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Choosing a culture medium for SCNT and iSCNT reconstructed embryos: from domestic to wildlife species

  • Cordova, A. (Department of Biomedical Sciences, Ontario Veterinary College, University of Guelph) ;
  • King, W.A. (Department of Biomedical Sciences, Ontario Veterinary College, University of Guelph) ;
  • Mastromonaco, G.F. (Department of Biomedical Sciences, Ontario Veterinary College, University of Guelph)
  • Received : 2017.08.03
  • Accepted : 2017.10.23
  • Published : 2017.11.30

Abstract

Over the past decades, in vitro culture media have been developed to successfully support IVF embryo growth in a variety of species. Advanced reproductive technologies, such as somatic cell nuclear transfer (SCNT), challenge us with a new type of embryo, with special nutritional requirements and altered physiology under in vitro conditions. Numerous studies have successfully reconstructed cloned embryos of domestic animals for biomedical research and livestock production. However, studies evaluating suitable culture conditions for SCNT embryos in wildlife species are scarce (for both intra- and interspecies SCNT). Most of the existing studies derive from previous IVF work done in conventional domestic species. Extrapolation to non-domestic species presents significant challenges since we lack information on reproductive processes and embryo development in most wildlife species. Given the challenges in adapting culture media and conditions from IVF to SCNT embryos, developmental competence of SCNT embryos remains low. This review summarizes research efforts to tailor culture media to SCNT embryos and explore the different outcomes in diverse species. It will also consider how these culture media protocols have been extrapolated to wildlife species, most particularly using SCNT as a cutting-edge technical resource to assist in the preservation of endangered species.

Keywords

References

  1. Vajta G, Gjerris M. Science and technology of farm animal cloning: state of the art. Anim Reprod Sci. 2006;92(3-4):211-30. https://doi.org/10.1016/j.anireprosci.2005.12.001
  2. Dai Y, Vaught TD, Boone J, Chen SH, Phelps CJ, Ball S, et al. Targeted disruption of the alpha1,3-galactosyltransferase gene in cloned pigs. Nat Biotechnol. 2002;20(3):251-5. https://doi.org/10.1038/nbt0302-251
  3. Phelps CJ, Koike C, Vaught TD, Boone J, Wells KD, Chen SH, et al. Production of alpha 1,3-galactosyltransferase-deficient pigs. Science. 2003;299(5605):411-4. https://doi.org/10.1126/science.1078942
  4. Baldassarre H, Wang B, Keefer CL, Lazaris A, Karatzas CN. State of the art in the production of transgenic goats. Reprod Fertil Dev. 2004;16(4):465-70. https://doi.org/10.1071/RD04028
  5. Reggio BC, James AN, Green HL, Gavin WG, Behboodi E, Echelard Y, et al. Cloned transgenic offspring resulting from somatic cell nuclear transfer in the goat: oocytes derived from both follicle-stimulating hormone-stimulated and nonstimulated abattoir-derived ovaries. Biol Reprod. 2001;65(5):1528-33. https://doi.org/10.1095/biolreprod65.5.1528
  6. Zhang YL, Zhang GM, Wan YJ, Jia RX, Li PZ, Han L, et al. Identification of transgenic cloned dairy goats harboring human lactoferrin and methylation status of the imprinted gene IGF2R in their lungs. Genetics and molecular research : GMR. 2015;14(3):11099-108. https://doi.org/10.4238/2015.September.22.3
  7. Mastromonaco GF, Gonzalez-Grajales LA, Filice M, Comizzoli P. Somatic cells, stem cells, and induced pluripotent stem cells: how do they now contribute to conservation? Adv Exp Med Biol. 2014;753:385-427.
  8. Mastromonaco GF, King WA. Cloning in companion animal, non-domestic and endangered species: can the technology become a practical reality? Reprod Fertil Dev. 2007;19(6):748-61. https://doi.org/10.1071/RD07034
  9. Hill JR, Winger QA, Burghardt RC, Westhusin ME. Bovine nuclear transfer embryo development using cells derived from a cloned fetus. Anim Reprod Sci. 2001;67(1-2):17-26. https://doi.org/10.1016/S0378-4320(01)00106-3
  10. Polejaeva IA, Chen SH, Vaught TD, Page RL, Mullins J, Ball S, et al. Cloned pigs produced by nuclear transfer from adult somatic cells. Nature. 2000; 407(6800):86-90. https://doi.org/10.1038/35024082
  11. Keefer CL, Keyston R, Lazaris A, Bhatia B, Begin I, Bilodeau AS, et al. Production of cloned goats after nuclear transfer using adult somatic cells. Biol Reprod. 2002;66(1):199-203. https://doi.org/10.1095/biolreprod66.1.199
  12. Keefer CL, Baldassarre H, Keyston R, Wang B, Bhatia B, Bilodeau AS, et al. Generation of dwarf goat (Capra hircus) clones following nuclear transfer with transfected and nontransfected fetal fibroblasts and in vitro-matured oocytes. Biol Reprod. 2001;64(3):849-56. https://doi.org/10.1095/biolreprod64.3.849
  13. Wakayama T, Perry AC, Zuccotti M, Johnson KR, Yanagimachi R. Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature. 1998;394(6691):369-74. https://doi.org/10.1038/28615
  14. Shin T, Kraemer D, Pryor J, Liu L, Rugila J, Howe L, et al. A cat cloned by nuclear transplantation. Nature. 2002;415(6874):859. https://doi.org/10.1038/nature723
  15. Galli C, Lagutina I, Crotti G, Colleoni S, Turini P, Ponderato N, et al. Pregnancy: a cloned horse born to its dam twin. Nature. 2003;424(6949):635.
