1. bookVolume 19 (2019): Issue 1 (January 2019)
Journal Details
License
Format
Journal
eISSN
2300-8733
First Published
25 Nov 2011
Publication timeframe
4 times per year
Languages
English
access type Open Access

Identifying Biomarkers of Autophagy and Apoptosis in Transfected Nuclear Donor Cells and Transgenic Cloned Pig Embryos

Published Online: 01 Feb 2019
Volume & Issue: Volume 19 (2019) - Issue 1 (January 2019)
Page range: 127 - 146
Received: 14 Jun 2018
Accepted: 01 Oct 2018
Journal Details
License
Format
Journal
eISSN
2300-8733
First Published
25 Nov 2011
Publication timeframe
4 times per year
Languages
English
Abstract

In this study, we first investigated the effects of 3-methyladenine (3-MA), an autophagy inhibitor, and the inducer – rapamycin (RAPA) on the incidence of programmed cell death (PCD) symptoms during in vitro development of porcine somatic cell nuclear transfer (SCNT)-derived embryos. The expression of autophagy inhibitor mTOR protein was decreased in porcine SCNT blastocysts treated with 3MA. The abundance of the autophagy marker LC3 increased in blastocysts following RAPA treatment. Exposure of porcine SCNT-derived embryos to 3-MA suppressed their developmental abilities to reach the blastocyst stage. No significant difference in the expression pattern of PCD-related proteins was found between non-transfected dermal cell and transfected dermal cell groups. Additionally, the pattern of PCD in SCNT-derived blastocysts generated using SC and TSC was not significantly different, and in terms of porcine SCNT-derived embryo development rates and total blastocyst cell numbers, there was no significant difference between non-transfected cells and transfected cells. In conclusion, regulation of autophagy affected the development of porcine SCNT embryos. Regardless of the type of nuclear donor cells (transfected or non-transfected dermal cells) used for SCNT, there was no difference in the developmental potential and quantitative profiles of autophagy/apoptosis biomarkers between porcine transgenic and non-transgenic cloned embryos. These results led us to conclude that PCD is important for controlling porcine SCNT-derived embryo development, and that transfected dermal cells can be utilized as a source of nuclear donors for the production of transgenic cloned progeny in pigs.

Keywords

Agrawal H., Selokar N.L., Saini M., Singh M.K., Chauhan M.S., Palta P., Sin-gla S.K., Manik R.S. (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: 986–996.Search in Google Scholar

Boya P., González-Polo R.A., Casares N., Perfettini J.L., Dessen P., Larochet-te N., Métivier D., Meley D., Souquere S., Yoshimori T., Pierron G., Codo-gno P., Kroemer G. (2005). Inhibition of macroautophagy triggers apoptosis. Mol. Cell Biol., 25: 1025–1040.Search in Google Scholar

Brill A., Torchinsky A., Carp H., Toder V. (1999). The role of apoptosis in normal and abnormal embryonic development. J. Assist. Reprod. Genet., 16: 512–519.Search in Google Scholar

Brink M.F., Bishop M.D., Pieper F.R. (2000). Developing efficient strategies for the generation of transgenic cattle which produce biopharmaceuticals in milk. Theriogenology, 53: 139–148.Search in Google Scholar

Brophy B., Smolenski G., Wheeler T., Wells D., L’ Huillier P., Laible G. (2003). Cloned transgenic cattle produce milk with higher levels of beta-casein and kappa-casein. Nat. Biotechnol., 21: 157–162.Search in Google Scholar

Callesen M.M., Árnadóttir S.S., Lyskjaer I., Ørntoft M.W., Høyer S., Dagnaes-Hansen F., Liu Y., Li R., Callesen H., Rasmussen M.H., Berthelsen M.F., Thomsen M.K., Schweiger P.J., Jensen K.B., Laurberg S., Ørntoft T.F., Elver-løv-Jakobsen J.E., Andersen C.L. (2017). A genetically inducible porcine model of intestinal cancer. Mol. Oncol., 11: 1616–1629.Search in Google Scholar

Campbell K.H., Mc Whir J., Ritchie W.A., Wilmut I. (1996). Sheep cloned by nuclear transfer from a cultured cell line. Nature, 380: 64–66.Search in Google Scholar

Chi D., Zeng Y., Xu M., Si L., Qu X., Liu H., Li J. (2017). LC3-dependent autophagy in pig 2-cell cloned embryos could influence the degradation of maternal mRNA and the regulation of epigenetic modification. Cell. Reprogram., 19: 354–362.Search in Google Scholar

