Hostname: page-component-8448b6f56d-dnltx Total loading time: 0 Render date: 2024-04-23T19:45:18.729Z Has data issue: false hasContentIssue false
  • English
  • Français

Histone Demethylase KDM4D Could Improve the Developmental Competence of Buffalo (Bubalus Bubalis) Somatic Cell Nuclear Transfer (SCNT) Embryos

Published online by Cambridge University Press:  22 January 2021

Yun Feng ,
Xin Zhao ,
Zhengda Li ,
Chan Luo ,
Ziyun Ruan ,
Jie Xu ,
Penglei Shen ,
Yanfei Deng ,
Jianrong Jiang  and
Deshun Shi
...Show all authors
Yun Feng
Affiliation:
Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning530005, P.R. China
Xin Zhao
Affiliation:
Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning530005, P.R. China Center of Reproductive Medicine, Guangxi Maternal and Child Health Hospital, Nanning530003, P.R. China
Zhengda Li
Affiliation:
Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning530005, P.R. China
Chan Luo
Affiliation:
Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning530005, P.R. China
Ziyun Ruan
Affiliation:
Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning530005, P.R. China
Jie Xu
Affiliation:
Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning530005, P.R. China
Penglei Shen
Affiliation:
Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning530005, P.R. China
Yanfei Deng
Affiliation:
Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning530005, P.R. China
Jianrong Jiang
Affiliation:
Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning530005, P.R. China
Deshun Shi*
Affiliation:
Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning530005, P.R. China
Fenghua Lu*
Affiliation:
Animal Reproduction Institute, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning530005, P.R. China
*
*Author for correspondence: Fenghua Lu and Deshun Shi, E-mail: lfhgggg@163.com (F. Lu) and ardsshi@gxu.edu.cn (D. Shi)
*Author for correspondence: Fenghua Lu and Deshun Shi, E-mail: lfhgggg@163.com (F. Lu) and ardsshi@gxu.edu.cn (D. Shi)
Get access

Abstract

Somatic cell nuclear transfer (SCNT) holds vast potential in agriculture. However, its applications are still limited by its low efficiency. Histone 3 lysine 9 trimethylation (H3K9me3) was identified as an epigenetic barrier for this. Histone demethylase KDM4D could regulate the level of H3K9me3. However, its effects on buffalo SCNT embryos are still unclear. Thus, we performed this study to explore the effects and underlying mechanism of KDM4D on buffalo SCNT embryos. The results revealed that compared with the IVF embryos, the expression level of KDM4D in SCNT embryos was significantly lower at 8- and 16-cell stage, while the level of H3K9me3 in SCNT embryos was significantly higher at 2-cell, 8-cell, and blastocyst stage. Microinjection of KDM4D mRNA could promote the developmental ability of buffalo SCNT embryos. Furthermore, the expression level of ZGA-related genes such as ZSCAN5B, SNAI1, eIF-3a, and TRC at the 8-cell stage was significantly increased. Meanwhile, the pluripotency-related genes like POU5F1, SOX2, and NANOG were also significantly promoted at the blastocyst stage. The results were reversed after KDM4D was inhibited. Altogether, these results revealed that KDM4D could correct the H3K9me3 level, increase the expression level of ZGA and pluripotency-related genes, and finally, promote the developmental competence of buffalo SCNT embryos.

Keywords

buffalohistone demethylationKDM4Dsomatic cell nuclear transfer (SCNT)
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 27 , Issue 2 , April 2021 , pp. 409 - 419
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of the Microscopy Society of America

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.)

Footnotes

†

Yun Feng and Xin Zhao contributed equally to this work.

