Somatic Cell Nuclei in Cloning

Strangers Traveling in a Foreign Land
  • Keith E. Latham
  • Shaorong Gao
  • Zhiming Han
Part of the Advances in Experimental Medicine and Biology book series (volume 591)


The recent successes in producing cloned offspring by somatic cell nuclear transfer are nothing short of remarkable. This process requires the somatic cell chromatin to substitute functionally for both the egg and the sperm genomes, and indeed the processing of the transferred nuclei shares aspects in common with processing of both parental genomes in normal fertilized embryos. Recent studies have yielded new information about the degree to which this substitution is accomplished. Overall, it has become evident that multiple aspects of genome processing and function are aberrant, indicating that the somatic cell chromatin only infrequently manages the successful transition to a competent surrogate for gamete genomes. This review focuses on recent results revealing these limitations and how they might be overcome.


Nuclear Transfer Somatic Cell Nuclear Transfer Linker Histone Meiotic Spindle Oocyte Activation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. 1.
    King TJ, Briggs R. Changes in the nuclei of differentiating gastrula cells, as demonstrated by nuclear transplantation. Proc Natl Acad Sci USA 1955; 41:321–325.PubMedGoogle Scholar
  2. 2.
    Wilmut I, Schnieke AE, McWhir J et al. Viable offspring derived from fetal and adult mammalian cells. Nature 1997; 385:810–813.PubMedGoogle Scholar
  3. 3.
    Wakayama T, Perry ACF, Zuccotti M et al. Full-term development of mice from enucleated oo-cytes injected with cumulus cell nuclei. Nature 1998; 394:369–374.PubMedGoogle Scholar
  4. 4.
    Cibelli JB, Stice SL, Golueke PJ et al. Cloned transgenic calves produced from nonquiescent fetal fibroblasts. Science 1998; 280:1256–1258.PubMedGoogle Scholar
  5. 5.
    Baguisi A, Behboodi E, Melican DT et al. Production of goats by somatic cell nuclear transfer. Nat Biotechnol 1999; 17:456–641.PubMedGoogle Scholar
  6. 6.
    Kato Y, Tani T, Sotomura Y et al. Eight calves cloned from somatic cells of a single adult. Science 1998; 282:2095–2098.PubMedGoogle Scholar
  7. 7.
    Keefer CL, Keyston R, Lazaris A et al. Production of cloned goats after nuclear transfer using adult somatic cells. Biol Reprod 2002; 66:199–203.PubMedGoogle Scholar
  8. 8.
    Kubota C, Yamakuchi H, Todoroki J et al. Six cloned calves produced from adult fibroblast cells after long-term culture. Proc Natl Acad Sci USA 2000; 97:990–995.PubMedGoogle Scholar
  9. 9.
    Park KW, Kuhholzer B, Lai L et al. Development and expression of the green fluorescent protein in porcine embryos derived from nuclear transfer of transgenic granulosa-derived cells. Anim Reprod Sci 2001; 68:111–120.PubMedGoogle Scholar
  10. 10.
    Galli C, Lagutina I, Crotti G et al. Pregnancy: A cloned horse born to its dam twin. Nature 2003; 424:635.PubMedGoogle Scholar
  11. 11.
    Lee JW, Wu SC, Tian XC et al. Production of cloned pigs by whole-cell intracytoplasmic micro-injection. Biol Reprod 2003; 69:995–1001.PubMedGoogle Scholar
  12. 12.
    Shin T, Kraemer D, Pryor J et al. A cat cloned by nuclear transplantation. Nature 2002; 415:859.PubMedGoogle Scholar
  13. 13.
    Woods GL, White KL, Vanderwall DK et al. A mule cloned from fetal cells by nuclear transfer. Science 2003; 301:1063.PubMedGoogle Scholar
  14. 14.
    Yin XJ, Tani T, Yonemura I et al. Production of cloned pigs from adult somatic cells by chemically assisted removal of maternal chromosomes. Biol Reprod 2002; 67:442–446.PubMedGoogle Scholar
  15. 15.
