Achievements and perspectives in cloned and transgenic cattle production by nuclear transfer: influence of cell type, epigenetic status and new technology
Genetically modified cattle production is motivated by many factors, including recombinant protein production for therapeutic purposes, disease models and animals presenting improved production traits. Nuclear transfer (NT), combined with efficient cultivation methods, genetic modification and donor cell selection is important for transgenic cattle production. Studies have found that adult cells (such as fibroblasts and cumulus cells, among others) used as nuclear donors achieved results similar to those of fetal cells, with the advantages of easier collection and a known genotype/phenotype. However, no consensus has been reached on the influence of cell type on transgene expression levels and post-reprogramming capacity after nuclear transfer, and these factors appear to be related to epigenetic factors. The development of new strategies, such as chromatin-modifying agents (CMAs), in vitro generation of induced pluripotent cells (iPS cells) and precise genome editing techniques are being explored and may influence nuclear reprogramming success for efficiently producing genetically modified bovine clones.
An LY, Yuan YG, Yu BL, Yang TJ, Cheng Y. 2012. Generation of human lactoferrin transgenic cloned goats using donor cells with dual markers and a modified selection procedure. Theriogenology, 78:1303-1311.
Arat S, Rzucidlo SJ, Gibbons J, Miyoshi K, Stice SL. 2001. Production of transgenic bovine embryos by transfer of transfected granulosa cells into enucleated oocytes. Mol Reprod Dev, 60:20-26.
Bagle TR, Kunkulol RR, Baig MS, More SY. 2012. Transgenic animals and their application in medicine. Int J Med Res Health Sci, 2:107-116.
Berg DK, Smith CS, Pearton DJ, Wells, DN, Broadhurst R, Donnison M, Pfeffer PL. 2011. Trophectoderm Lineage Determination in Cattle. Developmental Cell, 20:244-255.
Bevacqua RJ, Fernandez-Martín R, Savy V, Canel NG, Gismondi MI, Kues WA, Carlson DF, Fahrenkrug SC, Niemann H, Taboga OA, Ferraris S, Salamone DF. 2016. Efficient edition of the bovine PRNP prion gene in somatic cells and IVF embryos using the CRISPR/Cas9 system. Theriogenology, 86:1886-1896.
Beyhan Z, Ross PJ, Iager AE, Kocabas AM, Cunniff K, Rosa GJ, Cibelli JB. 2007. Transcriptional reprogramming of somatic cell nuclei during preimplantation development of cloned bovine embryos. Dev Biol, 15:637-49.
Blelloch R, Wang Z, Meissner A, Pollard S, Smith A, Jaenisch R. 2006. Reprogramming efficiency following somatic cell nuclear transfer is influenced by the differentiation and methylation state of the donor nucleus. Stem Cells, 24:2007-2013.
Blomberg L, Telugu B. 2012. Twenty Years of Embryonic Stem Cell Research in Farm Animals. Reprod Domest Anim, 47:80-85.
Bressan FF, De Bem, THC, Perecin F, Lopes FL, Ambrosio CE, Meirelles FV, Miglino MA. 2009. Unearthing the roles of imprinted genes in the placenta. Placenta, 30: 823-834.
Bressan FF, Miranda M Dos S, De Bem THC, Pereira FTVM, Binelli M, Meirelles FV. 2008. Production of transgenic animals by nuclear transfer: model for biological studies. Rev Bras Reprod Anim, 32:240-250.
Bressan FF, Perecin F, Sangalli JR, Meirelles FV. 2011. Reprogramming somatic cells: pluripotency through gene induction and nuclear transfer. Act Sci Vet, 39(Suppl 1):83-95.
Brevini TAL, Antonini S, Pennarossa G, Gandolfi F. 2008. Recent progress in embryonic stem cell research and its application in domestic species. Reprod Domest Anim, 43(Suppl 2):193-199.
Campbell KH, McWhir J, Ritchie WA, Wilmut I. 1996. Sheep cloned by nuclear transfer from a cultured cell line. Nature, 380:64-66.
Campbell KH. 1999. Nuclear equivalence, nuclear transfer, and the cell cycle. Cloning, 1:3-15.
Cao H, Yang P, Pu Y, Sun X, Yin H, Zhang Y, Zhang Y, Li Y, Liu Y, Fang F, Zhang Z, Tao Y, Zhang X. 2012. Characterization of bovine induced pluripotent stem cells by lentiviral transduction of reprogramming factor fusion proteins. Int J Biol Sci, 8:498-511.
