Early Cell Specification in Mammalian Fertilized and Somatic Cell Nuclear Transfer Embryos

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Somatic Cell Nuclear Transfer Technology

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2647))

Abstract

Early cell specification in mammalian preimplantation embryos is an intricate cellular process that leads to coordinated spatial and temporal expression of specific genes. Proper segregation into the first two cell lineages, the inner cell mass (ICM) and the trophectoderm (TE), is imperative for develo** the embryo proper and the placenta, respectively. Somatic cell nuclear transfer (SCNT) allows the formation of a blastocyst containing both ICM and TE from a differentiated cell nucleus, which means that this differentiated genome must be reprogrammed to a totipotent state. Although blastocysts can be generated efficiently through SCNT, the full-term development of SCNT embryos is impaired mostly due to placental defects. In this review, we examine the early cell fate decisions in fertilized embryos and compare them to observations in SCNT-derived embryos, in order to understand if these processes are affected by SCNT and could be responsible for the low success of reproductive cloning.

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References

  1. Ma H, Morey R, O’Neil RC, He Y, Daughtry B, Schultz MD et al (2014) Abnormalities in human pluripotent cells due to reprogramming mechanisms. Nature 511:177–183

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Yang X, Smith SL, Tian XC, Lewin H, Renard J-P, Wakayama T (2007) Nuclear reprogramming of cloned embryos and its implications for therapeutic cloning. Nat Genet 39:295–302

    CAS  PubMed  Google Scholar 

  3. Heyman Y, Chavatte-Palmer P, LeBourhis D, Camous S, Vignon X, Renard JP (2002) Frequency and occurrence of late-gestation losses from cattle cloned embryos. Biol Reprod 66:6–13

    CAS  PubMed  Google Scholar 

  4. Palmieri C, Loi P, Ptak G, Della Salda L (2008) Review Paper: A review of the pathology of abnormal placentae of somatic cell nuclear transfer clone pregnancies in cattle, sheep, and mice. Vet Pathol 45:865–880

    CAS  PubMed  Google Scholar 

  5. Matoba S, Wang H, Jiang L, Lu F, Iwabuchi KA, Wu X et al (2018) Loss of H3K27me3 imprinting in somatic cell nuclear transfer embryos disrupts post-implantation development. Cell Stem Cell 23:343–354.e5

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Cockburn K, Rossant J (2010) Making the blastocyst: lessons from the mouse. J Clin Invest 120:995–1003

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Hillman N, Sherman MI, Graham C (1972) The effect of spatial arrangement on cell determination during mouse development. J Embryol Exp Morphol 28:263–278

    CAS  PubMed  Google Scholar 

  8. Garner W, McLaren A (1974) Cell distribution in chimaeric mouse embryos before implantation. J Embryol Exp Morphol 32:495–503

    CAS  PubMed  Google Scholar 

  9. Tabansky I, Lenarcic A, Draft RW, Loulier K, Keskin DB, Rosains J et al (2013) Developmental bias in cleavage-stage mouse blastomeres. Curr Biol 23:21–31

    CAS  PubMed  Google Scholar 

  10. Casser E, Israel S, Witten A, Schulte K, Schlatt S, Nordhoff V et al (2017) Totipotency segregates between the sister blastomeres of two-cell stage mouse embryos. Sci Rep 7:1–15

    CAS  Google Scholar 

  11. Johnson WH, Loskutoff NM, Plante Y, Betteridge KJ (1995) Production of four identical calves by the separation of blastomeres from an in vitro derived four-cell embryo. Vet Rec 137:15–16

    CAS  PubMed  Google Scholar 

  12. Willadsen SM (1980) The viability of early cleavage stages containing half the normal number of blastomeres in the sheep. J Reprod Fertil 59:357–362

    CAS  PubMed  Google Scholar 

  13. Boiani M, Casser E, Fuellen G, Christians ES (2019) Totipotency continuity from zygote to early blastomeres: a model under revision. Reproduction 158:R49–R65

    CAS  PubMed  Google Scholar 

  14. Stephenson RO, Rossant J, Tam PPL (2012) Intercellular interactions, position, and polarity in establishing blastocyst cell lineages and embryonic axes. Cold Spring Harb Perspect Biol 4:1–15

    Google Scholar 

  15. Sasaki H (2010) Mechanisms of trophectoderm fate specification in preimplantation mouse development. Develop Growth Differ 52:263–273

    CAS  Google Scholar 

  16. Plusa B, Frankenberg S, Chalmers A, Hadjantonakis A-K, Moore CA, Papalopulu N et al (2005) Downregulation of Par3 and aPKC function directs cells towards the ICM in the preimplantation mouse embryo. J Cell Sci 118:505–515

    CAS  PubMed  Google Scholar 

  17. Anani S, Bhat S, Honma-Yamanaka N, Krawchuk D, Yamanaka Y (2014) Initiation of Hippo signaling is linked to polarity rather than to cell position in the pre-implantation mouse embryo. Development 141:2813–2824

    CAS  PubMed  Google Scholar 

  18. Maître J-L, Turlier H, Illukkumbura R, Eismann B, Niwayama R, Nédélec F et al (2016) Asymmetric division of contractile domains couples cell positioning and fate specification. Nature 536:344–348

    PubMed  PubMed Central  Google Scholar 

  19. Korotkevich E, Niwayama R, Courtois A, Friese S, Berger N, Buchholz F et al (2017) The apical domain is required and sufficient for the first lineage segregation in the mouse embryo. Dev Cell 40:235–247.e7

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Hirate Y, Hirahara S, Inoue KI, Suzuki A, Alarcon VB, Akimoto K et al (2013) Polarity-dependent distribution of angiomotin localizes hippo signaling in preimplantation embryos. Curr Biol 23:1181–1194