References

Agrawal, H, Selokar, NL, Saini, M, Singh, MK, Chauhan, MS, Palta, P, Singla, SK & Manik, RS (2018). m-carboxycinnamic acid bishydroxamide improves developmental competence, reduces apoptosis and alters epigenetic status and gene expression pattern in cloned buffalo (Bubalus bubalis) embryos. Reprod Domest Anim 53(4), 986–996.CrossRefGoogle ScholarPubMed
Aston, KI, Li, GP, Hicks, BA, Sessions, BR, Davis, AP, Rickords, LF, Stevens, JR & White, KL (2010). Abnormal levels of transcript abundance of developmentally important genes in various stages of preimplantation bovine somatic cell nuclear transfer embryos. Cell Reprogram 12(1), 23–32.CrossRefGoogle ScholarPubMed
Bai, G, Song, S, Zhang, Y, Huang, X, Huang, X, Sun, R & Lei, L (2017). Kdm6a overexpression improves the development of cloned mouse embryos. Zygote 26(1), 24–32.CrossRefGoogle ScholarPubMed
Becker, JS, Nicetto, D & Zaret, KS (2016). H3K9me3-Dependent heterochromatin: Barrier to cell fate changes. Trends Genet 32(1), 29–41.CrossRefGoogle ScholarPubMed
Campolo, F, Gori, M, Favaro, R, Nicolis, SK, Pellegrini, M, Botti, F, Rossi, P, Jannini, EA & Dolci, S (2013). Essential role of Sox2 for the establishment and maintenance of the germ cell line. Stem Cells 31(7), 1408–1421.CrossRefGoogle ScholarPubMed
Cao, Z, Li, Y, Chen, Z, Wang, H, Zhang, M, Zhou, N, Wu, R, Ling, Y, Fang, F, Li, N & Zhang, Y (2015). Genome-wide dynamic profiling of histone methylation during nuclear transfer-mediated porcine somatic cell reprogramming. PLoS ONE 10(12), e0144897.CrossRefGoogle ScholarPubMed
Chen, J, Liu, H, Liu, J, Qi, J, Wei, B, Yang, J, Liang, H, Chen, Y, Chen, J & Wu, Y (2013). H3k9 methylation is a barrier during somatic cell reprogramming into iPSCs. Nat Genet 45(1), 34–42.CrossRefGoogle ScholarPubMed
Chung, YG, Matoba, S, Liu, Y, Eum, JH, Lu, F, Jiang, W, Lee, JE, Sepilian, V, Cha, KY & Lee, DR (2015). Histone demethylase expression enhances human somatic cell nuclear transfer efficiency and promotes derivation of pluripotent stem cells. Cell Stem Cell 17(6), 758–766.CrossRefGoogle ScholarPubMed
Cloos, PAC, Christensen, J, Agger, K & Helin, K (2008). Erasing the methyl mark: Histone demethylases at the center of cellular differentiation and disease. Genes Dev 22(9), 1115–1140.CrossRefGoogle Scholar
Cui, XS, Xu, YN, Shen, XH, Zhang, LQ, Zhang, JB & Kim, NH (2011). Trichostatin A modulates apoptotic-related gene expression and improves embryo viability in cloned bovine embryos. Cell Reprogram 13(2), 179–189.CrossRefGoogle ScholarPubMed
Davis, JE, Insigne, KD, Jones, EM, Hastings, QA, Boldridge, WC & Kosuri, S (2020). Dissection of c-AMP response element architecture by using genomic and episomal massively parallel reporter assays. Cell Syst 11(1), 75–85.e7.CrossRefGoogle ScholarPubMed
Em, S, Shah, F, Kataria, M & Yadav, PS (2016). A comparative study on expression profile of developmentally important genes during pre-implantation stages in buffalo hand-made cloned embryos derived from adult fibroblasts and amniotic fluid derived stem cells. Cytotechnology 68(4), 1447–1461.CrossRefGoogle ScholarPubMed
Fukuda, A, Tomikawa, J, Miura, T, Hata, K, Nakabayashi, K, Eggan, K, Akutsu, H & Umezawa, A (2014). The role of maternal-specific H3K9me3 modification in establishing imprinted X-chromosome inactivation and embryogenesis in mice. Nat Commun 5(1), 5464–5464.CrossRefGoogle ScholarPubMed