  16. Chesne P, Adenot PG, Viglietta C, Baratte M, Boulanger L, Renard JP. Cloned rabbits produced by nuclear transfer from adult somatic cells. Nat Biotechnol. 2002;20(4):366-9. https://doi.org/10.1038/nbt0402-366
  17. Zhou Q, Renard JP, Le Friec G, Brochard V, Beaujean N, Cherifi Y, et al. Generation of fertile cloned rats by regulating oocyte activation. Science. 2003;302(5648):1179. https://doi.org/10.1126/science.1088313
  18. Lee BC, Kim MK, Jang G, HJ O, Yuda F, Kim HJ, et al. Dogs cloned from adult somatic cells. Nature. 2005;436(7051):641. https://doi.org/10.1038/436641a
  19. Li Z, Sun X, Chen J, Liu X, Wisely SM, Zhou Q, et al. Cloned ferrets produced by somatic cell nuclear transfer. Dev Biol. 2006;293(2):439-48. https://doi.org/10.1016/j.ydbio.2006.02.016
  20. Amarnath D, Li X, Kato Y, Tsunoda Y. Gene expression in individual bovine somatic cell cloned embryos at the 8-cell and blastocyst stages of preimplantation development. J Reprod Dev. 2007;53(6):1247-63. https://doi.org/10.1262/jrd.19096
  21. Machaty Z, Day BN, Prather RS. Development of early porcine embryos in vitro and in vivo. Biol Reprod. 1998;59(2):451-5. https://doi.org/10.1095/biolreprod59.2.451
  22. Rizos D, Clemente M, Bermejo-Alvarez P, de La Fuente J, Lonergan P, Gutierrez-Adan A. Consequences of in vitro culture conditions on embryo development and quality. Reprod Domest Anim. 2008;43(Suppl 4):44-50. https://doi.org/10.1111/j.1439-0531.2008.01230.x
  23. Rizos D, Fair T, Papadopoulos S, Boland MP, Lonergan P. Developmental, qualitative, and ultrastructural differences between ovine and bovine embryos produced in vivo or in vitro. Mol Reprod Dev. 2002;62(3):320-7. https://doi.org/10.1002/mrd.10138
  24. Xiong XR, Wang LJ, Wang YS, Hua S, Zi XD, Zhang Y. Different preferences of IVF and SCNT bovine embryos for culture media. Zygote. 2014;22(1):1-9. https://doi.org/10.1017/S0967199412000184
  25. Miyoshi K, Rzucidlo SJ, Gibbons JR, Arat S, Stice SL. Development of porcine embryos reconstituted with somatic cells and enucleated metaphase I and II oocytes matured in a protein-free medium. BMC Dev Biol. 2001;1:12. https://doi.org/10.1186/1471-213X-1-12
  26. Beyhan Z, Iager AE, Cibelli JB. Interspecies nuclear transfer: implications for embryonic stem cell biology. Cell Stem Cell. 2007;1(5):502-12. https://doi.org/10.1016/j.stem.2007.10.009
  27. Seaby RP, Alexander B, King WA, Mastromonaco GF. In vitro development of bison embryos using interspecies somatic cell nuclear transfer. Reprod Domest Anim. 2013;48(6):881-7. https://doi.org/10.1111/rda.12180
  28. Kwon DK, Kang JT, Park SJ, Gomez MN, Kim SJ, Atikuzzaman M, et al. Blastocysts derived from adult fibroblasts of a rhesus monkey ( Macaca mulatta) using interspecies somatic cell nuclear transfer. Zygote. 2011;19(3):199-204. https://doi.org/10.1017/S0967199411000232
  29. Yamochi T, Kida Y, Oh N, Ohta S, Amano T, Anzai M, et al. Development of interspecies cloned embryos reconstructed with rabbit (Oryctolagus cuniculus) oocytes and cynomolgus monkey (Macaca fascicularis) fibroblast cell nuclei. Zygote. 2013;21(4):358-66. https://doi.org/10.1017/S0967199412000019
  30. Hua S, Zhang Y, Song K, Song J, Zhang Z, Zhang L, et al. Development of bovine-ovine interspecies cloned embryos and mitochondria segregation in blastomeres during preimplantation. Anim Reprod Sci. 2008;105(3-4):245-57. https://doi.org/10.1016/j.anireprosci.2007.03.002
  31. Sugawara A, Sugimura S, Hoshino Y, Sato E. Development and spindle formation in rat somatic cell nuclear transfer (SCNT) embryos in vitro using porcine recipient oocytes. Zygote. 2009;17(3):195-202. https://doi.org/10.1017/S0967199409005322
  32. Yao L, Wang P, Liu J, Chen J, Tang H, Sha H. Ooplast transfer of triploid pronucleus zygote improve reconstructed human-goat embryonic development. Int J Clin Exp Med. 2014;7(10):3678-86.
  33. White KL, Bunch TD, Mitalipov S, Reed WA. Establishment of pregnancy after the transfer of nuclear transfer embryos produced from the fusion of argali (Ovis ammon) nuclei into domestic sheep (Ovis aries) enucleated oocytes. Cloning. 1999;1(1):47-54. https://doi.org/10.1089/15204559950020085
  34. Lagutina I, Fulka H, Lazzari G, Galli C. Interspecies somatic cell nuclear transfer: advancements and problems. Cell Reprogram. 2013;15(5):374-84. https://doi.org/10.1089/cell.2013.0036
  35. Keefer CL. Artificial cloning of domestic animals. Proc Natl Acad Sci U S A. 2015;112(29):8874-8. https://doi.org/10.1073/pnas.1501718112
  36. Akagi S, Geshi M, Nagai T. Recent progress in bovine somatic cell nuclear transfer. Animal science journal = Nihon chikusan Gakkaiho. 2013;84(3):191-9. https://doi.org/10.2508/chikusan.84.191
  37. Iwamoto D, Yamagata K, Kishi M, Hayashi-Takanaka Y, Kimura H, Wakayama T, et al. Early development of cloned bovine embryos produced from oocytes enucleated by fluorescence metaphase II imaging using a conventional halogen-lamp microscope. Cell Reprogram. 2015;17(2):106-14. https://doi.org/10.1089/cell.2014.0086
  38. Hosseini SM, Hajian M, Moulavi F, Asgari V, Forouzanfar M, Nasr-Esfahani MH. Cloned sheep blastocysts derived from oocytes enucleated manually using a pulled pasteur pipette. Cell Reprogram. 2013;15(1):15-23. https://doi.org/10.1089/cell.2012.0033
  39. Kwong PJ, Abdullah RB, Wan Khadijah WE. Increasing glucose in KSOMaa basal medium on culture Day 2 improves in vitro development of cloned caprine blastocysts produced via intraspecies and interspecies somatic cell nuclear transfer. Theriogenology. 2012;78(4):921-9. https://doi.org/10.1016/j.theriogenology.2012.04.009
  40. Kishikawa H, Wakayama T, Yanagimachi R. Comparison of oocyte-activating agents for mouse cloning. Cloning. 1999;1(3):153-9. https://doi.org/10.1089/15204559950019915
  41. Hyun SH, Lee GS, Kim DY, Kim HS, Lee SH, Kim S, et al. Effect of maturation media and oocytes derived from sows or gilts on the development of cloned pig embryos. Theriogenology. 2003;59(7):1641-9. https://doi.org/10.1016/S0093-691X(02)01211-6