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Yagi R, Kohn MJ, Karavanova I, Kaneko KJ, Vullhorst D, DePamphilis ML et al (2007) Transcription factor TEAD4 specifies the trophectoderm lineage at the beginning of mammalian development. Development 134:3827–3836

    CAS  PubMed  Google Scholar 

  22. Nishioka N, Yamamoto S, Kiyonari H, Sato H, Sawada A, Ota M et al (2008) Tead4 is required for specification of trophectoderm in pre-implantation mouse embryos. Mech Dev 125:270–283

    CAS  PubMed  Google Scholar 

  23. Nishioka N, Inoue KI, Adachi K, Kiyonari H, Ota M, Ralston A et al (2009) The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev Cell 16:398–410

    CAS  PubMed  Google Scholar 

  24. Chi F, Sharpley MS, Nagaraj R, Roy SS, Banerjee U (2020) Glycolysis-independent glucose metabolism distinguishes TE from ICM fate during mammalian embryogenesis. Dev Cell 53:9–26.e4

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Sakurai N, Takahashi K, Emura N, Hashizume T, Sawai K (2017) Effects of downregulating TEAD4 transcripts by RNA interference on early development of bovine embryos. J Reprod Dev 63:135–142

    CAS  PubMed  Google Scholar 

  26. Akizawa H, Kobayashi K, Bai H, Takahashi M, Kagawa S, Nagatomo H et al (2018) Reciprocal regulation of TEAD4 and CCN2 for the trophectoderm development of the bovine blastocyst. Reproduction 155:563–571

    CAS  PubMed  Google Scholar 

  27. Beck F, Erler T, Russell A, James R (1995) Expression of Cdx-2 in the mouse embryo and placenta: possible role in patterning of the extra-embryonic membranes. Dev Dyn 204:219–227

    CAS  PubMed  Google Scholar 

  28. Strumpf D, Mao CA, Yamanaka Y, Ralston A, Chawengsaksophak K, Beck F et al (2005) Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132:2093–2102

    CAS  PubMed  Google Scholar 

  29. Wu G, Gentile L, Fuchikami T, Sutter J, Psathaki K, Esteves TC et al (2010) Initiation of trophectoderm lineage specification in mouse embryos is independent of Cdx2. Development 137:4159–4169

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Goissis MD, Cibelli JB (2014) Functional characterization of CDX2 during bovine preimplantation development in vitro. Mol Reprod Dev 81:962–970

    CAS  PubMed  Google Scholar 

  31. Sakurai T, Bai H, Konno T, Ideta A, Aoyagi Y, Godkin JD et al (2010) Function of a transcription factor CDX2 beyond its trophectoderm lineage specification. Endocrinology 151:5873–5881

    CAS  PubMed  Google Scholar 

  32. Bou G, Liu S, Sun M, Zhu J, Xue B, Guo J et al (2017) CDX2 is essential for cell proliferation and polarity in porcine blastocysts. Development 144:1296–1306

    CAS  PubMed  Google Scholar 

  33. Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I et al (1998) Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95:379–391

    CAS  PubMed  Google Scholar 

  34. Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R (2003) Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 17:126–140

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S et al (2003) Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113:643–655

    CAS  PubMed  Google Scholar 

  36. Loh Y-H, Wu Q, Chew J-L, Vega VB, Zhang W, Chen X et al (2006) The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 38:431–440

    CAS  PubMed  Google Scholar 

  37. Chew J, Loh Y, Zhang W, Chen X, Tam W, Yeap L et al (2006) Reciprocal transcriptional regulation of complex in embryonic stem cells reciprocal transcriptional regulation of Pou5f1 and Sox2 via the Oct4/Sox2 complex in embryonic stem cells. Mol Cell Biol 25:6031–6046

    Google Scholar 

  38. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB et al (2008) Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133:1106–1117

    CAS  PubMed  Google Scholar 

  39. Niwa H, Toyooka Y, Shimosato D, Strumpf D, Takahashi K, Yagi R et al (2005) Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 123:917–929

    CAS  PubMed  Google Scholar 

  40. Chen AE, Egli D, Niakan K, Deng J, Akutsu H, Yamaki M et al (2009) Optimal timing of inner cell mass isolation increases the efficiency of human embryonic stem cell derivation and allows generation of sibling cell lines. Cell Stem Cell 4:103–106

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Cao S, Wang F, Chen Z, Liu Z, Mei C, Wu H et al (2009) Isolation and culture of primary bovine embryonic stem cell colonies by a novel method. J Exp Zool Part A Ecol Genet Physiol 311:368–376

    Google Scholar 

  42. Adjaye J, Huntriss J, Herwig R, BenKahla A, Brink TC, Wierling C et al (2005) Primary differentiation in the human blastocyst: comparative molecular portraits of inner cell mass and trophectoderm cells. Stem Cells 23:1514–1525

    CAS  PubMed  Google Scholar 

  43. Kuijk EW, Du Puy L, Van Tol HT, Oei CHY, Haagsman HP, Colenbrander B et al (2008) Differences in early lineage segregation between mammals. Dev Dyn 237:918–927

    CAS  PubMed  Google Scholar 

  44. Berg DK, Smith CS, Pearton DJ, Wells DN, Broadhurst R, Donnison M et al (2011) Trophectoderm lineage determination in cattle. Dev Cell 20:244–255

    CAS  PubMed  Google Scholar 

  45. Guo G, Huss M, Tong GQ, Wang C, Li Sun L, Clarke ND et al (2010) Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev Cell 18:675–685

