Nuclear reprogramming: What has been done and potential avenues for improvements

Central European Journal of Biology

Volumn 3, Issue 3, 2008, Pages 211-223

  Loi, Pasqualino ^a   Matsukawa, Kazutsugu ^b   Takahashi, Seiya ^b   Akagi, Satoshi ^b   Ptak, Grazyna ^a  

^a UNIVERSITY OF TERAMO   (Italy)

^b NATIONAL INSTITUTE OF LIVESTOCK AND GRASSLAND SCIENCE   (Japan)

Author keywords

Cloning; Nuclear reprogramming; Sheep

Indexed keywords

BOS; OVIS ARIES;

EID: 47349110625     PISSN: 1895104X     EISSN: 16443632     Source Type: Journal    
DOI: 10.2478/s11535-008-0025-6     Document Type: Review

References (103)

1. Gurdon J.B., Laskey R.A., Reeves O.R., The developmental capacity of nuclei transplanted from keratinized skin cells of adult frogs, J. Embryol. Exp. Morphol., 1975, 34, 93-112
2. Wilmut I., Schnieke A.E., McWhir J., Kind A.J., Campbell K.K., Viable offspring derived from fetal and adult mammalian cells, Nature, 1997, 385, 810-813
3. Meissner A., Jaenisch R., Mammalian nuclear transfer, Dev. Dyn., 2006, 235, 2460-2469
4. Ogura A., Inoue K., Ogonuki N., Lee J., Kohda T., Ishino F., Phenotypic effects of somatic cell cloning in the mouse, Cloning Stem Cells, 2002, 4, 397-405
5. Tsunoda Y., Kato Y., Recent progress and problems in animal cloning, Differentiation, 2002, 69, 158-161
6. Tamashiro K.L., Wakayama T., Yamazaki Y., Akutsu H., Woods S.C., Kondo S., Phenotype of cloned mice: development, behaviour, and physiology, Exp. Biol. Med., 2003, 228, 1193-1200
7. Kremenskoy M., Kremenska Y., Suzuki M., Imai K., Takahashi S., Hashizume K., DNA methylation profiles of donor nuclei cells and tissues of cloned bovine fetuses, J. Reprod. Dev., 2006, 52, 259-266
8. Loi P., Clinton M., Vackova I., Fulka J. Jr, Feil R., Palmieri C., Placental abnormalities associated with post-natal mortality in sheep somatic cell clones, Theriogenology, 2006, 65, 1110-1121
9. Morgan H.D., Santos F., Green K., Dean W., Reik W., Epigenetic reprogramming in mammals, Hum. Mol. Genet., 2006, 14, R47-R58
10. Rideout M. III, Eggan K., Jaenisch R., Nuclear cloning and epigenetic reprogramming of the genome, Science, 2001, 293, 1093-1098
11. Latham K.E., Early and delayed aspects of nuclear reprogramming during cloning, Biol. Cell., 2005, 97, 119-132
12. Lagutina I., Somatic cell nuclear transfer in horses: effect of oocyte morphology, embryo reconstruction method and donor cell type, Reproduction, 2005, 130, 559-567
13. Vajta G., Handmade cloning: the future way of nuclear transfer?, Trends Biotechnol., 2007, 25, 250-253
14. Wells D.N., Misica P.M., Day A.M., Peterson A.J., Tervit H.R., Cloning sheep from cultured embryonic cells, Reprod. Fertil. Dev., 1998, 10, 615-626
15. Li N., Wells D.N., Peterson A.J., Lee R.S., Perturbations in the biochemical composition of fetal fluids are apparent in surviving bovine somatic cell nuclear transfer pregnancies in the first half of gestation, Biol. Reprod., 2005, 73, 139-148
16. Cezar G.G., Bartolomei M.S., Forsberg E.J., First N.L., Bishop M.D., Eilertsen K., Genome-wide epigenetic alterations in cloned bovine fetuses, Biol. Reprod., 2003, 68, 1009-1014
17. Wakisaka-Saito N., Kohda T., Inoue K., Ogonuki N., Miki H., Hikichi T.,, Chorioallantoic placenta defects in cloned mice, Biochem. Biophys. Res. Commun., 2006, 349, 106-114
18. Hashizume K., Ishiwata H., Kizaki K., Yamada O., Takahashi T., Imai K.,, Implantation and placental development in somatic cell clone recipient cows, Cloning Stem Cells, 2002, 4, 197-209
19. Chavatte-Palmer P., de Sousa N., Laigre P., Camous S., Ponter A.A., Beckers J.F., et. al., Ultrasound fetal measurements and pregnancy associated glycoprotein secretion in early pregnancy in cattle recipients carrying somatic clones, Theriogenology, 2006, 66, 829-840