Cibelli J.B., Stice S.L., Golueke P.J., Kane J.J., Jerry J., Blackwell C., Poncede León F.A., Robl J.M. (1998). Cloned transgenic calves produced from nonquiescent fetal fibroblasts. Science, 280: 1256–1258.Search in Google Scholar

Denning C., Dickinson P., Burl S., Wylie D., Fletcher J., Clark A.J. (2001). Gene targeting in primary fetal fibroblasts from sheep and pig. Clon. Stem Cells, 3: 221–231.Search in Google Scholar

Deryugina E.I., Quigley J.P. (2006). Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev., 25: 9–34.Search in Google Scholar

Fabian D., Koppel J., Maddox-Hyttel P. (2005). Apoptotic processes during mammalian preimplantation development. Theriogenology, 64: 221–231.Search in Google Scholar

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.Search in Google Scholar

Galluzzi L., Maiuri M.C., Vitale I., Zischka H., Castedo M., Zitvogel L., Kro-emer G. (2007). Cell death modalities: classification and pathophysiological implications. Cell Death Differ., 14: 1237–1243.Search in Google Scholar

Galoian K., Temple H.T., Galoyan A. (2012). mTORC1 inhibition and ECM-cell adhesion-independent drug resistance via PI3K-AKT and PI3K-RAS-MAPK feedback loops. Tumour Biol., 33: 885–890.Search in Google Scholar

Gómez M.C., Pope C.E. (2015). Cloning endangered felids by interspecies somatic cell nuclear transfer. Methods Mol. Biol., 1330: 133–152.Search in Google Scholar

Himaki T., Yokomine T.A., Sato M., Takao S., Miyoshi K., Yoshida M. (2011). Effects of trichostatin A on in vitro development and transgene function in somatic cell nuclear transfer embryos derived from transgenic Clawn miniature pig cells. Anim Sci. J., 81: 558–563.Search in Google Scholar

Iguma L.T., Lisauskas S.F., Melo E.O., Franco M.M., Pivato I., Vianna G.R., Sou-sa R.V., Dode M.A., Aragão F.J., Rech E.L., Rumpf R. (2005). Development of bovine embryos reconstructed by nuclear transfer of transfected and non-transfected adult fibroblast cells. Genet. Mol. Res., 4: 55–66.Search in Google Scholar

Ji Q., Zhu K., Liu Z., Song Z., Huang Y., Zhao H., Chen Y., He Z., Mo D., Cong P. (2013). Improvement of porcine cloning efficiency by trichostain A through early-stage induction of embryo apoptosis. Theriogenology, 79: 815–823.Search in Google Scholar

Jia L., Dourmashkin R.R., Allen P.D., Gray A.B., Newland A.C., Kelsey S.M. (1997). Inhibition of autophagy abrogates tumour necrosis factor alpha induced apoptosis in human T-lymphoblastic leukaemic cells. Br. J. Haematol., 98: 673–685.Search in Google Scholar

Jia L., Dourmashkin R.R., Allen P.D., Gray A.B., Newland A.C., Kelsey S.M. (2014). Self-consumption: the interplay of autophagy and apoptosis. Nat. Rev. Mol. Cell Biol., 15: 81–94.Search in Google Scholar

Jin L., Guo Q., Zhu H.Y., Xing X.X., Zhang G.L., Xuan M.F., Luo Q.R., Luo Z.B., Wang J.X., Yin X.J., Kang J.D. (2017). Quisinostat treatment improves histone acetylation and developmental competence of porcine somatic cell nuclear transfer embryos. Mol. Reprod. Dev., 84: 340–346.Search in Google Scholar

Jin L., Guo Q., Zhang G.L., Xing X.X., Xuan M.F., Luo Q.R., Luo Z.B., Wang J.X., Yin X.J., Kang J.D. (2018). The histone deacetylase inhibitor, CI994, improves nuclear reprogramming and in vitro developmental potential of cloned pig embryos. Cell. Reprogram., 20: 205–213.Search in Google Scholar

Kasinathan P., Knott J.G., Moreira P.N., Burnside A.S., Jerry D.J., Robl J.M. (2001). Effect of fibroblast donor cell age and cell cycle on development of bovine nuclear transfer embryos in vitro. Biol. Reprod., 64: 1487–1493.Search in Google Scholar