    Kasinathan P, Knott JG, Wang Z et al. Production of calves from G1 fibroblasts. Nat Biotechnol 2001; 19:1176–1178.PubMedGoogle Scholar
  16. 16.
    Lee BC, Kim MK, Jang G et al. Dogs cloned from adult somatic cells. Nature 2005; 436:641.PubMedGoogle Scholar
  17. 17.
    Lee KY, Huang H, Ju B et al. Cloned zebrafish by nuclear transfer from long-term-cultured cells. Nat Biotechnol 2002; 20:795–799.PubMedGoogle Scholar
  18. 18.
    Rhind SM, Taylor JE, De Sousa PA et al. Human cloning: Can it be made safe? Nat Rev Genet 2003; 4:855–864.PubMedGoogle Scholar
  19. 19.
    Hochedlinger K, Jaenisch R. Monoclonal mice generated by nuclear transfer from mature B and T donor cells. Nature 2002; 415:1035–1038.PubMedGoogle Scholar
  20. 20.
    Sullivan EJ, Kasinathan S, Kasinathan P et al. Cloned calves from chromatin remodeled in vitro. Biol Reprod 2004; 70:146–153.PubMedGoogle Scholar
  21. 21.
    Enright BP, Sung LY, Chang CC et al. Methylation and acetylation characteristics of cloned bovine embryos from donor cells treated with 5-aza-2′-deoxycytidine. Biol Reprod 2005; 72:944–948.PubMedGoogle Scholar
  22. 22.
    Challah-Jacques M, Chesne P, Renard JP. Production of cloned rabbits by somatic nuclear transfer. Cloning Stem Cells 2003; 5:295–299.PubMedGoogle Scholar
  23. 23.
    Campbell KH, Alberio R. Reprogramming the genome: Role of the cell cycle. Reprod Suppl 2003; 61:477–494.PubMedGoogle Scholar
  24. 24.
    Wakayama T, Yanagimachi R. Effect of cytokinesis inhibitors, DMSO and the timing of oocyte activation on mouse cloning using cumulus cell nuclei. Reproduction 2001; 122:49–60.PubMedGoogle Scholar
  25. 25.
    Wakayama T, Yanagimachi R. Mouse cloning with nucleus donor cells of different age and type. Mol Reprod Dev 2001; 58:376–383.PubMedGoogle Scholar
  26. 26.
    Wakayama T, Yanagimachi R. Cloning the laboratory mouse. Semin Cell Dev Biol 1999; 10:253–258.PubMedGoogle Scholar
  27. 27.
    Chung YG, Mann MR, Bartolomei MS et al. Nuclear-cytoplasmic ‘tug-of war’ during cloning: Effects of somatic cell nuclei on culture medium preferences in the preimplantation cloned mouse embryo. Biol Reprod 2002; 66:1178–1184.PubMedGoogle Scholar
  28. 28.
    Gao S, Chung YG, Williams JW et al. Somatic cell-like features of cloned mouse embryos prepared with cultured myoblast nuclei. Biol Reprod 2003; 69:48–56.PubMedGoogle Scholar
  29. 29.
    Gao S, Czirr E, Chung YG et al. Genetic variation in oocyte phenotype revealed through parthenogenesis and cloning: Correlation with differences in pronuclear epigenetic modification. Biol Reprod 2004; 70:1162–1170.PubMedGoogle Scholar
  30. 30.
    Heindryckx B, Rybouchkin A, Van Der Elst J et al. Effect of culture media on in vitro development of cloned mouse embryos. Cloning Stem Cells 2001; 3:41–50.Google Scholar
  31. 31.
    Hoshino Y, Uchida M, Shimatsu Y et al. Developmental competence of somatic cell nuclear transfer embryos reconstructed from oocytes matured in vitro with follicle shells in miniature pig. Cloning Stem Cells 2005; 7:17–26.PubMedGoogle Scholar
  32. 32.
    Mastromonaco GF, Semple E, Robert C et al. Different culture media requirements of IVF and nuclear transfer bovine embryos. Reprod Domest Anim 2004; 39:462–467.PubMedGoogle Scholar
  33. 33.
