Significant improvement in cloning efficiency of an inbred miniature pig by histone deacetylase inhibitor treatment after somatic cell nuclear transfer

Biology of Reproduction

Volumn 81, Issue 3, 2009, Pages 525-530

  Zhao, Jianguo ^a   Ross, Jason W ^a   Hao, Yanhong ^a   Spate, Lee D ^a   Walters, Eric M ^a   Samuel, Melissa S ^a   Rieke, August ^a   Murphy, Clifton N ^a   Prather, Randall S ^a  

^a UNIVERSITY OF MISSOURI   (United States)

Author keywords

Developmental biology; Early development; Embryo; HDAC inhibitor; Histone acetylation; Inbred; SCNT

Indexed keywords

6 (1,3 DIOXO 1H,3H BENZO[DE]ISOQUINOLIN 2 YL) N HYDROXYHEXANAMIDE;

ACETYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLASTOCYST; CELL NUCLEUS TRANSPLANTATION; CLONING; CONTROLLED STUDY; DONOR; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO TRANSFER; FEMALE; FERTILIZATION IN VITRO; FETUS; FIBROBLAST; INBRED STRAIN; MALE; MINIPIG; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; SOMATIC CELL;

ANIMALS; CLONING, ORGANISM; EFFICIENCY; EMBRYO TRANSFER; EMBRYONIC DEVELOPMENT; ENZYME INHIBITORS; FEMALE; FERTILIZATION IN VITRO; HISTONE DEACETYLASE INHIBITORS; HYDROXYLAMINES; INBREEDING; MALE; NUCLEAR TRANSFER TECHNIQUES; PREGNANCY; QUINOLINES; SWINE; SWINE, MINIATURE;

ANIMALIA; SUIDAE;

EID: 69849091474     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.109.077016     Document Type: Article

References (52)

