Gene expression and development of early pig embryos produced by serial nuclear transfer

Molecular Reproduction and Development

Volumn 76, Issue 6, 2009, Pages 555-563

  Xing, Xiaojun ^a,b   Magnani, Luca ^a,c   Lee, Kiho ^a   Wang, Chunmin ^a   Cabot, Ryan A ^a   Machaty, Zoltan ^a  

^a PURDUE UNIVERSITY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLASTOCYST; CELL NUCLEUS TRANSPLANTATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FERTILIZATION IN VITRO; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; SWINE;

ANIMALS; CATTLE; CLONING, ORGANISM; EMBRYO, MAMMALIAN; EPIGENESIS, GENETIC; FEMALE; FERTILIZATION IN VITRO; GENE EXPRESSION; HOMEODOMAIN PROTEINS; NUCLEAR TRANSFER TECHNIQUES; OCTAMER TRANSCRIPTION FACTOR-3; PREGNANCY; SOXB1 TRANSCRIPTION FACTORS; SWINE;

SUIDAE; SUS;

EID: 65949092543     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.20974     Document Type: Article

References (68)

1. Abeydeera LR, Wang WH, Cantley TC, Rieke A, Day BN. 1998. Coculture with follicular shell pieces can enhance the developmental competence of pig oocytes after in vitro fertilization: relevance to intracellular glutathione. Biol Reprod 58:213-218.
2. Armstrong L, Lako M, Dean W, Stojkovic M. 2006. Epigenetic modification is central to genome reprogramming in somatic cell nuclear transfer. Stem Cells 24:805-814.
3. Bai Z, Yong J, Qing T, Cheng J, Shen W, Ding M, Deng H. 2007. Serial nuclear transfer improves the developmental potential of mouse embryos cloned from oocytes matured in a protein-free medium. Mol Reprod Dev 74:560-567.
4. Boiani M, Eckardt S, Schöler HR, McLaughlin KJ. 2002. Oct4 distribution and level in mouse clones: Consequences for pluripotency. Genes Dev 16:1209-1219.
5. Bortvin A, Eggan K, Skaletsky H, Akutsu H, Berry DL, Yanagimachi R, Page DC, Jaenisch R. 2003. Incomplete reactivation of Oct4-related genes in mouse embryos cloned from somatic nuclei. Development 130:1673-1680.
6. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, Guenther MG, Kumar RM, Murray HL, Jenner RG, Gifford DK, Melton DA, Jaenisch R, Young RA. 2005. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122:947-956.
7. Chambers I, Silva J, Colby D, Nichols J, Nijmeijer B, Robertson M, Vrana J, Jones K, Grotewold L, Smith A. 2007. Nanog safeguards pluripotency and mediates germline development. Nature 450:1230-1234.
8. Chung YG, Ratnam S, Chaillet JR, Latham KE. 2003. Abnormal regulation of DNA methyltransferase expression in cloned mouse embryos. Biol Reprod 69:146-153.
9. Czermin B, Melfi R, McCabe D, Seitz V, Imhof A, Pirrotta V. 2002. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal polycomb sites. Cell 111:185-196.
10. Danam RP, Howell SR, Brent TP, Harris LC. 2005. Epigenetic regulation of O6-methylguanine-DNA methyltransferase gene expression by histone acetylation and methyl-CpG binding proteins. Mol Cancer Ther 4:61-69.
11. Daniels R, Hall V, Trounson AO. 2000. Analysis of gene transcription in bovine nuclear transfer embryos reconstructed with granulosa cell nuclei. Biol Reprod 63:1034-1040.
12. Eckardt S, McLaughlin KJ. 2004. Interpretation of reprogramming to predict the success of somatic cell cloning. Anim Reprod Sci 82-83:97-108.
13. Ectors FJ, Delval A, Smith LC, Touati K, Remy B, Beckers JF, Ectors F. 1995. Viability of cloned bovine embryos after one or two cycles of nuclear transfer and in vitro culture. Theriogenology 44:925-933.