    Gasparrini B, Gao S, Ainslie A et al. Cloned mice derived from embryonic stem cell karyoplasts and activated cytoplasts prepared by induced enucleation. Biol Reprod 2003; 68:1259–1266.PubMedGoogle Scholar
  34. 34.
    Ibanez E, Albertini DF, Overstrom EW. Demecolcine-induced oocyte enucleation for somatic cell cloning: Coordination between cell-cycle egress, kinetics of cortical cytoskeletal interactions, and second polar body extrusion. Biol Reprod 2003; 68:1249–1258.PubMedGoogle Scholar
  35. 35.
    Tateno H, Latham KE, Yanagimachi R. Reproductive semi-cloning respecting biparental origin. A biologically unsound principle. Hum Reprod 2003; 18:472–473.PubMedGoogle Scholar
  36. 36.
    Tateno H, Akutsu H, Kamiguchi Y et al. Inability of mature oocytes to create functional haploid genomes from somatic cell nuclei. Fertil Steril 2003; 79:216–218.PubMedGoogle Scholar
  37. 37.
    Latham KE, Schultz RM. Embryonic genome activation. Front Biosci 2001; 6:D748–759.PubMedGoogle Scholar
  38. 38.
    Latham KE. Mechanisms and control of embryonic genome activation in mammalian embryos. Int Rev Cytol 1999; 193:71–124.PubMedGoogle Scholar
  39. 39.
    Santos F, Peters AH, Otte AP et al. Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Dev Biol 2005; 280:225–236.PubMedGoogle Scholar
  40. 40.
    Santos F, Hendrich B, Reik W et al. Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol 2002; 241:172–182.PubMedGoogle Scholar
  41. 41.
    Aoki F, Worrad DM, Schultz RM. Regulation of transcriptional activity during the first and second cell cycles in the preimplantation mouse embryo. Dev Biol 1997; 181:296–307.PubMedGoogle Scholar
  42. 42.
    Santos F, Zakhartchenko V, Stojkovic M et al. Epigenetic marking correlates with developmental potential in cloned bovine preimplantation embryos. Curr Biol 2003; 13:1116–1121.PubMedGoogle Scholar
  43. 43.
    Beaujean N, Taylor J, Gardner J et al. Effect of limited DNA methylation reprogramming in the normal sheep embryo on somatic cell nuclear transfer. Biol Reprod 2004; 71:185–193.PubMedGoogle Scholar
  44. 44.
    Ozil JP, Markoulaki S, Toth S et al. Egg activation events are regulated by the duration of a sustained [Ca2+]cyt signal in the mouse. Dev Biol 2005; 282(1):39–54.PubMedGoogle Scholar
  45. 45.
    Gao S, Chung YG, Parseghian MH et al. Rapid H1 linker histone transitions following fertilization or somatic cell nuclear transfer: Evidence for a uniform developmental program in mice. Dev Biol 2004; 266:62–75.PubMedGoogle Scholar
  46. 46.
    Peaston AE, Evsikov AV, Graber JH et al. Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos. Dev Cell 2004; 7:597–606.PubMedGoogle Scholar
  47. 47.
    Evsikov AV, de Vries WN, Peaston AE et al. Systems biology of the 2-cell mouse embryo. Cytogenet Genome Res 2004; 105:240–250.PubMedGoogle Scholar
  48. 48.
    Zeng F, Baldwin DA, Schultz RM. Transcript profiling during preimplantation mouse development. Dev Biol 2004; 272:483–496.PubMedGoogle Scholar
  49. 49.
    Latham KE, Garrels JI, Chang C et al. Quantitative analysis of protein synthesis in mouse embryos. I. Extensive reprogramming at the one-and two-cell stages. Development 1991; 112:921–932.PubMedGoogle Scholar
  50. 50.
    Gao S, Han Z, Kihara M et al. Protease inhibitor MG132 in cloning: No end to the nightmare. Trends Biotechnol 2005; 23:66–68.PubMedGoogle Scholar
  51. 51.