George, A, Shah, RA, Sharma, R, Palta, P, Singla, SK, Manik, RS & 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(3), 444–447.CrossRefGoogle ScholarPubMed
Glanzner, WG, Gutierrez, K, Rissi, VB, de Macedo, MP, Lopez, R, Currin, L, Dicks, N, Baldassarre, H, Agellon, LB & Bordignon, V (2020). Histone lysine demethylases KDM5B and KDM5C modulate genome activation and stability in porcine embryos. Front Cell Dev Biol 8, 151.CrossRefGoogle ScholarPubMed
Gupta, MK, Heo, YT, Kim, DK, Lee, HT & Uhm, SJ (2019). 5-Azacytidine improves the meiotic maturation and subsequent in vitro development of pig oocytes. Anim Reprod Sci 208, 106118.CrossRefGoogle ScholarPubMed
Hiendleder, S, Zakhartchenko, V, Wenigerkind, H, Reichenbach, H, Brüggerhoff, K, Prelle, K, Brem, G, Stojkovic, M & Wolf, E (2003). Heteroplasmy in bovine fetuses produced by intra- and inter-subspecific somatic cell nuclear transfer: Neutral segregation of nuclear donor mitochondrial DNA in various tissues and evidence for recipient cow mitochondria in fetal blood. Biol Reprod 68(1), 159–166.CrossRefGoogle ScholarPubMed
Hillringhaus, L, Yue, WW, Rose, NR, Ng, SS, Gileadi, C, Loenarz, C, Bello, SH, Bray, J, Schofield, CJ & Oppermann, U (2011). Structural and evolutionary basis for the dual substrate selectivity of human kdm4 histone demethylase family. J Biol Chem 286(48), 41616–41625.CrossRefGoogle ScholarPubMed
Huang, J, Zhang, H, Yao, J, Qin, G, Wang, F, Wang, X, Luo, A, Zheng, Q, Cao, C & Zhao, J (2016). BIX-01294 increases pig cloning efficiency by improving epigenetic reprogramming of somatic cell nuclei. Reproduction 151(1), 39–49.CrossRefGoogle ScholarPubMed
Inoue, K, Kohda, T, Lee, J, Ogonuki, N, Mochida, K, Noguchi, Y, Tanemura, K, Kanekoishino, T, Ishino, F & Ogura, A (2002). Faithful expression of imprinted genes in cloned mice. Science 295(5553), 297–297.CrossRefGoogle ScholarPubMed
Jambhekar, A, Dhall, A & Shi, Y (2019). Roles and regulation of histone methylation in animal development. Nat Rev Mol Cell Biol 20(10), 625–641.CrossRefGoogle ScholarPubMed
Kang, H & Roh, S (2011). Extended exposure to trichostatin A after activation alters the expression of genes important for early development in nuclear transfer murine embryos. J Vet Med Sci 73(5), 623–631.CrossRefGoogle ScholarPubMed
Keramari, M, Razavi, J, Ingman, KA, Patsch, C, Edenhofer, F, Ward, CM & Kimber, SJ (2010). Sox2 is essential for formation of trophectoderm in the preimplantation embryo. PLoS ONE 5(11), e13952.CrossRefGoogle ScholarPubMed
Krishnan, S & Trievel, RC (2013). Structural and functional analysis of JMJD2D reveals molecular basis for site-specific demethylation among JMJD2 demethylases. Structure 21(1), 98–108.CrossRefGoogle ScholarPubMed
Labbe, RM, Holowatyj, A & Yang, Z (2014). Histone lysine demethylase (KDM) subfamily 4: Structures, functions and therapeutic potential. Am J Transl Res 6(1), 1–15.Google Scholar
Le Bin, GC, Munoz-Descalzo, S, Kurowski, A, Leitch, H, Lou, X, Mansfield, W, Etienne-Dumeau, C, Grabole, N, Mulas, C, Niwa, H, Hadjantonakis, AK & Nichols, J (2014). Oct4 is required for lineage priming in the developing inner cell mass of the mouse blastocyst. Development 141(5), 1001–1010.CrossRefGoogle ScholarPubMed