Carlson DF, Tan W, Lillico SG, Stverakova D, Proudfoot C, Christian M, Voytas DF, Long CR, Whitelaw CBA, Fahrenkrug SC. 2012. Efficient TALEN-mediated gene knockout in livestock. Proc Natl Acad Sci, 109:17382-17387.
Cervera RP, Martí-Gutiérrez N, Escorihuela E, Moreno R, Stojkovic M. 2009. Trichostatin A affects histone acetylation and gene expression in porcine somatic cell nucleus transfer embryos. Theriogenology, 72:1097-1110.
Cheng D, Guo Y, Li Z, Liu Y, Gao X, Gao Y, Cheng X, Hu J, Wang H. 2012. Porcine induced pluripotent stem cells require LIF and maintain their developmental potential in early stage of embryos. PLoS One, 7:e51778.
Cheng X, Blumenthal RM. 2010. Coordinated chromatin control: structural and functional linkage of DNA and histone methylation. Biochemistry, 49:2999- 3008.
Cho J, Bhuiyan, MMU, Shin S, Park E, Jang G, Kang S, Lee B, Hwang W. 2004. Development potential of transgenic somatic cell nuclear transfer embryos according to various factors of donor cell. J Vet Med Sci, 66:1567-1573.
Choi W, Yum S, Lee S, Lee W, Lee J, Kim S, Koo O, Lee B, Jang G. 2015. Disruption of exogenous eGFP gene using RNA-guided endonuclease in bovine transgenic somatic cells. Zygote, 23:916-23.
Cibelli JB, Stice SL, Golueke PJ, Kane JJ, Jerry J, Blackwell C, Ponce de León FA, Robl JM. 1998. Cloned transgenic calves produced from nonquiescent fetal fibroblasts. Science, 280:1256–1258.
Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science, 339:819-823.
Deng W, Shi X, Tjian R, Lionnet T, Singer RH. 2015. CASFISH: CRISPR/Cas9-mediated in situ labeling of genomic loci in fixed cells. Proc Natl Acad Sci USA, 112:11870-11875.
Ezashi T, Yuan Y, Roberts RM. 2016. Pluripotent Stem Cells from Domesticated Mammals. Annu Rev Anim Biosci, 4:223-253.
Feng X, Cao S, Wang H, Meng C, Li J, Jiang J, Qian Y, Su L, He Q, Zhang Q. 2015. Production of transgenic dairy goat expressing human α-lactalbumin by somatic cell nuclear transfer. Transgenic Res, 24:73- 85.
Gandolfi F, Pennarossa G, Maffei, S, Brevini T. 2012. Why is it so Difficult to Derive Pluripotent Stem Cells in Domestic Ungulates? Reprod Domest Anim, 47:11-17.
Gao Y, Wu H, Wang Y, Liu X, Chen L, Li Q, Cui C, Liu X, Zhang J, Zhang Y. 2017. Single Cas9 nickase induced generation of NRAMP1 knockin cattle with reduced off-target effects. Genome Biol, 18:13.
García R, Ayala PA, Perdomo SP. 2012. Epigenetic: definition, molecular basis and implications for health and human evolution. Rev Cienc Salud, 10:59-71.
Gonçalves N, Ambrósio C, Piedrahita J. 2014. Stem Cells and Regenerative Medicine in Domestic and Companion Animals: A Multispecies Perspective. Reprod Domest Anim, 49:2-10.
Gong G, Dai Y, Fan B, Zhu H, Wang H, Wang L, Fang C, Wan R, Liu Y, Li R, Li N. 2004. Production of transgenic blastocyst by nuclear transfer from different types of somatic cells in cattle. Sci China C Life Sci, 47:183-189.
Hale CR, Zhao P, Olson S, Duff MO, Graveley BR, Wells L, Terns RM, Terns MP. 2009. RNA-Guided RNA Cleavage by a CRISPR RNA-Cas. Protein Complex Cell, 139:945-956.
He X, Ma L, He X, Si W, Zheng YM. 2016. Improved development of somatic cell cloned bovine embryos by a mammary gland epithelia cells in vitro model. J Vet Sci, 17:145-152.