    Becker M, Becker A, Miyara F et al. Differential in vivo binding dynamics of somatic and oocyte-specific linker histones in oocytes and during ES cell nuclear transfer. Mol Biol Cell 2005; 16:3887–3895.PubMedGoogle Scholar
  52. 52.
    Sampath SC, Ohi R, Leismann O. The chromosomal passenger complex is required for chromatin-induced microtubule stabilization and spindle assembly. Cell 2004; 118:187–202.PubMedGoogle Scholar
  53. 53.
    Can A, Semiz O, Cinar O. Centrosome and microtubule dynamics during early stages of meiosis in mouse oocytes. Mol Hum Reprod 2003; 9:749–756.PubMedGoogle Scholar
  54. 54.
    Carazo-Salas RE, Karsenti E. Long-range communication between chromatin and microtubules in Xenopus egg extracts. Curr Biol 2003; 13:1728–1733.PubMedGoogle Scholar
  55. 55.
    Kalitsis P, Fowler KJ, Earle E et al. Partially functional Cenpa-GFP fusion protein causes increased chromosome missegregation and apoptosis during mouse embryogenesis. Chromosome Re 2003; 11:345–357.Google Scholar
  56. 56.
    Askjaer P, Galy V, Hannak E et al. Ran GTPase cycle and importins alpha and beta are essential for spindle formation and nuclear envelope assembly in living Caenorhabditis elegans embryos. Mol Biol Cell 2002; 13:4355–4370.PubMedGoogle Scholar
  57. 57.
    Bilbao-Cortes D, Hetzer M, Langst G et al. Ran binds to chromatin by two distinct mechanisms. Curr Biol 2002; 12:1151–1156.PubMedGoogle Scholar
  58. 58.
    Hetzer M, Gruss OJ, Mattaj IW. The Ran GTPase as a marker of chromosome position in spindle formation and nuclear envelope assembly. Nat Cell Biol 2002; 4:E177–184.PubMedGoogle Scholar
  59. 59.
    Kim BK, Lee YJ, Cui XS et al. Chromatin and microtubule organisation in maturing and preactivated porcine oocytes following intracytoplasmic sperm injection. Zygote 2002; 10:123–129.PubMedGoogle Scholar
  60. 60.
    Combelles CM, Albertini DF. Microtubule patterning during meiotic maturation in mouse oocytes is determined by cell cycle-specific sorting and redistribution of gamma-tubulin. Dev Biol 2001; 239:281–294.PubMedGoogle Scholar
  61. 61.
    Jones MH, He X, Giddings TH et al. Yeast Dam1p has a role at the kinetochore in assembly of the mitotic spindle. Proc Natl Acad Sci USA 2001; 98:13675–13680.PubMedGoogle Scholar
  62. 62.
    Nachury MV, Maresca TJ, Salmon WC et al. Importin beta is a mitotic target of the small GTPase Ran in spindle assembly. Cell 2001; 104:95–106.PubMedGoogle Scholar
  63. 63.
    Gruss OJ, Carazo-Salas RE, Schatz CA et al. Ran induces spindle assembly by reversing the inhibitory effect of importin alpha on TPX2 activity. Cell 2001; 104:83–93.PubMedGoogle Scholar
  64. 64.
    Carazo-Salas RE, Guarguaglini G, Gruss OJ et al. Generation of GTP-bound Ran by RCC1 is required for chromatin-induced mitotic spindle formation. Nature 1999; 400:178–181.PubMedGoogle Scholar
  65. 65.
    Cutts SM, Fowler KJ, Kile BT et al. Defective chromosome segregation, microtubule bundling and nuclear bridging in inner centromere protein gene (Incenp)-disrupted mice. Hum Mol Genet 1999; 8:1145–1155.PubMedGoogle Scholar
  66. 66.
    Williams BC, Murphy TD, Goldberg ML et al. Neocentromere activity of structurally acentric mini-chromosomes in Drosophila. Nat Genet 1998; 18:30–37.PubMedGoogle Scholar
  67. 67.
    Heald R, Tournebize R, Blank T et al. Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 1996; 382:420–425.PubMedGoogle Scholar
  68. 68.