20. Constant F., Guillomot M., Heyman Y., Vignon X., Laigre P., Servely J.L., 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, 122-130
21. Hill J.R., Burghardt R.C., Jones K., Long C.R., Looney C.R., Shin T., et. al., Evidence for placental abnormality as the major cause of mortality in firsttrimester somatic cell cloned bovine fetuses, Biol. Reprod., 2000, 63, 1787-1794
22. Palmieri C., Loi P., Reynolds L.P., Ptak G., Della Salda L., Placental abnormalities in ovine somatic cell clones at term: a light and electron microscopic investigation, Placenta, 2007, 28, 577-584
23. Tian X.C., Smith S.L., Zhang S.Q., Kubota C., Curchoe C., Xue F., et. al., Nuclear reprogramming by somatic cell nuclear transfer-the cattle story, Soc. Reprod. Fertil. Suppl., 2007, 64, 327-239
24. Young L.E., Schnieke A.E., McCreath K.J., Wieckowski S., Konfortova G., Fernandes K., et. al., Conservation of IGF2-H19 and IGF2R imprinting in sheep: effects of somatic cell nuclear transfer, Mech. Dev., 2003, 120, 1433-1442
25. Xue F., Tian X.C., Du F., Kubota C., Taneja M., Dinnyes A., et. al., Aberrant patterns of X chromosome inactivation in bovine clones, Nat. Genet., 2002, 31, 216-220
26. Weier J.F., Weier H.U., Jung C.J., Gormley M., Zhou Y., Chu L.W., et. al., Human cytotrophoblasts acquire aneuploidies as they differentiate to an invasive phenotype, Dev. Biol., 2005, 279, 420-432
27. Nagy A., Gocza E., Diaz E.M., Prideaux V.R., Ivanyi E., Markkula M., et. al., Embryonic stem cells alone are able to support fetal development in the mouse, Development, 1990, 110, 815-821
28. Reik W., Epigenetic asymmetry in the mammalian zygote and early embryo: relationship to lineage commitment?, Philos. Trans. R. Soc. Lond. B. Biol. Sci., 2003, 358, 1403-1409
29. Bird A., DNA methylation patterns and epigenetic memory, Genes Dev., 2002, 16, 6-21
30. Santos F., Peters A.H., Otte A.P., Reik W., Dean W., Dynamic chromatin modifications characterise the first cell cycle in mouse embryos, Dev. Biol., 2005, 280, 225-236
31. Mayer W., Niveleau A., Walter J., Fundele R., Haaf T., Demethylation of the zygotic paternal genome, Nature, 2000, 403, 501-502
32. Howell C.Y., Bestor T.H., Ding F., Latham K.E., Mertineit C., Trasler J.M., et. al., Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene, Cell, 2001, 104, 829-838
33. Haaf T., Methylation dynamics in the early mammalian embryo: implications of genome reprogramming defects for development, Curr. Top. Microbiol. Immunol., 2006, 310, 13-22
34. Reik W., Stability and flexibility of epigenetic gene regulation in mammalian development, Nature, 2007, 47, 425-432
35. Santos F., Zakhartchenko V., Stojkovic M., Peters A., Jenuwein T., Wolf E., et. al., Epigenetic marking correlates with developmental potential in cloned bovine preimplantation embryo, Curr. Biol., 2003, 13, 1116-1121
36. Beaujean N., Taylor J., Gardner J., Wilmut I., Meehan R., Young L., Effect of limited DNA methylation reprogramming in the normal sheep embryo on somatic cell nuclear transfer, Biol. Reprod., 2004, 71, 185-193
37. Shi W., Dirim F., Wolf E., Zakhartchenko V., Haaf T., Methylation reprogramming and chromosomal aneuploidy in in vivo fertilized and cloned rabbit preimplantation embryos, Biol. Reprod., 2004, 71, 340-347
38. Fulka H., Mrazek M., Tepla O., Fulka J. Jr., DNA methylation pattern in human zygotes and developing embryos, Reproduction, 2004, 128, 703-708
39. Beaujean N., Taylor J.E., McGarry M., Gardner J.O., Wilmut I., Loi P., et. al., The effect of interspecific oocytes on demethylation of sperm DNA, Proc. Natl. Acad. Sci. USA, 2004, 101, 7636-7440