    CAS  PubMed  Google Scholar 

  46. Wicklow E, Blij S, Frum T, Hirate Y, Lang R, Sasaki H et al (2014) HIPPO pathway members restrict SOX2 to the inner cell mass where it promotes ICM fates in the mouse blastocyst. PLoS Genet 10:e1004618

    PubMed  PubMed Central  Google Scholar 

  47. Frum T, Watts JL, Ralston A (2019) TEAD4, YAP1 and WWTR1 prevent the premature onset of pluripotency prior to the 16-cell stage. Development 146:dev179861. https://doi.org/10.1242/dev.179861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Goissis MD, Cibelli JB (2014) Functional characterization of SOX2 in bovine preimplantation embryos. Biol Reprod 90:30–30

    PubMed  Google Scholar 

  49. Plachta N, Bollenbach T, Pease S, Fraser SE, Pantazis P (2011) Oct4 kinetics predict cell lineage patterning in the early mammalian embryo. Nat Cell Biol 13:117–123

    CAS  PubMed  Google Scholar 

  50. Goolam M, Scialdone A, Graham SJL, Voet T, Marioni JC, Zernicka-goetz M et al (2016) Heterogeneity in Oct4 and Sox2 targets biases cell fate in 4-cell mouse embryos article heterogeneity in Oct4 and Sox2 targets biases cell fate in 4-cell mouse embryos. Cell 165:61–74

    CAS  PubMed  PubMed Central  Google Scholar 

  51. White MD, Angiolini JF, Alvarez YD, Kaur G, Zhao ZW, Mocskos E et al (2016) Long-lived binding of Sox2 to DNA predicts cell fate in the four-cell mouse embryo. Cell 165:75–87

    CAS  PubMed  Google Scholar 

  52. Waksmundzka M, Wiśniewska A, Maleszewski M (2006) Allocation of cells in mouse blastocyst is not determined by the order of cleavage of the first two blastomeres. Biol Reprod 75:582–587

    CAS  PubMed  Google Scholar 

  53. Kurotaki Y, Hatta K, Nakao K, Nabeshima YI, Fujimori T (2007) Blastocyst axis is specified independently of early cell lineage but aligns with the ZP shape. Science 316:719–723

    CAS  PubMed  Google Scholar 

  54. Sepulveda-Rincon LP, Dube D, Adenot P, Laffont L, Ruffini S, Gall L et al (2016) Random allocation of blastomere descendants to the trophectoderm and ICM of the bovine blastocyst. Biol Reprod 95:123–123

    PubMed  PubMed Central  Google Scholar 

  55. Beyer TA, Weiss A, Khomchuk Y, Huang K, Ogunjimi AA, Varelas X et al (2013) Switch enhancers interpret TGF-β and hippo signaling to control cell fate in human embryonic stem cells. Cell Rep 5:1611–1624

    CAS  PubMed  Google Scholar 

  56. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K et al (2003) The homeoprotein nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113:631–642

    CAS  PubMed  Google Scholar 

  57. Gardner RL, Rossant J (1979) Investigation of the fate of 4–5 day post-coitum mouse inner cell mass cells by blastocyst injection. J Embryol Exp Morphol 52:141–152

    CAS  PubMed  Google Scholar 

  58. Gardner RL (1982) Investigation of cell lineage and differentiation in the extraembryonic endoderm of the mouse embryo. J Embryol Exp Morphol 68:175–198

    CAS  PubMed  Google Scholar 

  59. Chazaud C, Yamanaka Y, Pawson T, Rossant J (2006) Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev Cell 10:615–624

    CAS  PubMed  Google Scholar 

  60. Plusa B, Piliszek A, Frankenberg S, Artus J, Hadjantonakis A-K (2008) Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst. Development 135:3081–3091

    CAS  PubMed  Google Scholar 

  61. Kang M, Piliszek A, Artus J, Hadjantonakis A-K (2013) FGF4 is required for lineage restriction and salt-and-pepper distribution of primitive endoderm factors but not their initial expression in the mouse. Development 140:267–279

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Arman E, Haffner-Krausz R, Chen Y, Heath JK, Lonai P (1998) Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc Natl Acad Sci U S A 95:5082–5087

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Yamanaka Y, Lanner F, Rossant J (2010) FGF signal-dependent segregation of primitive endoderm and epiblast in the mouse blastocyst. Development 137:715–724

    CAS  PubMed  Google Scholar 

  64. Frankenberg S, Gerbe F, Bessonnard S, Belville C, Pouchin P, Bardot O et al (2011) Primitive endoderm differentiates via a three-step mechanism involving Nanog and RTK signaling. Dev Cell 21:1005–1013

    CAS  PubMed  Google Scholar 

  65. Schrode N, Saiz N, Di Talia S, Hadjantonakis AK (2014) GATA6 levels modulate primitive endoderm cell fate choice and timing in the mouse blastocyst. Dev Cell 29:454–467. https://doi.org/10.1016/j.devcel.2014.04.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Bessonnard S, De Mot L, Gonze D, Barriol M, Dennis C, Goldbeter A et al (2014) Gata6, Nanog and Erk signaling control cell fate in the inner cell mass through a tristable regulatory network. Development 141:3637–3648

    CAS  PubMed  Google Scholar 

  67. Kuijk EW, van Tol LTA, van de Velde H, Wubbolts R, Welling M, Geijsen N et al (2012) The roles of FGF and MAP kinase signaling in the segregation of the epiblast and hypoblast cell lineages in bovine and human embryos. Development 139:871–882

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Canizo JR, Rivolta AEY, Echegaray CV, Suvá M, Alberio V, Aller JF et al (2019) A dose-dependent response to MEK inhibition determines hypoblast fate in bovine embryos. BMC Dev Biol 9:1–13