Keefer C.L. (2008). Lessons learned from nuclear transfer (cloning). Theriogenology, 69: 48–54.Search in Google Scholar

Keefer C.L. (2015). Artificial cloning of domestic animals. Proc. Natl. Acad. Sci. USA, 112: 8874–8878.Search in Google Scholar

Kim G.A., Lee E.M., Jin J.X., Lee S., Taweechaipaisankul A., Hwang J.I., Alam Z., Ahn C., Lee B.C. (2017). Generation of CMAHKO/GTKO/shTNFRI-Fc/HO-1 quadruple gene modified pigs. Transgenic Res., 26: 435–445.Search in Google Scholar

Kim S.H., Zhao M.H., Liang S., Cui X.S., Kim N.H. (2015). Inhibition of cathepsin B activity reduces apoptosis by preventing cytochrome c release from mitochondria in porcine parthenotes. J. Reprod. Dev., 61: 261–268.Search in Google Scholar

Knight Z.A., Shokat K.M. (2007). Chemically targeting the PI3K family. Biochem. Soc. Trans., 35: 245–249.Search in Google Scholar

Kolber-Simonds D., Lai L., Watt S.R., Denaro M., Arn S. (2004). Production of alpha-1,3-galactosyltransferase null pigs by means of nuclear transfer with fibroblasts bearing loss of heterozygosity mutations. Proc. Natl. Acad. Sci. USA, 101: 7335–7340.Search in Google Scholar

Kwon D.J., Kim D.H., Hwang I.S., Kim D.E., Kim H.J., Kim J.S., Lee K., Im G.S., Lee J.W., Hwang S. (2017). Generation of α-1,3-galactosyltransferase knocked-out transgenic cloned pigs with knocked-in five human genes. Transgenic Res., 26: 153–163.Search in Google Scholar

Lee H.R., Gupta M.K., Kim D.H., Hwang J.H., Kwon B., Lee H.T. (2016). Poly(ADP-ribosyl)ation is involved in pro-survival autophagy in porcine blastocysts. Mol. Reprod. Dev., 83: 37–49.Search in Google Scholar

Lee P.S., Tsang S.W., Moses M.A., Trayes-Gibson Z., Hsiao L.L., Jensen R., Squil-lace R., Kwiatkowski D.J. (2010). Rapamycin-insensitive up-regulation of MMP2 and other genes in tuberous sclerosis complex 2-deficient lymphangioleiomyomatosis-like cells. Am. J. Respir. Cell Mol. Biol., 42: 227–234.Search in Google Scholar

Lee S., Jin J.X., Khoirinaya C., Kim G.A., Lee B.C. (2015). Lanosterol influences cytoplasmic maturation of pig oocytes in vitro and improves preimplantation development of cloned embryos. Theriogenology, 61: 261–268.Search in Google Scholar

Lee S.C., Lee H., Oh K.B., Hwang I.S., Yang H., Park M.R., Ock S.A., Woo J.S., Im G.S., Hwang S. (2017). Production and breeding of transgenic cloned pigs expressing human CD73. Dev. Reprod., 21: 157–165.Search in Google Scholar

Lee S.E., Hwang K.C., Sun S.C., Xu Y.N., Kim N.H. (2011). Modulation of autophagy influences development and apoptosis in mouse embryos developing in vitro. Mol. Reprod. Dev., 78: 498–509.Search in Google Scholar

Lee S.H., Xu Y.N., Heo Y.T., Cui X.S., Kim N.H. (2013). Effects of trichostatin A and 5-aza-2’deoxycytidine on nuclear reprogramming in pig cloned embryos. Reprod. Dev. Biol., 37: 269–279.Search in Google Scholar

Li Z., He X., Chen L., Shi J., Zhou R., Xu W., L iu D., Wu Z. (2013). Bone marrow mesenchymal stem cells are an attractive donor cell type for production of cloned pigs as well as genetically modified cloned pigs by somatic cell nuclear transfer. Cell. Reprogram., 15: 459–470.Search in Google Scholar

Lin T., Lee J.E., Oqani R.K., Kim S.Y., Cho E.S., Jeong Y.D., Baek J.J., Jin D.I. (2016). Tauroursodeoxycholic acid improves pre-implantation development of porcine SCNT embryo by endoplasmic reticulum stress inhibition. Reprod. Biol., 16: 269–278.Search in Google Scholar