14. Enright BP, Sung LY, Chang CC, Yang X, Tian XC. 2005. Methylation and acetylation characteristics of cloned bovine embryos from donor cells treated with 5-aza-2′-deoxycytidine. Biol Reprod 72:944-948.
15. Fan HY, Sun QY. 2004. In vitro maturation and fertilization of pig oocytes. Methods Mol Biol 253:227-234.
16. Gurdon JB, Laskey RA, Reeves OR. 1975. The developmental capacity of nuclei transplanted from keratinized skin cells of adult frogs. J Embryol Exp Morphol 34:93-112.
17. Heindryckx B, Rybouchkin A, Van Der Elst J, Dhont M. 2002. Serial pronuclear transfer increases the developmental potential of in vitro-matured oocytes in mouse cloning. Biol Reprod 67:1790-1795.
18. Hochedlinger K, Jaenisch R. 2003. Nuclear transplantation embryonic stem cells, and the potential for cell therapy. N Engl J Med 349:275-286.
19. Humpherys D, Eggan K, Akutsu H, Friedman A, Hochedlinger K, Yanagimachi R, Lander ES, Golub TR, Jaenisch R. 2002. Abnormal gene expression in cloned mice derived from embryonic stem cell and cumulus cell nuclei. Proc Natl Acad Sci USA 99:12889-12894.
20. Jaenisch R, Young R. 2008. Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 132:567-582.
21. Jarrell VL, Day BN, Prather RS. 1991. The transition from maternal to zygotic control of development occurs during the 4-cell stage in the domestic pig, Sus scrofa: Quantitative and qualitative aspects of protein synthesis. Biol Reprod 44:62-68.
22. Jouneau A, Zhou Q, Camus A, Brochard V, Maulny L, Collignon J, Renard JP. 2006. Developmental abnormalities of NT mouse embryos appear early after implantation. Development 133:1597-1607.
23. Kang YK, Koo DB, Park JS, Choi YH, Chung AS, Lee KK, Han YM. 2001. Aberrant methylation of donor genome in cloned bovine embryos. Nat Genet 28:173-177.
24. Kang YK, Park JS, Koo DB, Choi YH, Kim SU, Lee KK, Han YM. 2002. Limited demethylation leaves mosaic-type methylation states in cloned bovine pre-implantation embryos. EMBO J 21:1092-1100.
25. Kikyo N, Wolffe AP. 2000. Reprogramming nuclei: Insights from cloning, nuclear transfer and heterokaryons. J Cell Sci 113:11-20.
26. Kubota C, Tian XC, Yang X. 2004. Serial bull cloning by somatic cell nuclear transfer. Nat Biotechnol 22:693-694.
27. Kumar BM, Jin HF, Kim JG, Ock SA, Hong Y, Balasubramanian S, Choe SY, Rho GJ. 2007. Differential gene expression patterns in porcine nuclear transfer embryos reconstructed with fetal fibroblasts and mesenchymal stem cells. Dev Dyn 236:435-446.
28. Kwon OY, Kono T. 1996. Production of identical sextuplet mice by transferring metaphase nuclei from four-cell embryos. Proc Natl Acad Sci USA 93:13010-13013.
29. Lee E, Lee SH, Kim S, Jeong YW, Kim JH, Koo OJ, Park SM, Hashem MA, Hossein MS, Son HY, Lee CK, Hwang WS, Kang SK, Lee BC. 2006. Analysis of nuclear reprogramming in cloned miniature pig embryos by expression of Oct-4 and Oct-4 related genes. Biochem Biophys Res Commun 348:1419-1428.
30. Li GP, Tan JH, Sun QY, Meng QG, Yue KZ, Sun XS, Li ZY, Wang HB, Xu LB. 2000. Cloned piglets born after nuclear transplantation of embryonic blastomeres into porcine oocytes matured in vivo. Cloning 2:45-52.
31. Li X, Kato Y, Tsunoda Y. 2005. Comparative analysis of development-related gene expression in mouse preimplantation embryos with different developmental potential. Mol Reprod Dev 72:152-160.
32. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402-408.
33. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, Chen X, Bourque G, George J, Leong B, Liu J, Wong KY, Sung KW, Lee CW, Zhao XD, Chiu KP, Lipovich L, Kuznetsov VA, Robson P, Stanton LW, Wei CL, Ruan Y, Lim B, Ng HH. 2006. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 38:431-440.
34. Magnani L, Cabot RA. 2008. In vitro and in vivo derived porcine embryos possess similar, but not identical, patterns of Oct4, Nanog, and Sox2 mRNA expression during cleavage development. Mol Reprod Dev 75:1726-1735.
35. Mann MR, Chung YG, Nolen LD, Verona RI, Latham KE, Bartolomei MS. 2003. Disruption of imprinted gene methylation and expression in cloned pre-implantation stage mouse embryos. Biol Reprod 69:902-914.
36. Masui S, Nakatake Y, Toyooka Y, Shimosato D, Yagi R, Takahashi K, Okochi H, Okuda A, Matoba R, Sharov AA, Ko MS, Niwa H. 2007. Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nat Cell Biol 9:625-635.
37. Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, Schöler H, Smith A. 1998. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95:379-391.
38. Niwa H, Miyazaki J, Smith AG. 2000. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 24:372-376.
39. Nowak SJ, Corces VG. 2004. Phosphorylation of histone H3: A balancing act between chromosome condensation and transcriptiona activation. Trends Genet 20:214-220.
40. Oback B, Wells DN. 2007. Donor cell differentiation, reprogramming, and cloning efficiency: Elusive or illusive correlation? Mol Reprod Dev 74:646-654.
41. Ono Y, Kono T. 2006. Irreversible barrier to the reprogramming of donor cells in cloning with mouse embryos and embryonic stem cells. Biol Reprod 75:210-216.
42. Ono Y, Shimozawa N, Ito M, Kono T. 2001a. Cloned mice from fetal fibroblast cells arrested at metaphase by a serial nuclear transfer. Biol Reprod 64:44-50.
43. Ono Y, Shimozawa N, Muguruma K, Kimoto S, Hioki K, Tachibana M, Shinkai Y, Ito M, Kono T. 2001b. Production of cloned mice from embryonic stem cells arrested at metaphase. Reproduction 122:731-736.
44. Orr NH, DiBerardino MA, McKinnell RG. 1986. The genome of frog erythrocytes displays centuplicate replications. Proc Natl Acad Sci USA 83:1369-1373.
45. Park KW, Lai L, Cheong HT, Cabot R, Sun QY, Wu G, Rucker EB, Durtschi D, Bonk A, Samuel M, Rieke A, Day BN, Murphy CN, Carter DB, Prather RS. 2002. Mosaic gene expression in nuclear transfer-derived embryos and the production of cloned transgenic pigs from ear-derived fibroblasts. Biol Reprod 66:1001-1005.
46. Peura TT, Lane MW, Lewis IM, Trounson AO. 2001. Development of bovine embryo-derived clones after increasing rounds of nuclear recycling. Mol Reprod Dev 58:384-389.
47. Piotrowska K, Modliński JA, Korwin-Kossakowski M, Karasiewicz J. 2000. Effects of pre-activation of ooplasts or synchronization of blastomere nuclei in G1 on pre-implantation development of rabbit serial nuclear transfer embryos. Biol Reprod 63:677-682.
48. Polejaeva IA, Chen SH, Vaught TD, Page RL, Mullins J, Ball S, Dai Y, Boone J, Walker S, Ayares DL, Colman A, Campbell KH. 2000. Cloned pigs produced by nuclear transfer from adult somatic cells. Nature 407:86-90.