  42. Mallol A, Santalo J, Ibanez E. Improved development of somatic cell cloned mouse embryos by vitamin C and latrunculin A. PLoS One. 2015;10(3):e0120033. https://doi.org/10.1371/journal.pone.0120033
  43. Wakayama T, Yanagimachi R. Effect of cytokinesis inhibitors, DMSO and the timing of oocyte activation on mouse cloning using cumulus cell nuclei. Reproduction. 2001;122(1):49-60. https://doi.org/10.1530/rep.0.1220049
  44. Gurdon JB, Wilmut I. Nuclear transfer to eggs and oocytes. Cold Spring Harb Perspect Biol. 2011;3(6)
  45. Mason K, Liu Z, Aguirre-Lavin T, Beaujean N. Chromatin and epigenetic modifications during early mammalian development. Anim Reprod Sci. 2012;134(1-2):45-55. https://doi.org/10.1016/j.anireprosci.2012.08.010
  46. Wells DN, Misica PM, Day TA, Tervit HR. Production of cloned lambs from an established embryonic cell line: a comparison between in vivo- and in vitromatured cytoplasts. Biol Reprod. 1997;57(2):385-93. https://doi.org/10.1095/biolreprod57.2.385
  47. De Sousa PA, Dobrinsky JR, Zhu J, Archibald AL, Ainslie A, Bosma W, et al. Somatic cell nuclear transfer in the pig: control of pronuclear formation and integration with improved methods for activation and maintenance of pregnancy. Biol Reprod. 2002;66(3):642-50. https://doi.org/10.1095/biolreprod66.3.642
  48. Pandey A, Singh N, Gupta SC, Rana JS, Gupta N. Relative expression of cell growth regulatory genes insulin-like growth factors (IGF-1 and IGF-2) and their receptors (IGF-1R and IGF-2R) in somatic cell nuclear transferred (SCNT) and in vitro fertilized (IVF) pre-implantation buffalo embryos. Cell Biol Int. 2009;33(5):555-64. https://doi.org/10.1016/j.cellbi.2009.02.013
  49. Tang S, Liu J, Du S, Li LL, Zheng CY, Zhao MT, et al. Optimization of embryo culture conditions in the production of cloned goat embryos, following somatic cell nuclear transfer. Small Ruminant Research. 2011;96(1):64-9. https://doi.org/10.1016/j.smallrumres.2010.11.009
  50. Cui XS, Lee JY, Choi SH, Kwon MS, Kim T, Kim NH. Mouse granulocytemacrophage colony-stimulating factor enhances viability of porcine embryos in defined culture conditions. Anim Reprod Sci. 2004;84(1-2):169-77. https://doi.org/10.1016/j.anireprosci.2003.11.005
  51. Ju S, Rui R. Effects of cumulus cells on in vitro maturation of oocytes and development of cloned embryos in the pig. Reprod Domest Anim. 2012;47(4):521-9. https://doi.org/10.1111/j.1439-0531.2011.01912.x
  52. Kun Z, Shaohua W, Yufang M, Yankun L, Hengxi W, Xiuzhu S, et al. Effects of leptin supplementation in in vitro maturation medium on meiotic maturation of oocytes and preimplantation development of parthenogenetic and cloned embryos in pigs. Anim Reprod Sci. 2007;101(1-2):85-96. https://doi.org/10.1016/j.anireprosci.2006.08.021
  53. Nakano M, Kato Y, Tsunoda Y. Effect of melatonin treatment on the developmental potential of parthenogenetic and somatic cell nucleartransferred porcine oocytes in vitro. Zygote. 2012;20(2):199-207. https://doi.org/10.1017/S0967199411000190
  54. Lee S, Jin JX, Khoirinaya C, Kim GA, Lee BC. Lanosterol influences cytoplasmic maturation of pig oocytes in vitro and improves preimplantation development of cloned embryos. Theriogenology. 2016;85(4):575-84. https://doi.org/10.1016/j.theriogenology.2015.09.041
  55. Lee J, Park JI, Yun JI, Lee Y, Yong H, Lee ST, et al. Rapamycin treatment during in vitro maturation of oocytes improves embryonic development after parthenogenesis and somatic cell nuclear transfer in pigs. J Vet Sci. 2015;16(3):373-80. https://doi.org/10.4142/jvs.2015.16.3.373
  56. Lee J, Park JI, Lee GS, Choi JH, Lee ST, Park CK, et al. Colcemid treatment during oocyte maturation improves preimplantation development of cloned pig embryos by influencing meiotic progression and cytoplasmic maturation. Mol Reprod Dev. 2015;82(6):489-97. https://doi.org/10.1002/mrd.22498
  57. Su J, Wang Y, Zhang L, Wang B, Liu J, Luo Y, et al. Oocyte-secreted factors in oocyte maturation media enhance subsequent development of bovine cloned embryos. Mol Reprod Dev. 2014;81(4):341-9. https://doi.org/10.1002/mrd.22302
  58. Ha AN, Fakruzzaman M, Lee KL, Bang JI, Deb GK, Wang Z, et al. Effects of co-culture of cumulus oocyte complexes with denuded oocytes during in vitro maturation on the developmental competence of cloned bovine embryos. Reprod Domest Anim. 2015;50(2):292-8. https://doi.org/10.1111/rda.12487
  59. Kubota C, Yamakuchi H, Todoroki J, Mizoshita K, Tabara N, Barber M, et al. Six cloned calves produced from adult fibroblast cells after long-term culture. Proc Natl Acad Sci U S A. 2000;97(3):990-5. https://doi.org/10.1073/pnas.97.3.990
  60. Wilmut I, Schnieke AE, McWhir J, Kind AJ, Campbell KH. Viable offspring derived from fetal and adult mammalian cells. Nature. 1997;385(6619):810-3. https://doi.org/10.1038/385810a0
  61. Cibelli JB, Stice SL, Golueke PJ, Kane JJ, Jerry J, Blackwell C, et al. Cloned transgenic calves produced from nonquiescent fetal fibroblasts. Science. 1998;280(5367):1256-8. https://doi.org/10.1126/science.280.5367.1256
  62. Schnieke AE, Kind AJ, Ritchie WA, Mycock K, Scott AR, Ritchie M, et al. Human factor IX transgenic sheep produced by transfer of nuclei from transfected fetal fibroblasts. Science. 1997;278(5346):2130-3. https://doi.org/10.1126/science.278.5346.2130
  63. Kato Y, Tani T, Tsunoda Y. Cloning of calves from various somatic cell types of male and female adult, newborn and fetal cows. J Reprod Fertil. 2000;120(2):231-7. https://doi.org/10.1530/reprod/120.2.231
  64. HJ O, Kim MK, Jang G, Kim HJ, Hong SG, Park JE, et al. Cloning endangered gray wolves (Canis lupus) from somatic cells collected postmortem. Theriogenology. 2008;70(4):638-47. https://doi.org/10.1016/j.theriogenology.2008.04.032