Luo Y., Wang Y., Liu J., Lan H., Shao M., Yu Y., Quan F., Zhang Y. (2015). Production of transgenic cattle highly expressing human serum albumin in milk by phiC31 integrase-mediated gene delivery. Transgenic Res., 24: 875–883.Search in Google Scholar

Malemud C.J. (2006). Matrix metalloproteinases (MMPs) in health and disease: an overview. Front Biosci., 11: 1696–1701.Search in Google Scholar

Mastromonaco G.F., Perrault S.D., Betts D.H., King W.A. (2003). Role of chromosome stability and telomere length in the production of viable cell lines for somatic cell nuclear transfer. BMC Dev. Biol., 6: 41.Search in Google Scholar

Meurens F., Summerfield A., Nauwynck H., Saif L., Gerdts V. (2012). The pig: a model for human infectious diseases. Trends Microbiol., 30: 50–57.Search in Google Scholar

Miyamoto K., Hoshino Y., Minami N., Yamada M., Imai H. (2007). Effects of synchronization of donor cell cycle on embryonic development and DNA synthesis in porcine nuclear transfer embryos. J. Reprod. Dev., 53: 237–246.Search in Google Scholar

Nikoletopoulou V., Markaki M., Palikaras K., Tavernarakis N. (2013). Crosstalk between apoptosis, necrosis and autophagy. Biochim. Biophys. Acta, 1833: 3448–3459.Search in Google Scholar

Olivera R., Moro L.N., Jordan R., Pallarols N., Guglielminetti A., Luzzani C., Miriuka S.G., Vichera G. (2018). Bone marrow mesenchymal stem cells as nuclear donors improve viability and health of cloned horses. Stem Cells Cloning, 11: 13–22.Search in 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.Search in Google Scholar

Page-Mc Caw A., Ewald A.J., Werb Z. (2007). Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol., 8: 221–233.Search in Google Scholar

Pan T., Rawal P., Wu Y., Xie W., Jankovic J., Le W. (2009). Rapamycin protects against rotenone-induced apoptosis through autophagy induction. Neuroscience, 164: 541–551.Search in Google Scholar

Samiec M. (2004). Development of pig cloning studies: past, present and future. J. Anim. Feed Sci., 13: 211–238.Search in Google Scholar

Samiec M. (2005). 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: 393–422.Search in Google Scholar

Samiec M., Skrzyszowska M. (2010 a). Preimplantation developmental capability of cloned pig embryos derived from different types of nuclear donor somatic cells. Ann. Anim. Sci., 10: 385–398.Search in Google Scholar

Samiec M., Skrzyszowska M. (2010 b). The use of different methods of oocyte activation for generation of porcine fibroblast cell nuclear-transferred embryos. Ann. Anim. Sci., 10: 399–411.Search in Google Scholar

Samiec M., Skrzyszowska M. (2011 a). Transgenic mammalian species, generated by somatic cell cloning, in biomedicine, biopharmaceutical industry and human nutrition/dietetics – recent achievements. Pol. J. Vet. Sci., 14: 317–328.10.2478/v10181-011-0050-721721422Search in Google Scholar

Samiec M., Skrzyszowska M. (2011 b). The possibilities of practical application of transgenic mammalian species generated by somatic cell cloning in pharmacology, veterinary medicine and xenotransplantology. Pol. J. Vet. Sci., 14: 329–340.10.2478/v10181-011-0051-621721423Search in Google Scholar

Samiec M., Skrzyszowska M. (2012 a). 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: 383–393.Search in Google Scholar

Samiec M., Skrzyszowska M. (2012 b). Roscovitine is a novel agent that can be used for the activation of porcine oocytes reconstructed with adult cutaneous or fetal fibroblast cell nuclei. Theriogenology, 78: 1855–1867.10.1016/j.theriogenology.2012.06.02922979963Search in Google Scholar

Samiec M., Skrzyszowska M. (2013). Assessment of in vitro developmental capacity of porcine nuclear-transferred embryos reconstituted with cumulus oophorus cells undergoing vital diagnostics for apoptosis detection. Ann. Anim. Sci., 13: 513–529.Search in 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: 128–139.Search in Google Scholar

Samiec M., Skrzyszowska M. (2018 a). 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: 217–227.Search in Google Scholar

Samiec M., Skrzyszowska M. (2018 b). 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: 623–638.10.2478/aoas-2018-0015Search in Google Scholar

