Production efficiency and telomere length of the cloned pigs following serial somatic cell nuclear transfer

Journal of Reproduction and Development

Volumn 54, Issue 4, 2008, Pages 254-258

  Kurome, Mayuko ^a,e   Hisatomi, Hisashi ^b   Matsumoto, Shirou ^c   Tomii, Ryo ^a   Ueno, Satoshi ^a   Hiruma, Katsumi ^a   Saito, Hitoshi ^a   Nakamura, Kimitoshi ^c   Okumura, Kenji ^c   Matsumoto, Mitsuhito ^d   Kaji, Yuji ^d   Endo, Fumio ^c   Nagashima, Hiroshi ^a  

^a MEIJI UNIVERSITY   (Japan)

^b SEIKEI UNIVERSITY   (Japan)

^c KUMAMOTO UNIVERSITY   (Japan)

^d NATIONAL AGRICULTURAL RESEARCH CENTER FOR KYUSHU OKINAWA REGION   (Japan)

^e UNIVERSITY OF MUNICH   (Germany)

Author keywords

Aging; Pig cloning; Progenitor cell; Somatic cell nuclear transfer (SCNT); Telomere

Indexed keywords

AGING; ANIMAL; ARTICLE; CELL NUCLEUS TRANSPLANTATION; CHEMISTRY; CLONING; EMBRYO (ANATOMY); EMBRYO CULTURE; EVALUATION; FEMALE; GENETICS; PHYSIOLOGY; PRENATAL DEVELOPMENT; PRODUCTIVITY; SWINE; TELOMERE;

AGING; ANIMALS; CLONING, ORGANISM; EFFICIENCY; EMBRYO CULTURE TECHNIQUES; EMBRYO, MAMMALIAN; FEMALE; NUCLEAR TRANSFER TECHNIQUES; SWINE; TELOMERE;

SUIDAE; SUS;

EID: 50249123514     PISSN: 09168818     EISSN: 13484400     Source Type: Journal    
DOI: 10.1262/jrd.20038     Document Type: Article

References (52)