40. Boiani M., Eckardt S., Scholer H.R., McLaughlin K.J., Oct4 distribution and level in mouse clones: consequences for pluripotency, Genes Dev., 2002, 16, 1209-1219
41. Smith C., Berg D., Beaumont S., Standley N.T., Wells D.N., Pfeffer P.L., Simultaneous gene quantitation of multiple genes in individual bovine nuclear transfer blastocysts, Reproduction, 2007, 133, 231-242
42. Somers J., Smith C., Donnison M., Wells D.N., Henderson H., McLeay L., et. al., Gene expression profiling of individual bovine nuclear transfer blastocysts, Reproduction, 2006, 131, 1073-1084
43. Smith S.L., Everts R.E., Tian X.C., Du F., Sung L.Y., Rodriguez-Zas S.L., et. al., Global gene expression profiles reveal significant nuclear reprogramming by the blastocyst stage after cloning, Proc. Natl. Acad. Sci. USA., 2005, 102, 17582-17587
44. Jouneau A., Zhou Q., Camus A., Brochard V., Maulny L., Collignon J., et. al., Developmental abnormalities of NT mouse embryos appear early after implantation, Development, 2006, 133, 1597-1607
45. Wuensch A., Habermann F.A., Kurosaka S., Klose R., Zakhartchenko V., Reichenbach H.D., et. al., Quantitative monitoring of pluripotency gene activation after somatic cloning in cattle, Biol. Reprod., 2007, 76, 983-991
46. Wells D.N., Cloning in livestock agriculture, Reprod. Suppl., 2003, 61, 131-150
47. Robl J.M., Wang Z., Kasinathan P., Kuroiwa Y., Transgenic animal production and animal biotechnology, Theriogenology, 2007, 67, 127-133
48. Niemann H., Kues W.A., Transgenic farm animals: an update, Reprod. Fertil. Dev., 2007, 19, 762-770
49. Prather R.S., Hawley R.J., Carter D.B., Lai L., Greenstein J.L., Transgenic swine for biomedicine and agriculture, Theriogenology, 2003, 59, 115-123
50. Trounson A.O., Future and applications of cloning, Methods Mol. Biol., 2006, 348, 319-332
51. Loi P., Ptak G., Barboni B., Fulka J. Jr, Cappai P., Clinton M., Genetic rescue of an endangered mammal by cross-species nuclear transfer using postmortem somatic cells, Nat. Biotechnol., 2001, 19, 962-964
52. Holt W.V., Pickard A.R., Prather R.S., Wildlife conservation and reproductive cloning, Reproduction, 2004, 127, 317-324
53. Campbell K.H., McWhir J., Ritchie W.A., Wilmut I., Sheep cloned by nuclear transfer from a cultured cell line, Nature, 1996, 7, 64-66
54. Wakayama T., Perry A.C., Zuccotti M., Johnson K.R., Yanagimachi R., Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei, Nature, 1998, 23, 369-374
55. Withfield J.F., Boynton A.L., Rixon R.H., Youdale T., The control of animal cell proliferation by calcium, Ca2+-calmodulin, and cyclic AMP, In: Boynton A.L., Leffert H.L. (Eds.), Control of Animal Cell Proliferation, vol. 1., Academic Press, London, 1985, 331-365
56. Martínez-Balbás M.A., Dey A., Rabindran S.K., Ozato K., Wu C., Displacement of sequence-specific transcription factors from mitotic chromatin, Cell, 1995, 83, 29-38
57. Cibelli J.B., Stice S.L., Golueke P.J., Kane J.J., Jerry J., Blackwell C., et. al., Cloned transgenic calves produced from nonquiescent fetal fibroblasts, Science, 1998, 22, 1256-1258
58. Campbell K.H., Loi P., Otaegui P.J., Wilmut I., Cell cycle co-ordination in embryo cloning by nuclear transfer, Rev. Reprod., 1996, 1, 40-46
59. Wakayama T., Production of cloned mice and ES cells from adult somatic cells by nuclear transfer: how to improve cloning efficiency?, J. Reprod. Dev., 2007, 53, 13-26
60. Gurdon J.B., From nuclear transfer to nuclear reprogramming: the reversal of cell differentiation, Annu. Rev. Cell Dev. Biol., 2006, 22, 1-22
61. Enright B.P., Kubota C., Yang X., Tian X.C., Epigenetic characteristics and development of embryos cloned from donor cells treated by trichostatin A or 5-aza-2′-deoxycytidine, Biol. Reprod., 2003, 69, 896-901