Samiec M., Skrzyszowska M., Lipiński D. (2012). Pseudophysiological transcomplementary activation of reconstructed oocytes as a highly efficient method used for producing nuclear-transferred pig embryos originating from transgenic foetal fibroblast cells. Pol. J. Vet. Sci., 15: 509–516.Search in Google Scholar

Samiec M., Skrzyszowska M., Opiela J. (2013 a). Creation of cloned pig embryos using contact-inhibited or serum-starved fibroblast cells analysed intra vitam for apoptosis occurrence. Ann. Anim. Sci., 13: 275–293.10.2478/aoas-2013-0009Search in Google Scholar

Samiec M., Skrzyszowska M., Bochenek M. (2013 b). In vitro development of porcine nuclear-transferred embryos derived from fibroblast cells analysed cytometrically for apoptosis incidence and accuracy of cell cycle synchronization at the G0/G1 stages. Ann. Anim. Sci., 13: 735–752.10.2478/aoas-2013-0049Search in Google Scholar

Samiec M., Opiela J., Lipiński D., Romanek J. (2015). Trichostatin A-mediated epigenetic transformation of adult bone marrow-derived mesenchymal stem cells biases the in vitro developmental capability, quality, and pluripotency extent of porcine cloned embryos. Biomed. Res. Int., 2015: 814686.Search in Google Scholar

Sandrin V., Boson B., Salmon P., Gay W., Nègre D., Le Grand R., Trono D., Cos-set F.L. (2002). Lentiviral vectors pseudotyped with a modified RD114 envelope glycoprotein show increased stability in sera and augmented transduction of primary lymphocytes and CD34+ cells derived from human and nonhuman primates. Blood, 100: 823–832.Search in Google Scholar

Schwartz L.M., Smith S.W., Jones M.E., Osborne B.A. (1993). Do all programmed cell deaths occur via apoptosis? Proc. Natl. Acad Sci. USA, 90: 980–984.Search in Google Scholar

Shen X., Zhang N., Wang Z., Bai G., Zheng Z., Gu Y., Wu Y., Liu H., Zhou D., Lei L. (2015). Induction of autophagy improves embryo viability in cloned mouse embryos. Sci. Rep., 5: 17829.Search in Google Scholar

Skrzyszowska M., Smorąg Z., Słomski R., Kątska-Książkiewicz L., Kalak R., Michalak E., Wielgus K., Lehmann J., Lipiński D., Szalata M., Pławski A., Samiec M., Jura J., Gajda B., Ryńska B., Pieńkowski M. (2006). Generation of transgenic rabbits by the novel technique of chimeric somatic cell cloning. Biol. Reprod., 74: 1114–1120.Search in Google Scholar

Song B.S., Kim J.S., Yoon S.B., Lee K.S., Koo D.B., Lee D.S., Choo Y.K., Huh J.W., Lee S.R., Kim S.U., Kim S.H., Kim H.M., Chang K.T. (2001). Inactivated Sendai-virusmediated fusion improves early development of cloned bovine embryos by avoiding endoplasmic-reticulum-stress-associated apoptosis. Reprod. Fert. Develop., 23: 826–836.Search in Google Scholar

Song B.S., Yoon S.B., Kim J.S., Sim B.W., Kim Y.H., Cha J.J., Choi S.A., Min H.K., Lee Y., Huh J.W., Lee S.R., Kim S.H., Koo D.B., Choo Y.K., Kim H.M., Kim S.U., Chang K.T. (2012). Induction of autophagy promotes preattachment development of bovine embryos by reducing endoplasmic reticulum stress. Biol. Reprod., 87: 1–11.Search in Google Scholar

Staunstrup N.H., Stenderup K., Mortensen S., Primo M.N., Rosada C., Steini-che T., Liu Y., Li R., Schmidt M., Purup S., Dagnæs-Hansen F., Schrøder L.D., Svensson L., Petersen T.K., Callesen H., Bolund L., Mikkelsen J.G. (2017). Psoriasiform skin disease in transgenic pigs with high-copy ectopic expression of human integrins α2 and β1. Dis. Model. Mech., 10: 869–880.Search in Google Scholar

Tanabe Y., Kuwayama H., Wakayama S., Nagatomo H., Ooga M., Kamimura S., Kishigami S., Wakayama T. (2017). Production of cloned mice using oocytes derived from ICR-outbred strain. Reproduction, 154: 859–866.Search in Google Scholar