    Brunet S, Polanski Z, Verlhac MH et al. Bipolar meiotic spindle formation without chromatin. Curr Biol 1998; 8:1231–1234.PubMedGoogle Scholar
  69. 69.
    Woods LM, Hodges CA, Baart E et al. Chromosomal influence on meiotic spindle assembly: Abnormal meiosis I in female Mlhl mutant mice. J Cell Biol 1999; 145:1395–1406.PubMedGoogle Scholar
  70. 70.
    Yarm FR. Plk phosphorylation regulates the microtubule-stabilizing protein TCTP. Mol Cell Biol 2002; 22:6209–6221.PubMedGoogle Scholar
  71. 71.
    Craig R, Norbury C. The novel murine calmodulin-binding protein Sha1 disrupts mitotic spindle and replication checkpoint functions in fission yeast. J Cell Sci 1998; 111:3609–3619.PubMedGoogle Scholar
  72. 72.
    Simerly C, Dominko T, Navara C et al. Molecular correlates of primate nuclear transfer failures. Science 2003; 300:297.PubMedGoogle Scholar
  73. 73.
    Simerly C, Navara C, Hwan Hyun 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; 276:237–252.PubMedGoogle Scholar
  74. 74.
    Miyara F, Han Z, Gao S et al. Nonequivalence of embryonic and somatic cell nuclei affecting spindle composition in clones. Dev Biol 2006; 289:206–217.PubMedGoogle Scholar
  75. 75.
    Baharvand H, Matthaei KI. The ultrastructure of mouse embryonic stem cells. Reprod Biomed Online 2003; 7:330–335.PubMedGoogle Scholar
  76. 76.
    Sathananthan H, Pera M, Trounson A. The fine structure of human embryonic stem cells. Reprod Biomed Online 2002; 4:56–61.PubMedGoogle Scholar
  77. 77.
    Chung YG, Ratnam S, Chaillet JR et al. Abnormal regulation of DNA methyltransferase expression in cloned mouse embryos. Biol Reprod 2003; 69:146–153.PubMedGoogle Scholar
  78. 78.
    Latham KE. Early and delayed aspects of nuclear reprogramming during cloning. Biol Cell 2005; 97:119–132.PubMedGoogle Scholar
  79. 79.
    Kang YK, Koo DB, Park JS et al. Influence of oocyte nuclei on demethylation of donor genome in cloned bovine embryos. FEBS Let 2001; 499:55–58.Google Scholar
  80. 80.
    Nolen LD, Gao S, Han Z et al. X chromosome reactivation and regulation in cloned embryos. Dev Biol 2005; 279:525–540.PubMedGoogle Scholar
  81. 81.
    Shi W, Dirim F, Wolf E et al. Methylation reprogramming and chromosomal aneuploidy in in vivo fertilized and cloned rabbit preimplantation embryos. Biol Reprod 2004; 71:340–347.PubMedGoogle Scholar
  82. 82.
    Booth PJ, Viuff D, Tan S et al. Numerical chromosome errors in day 7 somatic nuclear transfer bovine blastocysts. Biol Reprod 2003; 68:922–928.PubMedGoogle Scholar
  83. 83.
    Brackett BG. In vitro culture of the zygote and embryo. In: Mastroianni Jr L, Biggers JD, eds. Fertilization and embryonic development in vitro. New York: Plenum Press, 1981:63–79.Google Scholar
  84. 84.
    Van Winkle LJ. Amino acid transport regulation and early embryo development. Biol Reprod 2001; 64:1–12.PubMedGoogle Scholar
  85. 85.
    Baltz JM, Biggers JD, Lechene C. A novel H+ permeability dominating intracellular pH in the early mouse embryo. Development 1993; 118:1353–1361.PubMedGoogle Scholar
  86. 86.
    Baltz JM, Biggers JD, Lechene C. Relief from alkaline load in two-cell stage mouse embryos by bicarbonate/chloride exchange. J Biol Chem 1991; 266:17212–17217.PubMedGoogle Scholar
  87. 87.