  65. Cho JK, Lee BC, Park JI, Lim JM, Shin SJ, Kim KY, et al. Development of bovine oocytes reconstructed with different donor somatic cells with or without serum starvation. Theriogenology. 2002;57(7):1819-28. https://doi.org/10.1016/S0093-691X(01)00699-9
  66. Daniels R, Hall VJ, French AJ, Korfiatis NA, Trounson AO. Comparison of gene transcription in cloned bovine embryos produced by different nuclear transfer techniques. Mol Reprod Dev. 2001;60(3):281-8. https://doi.org/10.1002/mrd.1089
  67. Wells DN, Misica PM, Tervit HR. Production of cloned calves following nuclear transfer with cultured adult mural granulosa cells. Biol Reprod. 1999;60(4):996-1005. https://doi.org/10.1095/biolreprod60.4.996
  68. Zakhartchenko V, Alberio R, Stojkovic M, Prelle K, Schernthaner W, Stojkovic P, et al. Adult cloning in cattle: potential of nuclei from a permanent cell line and from primary cultures. Mol Reprod Dev. 1999;54(3):264-72. https://doi.org/10.1002/(SICI)1098-2795(199911)54:3<264::AID-MRD7>3.0.CO;2-Y
  69. Kues WA, Anger M, Carnwath JW, Paul D, Motlik J, Niemann H. Cell cycle synchronization of porcine fetal fibroblasts: effects of serum deprivation and reversible cell cycle inhibitors. Biol Reprod. 2000;62(2):412-9. https://doi.org/10.1095/biolreprod62.2.412
  70. Onishi A, Iwamoto M, Akita T, Mikawa S, Takeda K, Awata T, et al. Pig cloning by microinjection of fetal fibroblast nuclei. Science. 2000;289(5482):1188-90. https://doi.org/10.1126/science.289.5482.1188
  71. Ogura A, Inoue K, Ogonuki N, Noguchi A, Takano K, Nagano R, et al. Production of male cloned mice from fresh, cultured, and cryopreserved immature Sertoli cells. Biol Reprod. 2000;62(6):1579-84. https://doi.org/10.1095/biolreprod62.6.1579
  72. Enright BP, Kubota C, Yang X, Tian XC. Epigenetic characteristics and development of embryos cloned from donor cells treated by trichostatin A or 5-aza-2'-deoxycytidine. Biol Reprod. 2003;69(3):896-901. https://doi.org/10.1095/biolreprod.103.017954
  73. Hoshikawa Y, Kwon HJ, Yoshida M, Horinouchi S, Beppu T, Trichostatin A. induces morphological changes and gelsolin expression by inhibiting histone deacetylase in human carcinoma cell lines. Exp Cell Res. 1994;214(1):189-97. https://doi.org/10.1006/excr.1994.1248
  74. Huan YJ, Zhu J, Xie BT, Wang JY, Liu SC, Zhou Y, et al. Treating cloned embryos, but not donor cells, with 5-aza-2'-deoxycytidine enhances the developmental competence of porcine cloned embryos. J Reprod Dev. 2013;59(5):442-9. https://doi.org/10.1262/jrd.2013-026
  75. Jones KL, Hill J, Shin TY, Lui L, Westhusin MDNA. hypomethylation of karyoplasts for bovine nuclear transplantation. Mol Reprod Dev. 2001;60(2):208-13. https://doi.org/10.1002/mrd.1079
  76. Ding X, Wang Y, Zhang D, Wang Y, Guo Z, Zhang Y. Increased pre-implantation development of cloned bovine embryos treated with 5-aza-2'-deoxycytidine and trichostatin A. Theriogenology. 2008;70(4):622-30. https://doi.org/10.1016/j.theriogenology.2008.04.042
  77. JN Y, Xue CY, Wang XG, Lin F, Liu CY, FZ L, et al. 5-AZA-2'-deoxycytidine (5-AZA-CdR) leads to down-regulation of Dnmt1o and gene expression in preimplantation mouse embryos. Zygote. 2009;17(2):137-45. https://doi.org/10.1017/S0967199408005169
  78. McElroy SL, Kim JH, Kim S, Jeong YW, Lee EG, Park SM, et al. Effects of culture conditions and nuclear transfer protocols on blastocyst formation and mRNA expression in pre-implantation porcine embryos. Theriogenology. 2008;69(4):416-25. https://doi.org/10.1016/j.theriogenology.2007.10.010
  79. Jouneau A, Renard JP. Reprogramming in nuclear transfer. Curr Opin Genet Dev. 2003;13(5):486-91. https://doi.org/10.1016/j.gde.2003.08.007
  80. Chung YG, Mann MR, Bartolomei MS, Latham KE. Nuclear-cytoplasmic "tug of war" during cloning: effects of somatic cell nuclei on culture medium preferences of preimplantation cloned mouse embryos. Biol Reprod. 2002;66(4):1178-84. https://doi.org/10.1095/biolreprod66.4.1178
  81. Campbell KH, Loi P, Cappai P, Wilmut I. Improved development to blastocyst of ovine nuclear transfer embryos reconstructed during the presumptive Sphase of enucleated activated oocytes. Biol Reprod. 1994;50(6):1385-93. https://doi.org/10.1095/biolreprod50.6.1385
  82. Jeon HY, Jeong YW, Kim YW, Jeong YI, Hossein SM, Yang H, et al. Senescence is accelerated through donor cell specificity in cloned pigs. Int J Mol Med. 2012;30(2):383-91. https://doi.org/10.3892/ijmm.2012.1003
  83. Alexander B, Coppola G, Di Berardino D, Rho GJ, St John E, Betts DH, et al. The effect of 6-dimethylaminopurine (6-DMAP) and cycloheximide (CHX) on the development and chromosomal complement of sheep parthenogenetic and nuclear transfer embryos. Mol Reprod Dev. 2006;73(1):20-30. https://doi.org/10.1002/mrd.20372
  84. Mastromonaco GF, Semple E, Robert C, Rho GJ, Betts DH, King WA. Different culture media requirements of IVF and nuclear transfer bovine embryos. Reprod Domest Anim. 2004;39(6):462-7. https://doi.org/10.1111/j.1439-0531.2004.00548.x
  85. Lonergan P, Rizos D, Gutierrez-Adan A, Fair T, Boland MP. Effect of culture environment on embryo quality and gene expression - experience from animal studies. Reprod Biomed Online. 2003;7(6):657-63. https://doi.org/10.1016/S1472-6483(10)62088-3
  86. Shamsuddin M, Larsson B, Gustafsson H, Rodriguez-Martinez H. In vitro development up to hatching of bovine in vitro-matured and fertilized oocytes with or without support from somatic cells. Theriogenology. 1993;39(5):1067-79. https://doi.org/10.1016/0093-691X(93)90007-R
  87. Lim JM, Lee BC, Lee ES, Chung HM, Ko JJ, Park SE, et al. In vitro maturation and in vitro fertilization of bovine oocytes cultured in a chemically defined, protein-free medium: effects of carbohydrates and amino acids. Reprod Fertil Dev. 1999;11(2):127-32. https://doi.org/10.1071/RD99001
  88. Rosenkrans CF Jr, Zeng GQ, MC GT, Schoff PK, First NL. Development of bovine embryos in vitro as affected by energy substrates. Biol Reprod. 1993;49(3):459-62. https://doi.org/10.1095/biolreprod49.3.459