62. Kiziltepe T., Hideshima T., Catley L., Raje N., Yasui H., Shiraishi N., et. al., 5-Azacytidine, a DNA methyltransferase inhibitor, induces ATR-mediated DNA double-strand break responses, apoptosis, and synergistic cytotoxicity with doxorubicin and bortezomib against multiple myeloma cells, Mol. Cancer Ther., 2007, 6, 1718-1727
63. van der Heijden G.W., Dieker J.W., Derijck A.A., Muller S., Berden J.H., Braat D.D., Asymmetry in histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote, Mech. Dev., 2005, 122, 1008-1022
64. Yoshida N., Brahmajosyula M., Shoji S., Amanai M., Perry A.C., Epigenetic discrimination by mouse metaphase II oocytes mediates asymmetric chromatin remodeling independently of meiotic exit, Dev. Biol., 2007, 301, 464-477
65. Kishigami S., Mizutani E., Ohta H., Hikichi T., Thuan N.V., Wakayama S., et. al., Significant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer, Biochem. Biophys. Res. Commun., 2006, 3, 183-189
66. Rybouchkin A., Kato Y., Tsunoda Y., Role of histone acetylation in reprogramming of somatic nuclei following nuclear transfer, Biol. Reprod., 2006, 74, 1083-1089
67. Kishigami S., Bui H.T., Wakayama S., Tokunaga K., Van Thuan N., Hikichi T., et. al., Successful mouse cloning of an outbred strain by trichostatin A treatment after somatic nuclear transfer, J. Reprod. Dev., 2007, 53, 165-170
68. 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
69. Iwatani M., Ikegami K., Kremenska Y., Hattori N., Tanaka S., Yagi S., et. al., Dimethyl sulfoxide has an impact on epigenetic profile in mouse embryoid body, Stem Cells, 2006, 24, 2549-2556
70. Di Berardino M.A., Origin and progress of nuclear transfer in nonmammalian animals, Methods Mol. Biol., 2006, 348, 3-32
71. Lemaitre J.M., Danis E., Pasero P., Vassetzky Y., Mechali M., Mitotic remodeling of the replicon and chromosome structure, Cell, 2005, 2, 787-801
72. Kubota C., Tian X.C., Yang X., Serial bull cloning by somatic cell nuclear transfer, Nat. Biotechnol., 2004, 22, 693-694
73. Loi P., Clinton M., Fulka J. Jr, Cappai P., Feil R., Moor R.M., Nuclei of nonviable ovine somatic cells develop into lambs after nuclear transplantation, Biol. Reprod., 2002, 67, 126-132
74. Sullivan E.J., Kasinathan S., Kasinathan P., Robl J.M., Collas P., Cloned calves from chromatin remodeled in vitro, Biol. Reprod., 2004, 70, 146-153
75. Tani T., Shimada H., Kato Y., Tsunoda Y., Bovine oocytes with the potential to reprogram somatic cell nuclei have a unique 23-kDa protein, phosphorylated transcriptionally controlled tumor protein (TCTP), Stem Cells, 2007, 9, 267-280
76. Simerly C., Dominko T., Navara C., Payne C., Capuano S., Gosman G., et. al., Molecular correlates of primate nuclear transfer failures, Science, 2003, 300, 225-227
77. Simerly C., Navara C., Hyun S.H., Lee B.C., Kang S.K., 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, 15, 237-252
78. Wakayama S., Cibelli J.B., Wakayama T., Effect of timing of the removal of oocyte chromosomes before or after injection of somatic nucleus on development of NT embryos, Cloning Stem Cells, 2003, 5, 181-189
79. Meng L., Ely J.J., Stouffer R.L., Wolf D.P., Rhesus monkeys produced by nuclear transfer, Biol. Reprod., 1997, 57, 454-459
80. Peura T.T., Improved in vitro development rates of sheep somatic nuclear transfer embryos by using a reverse-order zona-free cloning method, Cloning Stem Cells, 2003, 5, 13-24
81. Boiani M., Eckardt S., Leu N.A., Scholer H.R., McLaughlin K.J., Pluripotency deficit in clones overcome by clone-clone aggregation: epigenetic complementation?, EMBO J., 2003, 22, 5304-5312
82. St John J.C., Bowles E.J., Amaral A., Sperm mitochondria and fertilisation, Soc. Reprod. Fertil. Suppl., 2007, 65, 399-416