Hosseini SM, Dufort I, Nieminen J, Moulavi F, Ghanaei HR, Hajian M, Jafarpour F, Forouzanfar M, Gourbai H, Shahverdi AH, Nasr-Esfahani MH, Sirard MA. 2016. Epigenetic modification with trichostatin A does not correct specific errors of somatic cell nuclear transfer at the transcriptomic level; highlighting the non-random nature of oocyte-mediated reprogramming errors. BMC genomics, 4:17:16.
Houdebine LM. 2009. Production of pharmaceutical proteins by transgenic animals. Comp Immunol Microbiol Infect Dis, 32:107-121.
Hsu PD, Lander ES, Zhang F. 2014. Development and Applications of CRISPR-Cas9 for Genome Engineering. Cell, 157:1262-1278.
Hu S, Ni W, Chen C, Sai W, Hazi W, He Z, Meng R, Guo J. 2012. Comparison between the effects of Valproic acid and Trichostatin A on in vitro development of sheep somatic cell nuclear transfer embryos. J Anim Vet Adv, 11:1868-1872.
Iager AE, Ragina NP, Ross PJ, Beyhan Z, Cunniff K, Rodriguez RM, Cibelli JB. 2008. Trichostatin A improves histone acetylation in bovine somatic cell nuclear transfer early embryos. Cloning Stem Cells, 10:371-379.
Illmensee K, Hoppe PC. 1981. Nuclear transplantation in Mus musculus: developmental potential of nuclei from preimplantation embryos. Cell, 23:9-18.
Inoue K, Ogonuki N, Miki H, Hirose M, Noda S, Kim JM, Aoki F, Miyoshi H, Ogura A. 2006. Inefficient reprogramming of the hematopoietic stem cell genome following nuclear transfer. J Cell Sci, 119:1985-1991.
Jansen R, Embden JD, Gaastra W, Schouls LM. 2002. Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol, 43:1565- 1575.
Jeong YH, Kim YJ, Kim EY, Kim SE, Kim J, Park MJ, Lee HG, Park SP, Kang MJ. 2016. Knock-in fibroblasts and transgenic blastocysts for expression of human FGF2 in the bovine β-casein gene locus using CRISPR/Cas9 nuclease-mediated homologous recombination. Zygote, 24:442-456.
Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 2012. A programmable dual-RNAguided DNA endonuclease in adaptive bacterial immunity. Science, 337:816-821.
Kato Y, Tani T, Sotomaru Y, Kurokawa K, Kato J, Doguchi H, Yasue H, Tsunoda Y. 1998. Eight calves cloned from somatic cells of a single adult. Science, 282:2095-2098.
Kato Y, Tani T, Tsunoda Y. 2000. Cloning of calves from various somatic cell types of male and female adult, newborn and fetal cows. J Reprod Fertil, 120:231-237.
Kishigami S, Mizutani E, Ohta H, Hikichi T, Thuan NV, Wakayama S, Bui HT, Wakayama T. 2006.
Significant improvement of mouse cloning technique by treatment with Trichostatin A after somatic nuclear transfer. Biochem Biophys Res Commun, 340:183-189.
Koh S, Piedrahita JA. 2014. From “ES-like” cells to induced pluripotent stem cells: a historical perspective in domestic animals. Theriogenology, 81:103-111.
Kong Q, Ji G, Xie B, Li J, Mao J, Wang J, Liu S, Liu L, Liu Z. 2014 Telomere elongation facilitated by trichostatin a in cloned embryos and pigs by somatic cell nuclear transfer. Stem Cell Rev, 10:399-407.
Liu Z, Wan H, Wang E, Zhao X, Ding C, Zhou S, Li T, Shuai L, Feng C, Yu Y, Zhou Q, Beaujean N. 2012. Induced pluripotent stem-induced cells show better constitutive heterochromatin remodeling and developmental potential after nuclear transfer than their parental cells. Stem Cells Dev, 21:3001-3009.
Lotti SN, Polkoff KM, Rubessa M, Wheeler MB. 2017. Modification of the Genome of Domestic Animals. Anim Biotechnol, 28:198-210.
Lu D, Liu S, Ding F, Wang H, Li J, Li L, Dai Y, Lib N. 2016. Large-scale production of functional human lysozyme from marker-free transgenic cloned cows. Sci Rep, 6:22947.
Luo C, Lu F, Wang X, Wang Z, Li X, Gong F, Jiang J, Liu Q, Shi D. 2013. Treatment of donor cells with trichostatin A improves in vitro development and reprogramming of buffalo (Bubalus bubalis) nucleus transfer embryos. Theriogenology, 80:878-886.