1. Prather RS, Hawley RJ, Carter DB, Lai L, Greenstein JL. Transgenic swine for biomedicine and agriculture. Theriogenology 2003; 59:115-123.
2. McCreath KJ, Howcroft J, Campbell KH, Colman A, Schnieke AE, Kind AJ. Production of gene-targeted sheep by nuclear transfer from cultured somatic cells. Nature 2000; 405:1066-1069. (Pubitemid 30447792)
3. Park KW, Cheong HT, Lai LX, Im GS, Kuhholzer B, Bonk A, Samuel M, Rieke A, Day BN, Murphy CN, Carter DB, Prather RS. Production of nuclear transfer-derived swine that express the enhanced green fluorescent protein. Anim Biotechnol 2001; 12:173-181. (Pubitemid 33669076)
4. Lai L, Kolber-Simonds D, Park KW, Cheong HT, Greenstein JL, Im GS, Samuel M, Bonk A, Rieke A, Day BN, Murphy CN, Carter DB, et al. Production of alpha-1,3-galactosyltransferase knockout pigs by nuclear transfer cloning. Science 2002; 295:1089-1092. (Pubitemid 34132242)
5. Rogers CS, Stoltz DA, Meyerholz DK, Ostedgaard LS, Rokhlina T, Taft PJ, Rogan MP, Pezzulo AA, Karp PH, Itani OA, Kabel AC, Wohlford- Lenane CL, et al. Disruption of the CFTR gene produces a model of cystic fibrosis in newborn pigs. Science 2008; 321:1837-1841.
6. Rogers CS, Hao Y, Rokhlina T, Samuel M, Stoltz DA, Li Y, Petroff E, Vermeer DW, Kabel AC, Yan Z, Spate L, Wax D, et al. Production of CFTR-null and CFTR-DeltaF508 heterozygous pigs by adeno-associated virus-mediated gene targeting and somatic cell nuclear transfer. J Clin Invest 2008; 118:1571-1577.
7. Estrada JL, Collins B, York A, Bischoff S, Sommer J, Tsai S, Petters RM, Piedrahita JA. Successful cloning of the Yucatan minipig using commercial/occidental breeds as oocyte donors and embryo recipients. Cloning Stem Cells 2008; 10:287-296. (Pubitemid 351748828)
8. Vodicka P, Smetana K Jr, Dvorankova B, Emerick T, Xu YZ, Ourednik J, Ourednik V, Motlik J. The miniature pig as an animal model in biomedical research. Ann N Y Acad Sci 2005; 1049:161-171. (Pubitemid 40967583)
9. Sachs DH, Leight G, Cone J, Schwarz S, Stuart L, Rosenberg S. Transplantation in miniature swine, I: fixation of the major histocompatibility complex. Transplantation 1976; 22:559-567.
10. Mezrich JD, Haller GW, Arn JS, Houser SL, Madsen JC, Sachs DH. Histocompatible miniature swine: an inbred large-animal model. Transplantation 2003; 27:904-907.
11. Prather RS, Gibson J, Parry TW, Hoffman KE. Reproductive measurements in Sinclair and NIH miniature pigs: a retrospective analysis. Theriogenology 1997; 47:433-440. (Pubitemid 28137110)
12. Conley AJ, Jung YC, Schwartz NK, Warner CM, Rothschild MF, Ford SP. Influence of SLA haplotype on ovulation rate and litter size in miniature pigs. J Reprod Fertil 1988; 82:595-601. (Pubitemid 18083025)
13. Wilmut I, Beaujean N, de Sousa PA, Dinnyes A, King TJ, Paterson LA, Wells DN, Young LE. Somatic cell nuclear transfer. Nature 2002; 419: 583-586.
14. Kishigami S, Mizutani E, Ohta H, Hikichi T, Thuan NV, Wakayama S, Bui HT, Wakayama T. Significant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer. Biochem Biophys Res Commun 2006; 340:183-189. (Pubitemid 41827663)
15. Rybouchkin A, Kato Y, Tsunoda Y. Role of histone acetylation in reprogramming of somatic nuclei following nuclear transfer. Biol Reprod 2006; 74:1083-1089. (Pubitemid 47394287)
16. Kishigami S, Bui HT, Wakayama S, Tokunaga K, Van Thuan N, Hikichi T, Mizutani E, Ohta H, Suetsugu R, Sata T, Wakayama T. Successful mouse cloning of an outbred strain by trichostatin A treatment after somatic nuclear transfer. J Reprod Dev 2007; 53:165-170. (Pubitemid 46397253)
17. Li J, Svarcova O, Villemoes K, Kragh PM, Schmidt M, Bogh IB, Zhang Y, Du Y, Lin L, Purup S, Xue Q, Bolund L, et al. High in vitro development after somatic cell nuclear transfer and trichostatin A treatment of reconstructed porcine embryos. Theriogenology 2008; 70: 800-808.