  89. George F, Daniaux C, Genicot G, Verhaeghe B, Lambert P, Donnay I. Set up of a serum-free culture system for bovine embryos: embryo development and quality before and after transient transfer. Theriogenology. 2008;69(5):612-23. https://doi.org/10.1016/j.theriogenology.2007.11.008
  90. Choi YH, Lee BC, Lim JM, Kang SK, Hwang WS. Optimization of culture medium for cloned bovine embryos and its influence on pregnancy and delivery outcome. Theriogenology. 2002;58(6):1187-97. https://doi.org/10.1016/S0093-691X(02)00946-9
  91. Kane MT, Headon DR. The role of commercial bovine serum albumin preparations in the culture of one-cell rabbit embryos to blastocysts. J Reprod Fertil. 1980;60(2):469-75. https://doi.org/10.1530/jrf.0.0600469
  92. Thompson JG, Gardner DK, Pugh PA, McMillan WH, Tervit HR. Lamb birth weight is affected by culture system utilized during in vitro pre-elongation development of ovine embryos. Biol Reprod. 1995;53(6):1385-91. https://doi.org/10.1095/biolreprod53.6.1385
  93. Lazzari G, Wrenzycki C, Herrmann D, Duchi R, Kruip T, Niemann H, et al. Cellular and molecular deviations in bovine in vitro-produced embryos are related to the large offspring syndrome. Biol Reprod. 2002;67(3):767-75. https://doi.org/10.1095/biolreprod.102.004481
  94. Lane M, Gardner DK, Hasler MJ, Hasler JF. Use of G1.2/G2.2 media for commercial bovine embryo culture: equivalent development and pregnancy rates compared to co-culture. Theriogenology. 2003;60(3):407-19. https://doi.org/10.1016/S0093-691X(03)00030-X
  95. Wang YS, Tang S, An ZX, Li WZ, Liu J, Quan FS, et al. Effect of mSOF and G1. 1/G2.2 media on the developmental competence of SCNT-derived bovine embryos. Reprod Domest Anim. 2011;46(3):404-9. https://doi.org/10.1111/j.1439-0531.2010.01679.x
  96. Srirattana K, Imsoonthornruksa S, Laowtammathron C, Sangmalee A, Tunwattana W, Thongprapai T, et al. Full-term development of gaur-bovine interspecies somatic cell nuclear transfer embryos: effect of trichostatin A treatment. Cell Reprogram. 2012;14(3):248-57. https://doi.org/10.1089/cell.2011.0099
  97. Lu F, Shi D, Wei J, Yang S, Wei Y. Development of embryos reconstructed by interspecies nuclear transfer of adult fibroblasts between buffalo (Bubalus bubalis) and cattle (Bos indicus). Theriogenology. 2005;64(6):1309-19. https://doi.org/10.1016/j.theriogenology.2005.03.005
  98. Kitiyanant Y, Saikhun J, Chaisalee B, White KL, Pavasuthipaisit K. Somatic cell cloning in Buffalo (Bubalus bubalis): effects of interspecies cytoplasmic recipients and activation procedures. Cloning Stem Cells. 2001;3(3):97-104. https://doi.org/10.1089/153623001753205052
  99. Saikhun J, Pavasuthipaisit K, Jaruansuwan M, Kitiyanant Y. Xenonuclear transplantation of buffalo (Bubalus bubalis) fetal and adult somatic cell nuclei into bovine (Bos indicus) oocyte cytoplasm and their subsequent development. Theriogenology. 2002;57(7):1829-37. https://doi.org/10.1016/S0093-691X(02)00667-2
  100. Sansinena MJ, Hylan D, Hebert K, Denniston RS, Godke RA. Banteng (Bos javanicus) embryos and pregnancies produced by interspecies nuclear transfer. Theriogenology. 2005;63(4):1081-91. https://doi.org/10.1016/j.theriogenology.2004.05.025
  101. Li Y, Li S, Dai Y, Du W, Zhao C, Wang L, et al. Nuclear reprogramming in embryos generated by the transfer of yak (Bos grunniens) nuclei into bovine oocytes and comparison with bovine-bovine SCNT and bovine IVF embryos. Theriogenology. 2007;67(8):1331-8. https://doi.org/10.1016/j.theriogenology.2006.10.022
  102. Srirattana K, Lorthongpanich C, Laowtammathron C, Imsoonthornruksa S, Ketudat-Cairns M, Phermthai T, et al. Effect of donor cell types on developmental potential of cattle (Bos taurus) and swamp buffalo (Bubalus bubalis) cloned embryos. J Reprod Dev. 2010;56(1):49-54. https://doi.org/10.1262/jrd.09-135A
  103. Li Q, Wang YS, Wang LJ, Zhang H, Li RZ, Cui CC, et al. Vitamin C supplementation enhances compact morulae formation but reduces the hatching blastocyst rate of bovine somatic cell nuclear transfer embryos. Cell Reprogram. 2014;16(4):290-7. https://doi.org/10.1089/cell.2013.0088
  104. Su J, Wang Y, Li W, Gao M, Ma Y, Hua S, et al. Effects of 3-hydroxyflavone on the cellular and molecular characteristics of bovine embryos produced by somatic-cell nuclear transfer. Mol Reprod Dev. 2014;81(3):257-69. https://doi.org/10.1002/mrd.22293
  105. Yoshioka K, Suzuki C, Itoh S, Kikuchi K, Iwamura S, Rodriguez-Martinez H. Production of piglets derived from in vitro-produced blastocysts fertilized and cultured in chemically defined media: effects of theophylline, adenosine, and cysteine during in vitro fertilization. Biol Reprod. 2003;69(6):2092-9. https://doi.org/10.1095/biolreprod.103.020081
  106. Ozawa M, Nagai T, Fahrudin M, Karja NW, Kaneko H, Noguchi J, et al. Addition of glutathione or thioredoxin to culture medium reduces intracellular redox status of porcine IVM/IVF embryos, resulting in improved development to the blastocyst stage. Mol Reprod Dev. 2006;73(8):998-1007. https://doi.org/10.1002/mrd.20533
  107. Redel BK, Spate LD, Lee K, Mao J, Whitworth KM, Prather RS. Glycine supplementation in vitro enhances porcine preimplantation embryo cell number and decreases apoptosis but does not lead to live births. Mol Reprod Dev. 2016;83(3):246-58. https://doi.org/10.1002/mrd.22618
  108. Betthauser J, Forsberg E, Augenstein M, Childs L, Eilertsen K, Enos J, et al. Production of cloned pigs from in vitro systems. Nat Biotechnol. 2000;18(10):1055-9. https://doi.org/10.1038/80242
  109. Im GS, Lai L, Liu Z, Hao Y, Wax D, Bonk A, et al. In vitro development of preimplantation porcine nuclear transfer embryos cultured in different media and gas atmospheres. Theriogenology. 2004;61(6):1125-35. https://doi.org/10.1016/j.theriogenology.2003.06.006