Matoba S, Liu Y, Lu F, Iwabuchi KA, Shen L, Inoue A, Zhang Y. 2014. Embryonic development following somatic cell nuclear transfer impeded by persisting histone methylation. Cell, 159:884-895.
McGrath J, Solter D. 1983. Nuclear transplantation in the mouse embryo by microsurgery and cell fusion. Science, 220:1300-1302.
Menchaca A, Anegon I, Whitelaw CBA, Baldassarre H, Crispo M. 2016. New insights and current tools for genetically engineered (GE) sheep and goats. Theriogenology, 86:160-169.
Miyoshi K, Mori H, Mizobe Y, Akasaka E, Ozawa A, Yoshida M, Sato M. 2010. Valproic acid enhances in vitro development and Oct-3/4 expression of miniature pig somatic cell nuclear transfer embryos. Cel Reprogram, 12:67-74.
Mojica FJ, Diez-Villasenor C, Soria E, Juez G. 2000. Biological significance of a family of regularly spaced repeats in the genomes of Archaea, Bacteria and mitochondria. Mol Microbiol, 36:244-246.
Monzani PS, Bressan FF, Mesquita LG, Sangalli JR, Meirelles FV. 2011. Casein gene expression by in vitro cultured bovine mammary epithelial cells derived from developing mammary glands. Genet Mol Res GMR, 10:604-614.
Monzani PS, Sangalli JR, De Bem THC, Bressan FF, Fantinato-Neto P, Pimentel JRV, Birgel-Junior EH, Fontes AM, Covas DT, Meirelles FV. 2013. Breeding of transgenic cattle for human coagulation factor IX by a combination of lentiviral system and cloning. Genet Mol Res, 12:3675-3688.
Muñoz M, Rodríguez A, De Frutos C, Caamaño JN, Díez C, Facal N, Gómez E. 2008. Conventional pluripotency markers are unspecific for bovine embryonic-derived cell-lines. Theriogenology, 69:1159- 1164.
Murakami M, Fahrudin M, Varisanga MD, Suzuki T. 1999. Fluorescence expression by bovine embryos after pronuclear microinjection with the EGFP gene. J Vet Med Sci, 61:843-847.
Ni W, Qiao J, Hu S, Zhao X, Regouski M, Yang M, Polejaeva IA ,Chen C. 2014. Efficient gene knockout in goats using CRISPR/Cas9 system. PLoS ONE 9(9): e106718.
Niu D, Wei H-J, Lin L, George H, Wang T, Lee I-H, Zhao H-Y, Wang Y, Kan Y, Shrock E, Lesha E, Wang G, Luo Y, Qing Y, Jiao D, Zhao H, Zhou X, Wang S, Wei H, Güell M, Church GM, Yang L. 2017. Inactivation of porcine endogenous retrovirus in pigs using CRISPR-Cas9. Science, 357:1303-1307.
Nowak-Imialek M, Kues W, Carnwath JW, Niemann H. 2011. Pluripotent stem cells and reprogrammed cells in farm animals. Microsc Microanal, 17:474-497.
Park K-E, Telugu BPVL. 2014. Role of stem cells in large animal genetic engineering in the TALENs/CRISPR era. Reprod FertiL Dev, 26: 65-73. Peng R, Lin G, Li J. 2016. Potential pitfalls of CRISPR/Cas9-mediated genome editing. FEBS J, 283:1218-1231.
Petersen B, Niemann H. 2015. Molecular scissors and their application in genetically modified farm animals. Transgenic Res, 24:381-396.
Picanço-Castro V, Russo-Carbolante E, Reis LCJ, Fraga AM, de Magalhães DAR, Orellana MD, Panepucci RA, Pereira LV, Covas DT. 2011.
Pluripotent reprogramming of fibroblasts by lentiviral mediated insertion of SOX2, C-MYC, and TCL-1A. Stem Cells Dev, 20:169-180.
Prather RS, Barnes FL, Sims MM, Robl JM, Eyestone WH, and First NL. 1987. Nuclear transplantation in the bovine embryo: assessment of donor nuclei and recipient oocyte. Biol Reprod, 37:859- 866.
Puri MC, Nagy A. 2012. Concise review: Embryonic stem cells versus induced pluripotent stem cells: the game is on. Stem Cells, 30:10-14.