Liu, S, Bou, G, Sun, R, Guo, S, Xue, B, Wei, R, Cooney, AJ & Liu, Z (2015). Sox2 is the faithful marker for pluripotency in pig: Evidence from embryonic studies. Dev Dyn 244(4), 619–627.CrossRefGoogle ScholarPubMed
Liu, W, Liu, X, Wang, C, Gao, Y, Gao, R, Kou, X, Zhao, Y, Li, J, Wu, Y & Xiu, W (2016). Identification of key factors conquering developmental arrest of somatic cell cloned embryos by combining embryo biopsy and single-cell sequencing. Cell Discovery 2(1), 16010–16010.CrossRefGoogle ScholarPubMed
Liu, X, Wang, Y, Gao, Y, Su, J, Zhang, J, Xing, X, Zhou, C, Yao, K, An, Q & Zhang, Y (2018 a). H3k9 demethylase KDM4E is an epigenetic regulator for bovine embryonic development and a defective factor for nuclear reprogramming. Development 145(4), dev158261.CrossRefGoogle Scholar
Liu, Z, Cai, Y, Wang, YY, Nie, Y, Zhang, C, Xu, Y, Zhang, X, Lu, Y, Wang, Z & Poo, M (2018 b). Cloning of macaque monkeys by somatic cell nuclear transfer. Cell 172(4), 245.CrossRefGoogle ScholarPubMed
Loh, Y, Zhang, W, Chen, X, George, J & Ng, H (2007). Jmjd1a and Jmjd2c histone H3 Lys 9 demethylases regulate self-renewal in embryonic stem cells. Genes Dev 21(20), 2545–2557.CrossRefGoogle ScholarPubMed
Madheshiya, PK, Sahare, AA, Jyotsana, B, Singh, KP, Saini, M, Raja, AK, Kaith, S, Singla, SK, Chauhan, MS & Manik, RS (2015). Production of a cloned buffalo (Bubalus bubalis) calf from somatic cells isolated from urine. Cell Reprogram 17(3), 160–169.CrossRefGoogle ScholarPubMed
Matoba, S, Liu, Y, Lu, F, Iwabuchi, K, Shen, L, Inoue, A & Zhang, Y (2014). Embryonic development following somatic cell nuclear transfer impeded by persisting histone methylation. Cell 159(4), 884–895.CrossRefGoogle ScholarPubMed
Matoba, S & Zhang, Y (2018). Somatic cell nuclear transfer reprogramming: Mechanisms and applications. Cell Stem Cell 23(4), 471–485.CrossRefGoogle ScholarPubMed
Mehta, P, Kaushik, R, Singh, KP, Sharma, A, Singh, MK, Chauhan, MS, Palta, P, Singla, SK & Manik, RS (2019). Comparative analysis of buffalo (Bubalus bubalis) non-transgenic and transgenic embryos containing human insulin gene, produced by SCNT. Theriogenology 135, 25–32.CrossRefGoogle ScholarPubMed
Monika, S & Selokar, NL (2018). Approaches used to improve epigenetic reprogramming in buffalo cloned embryos. Indian J Med Res 148(Suppl), S115–S119.Google Scholar
Opiela, J, Samiec, M & Romanek, J (2017). In vitro development and cytological quality of inter-species (porcine→bovine) cloned embryos are affected by trichostatin A-dependent epigenomic modulation of adult mesenchymal stem cells. Theriogenology 97, 27–33.CrossRefGoogle ScholarPubMed
Ortega, MS, Kelleher, AM, Oneil, EV, Benne, JA, Cecil, R & Spencer, TE (2019). NANOG is required to form the epiblast and maintain pluripotency in the bovine embryo. Mol Reprod Dev 87(1), 152–160.CrossRefGoogle ScholarPubMed
Qiu, JJ, Zhang, WW, Wu, ZL, Wang, YH, Qian, M & Li, Y (2003). Delay of ZGA initiation occurred in 2-cell blocked mouse embryos. Cell Res 13(3), 179–185.CrossRefGoogle ScholarPubMed
Ruan, Z, Zhao, X, Li, Z, Qin, X, Shao, Q, Ruan, Q, Deng, Y, Jiang, J, Huang, B & Lu, F (2019). Effect of sex differences in donor foetal fibroblast on the early development and DNA methylation status of buffalo (Bubalus bubalis) nuclear transfer embryos. Reprod Domest Anim 54(1), 11–22.CrossRefGoogle ScholarPubMed