  110. Petters RM, Wells KD. Culture of pig embryos. J Reprod Fertil Suppl. 1993;48:61-73.
  111. Dobrinsky JR, Johnson LA, Rath D. Development of a culture medium (BECM-3) for porcine embryos: effects of bovine serum albumin and fetal bovine serum on embryo development. Biol Reprod. 1996;55(5):1069-74. https://doi.org/10.1095/biolreprod55.5.1069
  112. Yoshioka K, Suzuki C, Tanaka A, Anas IM, Iwamura S. Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol Reprod. 2002;66(1):112-9. https://doi.org/10.1095/biolreprod66.1.112
  113. Robl JM, Davis DL. Effects of serum on swine morulae and blastocysts in vitro. J Anim Sci. 1981;52(6):1450-6. https://doi.org/10.2527/jas1981.5261450x
  114. Pinyopummintr T, Bavister BD. In vitro-matured/in vitro-fertilized bovine oocytes can develop into morulae/blastocysts in chemically defined, protein-free culture media. Biol Reprod. 1991;45(5):736-42. https://doi.org/10.1095/biolreprod45.5.736
  115. Lee K, Redel BK, Spate L, Teson J, Brown AN, Park KW, et al. Piglets produced from cloned blastocysts cultured in vitro with GM-CSF. Mol Reprod Dev. 2013;80(2):145-54. https://doi.org/10.1002/mrd.22143
  116. Lee GS, Kim HS, Hyun SH, Jeon HY, Nam DH, Jeong YW, et al. Effect of epidermal growth factor in preimplantation development of porcine cloned embryos. Mol Reprod Dev. 2005;71(1):45-51. https://doi.org/10.1002/mrd.20098
  117. Ju S, Rui R, Lu Q, Lin P, Guo H. Analysis of apoptosis and methyltransferase mRNA expression in porcine cloned embryos cultured in vitro. J Assist Reprod Genet. 2010;27(1):49-59. https://doi.org/10.1007/s10815-009-9378-7
  118. Yamanaka K, Sugimura S, Wakai T, Kawahara M, Sato E. Difference in sensitivity to culture condition between in vitro fertilized and somatic cell nuclear transfer embryos in pigs. J Reprod Dev. 2009;55(3):299-304. https://doi.org/10.1262/jrd.20174
  119. Huang Y, Tang X, Xie W, Zhou Y, Li D, Zhou Y, et al. Vitamin C enhances in vitro and in vivo development of porcine somatic cell nuclear transfer embryos. Biochem Biophys Res Commun. 2011;411(2):397-401. https://doi.org/10.1016/j.bbrc.2011.06.160
  120. Lagutina I, Zakhartchenko V, Fulka H, Colleoni S, Wolf E, Fulka J Jr, et al. Formation of nucleoli in interspecies nuclear transfer embryos derived from bovine, porcine, and rabbit oocytes and nuclear donor cells of various species. Reproduction. 2011;141(4):453-65. https://doi.org/10.1530/REP-10-0266
  121. Sugimura S, Narita K, Yamashiro H, Sugawara A, Shoji T, Terashita Y, et al. Interspecies somatic cell nucleus transfer with porcine oocytes as recipients: A novel bioassay system for assessing the competence of canine somatic cells to develop into embryos. Theriogenology. 2009;72(4):549-59. https://doi.org/10.1016/j.theriogenology.2009.04.011
  122. Gupta MK, Das ZC, Heo YT, Joo JY, Chung HJ, Song H, et al. Transgenic chicken, mice, cattle, and pig embryos by somatic cell nuclear transfer into pig oocytes. Cell Reprogram. 2013;15(4):322-8.
  123. Lee E, Bhuiyan MM, Watanabe H, Matsuoka K, Fujise Y, Ishikawa H, et al. Production of cloned sei whale (Balaenoptera borealis) embryos by interspecies somatic cell nuclear transfer using enucleated pig oocytes. J Vet Sci. 2009;10(4):285-92. https://doi.org/10.4142/jvs.2009.10.4.285
  124. Dominko T, Ramalho-Santos J, Chan A, Moreno RD, Luetjens CM, Simerly C, et al. Optimization strategies for production of mammalian embryos by nuclear transfer. Cloning. 1999;1(3):143-52. https://doi.org/10.1089/15204559950019906
  125. Uhm SJ, Gupta MK, Kim T, Lee HT. Expression of enhanced green fluorescent protein in porcine- and bovine-cloned embryos following interspecies somatic cell nuclear transfer of fibroblasts transfected by retrovirus vector. Mol Reprod Dev. 2007;74(12):1538-47. https://doi.org/10.1002/mrd.20755
  126. Melican D, Butler R, Hawkins N, Chen LH, Hayden E, Destrempes M, et al. Effect of serum concentration, method of trypsinization and fusion/ activation utilizing transfected fetal cells to generate transgenic dairy goats by somatic cell nuclear transfer. Theriogenology. 2005;63(6):1549-63. https://doi.org/10.1016/j.theriogenology.2004.05.029
  127. Chen DY, Jiang MX, Zhao ZJ, Wang HL, Sun QY, Zhang LS, et al. Cloning of Asian yellow goat (C. hircus) by somatic cell nuclear transfer: telophase enucleation combined with whole cell intracytoplasmic injection. Mol Reprod Dev. 2007;74(1):28-34. https://doi.org/10.1002/mrd.20600
  128. Guo J, An Z, Li Y, Li X, Li Y, Guo Z, et al. Cloned goats (Capra hircus) from adult ear cells. Sci China C Life Sci. 2002;45(3):260-7. https://doi.org/10.1360/02yc9029
  129. Baguisi A, Behboodi E, Melican DT, Pollock JS, Destrempes MM, Cammuso C, et al. Production of goats by somatic cell nuclear transfer. Nat Biotechnol. 1999;17(5):456-61. https://doi.org/10.1038/8632
  130. Hosseini SM, Hajian M, Ostadhosseini S, Forouzanfar M, Abedi P, Jafarpour F, et al. Contrasting effects of G1.2/G2.2 and SOF1/SOF2 embryo culture media on pre- and post-implantation development of non-transgenic and transgenic cloned goat embryos. Reprod Biomed Online. 2015;31(3):372-83. https://doi.org/10.1016/j.rbmo.2015.06.008
  131. Willadsen SM. Nuclear transplantation in sheep embryos. Nature. 1986;320(6057):63-5. https://doi.org/10.1038/320063a0
  132. McLaughlin KJ, Davies L, Seamark RF. In vitro embryo culture in the production of identical merino lambs by nuclear transplantation. Reprod Fertil Dev. 1990;2(6):619-22. https://doi.org/10.1071/RD9900619
  133. Loi P, Boyazoglu S, Gallus M, Ledda S, Naitana S, Wilmut I, et al. Embryo cloning in sheep: work in progress. Theriogenology. 1997;48(1):1-10. https://doi.org/10.1016/S0093-691X(97)00187-8