Reik W, Dean W, Walter J. 2001. Epigenetic reprogramming in mammalian development. Science, 293:1089-1093.
Rémy S, Tesson L, Ménoret S, Usal C, Scharenberg AM, Anegon I. 2010. Zinc-finger nucleases: a powerful tool for genetic engineering of animals. Transgenic Res, 19:363-371.
Ren Z, Wang Y, Ren Y, Zhang Z, Gu W, Wu Z, Chen L, Mou L, Li R, Yang H, Daib Y. 2017. Enhancement of porcine intramuscular fat content by overexpression of the cytosolic form of phosphoenolpyruvate carboxykinase in skeletal muscle. Sci Rep, 7:43746.
Rülicke TH, Montagutelli X, Pintado B, Thon R, Hedrich HJ. 2007. FELASA guidelines for the production and nomenclature of transgenic rodents. Lab Anim, 41:301-311.
Salozhin SV, Prokhorchuk EB, Georgiev GP. 2005. Methylation of DNA-one of the major epigenetic markers. Biochemistry Mosc, 70:525-532.
Sangalli JR, Chiaratti MR, De Bem THC, de Araújo RR, Bressan FF, Sampaio RV, Perecin F, Smith LC, King WA, Meirelles FV. 2014. Development to term of cloned cattle derived from donor cells treated with valproic Acid. PLoS One, 9:e101022.
Sangalli JR, De Bem THC, Perecin F, Chiaratti MR, Oliveira L de J, de Araújo RR, Valim Pimentel JR, Smith LC, Meirelles FV. 2012. Treatment of nucleardonor cells or cloned zygotes with chromatin-modifying agents increases histone acetylation but does not improve full-term development of cloned cattle. Cell Reprogram, 14:235-247.
Schmittwolf C, Kirchhof N, Jauch A, Dürr M, Harder F, Zenke M, Müller AM. 2005. In vivo haematopoietic activity is induced in neurosphere cells by chromatin-modifying agents. EMBO J, 24:554-566.
Schnieke AE, Kind AJ, Ritchie WA, Mycock K, Scott AR, Ritchie M, Wilmut I, Colman A, Campbell KH. 1997. Human factor IX transgenic sheep produced by transfer of nuclei from transfected fetal fibroblasts. Science, 278:2130-2133.
Shi LH, Ai JS, Ouyang YC, Huang JC, Lei ZL, Wang Q, Yin S, Han ZM, Sun QY, Chen DY. 2008. Trichostatin A and nuclear reprogramming of cloned rabbit embryos. J Anim Sci, 86:1106-1113.
Shi W, Hoeflich A, Flaswinkel H, Stojkovic M, Wolf E, Zakhartchenko V. 2003. Induction of a senescentlike phenotype does not confer the ability of bovine immortal cells to support the development of nuclear transfer embryos. Biol Reprod, 69:301-309.
Smith LC, Suzuki J, Goff AK, Filion F, Therrien J, Murphy BD, Kohan-Ghadr HR, Lefebvre R, Brisville AC, Buczinski S, G Fecteau, Perecin F, Meirelles FV. 2012. Developmental and epigenetic anomalies in cloned cattle. Reprod Domest Anim, 47(Suppl 4):107-114.
Smith LC, Therrien J, Filion F, Bressan F, Meirelles FV. 2015. Epigenetic consequences of artificial reproductive technologies to the bovine imprinted genes SNRPN, H19/IGF2, and IGF2R. Front Genet, 6:58.
Song Y, Hai T, Wang Y, Guo R, Li W, Wang L, Zhou Q. 2014. Epigenetic reprogramming, gene expression and in vitro development of porcine SCNT embryos are significantly improved by a histone deacetylase inhibitor-m-carboxycinnamic acid bishydroxamide (CBHA). Protein Cell, 5:382-393.
Sung LY, Gao S, Shen H, Yu H, Song Y, Smith SL, Chang CC, Inoue K, Kuo L, Lian J, Li A, Tian XC, Tuck DP, Weissman SM, Yang X, Cheng T. 2006. Differentiated cells are more efficient than adult stem cells for cloning by somatic cell nuclear transfer Nature Genetics, 38:1323-1328.
Suzuki J, Therrien J, Filion F, Lefebvre R, Goff AK, Smith LC. 2009. In vitro culture and somatic cell nuclear transfer affect imprinting of SNRPN gene in pre- and post-implantation stages of development in cattle. BMC Dev Biol, 9:9.