Tanida I., Ueno T., Kominami E. (2004). LC3 conjugation system in mammalian autophagy. Int. J. Biochem. Cell Biol., 36: 2503–2518.Search in Google Scholar

Tsukada M., Ohsumi Y. (1993). Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett., 333: 169–174.Search in Google Scholar

Tsukamoto S. (2014). Autophagic activity as an indicator for selecting good quality embryos. Reprod. Med. Biol., 14: 57–64.Search in Google Scholar

Tsukamoto S., Yamamoto A. (2013). The role of autophagy in early mammalian embryonic development. J. Mamm. Ova. Res., 30: 86–94.Search in Google Scholar

Vajta G. (2007). Handmade cloning: the future way of nuclear transfer? Trends Biotechnol., 25: 250–253.Search in Google Scholar

Verma G., Arora J.S., Sethi R.S., Mukhopadhyay C.S., Verma R. (2015). Handmade cloning: recent advances, potential and pitfalls. J. Anim. Sci. Biotechnol., 6: 43.Search in Google Scholar

Wakayama T., Perry A.C., Zuccotti M., Johnson K.R., Yanagimachi R. (1998). Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature, 394: 369–374.Search in Google Scholar

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: 55–65.Search in Google Scholar

Wang M., Gao Y., Qu P., Qing S., Qiao F., Zhang Y., Mager J., Wang Y. (2017). Sperm-borne miR-449b influences cleavage, epigenetic reprogramming and apoptosis of SCNT embryos in bovine. Sci. Rep., 7: 13403.Search in Google Scholar

Wani N.A., Vettical B.S., Hong S.B. (2017). First cloned Bactrian camel (Camelus bactrianus) calf produced by interspecies somatic cell nuclear transfer: A step towards preserving the critically endangered wild Bactrian camels. PLoS One, 12 (5): e0177800.Search in Google Scholar

Wilmut I., Schnieke A.E., Mc Whir J., Kind A.J., Campbell K.H. (1997). Viable offspring derived from fetal and adult mammalian cells. Nature, 385: 810–813.Search in Google Scholar

Wongsrikeao P., Nagai T., Agung B., Taniguchi M., Kunishi M., Suto S., Otoi T. (2007). Improvement of transgenic cloning efficiencies by culturing recipient oocytes and donor cells with antioxidant vitamins in cattle. Mol. Reprod. Dev., 74: 694–702.Search in Google Scholar

Xu Y.N., Shen X.H., Lee S.E., Kwon J.S., Kim D.J., Heo Y.T., Cui X.S., Kim N.H. (2012). Autophagy influences maternal mRNA degradation and apoptosis in porcine parthenotes developing in vitro. J. Reprod. Dev., 58: 576–584.Search in Google Scholar

Yu M., Qiu Z.L., Li H., Zeng W.S., Chen L.N., Li Q.H., Quan S. (2011). Association between cell apoptosis and the quality of early mouse embryos. Nan Fang Yi Ke Da Xue Xue Bao, 31: 409–413.Search in Google Scholar

Yue Z., Jin S., Yang C., Levine A.J., Heintz N. (2003). Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc. Natl. Acad. Sci. USA., 100: 15077–15082.Search in Google Scholar

Zakhartchenko V., Mueller S., Alberio R., Schernthaner W., Stojkovic M., We-nigerkind H., Wanke R., Lassnig C., Mueller M., Wolf E., Brem G. (2001). Nuclear transfer in cattle with non-transfected and transfected fetal or cloned transgenic fetal and postnatal fibroblasts. Mol. Reprod. Dev., 60: 362–369.Search in Google Scholar

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. Cell. Reprogram., 19: 19–26.Search in Google Scholar

Zhang P., Liu P., Dou H., Chen L., Chen L., Lin L., Tan P., Vajta G., Gao J., Du Y., Ma R.Z. (2013). Handmade cloned transgenic sheep rich in omega-3 fatty acids. PLoS One, 8 (2): e55941.Search in Google Scholar

Zhang Y., Qu P., Ma X., Qiao F., Ma Y., Qing S., Zhang Y., Wang Y., Cui W. (2018). Tauroursodeoxycholic acid (TUDCA) alleviates endoplasmic reticulum stress of nuclear donor cells under serum starvation. PLoS One, 13 (5): e0196785.Search in Google Scholar

Recommended articles from Trend MD

Plan your remote conference with Sciendo