossRefGoogle Scholar
Wrenzycki, C, Herrmann, D and Niemann, H (2007). Messenger RNA in oocytes and embryos in relation to embryo viability. Theriogenology 68, S77–83.CrossRefGoogle ScholarPubMed
Yadav, PS, Kues, WA, Herrmann, D, Carnath, JW and Niemann, H (2005). Bovine ICM derived cells express the Oct4 ortholog. Mol Reprod Dev 72, 182–90.CrossRefGoogle ScholarPubMed
Zhao, H and Jin, Y (2017). Signaling networks in the control of pluripotency. Curr Opin Genet Dev 46, 141–8.CrossRefGoogle ScholarPubMed
Zhao, L, Wang, Z, Zhang, J, Yang, J, Gao, X, Wu, B, Zhao, G, Bao, S, Hu, S, Liu, P and Li, X (2017). Characterization of the single-cell derived bovine induced pluripotent stem cells. Tissue Cell 49, 521–7.CrossRefGoogle ScholarPubMed
Zhu, L, Zhang, S and Jin, Y (2014). Foxd3 suppresses NFAT-mediated differentiation to maintain self-renewal of embryonic stem cells. EMBO Rep 15, 1286–96.CrossRefGoogle ScholarPubMed