Takahashi K, Yamanaka S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126:663-676.
Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. 2007. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell, 131:861-872.
Wang LJ, Zhang H, Wang YS, Xu WB, Xiong XR, Li YY, Su JM., Hua S, Zhang Y. 2011. Scriptaid improves in vitro development and nuclear reprogramming of somatic cell nuclear transfer bovine embryos. Cell Reprogram, 13:431-439.
Wells DN, Misica PM, Tervit HR. 1999. Production of cloned calves following nuclear transfer with cultured adult mural granulosa cells. Biol Reprod, 60:996–1005.
Whyte JJ, Zhao J, Wells KD, Samuel MS, Whitworth KM, Walters EM, Laughlin MH, Prather, RS. 2011. Gene targeting with zinc finger nucleases to produce cloned eGFP knockout pigs . Mol Reprod Dev 78(1): 2-2 Willadsen SM. 1986. Nuclear transplantation in sheep embryos. Nature, 320:63-65.
Wilmut I, Bai Y, Taylor J. 2015. Somatic cell nuclear transfer: origins, the present position and future opportunities. Philos Trans R Soc Lond B Biol Sci, 370: 20140366.
Wilmut I, Beaujean N, de Sousa PA, Dinnyes A, King TJ, Paterson LA, Wells DN, Young LE. 2002. Somatic cell nuclear transfer. Nature, 419:583-587.
Wilmut I, Schnieke AE, McWhir J, Kind AJ, Campbell KH. 1997. Viable offspring derived from fetal and adult mammalian cells. Nature, 385:810-813.
Wu H, Wang Y, Zhang Y, Yang M, Lv J, Liu J, Zhang Y. 2015. TALE nickase-mediated SP110 knockin endows cattle with increased resistance to tuberculosis. Proc Natl Acad Sci USA, 112:1530-1539.
Wu J, Vilarino M, Suzuki K, Okamura D, Bogliotti YS, Park I, Rowe J, McNabb B, Ross PJ, Belmonte JCI. 2017. CRISPR-Cas9 mediated one-step disabling of pancreatogenesis in pigs. Sci Rep, 7:10487.
Xu W, Wang Y, Li Y, Wang L, Xiong X, Su J, Zhang Y. 2012. Valproic acid improves the in vitro development competence of bovine somatic cell nuclear transfer embryos. Cell Reprog, 14:138-145.
Yang X, Smith SL, Tian XC, Lewin HA, Renard JP, Wakayama T. 2007. Nuclear reprogramming of cloned embryos and its implications for therapeutic cloning. Nat Genet, 39:295-302.
Yu J, Vodyanik MA, Smuga-Otto K, AntosiewiczBourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, Thomson JA. 2007. Induced pluripotent stem cell lines derived from human somatic cells. Science, 318:1917-1920.
Zakartchenko V, Alberio R, Stojkovic M, Prelle K, Schernthaner W, Stojkovic P, Wenigerkind H, Wanke R, Düchler M, Steinborn R, Mueller M, Brem G, Wolf E. 1999. Adult cloning in cattle: potential of nuclei from a permanent cell line and from primary cultures. Mol Reprod Dev, 54: 264-272.
Zhan K, Lin M, Liu M, Sui Y, Babekir HM, Zhao G. 2017. Three-dimensional culture system can induce expression of casein in immortalized bovine mammary epithelial cells. Animal science Journal, 88:817-825
Zhang L, Huang Y, Wu Y, Si J, Huang Y, Jiang Q, Lan G, Guo Y, Jiang H. 2017. Scriptaid upregulates expression of development-related genes, inhibits apoptosis, and improves the development of somatic cell nuclear transfer mini-pig embryos. Cel Reprog, 19:19-26.
Zhao L, Wang Z, Zhang J, Yang J, Gao X, Wu B, Zhao G, Bao S, Hu S, Liu P, Li X. 2017. Characterization of the single-cell derived bovine induced pluripotent stem cells. Tissue cell, 49:521-527.
Zhou S, Ding C, Zhao X, Wang E, Dai X, Liu L, Li W, Liu Z, Wan H, Feng C, Tang Hai, Liu Wang, Qi Zhou. 2010. Successful generation of cloned mice using nuclear transfer from induced pluripotent stem cells. Cell Res, 20:850-853.