  134. Smith LC, Wilmut I. Influence of nuclear and cytoplasmic activity on the development in vivo of sheep embryos after nuclear transplantation. Biol Reprod. 1989;40(5):1027-35. https://doi.org/10.1095/biolreprod40.5.1027
  135. Wilmut I, Beaujean N, de Sousa PA, Dinnyes A, King TJ, Paterson LA, et al. Somatic cell nuclear transfer. Nature. 2002;419(6907):583-6. https://doi.org/10.1038/nature01079
  136. Peng XR, Liu T, Zhang Y. Addition of alpha-tocopherol to culture medium improves the quality and cryosurvival of nuclear-transferred ovine embryos. J Reprod Dev. 2008;54(6):403-7. https://doi.org/10.1262/jrd.19188
  137. Wen BQ, Li J, Li JJ, Tian SJ, Sun SC, Qi X, et al. The histone deacetylase inhibitor Scriptaid improves in vitro developmental competence of ovine somatic cell nuclear transferred embryos. Theriogenology. 2014;81(2):332-9. https://doi.org/10.1016/j.theriogenology.2013.09.032
  138. Choi I, Zhu J, Campbell KH. The combined treatment of calcium ionophore with strontium improves the quality of ovine SCNT embryo development. Zygote. 2013;21(2):139-50. https://doi.org/10.1017/S0967199412000470
  139. Wang L, Peng T, Zhu H, Lv Z, Liu T, Shuai Z, et al. In vitro development of reconstructed ibex (Capra ibex) embryos by nuclear transfer using goat (Capra hircus) oocytes. Small Ruminant Research. 2007;73(1-3):135-41. https://doi.org/10.1016/j.smallrumres.2006.12.009
  140. Pan X, Zhang Y, Guo Z, Wang F. Development of interspecies nuclear transfer embryos reconstructed with argali (Ovis ammon) somatic cells and sheep ooplasm. Cell Biol Int. 2014;38(2):211-8. https://doi.org/10.1002/cbin.10191
  141. Heindryckx B, Rybouchkin A, Van Der Elst J, Dhont M. Effect of culture media on in vitro development of cloned mouse embryos. Cloning. 2001;3(2):41-50. https://doi.org/10.1089/15204550152475545
  142. Li L, Lu X, Dean J. The maternal to zygotic transition in mammals. Mol Aspects Med. 2013;34(5):919-38. https://doi.org/10.1016/j.mam.2013.01.003
  143. Dai X, Hao J, Zhou QA. modified culture method significantly improves the development of mouse somatic cell nuclear transfer embryos. Reproduction. 2009;138(2):301-8. https://doi.org/10.1530/REP-09-0069
  144. Salehi M, Kato Y, Tsunoda Y. Effect of melatonin treatment on developmental potential of somatic cell nuclear-transferred mouse oocytes in vitro. Zygote. 2014;22(2):213-7. https://doi.org/10.1017/S0967199413000336
  145. Reiter RJ, Tan DX, Osuna C, Gitto E. Actions of melatonin in the reduction of oxidative stress. A review. J Biomed Sci. 2000;7(6):444-58. https://doi.org/10.1007/BF02253360
  146. Mayo JC, Sainz RM, Antoli I, Herrera F, Martin V, Rodriguez C. Melatonin regulation of antioxidant enzyme gene expression. Cellular and molecular life sciences : CMLS. 2002;59(10):1706-13. https://doi.org/10.1007/PL00012498
  147. Li S, Chen X, Fang Z, Shi J, Sheng HZ. Rabbits generated from fibroblasts through nuclear transfer. Reproduction. 2006;131(6):1085-90. https://doi.org/10.1530/rep.1.01065
  148. Yang F, Hao R, Kessler B, Brem G, Wolf E, Zakhartchenko V. Rabbit somatic cell cloning: effects of donor cell type, histone acetylation status and chimeric embryo complementation. Reproduction. 2007;133(1):219-30. https://doi.org/10.1530/rep.1.01206
  149. Du F, Xu J, Zhang J, Gao S, Carter MG, He C, et al. Beneficial effect of young oocytes for rabbit somatic cell nuclear transfer. Cloning Stem Cells. 2009;11(1):131-40. https://doi.org/10.1089/clo.2008.0042
  150. Meng Q, Polgar Z, Liu J, Dinnyes A. Live birth of somatic cell-cloned rabbits following trichostatin A treatment and cotransfer of parthenogenetic embryos. Cloning Stem Cells. 2009;11(1):203-8. https://doi.org/10.1089/clo.2008.0072
  151. Tian J, Song J, Li H, Yang D, Li X, Ouyang H, et al. Effect of donor cell type on nuclear remodelling in rabbit somatic cell nuclear transfer embryos. Reprod Domest Anim. 2012;47(4):544-52. https://doi.org/10.1111/j.1439-0531.2011.01915.x
  152. Sugimoto H, Kida Y, Oh N, Kitada K, Matsumoto K, Saeki K, et al. Production of somatic cell nuclear transfer embryos using in vitro-grown and in vitromatured oocytes in rabbits. Zygote. 2015;23(4):494-500. https://doi.org/10.1017/S0967199414000082
  153. Zhou Q, Yang SH, Ding CH, He XC, Xie YH, Hildebrandt TB, et al. A comparative approach to somatic cell nuclear transfer in the rhesus monkey. Hum Reprod. 2006;21(10):2564-71. https://doi.org/10.1093/humrep/del216
  154. Lorthongpanich C, Laowtammathron C, Chan AW, Ketudat-Cairns M, Parnpai R. Development of interspecies cloned monkey embryos reconstructed with bovine enucleated oocytes. J Reprod Dev. 2008;54(5):306-13. https://doi.org/10.1262/jrd.20049
  155. Lee MT, Bonneau AR, Giraldez AJ. Zygotic genome activation during the maternal-to-zygotic transition. Annu Rev Cell Dev Biol. 2014;30:581-613. https://doi.org/10.1146/annurev-cellbio-100913-013027
  156. Zheng YL, Jiang MX, Zhang YL, Sun QY, Chen DY. Effects of oocyte age, cumulus cells and injection methods on in vitro development of intracytoplasmic sperm injection rabbit embryos. Zygote. 2004;12(1):75-80. https://doi.org/10.1017/S0967199404002643
  157. Simerly C, Navara C, Hyun SH, Lee BC, Kang SK, Capuano S, et al. Embryogenesis and blastocyst development after somatic cell nuclear transfer in nonhuman primates: overcoming defects caused by meiotic spindle extraction. Dev Biol. 2004;276(2):237-52. https://doi.org/10.1016/j.ydbio.2004.10.006
  158. Hong SG, Jang G, Kim MK, HJ O, Park JE, Kang JT, et al. Dogs cloned from fetal fibroblasts by nuclear transfer. Anim Reprod Sci. 2009;115(1-4):334-9. https://doi.org/10.1016/j.anireprosci.2008.12.005