    Baltz JM, Biggers JD, Lechene C. Two-cell stage mouse embryos appear to lack mechanisms for alleviating intracellular acid loads. J Biol Chem 1991; 266:6052–6057.PubMedGoogle Scholar
  88. 88.
    Edwards LJ, Williams DA, Gardner DK. Intracellular pH of the mouse preimplantation embryo: Amino acids act as buffers of intracellular pH. Hum Reprod 1998; 13:3441–3448.PubMedGoogle Scholar
  89. 89.
    Phillips KP, Baltz JM. Intracellular pH regulation by HCO3 /Cl exchange is activated during early mouse zygote development. Dev Biol 1999; 208:392–405.PubMedGoogle Scholar
  90. 90.
    Zhao Y, Baltz JM. Bicarbonate/chloride exchange and intracellular pH throughout preimplantation mouse embryo development. Am J Physiol 1996; 271:C1512–1520.PubMedGoogle Scholar
  91. 91.
    Zhao Y, Chauvet PJ, Alper SL et al. Expression and function of bicarbonate/chloride exchangers in the preimplantation mouse embryo. J Biol Chem 1995; 270:24428–24434.PubMedGoogle Scholar
  92. 92.
    Shepard TH, Muffley LA, Smith LT. Mitochondrial ultrastructure in embryos after implantation. Hum Reprod 2000; 15(Suppl 2):218–228.PubMedGoogle Scholar
  93. 93.
    Sathananthan AH, Trounson AO. Mitochondrial morphology during preimplantational human embryogenesis. Hum Reprod 2000; 15(Suppl 2):148–159.PubMedGoogle Scholar
  94. 94.
    Matsumoto H, Shoji N, Sugawara S et al. Microscopic analysis of enzyme activity, mitochondrial distribution and hydrogen peroxide in two-cell rat embryos. J Reprod Fertil 1998; 113:231–238.PubMedGoogle Scholar
  95. 95.
    Shepard TH, Muffley LA, Smith LT. Ultrastructural study of mitochondria and their cristae in embryonic rats and primate (N. nemistrina). Anat Rec 1998; 252:383–392.PubMedGoogle Scholar
  96. 96.
    Hillman N, Tasca RJ. Ultrastructural and autoradiographic studies of mouse cleavage stages. Am J Anat 1969; 126:151–173.PubMedGoogle Scholar
  97. 97.
    Donnay I, Leese HJ. Embryo metabolism during the expansion of the bovine blastocyst. Mol Reprod Dev 1999; 53:171–178.PubMedGoogle Scholar
  98. 98.
    Houghton FD, Thompson JG, Kennedy CJ et al. Oxygen consumption and energy metabolism of the early mouse embryo. Mol Reprod Dev 1996; 44:476–485.PubMedGoogle Scholar
  99. 99.
    Martin KL, Leese HJ. Role of glucose in mouse preimplantation embryo development. Mol Reprod Dev 1995; 40:436–443.PubMedGoogle Scholar
  100. 100.
    Leese HJ, Barton AM. Pyruvate and glucose uptake by mouse ova and preimplantation embryos. J Reprod Fertil 1984; 72:9–13.PubMedGoogle Scholar
  101. 101.
    Lequarre AS, Grisart B, Moreau B et al. Glucose metabolism during bovine preimplantation development: Analysis of gene expression in single oocytes and embryos. Mol Reprod Dev 1997; 48:216–226.PubMedGoogle Scholar
  102. 102.
    Brown JJ, Whittingham DG. The roles of pyruvate, lactate and glucose during preimplantation development of embryos from F1 hybrid mice in vitro. Development 1991; 112:99–105.PubMedGoogle Scholar
  103. 103.
    Lawitts JA, Biggers JD. Optimization of mouse embryo culture media using simplex method. J Reprod Fert 1991; 91:543–546.Google Scholar
  104. 104.
    Ho Y, Wigglesworth K, Eppig JJ et al. Preimplantation development of mouse embryos in KSOM: Augmentation by amino acids and analysis of gene expression. Mol Reprod Dev 1995; 41:232–238.PubMedGoogle Scholar
  105. 105.