18. Zhang Y, Li J, Villemoes K, Pedersen AM, Purup S, Vajta G. An epigenetic modifier results in improved in vitro blastocyst production after somatic cell nuclear transfer. Cloning Stem Cells 2007; 9:357-363.
19. Ding X, Wang Y, Zhang D, Wang Y, Guo Z, Zhang Y. Increased preimplantation development of cloned bovine embryos treated with 5-aza-2′- deoxycytidine and trichostatin A. Theriogenology 2008; 70:622-630.
20. Iager AE, Ragina NP, Ross PJ, Beyhan Z, Cunniff K, Rodriguez RM, Cibelli JB. Trichostatin A improves histone acetylation in bovine somatic cell nuclear transfer early embryos. Cloning Stem Cells 2008; 10:371-379.
21. Shi LH, Miao YL, Ouyang YC, Huang JC, Lei ZL, Yang JW, Han ZM, Song XF, Sun QY, Chen DY. Trichostatin A (TSA) improves the development of rabbit-rabbit intraspecies cloned embryos, but not rabbithuman interspecies cloned embryos. Dev Dyn 2008; 237:640-648.
22. Meng Q, Polgar Z, Liu J, Dinnyes A. Live birth of somatic cell-cloned rabbits following trichostatin A treatment and cotransfer of parthenogenetic embryos. Cloning Stem Cells 2009; 11:203-208.
23. Wu X, Li Y, Li GP, Yang D, Yue Y, Wang L, Li K, Xin P, Bou S, Yu H. Trichostatin A improved epigenetic modifications of transfected cells but did not improve subsequent cloned embryo development. Anim Biotechnol 2008; 19:211-224.
24. Svensson K, Mattsson R, James TC, Wentzel P, Pilartz M, MacLaughlin J, Miller SJ, Olsson T, Eriksson UJ, Ohlsson R. The paternal allele of the H19 gene is progressively silenced during early mouse development: the acetylation status of histones may be involved in the generation of variegated expression patterns. Development 1998; 125:61-69. (Pubitemid 28048454)
25. Tsuji Y, Kato Y, Tsunoda Y. The developmental potential of mouse somatic cell nuclear-transferred oocytes treated with trichostatin A and 5- aza-20-deoxycytidine. Zygote 2009; 17:109-115.
26. Su GH, Sohn TA, Ryu B, Kern SE. A novel histone deacetylase inhibitor identified by high-throughput transcriptional screening of a compound library. Cancer Res 2000; 60:3137-3142. (Pubitemid 30407906)
27. Lai L, Prather RS. Production of cloned pigs by using somatic cells as donors. Cloning Stem Cells 2003; 5:233-241. (Pubitemid 38031849)
28. Prather RS, Boice ML, Gibson J, Hoffman KE, Parry TW. In vitro development of embryos from Sinclair miniature pigs: a preliminary report. Theriogenology 1995; 43:1001-1007.
29. Li R, Murphy CN, Spate L, Wax D, Isom C, Rieke A, Walters EM, Samuel M, Prather RS. Production of piglets after cryopreservation of embryos using a centrifugation-based method for delipation without micromanipulation. Biol Reprod 2009; 80:563-571.
30. Hao Y, Mathialagan N, Walters E, Mao J, Lai L, Becker D, Li W, Critser J, Prather RS. Osteopontin reduces polyspermy during in vitro fertilization of porcine oocytes. Biol Reprod 2006; 75:726-733. (Pubitemid 44720392)
31. Ohgane J, Wakayama T, Senda S, Yamazaki Y, Inoue K, Ogura A, Marh J, Tanaka S, Yanagimachi R, Shiota K. The Sall3 locus is an epigenetic hotspot of aberrant DNA methylation associated with placentomegaly of cloned mice. Genes Cells 2004; 9:253-260. (Pubitemid 38380232)
32. Kang YK, Koo DB, Park JS, Choi YH, Chung AS, Lee KK, Han YM. Aberrant methylation of donor genome in cloned bovine embryos. Nat Genet 2001; 28:173-177.
33. Santos F, Zakhartchenko V, Stojkovic M, Peters A, Jenuwein T, Wolf E, Reik W, Dean W. Epigenetic marking correlates with developmental potential in cloned bovine preimplantation embryos. Curr Biol 2003; 13: 1116-1121. (Pubitemid 36815259)
34. Dean W, Santos F, Stojkovic M, Zakhartchenko V, Walter J, Wolf E, Reik W. Conservation of methylation reprogramming in mammalian develop- ment: aberrant reprogramming in cloned embryos. Proc Natl Acad Sci U S A 2001; 98:13734-13738. (Pubitemid 33115967)