    Google Scholar 

  69. Ortega MS, Kelleher AM, O’Neil E, Benne J, Cecil R, Spencer TE (2020) NANOG is required to form the epiblast and maintain pluripotency in the bovine embryo. Mol Reprod Dev 87:152–160

    CAS  PubMed  Google Scholar 

  70. Atlasi Y, Stunnenberg HG (2017) The interplay of epigenetic marks during stem cell differentiation and development. Nat Rev Genet 18:643–658

    CAS  PubMed  Google Scholar 

  71. McLay DW, Clarke HJ (2003) Remodelling the paternal chromatin at fertilization in mammals. Reproduction 125:625–633

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Santos F, Dean W (2004) Epigenetic reprogramming during early development in mammals. Reproduction 127:643–651

    CAS  PubMed  Google Scholar 

  73. Saitou M, Kagiwada S, Kurimoto K (2012) Epigenetic reprogramming in mouse pre-implantation development and primordial germ cells. Development 139:15–31

    CAS  PubMed  Google Scholar 

  74. Santos F, Hendrich B, Reik W, Dean W (2002) Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol 241:172–182

    CAS  PubMed  Google Scholar 

  75. Nakanishi MO, Hayakawa K, Nakabayashi K, Hata K, Shiota K, Tanaka S (2012) Trophoblast-specific DNA methylation occurs after the segregation of the trophectoderm and inner cell mass in the mouse peri-implantation embryo. Epigenetics 7:173–182

    CAS  PubMed  Google Scholar 

  76. Gaspar-Maia A, Alajem A, Meshorer E, Ramalho-Santos M (2011) Open chromatin in pluripotency and reprogramming. Nat Rev Mol Cell Biol 12:36–47

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Beaujean N (2014) Histone post-translational modifications in preimplantation mouse embryos and their role in nuclear architecture. Mol Reprod Dev 81:100–112

    CAS  PubMed  Google Scholar 

  78. Liu H, Kim JM, Aoki F (2004) Regulation of histone H3 lysine 9 methylation in oocytes and early pre-implantation embryos. Development 131:2269–2280

    CAS  PubMed  Google Scholar 

  79. Lepikhov K, Walter J (2004) Differential dynamics of histone H3 methylation at positions K4 and K9 in the mouse zygote. BMC Dev Biol 4:2–6

    Google Scholar 

  80. Kourmouli N, Jeppesen P, Mahadevhaiah S, Burgoyne P, Wu R, Gilbert DM et al (2004) Heterochromatin and tri-methylated lysine 20 of histone H4 in animals. J Cell Sci 117:2491–2501

    CAS  PubMed  Google Scholar 

  81. Daujat S, Weiss T, Mohn F, Lange UC, Ziegler-Birling C, Zeissler U et al (2009) H3K64 trimethylation marks heterochromatin and is dynamically remodeled during developmental reprogramming. Nat Struct Mol Biol 16:777–781

    CAS  PubMed  Google Scholar 

  82. Wongtawan T, Taylor JE, Lawson KA, Wilmut I, Pennings S (2011) Histone H4K20me3 and HP1α are late heterochromatin markers in development, but present in undifferentiated embryonic stem cells. J Cell Sci 124:1878–1890

    CAS  PubMed  Google Scholar 

  83. Ahmed K, Dehghani H, Rugg-Gunn P, Fussner E, Rossant J, Bazett-Jones DP (2010) Global chromatin architecture reflects pluripotency and lineage commitment in the early mouse embryo. PLoS One 5:0010531

    Google Scholar 

  84. Liu X, Wang C, Liu W, Li J, Li C, Kou X et al (2016) Distinct features of H3K4me3 and H3K27me3 chromatin domains in pre-implantation embryos. Nature 537:558–562

    CAS  PubMed  Google Scholar 

  85. Erhardt S, Su IH, Schneider R, Barton S, Bannister AJ, Perez-Burgos L et al (2003) Consequences of the depletion of zygotic and embryonic enhancer of zeste 2 during preimplantation mouse development. Development 130:4235–4248

    CAS  PubMed  Google Scholar 

  86. Dahl JA, Reiner AH, Klungland A, Wakayama T, Collas P (2010) Histone H3 lysine 27 methylation asymmetry on developmentally-regulated promoters distinguish the first two lineages in mouse preimplantation embryos. PLoS One 5:0009150

    Google Scholar 

  87. VerMilyea MD, O’Neill LP, Turner BM (2009) Transcription-independent heritability of induced histone modifications in the mouse preimplantation embryo. PLoS One 4:e6086

    PubMed  PubMed Central  Google Scholar 

  88. Torres-Padilla ME, Parfitt DE, Kouzarides T, Zernicka-Goetz M (2007) Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 445:214–218

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Burton A, Muller J, Tu S, Padilla-Longoria P, Guccione E, Torres-Padilla ME (2013) Single-cell profiling of epigenetic modifiers identifies PRDM14 as an inducer of cell fate in the mammalian embryo. Cell Rep 5:687–701

    CAS  PubMed  Google Scholar 

  90. Payer B, Lee JT (2008) X chromosome dosage compensation: how mammals keep the balance. Annu Rev Genet 42:733–772

    CAS  PubMed  Google Scholar 

  91. Wutz A (2011) Gene silencing in X-chromosome inactivation: advances in understanding facultative heterochromatin formation. Nat Rev Genet 12:542–553

    CAS  PubMed  Google Scholar 

  92. Mak W, Nesterova TB, De Napoles M, Appanah R, Yamanaka S, Otte AP et al (2004) Reactivation of the paternal X chromosome in early mouse embryos. Science 303:666–669