    Chatot CL, Ziomek CA, Bavister BD et al. An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro. J Reprod Fertil 1989; 86:679–688.PubMedGoogle Scholar
  106. 106.
    Lane M, Gardner DK, Hasler MJ et al. Use of G1.2/G2.2 media for commercial bovine embryo culture: Equivalent development and pregnancy rates compared to coculture. Theriogenology 2003; 60:407–419.PubMedGoogle Scholar
  107. 107.
    Oh B, Hwang S, McLaughlin J et al. Timely translation during the mouse oocyte-to-embryo transition. Development 2000; 127:3795–3803.PubMedGoogle Scholar
  108. 108.
    Mendez R, Barnard D, Richter JD. Differential mRNA translation and meiotic progression require Cdc2-mediated CPEB destruction. EMBO J 2002; 21:1833–1844.PubMedGoogle Scholar
  109. 109.
    Ratnam S, Mertineit C, Ding F et al. Dynamics of Dnmt1 methyltransferase expression and intra-cellular localization during oogenesis and preimplantation development. Dev Biol 2002; 245:304–314.PubMedGoogle Scholar
  110. 110.
    Mann MR, Chung YG, Nolen LD et al. Disruption of imprinted gene methylation and expression in cloned preimplantation stage mouse embryos. Biol Reprod 2003; 69:902–914.PubMedGoogle Scholar
  111. 111.
    Stojkovic M, Buttner M, Zakhartchenko V et al. Secretion of interferon-tau by bovine embryos in long-term culture: Comparison of in vivo derived, in vitro produced, nuclear transfer and demi-embryos. Anim Reprod Sci 1999; 55:151–162.PubMedGoogle Scholar
  112. 112.
    Hill JR, Burghardt RC, Jones K. et al. Evidence for placental abnormality as the major cause of mortality in first-trimester somatic cell cloned bovine fetuses. Biol Reprod 2000; 63:1787–1794.PubMedGoogle Scholar
  113. 113.
    De Sousa PA, King T, Harkness L et al. Evaluation of gestational deficiencies in cloned sheep fetuses and placentae. Biol Reprod 2001; 65:23–30.PubMedGoogle Scholar
  114. 114.
    Heyman Y, Chavatte-Palmer P, LeBourhis D et al. Frequency and occurrence of late-gestation losses from cattle cloned embryos. Biol Reprod 2002; 66:6–13.PubMedGoogle Scholar
  115. 115.
    Humpherys D, Eggan K, Akutsu H et al. Abnormal gene expression in cloned mice derived from embryonic stem cell and cumulus cell nuclei. Proc Natl Acad Sci USA 2002; 99:12889–12894.PubMedGoogle Scholar
  116. 116.
    Ogura A, Inoue K, Ogonuki N et al. Phenotypic effects of somatic cell cloning in the mouse. Cloning Stem Cells. 2002; 4:397–405.PubMedGoogle Scholar
  117. 117.
    Lee RS, Peterson AJ, Donnison MJ et al. Cloned cattle fetuses with the same nuclear genetics are more variable than contemporary half-siblings resulting from artificial insemination and exhibit fetal and placental growth deregulation even in the first trimester. Biol Reprod 2004; 70:1–11.PubMedGoogle Scholar
  118. 118.
    Ravelich SR, Shelling AN, Ramachandran A et al. Altered placental lactogen and leptin expression in placentomes from bovine nuclear transfer pregnancies. Biol Reprod 2004; 71:1862–1869.PubMedGoogle Scholar
  119. 119.
    Hall VJ, Ruddock NT, French AJ. Expression profiling of genes crucial for placental and preimplantation development in bovine in vivo, in vitro, and nuclear transfer blastocysts. Mol Reprod Dev 2005; 72:16–24.PubMedGoogle Scholar
  120. 120.
    Humpherys D, Eggan K, Akutsu H et al. Epigenetic instability in ES cells and cloned mice. Science 2001; 293:95–97.PubMedGoogle Scholar
  121. 121.