  159. Jang G, Hong SG, HJ O, Kim MK, Park JE, Kim HJ, et al. A cloned toy poodle produced from somatic cells derived from an aged female dog. Theriogenology. 2008;69(5):556-63. https://doi.org/10.1016/j.theriogenology.2007.11.002
  160. Hong SG, HJ O, Park JE, Kim MJ, Kim GA, Koo OJ, et al. Production of transgenic canine embryos using interspecies somatic cell nuclear transfer. Zygote. 2012;20(1):67-72. https://doi.org/10.1017/S0967199410000651
  161. Kim DH, No JG, Choi MK, Yeom DH, Kim DK, Yang BC, et al. In vitro development of canine somatic cell nuclear transfer embryos in different culture media. J Vet Sci. 2015;16(2):233-5. https://doi.org/10.4142/jvs.2015.16.2.233
  162. Hwang I, Jeong YW, Kim JJ, Lee HJ, Kang M, Park KB, et al. Successful cloning of coyotes through interspecies somatic cell nuclear transfer using domestic dog oocytes. Reprod Fertil Dev. 2013;25(8):1142-8. https://doi.org/10.1071/RD12256
  163. Kim MK, Jang G, HJ O, Yuda F, Kim HJ, Hwang WS, et al. Endangered wolves cloned from adult somatic cells. Cloning Stem Cells. 2007;9(1):130-7. https://doi.org/10.1089/clo.2006.0034
  164. Yin XJ, Lee HS, Lee YH, Seo YI, Jeon SJ, Choi EG, et al. Cats cloned from fetal and adult somatic cells by nuclear transfer. Reproduction. 2005;129(2):245-9. https://doi.org/10.1530/rep.1.00403
  165. Gomez MC, Jenkins JA, Giraldo A, Harris RF, King A, Dresser BL, et al. Nuclear transfer of synchronized african wild cat somatic cells into enucleated domestic cat oocytes. Biol Reprod. 2003;69(3):1032-41. https://doi.org/10.1095/biolreprod.102.014449
  166. Skrzyszowska M, Katska L, Rynska B, Kania G, Smorag Z, Pienkowski M. In vitro developmental competence of domestic cat embryos after somatic cloning: a preliminary report. Theriogenology. 2002;58(8):1615-21. https://doi.org/10.1016/S0093-691X(02)01047-6
  167. Thongphakdee A, Numchaisrika P, Omsongkram S, Chatdarong K, Kamolnorranath S, Dumnui S, et al. In vitro development of marbled cat embryos derived from interspecies somatic cell nuclear transfer. Reprod Domest Anim. 2006;41(3):219-26. https://doi.org/10.1111/j.1439-0531.2005.00655.x
  168. Wen DC, Yang CX, Cheng Y, Li JS, Liu ZH, Sun QY, et al. Comparison of developmental capacity for intra- and interspecies cloned cat (Felis catus) embryos. Mol Reprod Dev. 2003;66(1):38-45. https://doi.org/10.1002/mrd.10333
  169. Moro LN, Hiriart MI, Buemo C, Jarazo J, Sestelo A, Veraguas D, et al. Cheetah interspecific SCNT followed by embryo aggregation improves in vitro development but not pluripotent gene expression. Reproduction. 2015;150(1):1-10. https://doi.org/10.1530/REP-15-0048
  170. Gomez MC, Pope CE, Kutner RH, Ricks DM, Lyons LA, Ruhe MT, et al. Generation of domestic transgenic cloned kittens using lentivirus vectors. Cloning Stem Cells. 2009;11(1):167-76. https://doi.org/10.1089/clo.2008.0054
  171. Yin XJ, Lee HS, XF Y, Kim LH, Shin HD, Cho SJ, et al. Production of secondgeneration cloned cats by somatic cell nuclear transfer. Theriogenology. 2008;69(8):1001-6. https://doi.org/10.1016/j.theriogenology.2008.01.017
  172. Young LE, Sinclair KD, Wilmut I. Large offspring syndrome in cattle and sheep. Rev Reprod. 1998;3(3):155-63. https://doi.org/10.1530/ror.0.0030155
  173. Bertolini M, Mason JB, Beam SW, Carneiro GF, Sween ML, Kominek DJ, et al. Morphology and morphometry of in vivo- and in vitro-produced bovine concepti from early pregnancy to term and association with high birth weights. Theriogenology. 2002;58(5):973-94. https://doi.org/10.1016/S0093-691X(02)00935-4
  174. Fernandez-Gonzalez R, Moreira P, Bilbao A, Jimenez A, Perez-Crespo M, Ramirez MA, et al. Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behavior. Proc Natl Acad Sci U S A. 2004;101(16):5880-5. https://doi.org/10.1073/pnas.0308560101
  175. Hill JR. Incidence of abnormal offspring from cloning and other assisted reproductive technologies. Annu Rev Anim Biosci. 2014;2:307-21. https://doi.org/10.1146/annurev-animal-022513-114109
  176. Lonergan P, Rizos D, Kanka J, Nemcova L, Mbaye AM, Kingston M, et al. Temporal sensitivity of bovine embryos to culture environment after fertilization and the implications for blastocyst quality. Reproduction. 2003;126(3):337-46. https://doi.org/10.1530/rep.0.1260337
  177. Heyman Y. Nuclear transfer: a new tool for reproductive biotechnology in cattle. Reprod Nutr Dev. 2005;45(3):353-61. https://doi.org/10.1051/rnd:2005026
  178. Constant F, Guillomot M, Heyman Y, Vignon X, Laigre P, Servely JL, et al. Large offspring or large placenta syndrome? Morphometric analysis of late gestation bovine placentomes from somatic nuclear transfer pregnancies complicated by hydrallantois. Biol Reprod. 2006;75(1):122-30. https://doi.org/10.1095/biolreprod.106.051581
  179. Yang CX, Han ZM, Wen DC, Sun QY, Zhang KY, Zhang LS, et al. In vitro development and mitochondrial fate of macaca-rabbit cloned embryos. Mol Reprod Dev. 2003;65(4):396-401. https://doi.org/10.1002/mrd.10320
  180. Zhao ZJ, Ouyang YC, Nan CL, Lei ZL, Song XF, Sun QY, et al. Rabbit oocyte cytoplasm supports development of nuclear transfer embryos derived from the somatic cells of the camel and Tibetan antelope. J Reprod Dev. 2006; 52(3):449-59. https://doi.org/10.1262/jrd.17095
  181. Sansinena MJ, Lynn J, Bondioli KR, Denniston RS, Godke RA. Ooplasm transfer and interspecies somatic cell nuclear transfer: heteroplasmy, pattern of mitochondrial migration and effect on embryo development. Zygote. 2011;19(2):147-56. https://doi.org/10.1017/S0967199410000419

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