49. Polejaeva IA, Walker S, Campbell K. 2006. A double nuclear transfer technique for cloning pigs. Methods Mol Biol 348:135-150.
50. Prather RS, Sims MM, First NL. 1989. Nuclear transplantation in early pig embryos. Biol Reprod 41:414-418.
51. Robl JM, Wang Z, Kasinathan P, Kuroiwa Y. 2007. Transgenic animal production and animal biotechnology. Theriogenology 67:127-133.
52. Rodda DJ, Chew JL, Lim LH, Loh YH, Wang B, Ng HH, Robson P. 2005. Transcriptional regulation of nanog by OCT4 and SOX2. J Biol Chem 280:24731-24737.
53. Santos F, Zakhartchenko V, Stojkovic M, Peters A, Jenuwein T, Wolf E, Reik W, Dean W. 2003. Epigenetic marking correlates with developmental potential in cloned bovine pre-implantation embryos. Curr Biol 13:1116-1121.
54. Stice SL, Keefer CL. 1993. Multiple generational bovine embryo cloning. Biol Reprod 48:715-719.
55. Takano H, Kozai C, Shimizu S, Kato Y, Tsunoda Y. 1997. Cloning of bovine embryos by multiple nuclear transfer. Theriogenology 47:1365-1373.
56. Tamashiro KL, Wakayama T, Akutsu H, Yamazaki Y, Lachey JL, Wortman MD, Seeley RJ, D'Alessio DA, Woods SC, Yanagimachi R, Sakai RR. 2002. Cloned mice have an obese phenotype not transmitted to their offspring. Nat Med 8:262-267.
57. Tazi J, Bird A. 1990. Alternative chromatin structure at CpG islands. Cell 60:909-920.
58. Varga-Weisz PD, Becker PB. 2006. Regulation of higher-order chromatin structures by nucleosome-remodelling factors. Curr Opin Genet Dev 16:151-156.
59. Viuff D, Greve T, Holm P, Callesen H, Hyttel P, Thomsen PD. 2002. Activation of the ribosomal RNA genes late in the third cell cycle of porcine embryos. Biol Reprod 66:629-634.
60. Wakayama T, Shinkai Y, Tamashiro KL, Niida H, Blanchard DC, Blanchard RJ, Ogura A, Tanemura K, Tachibana M, Perry AC, Colgan DF, Mombaerts P, Yanagimachi R. 2000. Cloning of mice to six generations. Nature 407:318-319.
61. Westhusin ME, Pryor JH, Bondioli KR. 1991. Nuclear transfer in the bovine embryo: A comparison of 5-day, 6-day, frozen-thawed, and nuclear transfer donor embryos. Mol Reprod Dev 28:119-123.
62. Whitworth KM, Agca C, Kim JG, Patel RV, Springer GK, Bivens NJ, Forrester LJ, Mathialagan N, Green JA, Prather RS. 2005. Transcriptional profiling of pig embryogenesis by using a 15-K member unigene set specific for pig reproductive tissues and embryos. Biol Reprod 72:1437-1451.
63. Willadsen SM. 1989. Cloning of sheep and cow embryos. Genome 31:956-962.
64. Yang X, Smith SL, Tian XC, Lewin HA, Renard JP, Wakayama T. 2007. Nuclear reprogramming of cloned embryos and its implications for therapeutic cloning. Nat Genet 39:295-302.
65. Yong Z, Yuqiang L. 1998. Nuclear-cytoplasmic interaction and development of goat embryos reconstructed by nuclear transplantation: Production of goats by serially cloning embryos. Biol Reprod 58:266-269.
66. Yoshioka K, Suzuki C, Tanaka A, Anas IM, Iwamura S. 2002. Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol Reprod 66:112-119.
67. Zakhartchenko V, Durcova-Hills G, Stojkovic M, Schernthaner W, Prelle K, Steinborn R, Müller M, Brem G, Wolf E. 1999. Effects of serum starvation and re-cloning on the efficiency of nuclear transfer using bovine fetal fibroblasts. J Reprod Fertil 115:325-331.
68. Zhu H, Craig JA, Dyce PW, Sunnen N, Li J. 2004. Embryos derived from porcine skin-derived stem cells exhibit enhanced preimplantation development. Biol Reprod 71:1890-1897.