    Rideout IIIrd WM, Eggan K, Jaenisch R. Nuclear cloning and epigenetic reprogramming of the genome. Science 2001; 293:1093–1098.PubMedGoogle Scholar
  122. 122.
    Ohgane J, Wakayama T, Kogo Y et al. DNA methylation variation in cloned mice. Genesis 2001; 30:45–50.PubMedGoogle Scholar
  123. 123.
    Latham KE. Cloning: Questions answered and unsolved. Differentiation 2004; 72:11–22.PubMedGoogle Scholar
  124. 124.
    Chen DY, Wen DC, Zhang YP et al. Interspecies implantation and mitochondria fate of panda-rabbit cloned embryos. Biol Reprod 2002; 67:637–642.PubMedGoogle Scholar
  125. 125.
    Cummins JM. Mitochondria: Potential roles in embryogenesis and nucleocytoplasmic transfer. Hum Reprod Update 2001; 7:217–228.PubMedGoogle Scholar
  126. 126.
    Inoue K, Kohda T, Lee J et al. Faithful expression of imprinted genes in cloned mice. Science 2002; 295:297.PubMedGoogle Scholar
  127. 127.
    Latham KE. Stage-specific and cell type-specific aspects of genomic imprinting effects in mammals. Differentiation 1995; 59:269–282.PubMedGoogle Scholar
  128. 128.
    Bruggerhoff K, Zakhartchenko V, Wenigerkind H et al. Bovine somatic cell nuclear transfer using recipient oocytes recovered by ovum pick-up: Effect of maternal lineage of oocyte donors. Biol Reprod 2002; 66:367–373.PubMedGoogle Scholar
  129. 129.
    Wakasugi N. A genetically determined incompatibility system between spermatozoa and eggs leading to embryonic death in mice. J Reprod Fertil 1974; 41:85–96.PubMedGoogle Scholar
  130. 130.
    Renard JP, Baldacci P, Richoux-Duranthon V et al. A maternal factor affecting mouse blastocyst formation. Development 1994; 120:797–802.PubMedGoogle Scholar
  131. 131.
    Babinet C, Richoux V, Guenet JL et al. The DDK inbred strain as a model for the study of interactions between parental genomes and egg cytoplasm in mouse preimplantation development. Development 1990; (Suppl):81–87.Google Scholar
  132. 132.
    Baldacci PA, Richoux V, Renard JP et al. The locus Om, responsible for the DDK syndrome, maps close to Sigje on mouse chromosome 11. Mamm Genome 1992; 2:100–5.PubMedGoogle Scholar
  133. 133.
    Pardo-Manuel de Villena F, de la Casa-Esperon E, Verner A et al. The maternal DDK syndrome phenotype is determined by modifier genes that are not linked to Om. Mamm Genome 1999; 10:492–497.PubMedGoogle Scholar
  134. 134.
    Pardo-Manuel de Villena F, Naumova AK, Verner AE et al. Confirmation of maternal transmission ratio distortion at Om and direct evidence that the maternal and paternal “DDK syndrome” genes are linked. Mamm Genome 1997; 8:642–646.PubMedGoogle Scholar
  135. 135.
    Pardo-Manuel de Villena F, de La Casa-Esperon E, Williams JW et al. Heritability of the maternal meiotic drive system linked to Om and high-resolution mapping of the Responder locus in mouse. Genetics 2000; 155:283–289.PubMedGoogle Scholar
  136. 136.
    Gao S, Wu G, Han Z et al. Recapitulation of the ovum mutant (Om) phenotype and loss of Om locus polarity in cloned mouse embryos. Biol Reprod 2005; 72:487–491.PubMedGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2007

Authors and Affiliations

  • Keith E. Latham
    • 1
  • Shaorong Gao
    • 2
    • 3
  • Zhiming Han
    • 2
  1. 1.Department of BiochemistryThe Fels Institute for Cancer Research and Molecular BiologyPhiladelphiaUSA
  2. 2.The Fels Institute for Cancer Research and Molecular BiologyTemple University Medical SchoolPhiladelphiaUSA
  3. 3.National Institute of Biological SciencesBeijingChina

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