    CAS  PubMed  Google Scholar 

  93. Silva J, Nichols J, Theunissen TW, Guo G, van Oosten AL, Barrandon O et al (2009) Nanog is the gateway to the pluripotent ground state. Cell 138:722–737

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Petropoulos S, Edsgärd D, Reinius B, Deng Q, Panula SP, Codeluppi S et al (2016) Single-cell RNA-Seq reveals lineage and X chromosome dynamics in human preimplantation embryos. Cell 165:1012–1026

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Vallot C, Patrat C, Collier AJ, Huret C, Casanova M, Liyakat Ali TM et al (2017) XACT noncoding RNA competes with XIST in the control of X chromosome activity during human early development. Cell Stem Cell 20:102–111

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Okamoto I, Patrat C, Thépot D, Peynot N, Fauque P, Daniel N et al (2011) Eutherian mammals use diverse strategies to initiate X-chromosome inactivation during development. Nature 472:370–374

    CAS  PubMed  Google Scholar 

  97. Ferreira AR, Machado GM, Diesel TO, Carvalho JO, Rumpf R, Melo EO et al (2010) Allele-specific expression of the MAOA gene and X chromosome inactivation in in vitro produced bovine embryos. Mol Reprod Dev 77:615–621

    CAS  PubMed  Google Scholar 

  98. Yu B, van Tol HTA, Stout TAE, Roelen BAJ (2020) Initiation of X chromosome inactivation during bovine embryo development. Cell 9:1016

    CAS  Google Scholar 

  99. Briggs R, King TJ (1952) Transplantation of living nuclei from blastula cells into enucleated frogs’ eggs. Proc Natl Acad Sci 38:455–463

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Gurdon JB, Melton DA (2008) Nuclear reprogramming in cells. Science 322:1811–1815

    CAS  PubMed  Google Scholar 

  101. Wilmut I, Schnieke AE, McWhir J, Kind AJ, Campbell KHS (1997) Viable offspring derived from fetal and adult mammalian cells. Nature 385:810–813

    CAS  PubMed  Google Scholar 

  102. Matoba S, Zhang Y (2018) Somatic cell nuclear transfer reprogramming: mechanisms and applications. Cell Stem Cell 23:471–485

    CAS  PubMed  PubMed Central  Google Scholar 

  103. Wakayama T, Tabar V, Rodriguez I, Perry ACF, Studer L, Mombaerts P (2001) Differentiation of embryonic stem cell lines generated from adult somatic cells by nuclear transfer. Science 292:740–743

    CAS  PubMed  Google Scholar 

  104. Tachibana M, Amato P, Sparman M, Gutierrez NM, Tippner-Hedges R, Ma H et al (2013) Human embryonic stem cells derived by somatic cell nuclear transfer. Cell 153:1228–1238

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Everts RE, Chavatte-Palmer P, Razzak A, Hue I, Green C, Oliveira R et al (2008) Aberrant gene expression patterns in placentomes are associated with phenotypically normal and abnormal cattle cloned by somatic cell nuclear transfer. Physiol Genomics 33:65–77

    CAS  PubMed  Google Scholar 

  106. Chavatte-Palmer P, Camous S, Jammes H, Le Cleac’h N, Guillomot M, RSF L (2012) Review: Placental perturbations induce the developmental abnormalities often observed in bovine somatic cell nuclear transfer. Placenta 33:S99–S104

    PubMed  Google Scholar 

  107. Ao Z, Liu D, Zhao C, Yue Z, Shi J, Zhou R et al (2017) Birth weight, umbilical and placental traits in relation to neonatal loss in cloned pigs. Placenta 57:94–101

    PubMed  Google Scholar 

  108. Loi P, Clinton M, Vackova I, Fulka J, Feil R, Palmieri C et al (2006) Placental abnormalities associated with post-natal mortality in sheep somatic cell clones. Theriogenology 65:1110–1121

    PubMed  Google Scholar 

  109. Tanaka S, Oda M, Toyoshima Y, Wakayama T, Tanaka M, Hattori N et al (2001) Placentomegaly in cloned mouse concepti caused by expansion of the spongiotrophoblast layer. Biol Reprod 65:1813–1821

    CAS  PubMed  Google Scholar 

  110. Lin J, Shi L, Zhang M, Yang H, Qin Y, Zhang J et al (2011) Defects in trophoblast cell lineage account for the impaired in vivo development of cloned embryos generated by somatic nuclear transfer. Cell Stem Cell 8:371–375

    CAS  PubMed  Google Scholar 

  111. Wang X, Qu J, Li J, He H, Liu Z, Huan Y (2020) Epigenetic reprogramming during somatic cell nuclear transfer: recent progress and future directions. Front Genet 11:1–13

    Google Scholar 

  112. Van Soom A, Ysebaert MT, De Kruif A (1997) Relationship between timing of development, morula morphology, and cell allocation to inner cell mass and trophectoderm in in vitro-produced bovine embryos. Mol Reprod Dev 47:47–56

    PubMed  Google Scholar 

  113. Leese HJ, Donnay I, Thompson JG (1998) Human assisted conception: a cautionary tale. Lessons from domestic animals. Hum Reprod 13:184–202

    PubMed  Google Scholar 

  114. Van Soom A, Boerjan M, Ysebaert MT, De Kruif A (1996) Cell allocation to the inner cell mass and the trophectoderm in bovine embryos cultured in two different media. Mol Reprod Dev 45:171–182

    PubMed  Google Scholar 

  115. Spielmann H, Jacob-Mueller U, Beckord W (1980) Immunosurgical studies on inner cell mass development in rat and mouse blastocysts before and during implantation in vitro. J Embryol Exp Morphol 60:255–269