35. Miyoshi K, Inoue S, Himaki T, Mikawa S, Yoshida M. Birth of cloned miniature pigs derived from somatic cell nuclear transferred embryos activated by ultrasound treatment. Mol Reprod Dev 2007; 74:1568-1574. (Pubitemid 350058422)
36. Li Y, Liu J, Dai J, Xing F, Fang Z, Zhang T, Shi Z, Zhang D, Chen X. Production of cloned miniature pigs by enucleation using the spindle view system. Reprod Domest Anim 2008; (in press). published online ahead of print 22 December 2008; DOI 10.1111/j.1439-0531.2008.01311.x.
37. Hao YH, Yong HY, Murphy CN, Wax D, Samuel M, Rieke A, Lai L, Liu Z, Durtschi DC, Welbern VR, Price EM, McAllister RM, et al. Production of endothelial nitric oxide synthase (eNOS) over-expressing piglets. Transgenic Res 2006; 15:739-750. (Pubitemid 44833186)
38. Kurome M, Ishikawa T, Tomii R, Ueno S, Shimada A, Yazawa H, Nagashima H. Production of transgenic and non-transgenic clones in miniature pigs by somatic cell nuclear transfer. J Reprod Dev 2008; 54: 156-163. (Pubitemid 351918066)
39. Wakai T, Sugimura S, Yamanaka K, Kawahara M, Sasada H, Tanaka H, Ando A, Kobayashi E, Sato E. Production of viable cloned miniature pig embryos using oocytes derived from domestic pig ovaries. Cloning Stem Cells 2008; 10:249-262. (Pubitemid 351748823)
40. Wakayama T, Yanagimachi R. Mouse cloning with nucleus donor cells of different age and type. Mol Reprod Dev 2001; 58:376-383. (Pubitemid 32179144)
41. Inoue K, Ogonuki N, Mochida K, Yamamoto Y, Takano K, Kohda T, Ishino F, Ogura A. Effects of donor cell type and genotype on the efficiency of mouse somatic cell cloning. Biol Reprod 2003; 69:1394-1400. (Pubitemid 37173877)
42. Simonsson S, Gurdon J. DNA demethylation is necessary for the epigenetic reprogramming of somatic cell nuclei. Nat Cell Biol 2004; 6: 984-990. (Pubitemid 39359851)
43. Armstrong L, Lako M, Dean W, Stojkovic M. Epigenetic modification is central to genome reprogramming in somatic cell nuclear transfer. Stem Cells 2006; 24:805-814. (Pubitemid 44464713)
44. Hebbes TR, Thorne AW, Crane-Robinson C. A direct link between core histone acetylation and transcriptionally active chromatin. EMBO J 1988; 7:1395-1402.
45. Hong L, Schroth GP, Matthews HR, Yau P, Bradbury EM. Studies of the DNA binding properties of histone H4 amino terminus: thermal denaturation studies reveal that acetylation markedly reduces the binding constant of the H4 "tail" to DNA. J Biol Chem 1993; 268:305-314.
46. Lee DY, Hayes JJ, Pruss D, Wolffe AP. A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell 1993; 72:73-84. (Pubitemid 23029694)
47. Zlatanova J, Caiafa P, Van Holde K. Linker histone binding and displacement: versatile mechanism for transcriptional regulation. FASEB J 2000; 14:1697-1704. (Pubitemid 30688619)
48. Eberharter A, Becker PB. Histone acetylation: a switch between repressive and permissive chromatin: second in review series on chromatin dynamics. EMBO Rep 2002; 3:224-229. (Pubitemid 34269514)
49. Cervoni N, Szyf M. Demethylase activity is directed by histone acetylation. J Biol Chem 2001; 276:40778-40787. (Pubitemid 37373223)
50. Ma J, Svoboda P, Schultz RM, Stein P. Regulation of zygotic gene activation in the preimplantation mouse embryo: global activation and repression of gene expression. Biol Reprod 2001; 64:1713-1721. (Pubitemid 32493489)
51. Gurvich N, Berman MG, Wittner BS, Gentleman RC, Klein PS, Green JB. Association of valproate-induced teratogenesis with histone deacetylase inhibition in vivo. FASEB J 2005; 19:1166-1168. (Pubitemid 40946453)
52. Kishigami S, Ohta H, Mizutani E, Wakayama S, Bui HT, Thuan NV, Hikichi T, Suetsugu R, Wakayama T. Harmful or helpful? Trischostatin A treatment of embryos generated by ICSI or ROSI. Cent Eur J Biol 2006; 1: 376-385. (Pubitemid 44325686)