83. Lloyd R.E., Lee J.H., Alberio R., Bowles E.J., Ramalho-Santos J., Campbell K.H., et. al., Aberrant nucleo-cytoplasmic cross-talk results in donor cell mtDNA persistence in cloned embryos, Genetics, 2006, 172, 2515-2527
84. Jiao F., Yan J.B., Yang X.Y., Li H., Wang Q., Huang S.Z., et. al., Effect of oocyte mitochondrial DNA haplotype on bovine somatic cell nuclear transfer efficiency, Mol. Reprod. Dev., 2007, 74, 1278-1286
85. Yang X.Y., Li H., Ma Q.W., Yan J.B., Zhao J.G., Li H.W., et. al., Improved efficiency of bovine cloning by autologous somatic cell nuclear transfer, Reproduction, 2006, 132, 733-739
86. Toth S., Huneau D., Banrezes B., Ozil J.P., Egg activation is the result of calcium signal summation in the mouse, Reproduction, 2006, 131, 27-34
87. Campbell K.H., Alberio R., Lee J.H., Ritchie W.A., Nuclear transfer in practice, Cloning Stem Cells, 2001, 3, 201-208
88. Schurmann A., Wells D.N., Oback B., Early zygotes are suitable recipients for bovine somatic nuclear transfer and result in cloned offspring, Reproduction, 2006, 132, 839-844
89. Ozil J.P., Banrezes B., Toth S., Pan H., Schultz R.M., Ca2+ oscillatory pattern in fertilized mouse eggs affects gene expression and development to term, Dev. Biol., 2006, 300, 534-544
90. Hochedlinger K., Jaenisch R., Monoclonal mice generated by nuclear transfer from mature B and T donor cells, Nature, 2002, 415, 1035-1038
91. Eggan K., Baldwin K., Tackett M., Osborne J., Gogos J., Chess A., et. al., Mice cloned from olfactory sensory neurons, Nature, 2004, 428, 44-49
92. Inoue K., Wakao H., Ogonuki N., Miki H., Seino K., Nambu-Wakao R., et. al., Generation of cloned mice by direct nuclear transfer from natural killer T cells, Curr. Biol., 2005, 15, 1114-1118
93. Wakayama T., Rodriguez I., Perry A.C., Yanagimachi R., Mombaerts P., Mice cloned from embryonic stem cells, Proc. Natl. Acad. Sci. USA, 1999, 96, 14984-14989
94. Rideout W.M. 3rd, Wakayama T., Wutz A., Eggan K., Jackson-Grusby L., Dausman J., et. al., Generation of mice from wild-type and targeted ES cells by nuclear cloning, Nat. Genet. 2000, 24, 109-110
95. Mizutani E., Ohta H., Kishigami S., Van Thuan N., Hikichi T., Wakayama S., Developmental ability of cloned embryos from neural stem cells, Reproduction, 2006, 132, 849-857
96. Inoue K., Noda S., Ogonuki N., Miki H., Inoue S., Katayama K., Differential developmental ability of embryos cloned from tissue-specific stem cells, Stem Cells, 2007, 25, 1279-1285
97. Inoue K., Ogonuki N., Miki H., Hirose M., Noda S., Kim J.M., Inefficient reprogramming of the hematopoietic stem cell genome following nuclear transfer, J. Cell. Sci., 2006, 119, 1985-1991
98. Oback B., Wells D.N., Donor cell differentiation, reprogramming, and cloning efficiency: Elusive or illusive correlation?, Mol. Reprod. Dev., 2006, 74, 646-654
99. Chung Y.G., Mann M.R., Bartolomei M.S., Latham K.E., 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, 1178-1184
100. Cavaleri F., Gentile L., Scholer H.R., Boiani M., Recombinant human albumin supports development of somatic cell nuclear transfer embryos in mice: toward the establishment of a chemically defined cloning protocol, Cloning Stem Cells, 2006, 8, 24-40
101. Boiani M., Gentile L., Gambles V.V., Cavaleri F., Redi C.A., Scholer H.R., Variable reprogramming of the pluripotent stem cell marker Oct4 in mouse clones: distinct developmental potentials in different culture environments, Stem Cells, 2005, 23, 1089-1094.
102. Ogushi S., Palmieri C., Fulka H., Saitou M., Miyano T., Fulka J. Jr., The maternal nucleolus is essential for early embryonic development in mammals, Science, 2008, 319, 613-616
103. Loi P., Beaujean N., Khochbin S., Fulka J. Jr, Ptak G., Asymmetric nuclear reprogramming in somatic cell nuclear transfer? Bioessays, 2008, 30, 66-74