    CAS  PubMed  Google Scholar 

  116. Iwasaki S, Yoshiba N, Ushijima H, Watanabe S, Nakahara T (1990) Morphology and proportion of inner cell mass of bovine blastocysts fertilized in vitro and in vivo. J Reprod Fertil 90:279–284

    CAS  PubMed  Google Scholar 

  117. Papaioannou VE, Ebert KM (1988) The preimplantation pig embryo: cell number and allocation to trophectoderm and inner cell mass of the blastocyst in vivo and in vitro. Development 102:793–803

    CAS  PubMed  Google Scholar 

  118. Koo D-B, Kang Y-K, Choi Y-H, Park JS, Kim H-N, Oh KB et al (2002) Aberrant allocations of inner cell mass and trophectoderm cells in bovine nuclear transfer blastocysts. Biol Reprod 67:487–492

    CAS  PubMed  Google Scholar 

  119. Ushijima H, Akiyama K, Tajima T (2008) Transition of cell numbers in bovine preimplantation embryos: in vivo collected and in vitro produced embryos. J Reprod Dev 54:239–243

    PubMed  Google Scholar 

  120. Boiani M, Eckardt S, Leu NA, Schöler HR, McLaughlin KJ (2003) Pluripotency deficit in clones overcome by clone-clone aggregation: epigenetic complementation? EMBO J 22:5304–5312

    CAS  PubMed  PubMed Central  Google Scholar 

  121. Misica-Turner PM, Oback FC, Eichenlaub M, Wells DN, Oback B (2007) Aggregating embryonic but not somatic nuclear transfer embryos increases cloning efficiency in cattle. Biol Reprod 76:268–278

    CAS  PubMed  Google Scholar 

  122. Akagi S, Yamaguchi D, Matsukawa K, Mizutani E, Hosoe M, Adachi N et al (2011) Developmental ability of somatic cell nuclear transferred embryos aggregated at the 8-cell stage or 16- to 32-cell stage in cattle. J Reprod Dev 57:500–506

    PubMed  Google Scholar 

  123. Bortvin A, Eggan K, Skaletsky H, Akutsu H, Berry DL, Yanagimachi R et al (2003) Incomplete reactivation of Oct4-related genes in mouse embryos cloned from somatic nuclei. Development 130:1673–1680

    CAS  PubMed  Google Scholar 

  124. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676

    CAS  PubMed  Google Scholar 

  125. Buganim Y, Faddah DA, Jaenisch R (2013) Mechanisms and models of somatic cell reprogramming. Nat Rev Genet 14:427–439

    CAS  PubMed  PubMed Central  Google Scholar 

  126. Wen D, Banaszynski LA, Liu Y, Geng F, Noh KM, **ang J et al (2014) Histone variant H3.3 is an essential maternal factor for oocyte reprogramming. Proc Natl Acad Sci U S A 111:7325–7330

    CAS  PubMed  PubMed Central  Google Scholar 

  127. Rodríguez-Alvarez L, Manriquez J, Velasquez A, Castro FO (2013) Constitutive expression of the embryonic stem cell marker OCT4 in bovine somatic donor cells influences blastocysts rate and quality after nucleus transfer. Vitr Cell Dev Biol Anim 49:657–667

    Google Scholar 

  128. Beyhan Z, Ross PJ, Iager AE, Kocabas AM, Cunniff K, Rosa GJ et al (2007) Transcriptional reprogramming of somatic cell nuclei during preimplantation development of cloned bovine embryos. Dev Biol 305:637–649

    CAS  PubMed  Google Scholar 

  129. Pfister-Genskow M, Myers C, Childs LA, Lacson JC, Patterson T, Betthauser JM et al (2005) Identification of differentially expressed genes in individual bovine preimplantation embryos produced by nuclear transfer: improper reprogramming of genes required for development. Biol Reprod 72:546–555

    CAS  PubMed  Google Scholar 

  130. Somers J, Smith C, Donnison M, Wells DN, Henderson H, McLeay L et al (2006) Gene expression profiling of individual bovine nuclear transfer blastocysts. Reproduction 131:1073–1084

    CAS  PubMed  Google Scholar 

  131. Min B, Cho S, Park JS, Lee YG, Kim N, Kang YK (2015) Transcriptomic features of bovine blastocysts derived by somatic cell nuclear transfer. G3 Genes, Genomes, Genet 5:2527–2538

    CAS  Google Scholar 

  132. Sood TJ, Lagah SV, Mukesh M, Singla SK, Chauhan MS, Manik RS et al (2019) RNA sequencing and transcriptome analysis of buffalo (Bubalus bubalis) blastocysts produced by somatic cell nuclear transfer and in vitro fertilization. Mol Reprod Dev 86:1149–1167

    CAS  PubMed  Google Scholar 

  133. Wuensch A, Habermann FA, Kurosaka S, Klose R, Zakhartchenko V, Reichenbach H-D et al (2007) Quantitative monitoring of pluripotency gene activation after somatic cloning in cattle. Biol Reprod 76:983–991

    CAS  PubMed  Google Scholar 

  134. Arnold DR, Bordignon V, Lefebvre R, Murphy BD, Smith LC (2006) Somatic cell nuclear transfer alters peri-implantation trophoblast differentiation in bovine embryos. Reproduction 132:279–290

    CAS  PubMed  Google Scholar 

  135. Rayon T, Menchero S, Rollán I, Ors I, Helness A, Crespo M et al (2016) Distinct mechanisms regulate Cdx2 expression in the blastocyst and in trophoblast stem cells. Sci Rep 6:1–10