Sadato, D, Ono, T, Gotoh Saito, S, Kajiwara, N, Nomura, N, Ukaji, M, Yang, L, Sakimura, K, Tajima, Y, Oboki, K & Shibasaki, F (2018). Eukaryotic translation initiation factor 3 (eIF3) subunit e is essential for embryonic development and cell proliferation. FEBS Open Bio 8(8), 1188–1201.CrossRefGoogle Scholar
Saikhun, J, Kitiyanant, N, Songtaveesin, C, Pavasuthipaisit, K & 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(1), 65–78.CrossRefGoogle ScholarPubMed
Samiec, M (2005 a). The role of mitochondrial genome (mtDNA) in somatic and embryo cloning of mammals. A review. J Anim Feed Sci 14(2), 213–233.CrossRefGoogle Scholar
Samiec, M (2005 b). The effect of mitochondrial genome on architectural remodeling and epigenetic reprogramming of donor cell nuclei in mammalian nuclear transfer-derived embryos. J Anim Feed Sci 14(3), 393–422.CrossRefGoogle Scholar
Samiec, M, Romanek, J, Lipiński, D & Opiela, J (2019). Expression of pluripotency-related genes is highly dependent on trichostatin A-assisted epigenomic modulation of porcine mesenchymal stem cells analysed for apoptosis and subsequently used for generating cloned embryos. Anim Sci J 90(9), 1127–1141.CrossRefGoogle Scholar
Samiec, M & Skrzyszowska, M (2010). The use of different methods of oocyte activation for generation of porcine fibroblast cell nuclear-transferred embryos. Ann Anim Sci 10(4), 399–411.Google Scholar
Samiec, M & Skrzyszowska, M (2011). Transgenic mammalian species, generated by somatic cell cloning, in biomedicine, biopharmaceutical industry and human nutrition/dietetics – Recent achievements. Pol J Vet Sci 14(2), 317–328.CrossRefGoogle ScholarPubMed
Samiec, M & Skrzyszowska, M (2012). High developmental capability of porcine cloned embryos following trichostatin A-dependent epigenomic transformation during in vitro maturation of oocytes pre-exposed to R-roscovitine. Anim Sci Pap Rep 30(4), 383–393.Google Scholar
Samiec, M & Skrzyszowska, M (2014). Biological transcomplementary activation as a novel and effective strategy applied to the generation of porcine somatic cell cloned embryos. Reprod Biol 14(2), 128–139.CrossRefGoogle ScholarPubMed
Samiec, M & Skrzyszowska, M (2018 a). Can reprogramming of overall epigenetic memory and specific parental genomic imprinting memory within donor cell-inherited nuclear genome be a major hindrance for the somatic cell cloning of mammals? – A review. Ann Anim Sci 18(3), 623–638.CrossRefGoogle Scholar
Samiec, M & Skrzyszowska, M (2018 b). Intrinsic and extrinsic molecular determinants or modulators for epigenetic remodeling and reprogramming of somatic cell-derived genome in mammalian nuclear-transferred oocytes and resultant embryos. Pol J Vet Sci 21(1), 217–227.Google ScholarPubMed
Samiec, M, Skrzyszowska, M & Opiela, J (2013). Creation of cloned pig embryos using contact-inhibited or serum-starved fibroblast cells analysed intra vitam for apoptosis occurrence. Ann Anim Sci 13(2), 275–293.CrossRefGoogle Scholar
Santos, F, Zakhartchenko, V, Stojkovic, M, Peters, AHFM, Jenuwein, T, Wolf, E, Reik, W & Dean, W (2003). Epigenetic marking correlates with developmental potential in cloned bovine preimplantation embryos. Curr Biol 13(13), 1116–1121.CrossRefGoogle ScholarPubMed