    Google Scholar 

  136. Rayon T, Menchero S, Nieto A, Xenopoulos P, Crespo M, Cockburn K et al (2014) Notch and Hippo converge on Cdx2 to specify the trophectoderm lineage in the mouse blastocyst. Dev Cell 30:410–422

    CAS  PubMed  PubMed Central  Google Scholar 

  137. Fujii T, Moriyasu S, Hirayama H, Hashizume T, Sawai K (2010) Aberrant expression patterns of genes involved in segregation of inner cell mass and trophectoderm lineages in bovine embryos derived from somatic cell nuclear transfer. Cell Reprogram 12:617–625

    CAS  PubMed  Google Scholar 

  138. Wu X, Song M, Yang X, Liu X, Liu K, Jiao C et al (2016) Establishment of bovine embryonic stem cells after knockdown of CDX2. Sci Rep 6:1–12

    Google Scholar 

  139. Munsie MJ, Michalska AE, O’Brien CM, Trounson AO, Pera MF, Mountford PS (2000) Isolation of pluripotent embryonic stem cells from reprogrammed adult mouse somatic cell nuclei. Curr Biol 10:989–992

    CAS  PubMed  Google Scholar 

  140. Wakayama S, Ohta H, Kishigami S, Van Thuan N, Hikichi T, Mizutani E et al (2005) Establishment of male and female nuclear transfer embryonic stem cell lines from different mouse strains and tissues. Biol Reprod 72:932–936

    CAS  PubMed  Google Scholar 

  141. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VSS et al (1998) Embryonic stem cell lines derived from human blastocysts. Science 282:1145–1147

    CAS  PubMed  Google Scholar 

  142. Rielland M, Brochard V, Lacroix MC, Renard JP, Jouneau A (2009) Early alteration of the self-renewal/differentiation threshold in trophoblast stem cells derived from mouse embryos after nuclear transfer. Dev Biol 334:325–334

    CAS  PubMed  Google Scholar 

  143. Oda M, Tanaka S, Yamazaki Y, Ohta H, Iwatani M, Suzuki M et al (2009) Establishment of trophoblast stem cell lines from somatic cell nuclear-transferred embryos. Proc Natl Acad Sci U S A 106:16293–16297

    CAS  PubMed  PubMed Central  Google Scholar 

  144. Xue F, Tian XC, Du F, Kubota C, Taneja M, Dinnyes A et al (2002) Aberrant patterns of X chromosome inactivation in bovine clones. Nat Genet 31:216–220

    CAS  PubMed  Google Scholar 

  145. Williams LH, Kalantry S, Starmer J, Magnuson T (2011) Transcription precedes loss of **st coating and depletion of H3K27me3 during X-chromosome reprogramming in the mouse inner cell mass. Development 138:2049–2057

    CAS  PubMed  PubMed Central  Google Scholar 

  146. Muñoz M, Rodríguez A, De Frutos C, Caamaño JN, Díez C, Facal N et al (2008) Conventional pluripotency markers are unspecific for bovine embryonic-derived cell-lines. Theriogenology 69:1159–1164

    PubMed  Google Scholar 

  147. Simmet K, Zakhartchenko V, Philippou-Massier J, Blum H, Klymiuk N, Wolf E (2018) OCT4/POU5F1 is required for NANOG expression in bovine blastocysts. Proc Natl Acad Sci 115:2770–2775

    CAS  PubMed  PubMed Central  Google Scholar 

  148. Inoue K, Kohda T, Sugimoto M, Sado T, Ogonuki N, Matoba S et al (2010) Impeding **st expression from the active X chromosome improves mouse somatic cell nuclear transfer. Science 330:496–499

    CAS  PubMed  Google Scholar 

  149. Ruan D, Peng J, Wang X, Ouyang Z, Zou Q, Yang Y et al (2018) XIST derepression in active X chromosome hinders pig somatic cell nuclear transfer. Stem Cell Rep 10:494–508

    CAS  Google Scholar 

  150. Matoba S, Inoue K, Kohda T, Sugimoto M, Mizutani E, Ogonuki N et al (2011) RNAi-mediated knockdown of **st can rescue the impaired postimplantation development of cloned mouse embryos. Proc Natl Acad Sci 108:20621–20626

    CAS  PubMed  PubMed Central  Google Scholar 

  151. Alberto ML, Meirelles FV, Perecin F, Ambrósio CE, Favaron PO, Franciolli ALR et al (2012) Development of bovine embryos derived from reproductive techniques. Reprod Fertil Dev 25:907

    Google Scholar 

  152. Posfai E, Tam OH, Rossant J (2014) Mechanisms of pluripotency in vivo and in vitro, 1st edn. Elsevier Inc

    Google Scholar 

  153. Morgani S, Nichols J, Hadjantonakis AK (2017) The many faces of pluripotency: in vitro adaptations of a continuum of in vivo states. BMC Dev Biol 17:10–12

    Google Scholar 

  154. Daigneault BW, Rajput S, Smith GW, Ross PJ (2018) Embryonic POU5F1 is required for expanded bovine blastocyst formation. Sci Rep 8:7753

    PubMed  PubMed Central  Google Scholar 

  155. Fogarty NME, McCarthy A, Snijders KE, Powell BE, Kubikova N, Blakeley P et al (2017) Genome editing reveals a role for OCT4 in human embryogenesis. Nature 550:67–73

    CAS  PubMed  PubMed Central  Google Scholar 

  156. Tecirlioglu RT, Cooney MA, Lewis IM, Korfiatis NA, Hodgson R, Ruddock NT et al (2005) Comparison of two approaches to nuclear transfer in the bovine: hand-made cloning with modifications and the conventional nuclear transfer technique. Reprod Fertil Dev 17:573–585

    CAS  PubMed  Google Scholar 

  157. Li Y, Li S, Dai Y, Du W, Zhao C, Wang L et al (2007) 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 67:1331–1338

    CAS  PubMed  Google Scholar 

  158. Ross PJ, Rodriguez RM, Iager AE, Beyhan Z, Wang K, Ragina NP et al (2009) Activation of bovine somatic cell nuclear transfer embryos by PLCZ cRNA injection. Reproduction 137:427–437

    CAS  PubMed  Google Scholar 

  159. Song BS, Kim JS, Kim CH, Han YM, Lee DS, Lee KK et al (2009) Prostacyclin stimulates embryonic development via regulation of the cAMP response element-binding protein-cyclo-oxygenase-2 signalling pathway in cattle. Reprod Fertil Dev 21:400–407

    CAS  PubMed  Google Scholar 

  160. Cui X-S, Xu Y-N, Shen X-H, Zhang L-Q, Zhang J-B, Kim N-H (2011) Trichostatin A modulates apoptotic-related gene expression and improves embryo viability in cloned bovine embryos. Cell Reprogram 13:179–189

    CAS  PubMed  Google Scholar 

  161. Hua S, Zhang H, Su JM, Zhang T, Quan FS, Liu J et al (2011) Effects of the removal of cytoplasm on the development of early cloned bovine embryos. Anim Reprod Sci 126:37–44

    CAS  PubMed  Google Scholar 

  162. Su J, Wang Y, Li Y, Li R, Li Q, Wu Y et al (2011) Oxamflatin significantly improves nuclear reprogramming, blastocyst quality, and in vitro development of bovine SCNT embryos. PLoS One 6:0023805

    Google Scholar 

  163. Goissis MD, Suhr ST, Cibelli JB (2013) Effects of donor fibroblasts expressing OCT4 on bovine embryos generated by somatic cell nuclear transfer. Cell Reprogram 15:24–34

    CAS  PubMed  Google Scholar 

  164. Chen H, Zhang L, Guo Z, Wang Y, He R, Qin Y et al (2015) Improving the development of early bovine somatic-cell nuclear transfer embryos by treating adult donor cells with vitamin C. Mol Reprod Dev 82:867–879

    CAS  PubMed  Google Scholar 

  165. An Q, Peng W, Cheng Y, Lu Z, Zhou C, Zhang Y et al (2019) Melatonin supplementation during in vitro maturation of oocyte enhances subsequent development of bovine cloned embryos. J Cell Physiol 234:17370–17381

    CAS  PubMed  Google Scholar 

  166. Chang HY, **e RX, Zhang L, Fu LZ, Zhang CT, Chen HH et al (2019) Overexpression of miR-101-2 in donor cells improves the early development of Holstein cow somatic cell nuclear transfer embryos. J Dairy Sci 102:4662–4673

    CAS  PubMed  Google Scholar 

  167. Sah S, Sharma AK, Singla SK, Singh MK, Chauhan MS, Manik RS et al (2020) Effects of treatment with a microRNA mimic or inhibitor on the developmental competence, quality, epigenetic status and gene expression of buffalo (Bubalus bubalis) somatic cell nuclear transfer embryos. Reprod Fertil Dev 32:508–521

    CAS  PubMed  Google Scholar 

  168. Hai T, Hao J, Wang L, Jouneau A, Zhou Q (2011) Pluripotency maintenance in mouse somatic cell nuclear transfer embryos and its improvement by treatment with the histone deacetylase inhibitor TSA. Cell Reprogram 13:47–56

    CAS  PubMed  Google Scholar 

  169. Mizutani E, Torikai K, Wakayama S, Nagatomo H, Ohinata Y, Kishigami S et al (2016) Generation of cloned mice and nuclear transfer embryonic stem cell lines from urine-derived cells. Sci Rep 6:1–8

    Google Scholar 

  170. Kim G, Roy PK, Fang X, Hassan BMS, Cho J (2019) Improved preimplantation development of porcine somatic cell nuclear transfer embryos by caffeine treatment. J Vet Sci 20:1–12

    Google Scholar 

  171. Zhou Q, Yang SH, Ding CH, He XC, **e YH, Hildebrandt TB et al (2006) A comparative approach to somatic cell nuclear transfer in the rhesus monkey. Hum Reprod 21:2564–2571

    CAS  PubMed  Google Scholar 

  172. Iager AE, Ragina NP, Ross PJ, Beyhan Z, Cunniff K, Rodriguez RM et al (2008) Trichostatin A improves histone acetylation in bovine somatic cell nuclear transfer early embryos. Cloning Stem Cells 10:371–379

    CAS  PubMed  Google Scholar 

  173. Zhang J, Hao L, Wei Q, Zhang S, Cheng H, Zhai Y et al (2020) TET3 overexpression facilitates DNA reprogramming and early development of bovine SCNT embryos. Reproduction 160:379–391

    CAS  PubMed  Google Scholar 

  174. 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

    CAS  PubMed  Google Scholar 

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Acknowledgments

The Sao Paulo State Research Foundation (FAPESP 2017/09576-3) and the National Council of Science and Technology (CNPq 408634/2018-9) currently fund Marcelo D. Goissis.

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Goissis, M.D., Cibelli, J.B. (2023). Early Cell Specification in Mammalian Fertilized and Somatic Cell Nuclear Transfer Embryos. In: Moura, M.T. (eds) Somatic Cell Nuclear Transfer Technology . Methods in Molecular Biology, vol 2647. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-3064-8_3

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