Selokar, NL, Sharma, P, Saini, M, Sheoran, S, Rajendran, R, Kumar, D, Sharma, RK, Motiani, RK, Kumar, P, Jerome, A, Khanna, S & Yadav, PS (2019). Successful cloning of a superior buffalo bull. Sci Rep 9(1), 11366.CrossRefGoogle ScholarPubMed
Shin, S & Janknecht, R (2007). Diversity within the JMJD2 histone demethylase family. Biochem Biophys Res Commun 353(4), 973–977.CrossRefGoogle ScholarPubMed
Sridharan, R, Gonzalescope, M, Chronis, C, Bonora, G, Mckee, R, Huang, C, Patel, S, Lopez, D, Mishra, N & Pellegrini, M (2013). Proteomic and genomic approaches reveal critical functions of H3K9 methylation and heterochromatin protein-1γ in reprogramming to pluripotency. Nat Cell Biol 15(7), 872–882.CrossRefGoogle ScholarPubMed
Srirattana, K, Matsukawa, K, Akagi, S, Tasai, M, Tagami, T, Nirasawa, K, Nagai, T, Kanai, Y, Parnpai, R & Takeda, K (2011). Constant transmission of mitochondrial DNA in intergeneric cloned embryos reconstructed from swamp buffalo fibroblasts and bovine ooplasm. Anim Sci J 82(2), 236–243.CrossRefGoogle ScholarPubMed
Tasripoo, K, Suthikrai, W, Sophon, S, Jintana, R, Nualchuen, W, Usawang, S, Bintvihok, A, Techakumphu, M & Srisakwattana, K (2014). First cloned swamp buffalo produced from adult ear fibroblast cell. Animal 8(7), 1139–1145.CrossRefGoogle ScholarPubMed
Wang, H, Cui, W, Meng, C, Zhang, J, Li, Y, Qian, Y, Xing, G, Zhao, D & Cao, S (2018). MC1568 enhances histone acetylation during oocyte meiosis and improves development of somatic cell nuclear transfer embryos in pig. Cell Reprogram 20(1), 55–65.CrossRefGoogle ScholarPubMed
Wang, J, Zhang, M, Zhang, Y, Kou, Z, Han, Z, Chen, D, Sun, Q & Gao, S (2010). The histone demethylase JMJD2C is stage-specifically expressed in preimplantation mouse embryos and is required for embryonic development. Biol Reprod 82(1), 105–111.CrossRefGoogle ScholarPubMed
Wang, X, Qu, J, Li, J, He, H, Liu, Z & Huan, Y (2020). Epigenetic reprogramming during somatic cell nuclear transfer: Recent progress and future directions. Front Genet 11, 205.CrossRefGoogle ScholarPubMed
Wei, J, Antony, J, Meng, F, MacLean, P, Rhind, R, Laible, G & Oback, B (2017). KDM4B-mediated reduction of H3K9me3 and H3K36me3 levels improves somatic cell reprogramming into pluripotency. Sci Rep 7(1), 7514–7514.CrossRefGoogle ScholarPubMed
Yamazaki, Y, Fujita, TC, Low, EW, Alarcon, VB, Yanagimachi, R & Marikawa, Y (2006). Gradual DNA demethylation of the Oct4 promoter in cloned mouse embryos. Mol Reprod Dev 73(2), 180–188.CrossRefGoogle ScholarPubMed
Zhao, X, Du, F, Liu, X, Ruan, Q, Wu, Z, Lei, C, Deng, Y, Luo, C, Jiang, J & Shi, D (2019 a). Brain-derived neurotrophic factor (BDNF) is expressed in buffalo (Bubalus bubalis) ovarian follicles and promotes oocyte maturation and early embryonic development. Theriogenology 130, 79–88.CrossRefGoogle ScholarPubMed
Zhao, X, Ruan, Z, Qin, X, Feng, Y, Yu, Q, Xu, J, Deng, Y, Shen, P, Shi, D & Lu, F (2019 b). The role of 5-aza-2′-deoxycytidine on methylation status of Xist gene in different genders of buffalo (Bubalus bubalis) bone marrow mesenchymal stem cells. Cell Reprogram 21(2), 89–98.CrossRefGoogle ScholarPubMed
Zhou, C, Zhang, J, Zhang, M, Wang, D, Ma, Y, Wang, Y, Wang, Y, Huang, Y & Zhang, Y (2020). Transcriptional memory inherited from donor cells is a developmental defect of bovine cloned embryos. FASEB J 34(1), 1637–1651.CrossRefGoogle ScholarPubMed