1. Meissner A, Jaenisch R. Mammalian nuclear transfer. Dev Dyn 2006; 235: 2460-2469.
2. Dean W, Santos F, Stojkovic M, Zakhartchenko V, Walter J, Wolf E, Reik W. Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos. Proc Natl Acad Sci USA 2001; 98: 13734-13738.
3. Rideout WM, Eggan K, Jaenisch R. Nuclear cloning and epigenetic reprogramming of the genome. Science 2001; 293: 1093-1098.
4. Cibelli JB, Campbell KH, Seidel GE, West MD, Lanza RP. The health profile of cloned animals. Nat Biotechnol 2002; 20: 13-14.
5. 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. Cloning of mice to six generations. Nature 2000; 407: 318-319.
6. Kubota C, Tian XC, Yang X. Serial bull cloning by somatic cell nuclear transfer. Nat Biotechnol 2004; 22: 693-694.
7. Dai Y, Vaught TD, Boone J, Chen SH, Phelps CJ, Ball S, Monahan JA, Jobst PM, McCreath KJ, Lamborn AE, Cowell-Lucero JL, Wells KD, Colman A, Polejaeva IA, Ayares DL. Targeted disruption of the alpha1,3- galactosyltransferase gene in cloned pigs. Nat Biotechnol 2002; 20: 251-255.
8. 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, Hawley RJ, Prather RS. Production of alpha-1,3-galactosyltransferase knockout pigs by nuclear transfer cloning. Science 2002; 295: 1089-1092.
9. Phelps CJ, Koike C, Vaught TD, Boone J, Wells KD, Chen SH, Ball S, Specht SM, Polejaeva IA, Monahan JA, Jobst PM, Sharma SB, Lamborn AE, Garst AS, Moore M, Demetris AJ, Rudert WA, Bottino R, Bertera S, Trucco M, Starzl TE, Dai Y, Ayares DL. Production of alpha 1,3-galactosyltransferase-deficient pigs. Science 2003; 299: 411-414.
10. Ramsoondar JJ, Machaty Z, Costa C, Williams BL, Fodor WL, Bondioli KR. Production of alpha 1,3-galactosyltransferase-knockout cloned pigs expressing human alpha 1,2-fucosylosyltransferase. Biol Reprod 2003; 69: 437-445.
11. Dor FJ, Tseng YL, Cheng J, Moran K, Sanderson TM, Lancos CJ, Shimizu A, Yamada K, Awwad M, Sachs DH, Hawley RJ, Schuurman HJ, Cooper DK. Alpha1,3-galactosyltransferase gene-knockout miniature swine produce natural cytotoxic anti-Gal antibodies. Transplantation 2004; 78: 15-20.
12. Kolber-Simonds D, Lai L, Watt SR, Denaro M, Arn S, Augenstein ML, Betthauser J, Carter DB, Greenstein JL, Hao Y, Im GS, Liu Z, Mell GD, Murphy CN, Park KW, Rieke A, Ryan DJ, Sachs DH, Forsberg EJ, Prather RS, Hawley RJ. Production of alpha-1,3-galactosyltransferase null pigs by means of nuclear transfer with fibroblasts bearing loss of heterozygosity mutations. Proc Natl Acad Sci USA 2004; 101: 7335-7340.
13. Takahagi Y, Fujimura T, Miyagawa S, Nagashima H, Shigehisa T, Shirakura R, Murakami H. Production of alpha 1,3-galactosyltransferase gene knockout pigs expressing both human decay-accelerating factor and N-acetylglucosaminyltransferase III. Mol Reprod Dev 2005; 71: 331-338.
14. Fujimura T, Murakami H, Kurome M, Takahagi Y, Shigehisa T, Nagashima H. Effects of recloning on the efficiency of production of alpha 1,3-galactosyltransferaseknockout pigs. J Reprod Dev 2008; 54: 58-62.
15. Lai L, Kang JX, Li R, Wang J, Witt WT, Yong HY, Hao Y, Wax DM, Murphy CN, Rieke A, Samuel M, Linville ML, Korte SW, Evans RW, Starzl TE, Prather RS, Dai Y. Generation of cloned transgenic pigs rich in omega-3 fatty acids. Nat Biotechnol 2006; 24: 435-436.
16. Kurome M, Tomii R, Ueno S, Hiruma H, Saito H, Nakamura K, Okumura K, Matsumoto S, Matsumoto M, Kaji Y, Endo F, Nagashima H. Production of third-generation clones of a pig by somatic cell nuclear transfer. Reprod Fretil Dev 2006; 18: 133 (Abstract 50).
17. Cho SK, Kim JH, Park JY, Choi YJ, Bang JI, Hwang KC, Cho EJ, Sohn SH, Uhm SJ, Koo DB, Lee KK, Kim T, Kim JH. Serial cloning of pigs by somatic cell nuclear transfer: Restoration of phenotypic normality during serial cloning. Dev Dyn 2007; 236: 3369-3382.
18. Han YM, Kang YK, Koo DB, Lee KK. Nuclear reprogramming of cloned embryos produced in vitro. Theriogenology 2003; 59: 33-44.
19. Shiels PG, Kind AJ, Campbell KH, Waddington D, Wilmut I, Colman A, Schnieke AE. Analysis of telomere lengths in cloned sheep. Nature 1999; 399: 316-317.
20. Miyashita N, Shiga K, Yonai M, Kaneyama K, Kobayashi S, Kojima T, Goto Y, Kishi M, Aso H, Suzuki T, Sakaguchi M, Nagai T. Remarkable differences in telomere lengths among cloned cattle derived from different cell types. Biol Reprod 2002; 66: 1649-1655.
21. Clark AJ, Ferrier P, Aslam S, Burl S, Denning C, Wylie D, Ross A, de Sousa P, Wilmut I, Cui W. Proliferative lifespan is conserved after nuclear transfer. Nat Cell Biol 2003; 5: 535-538.
22. Shiels PG, Jardine AG. Dolly, no longer the exception: telomeres and implications for transplantation. Cloning Stem Cells 2003; 5: 157-160.
23. Betts DH, Perrault SD, Petrik J, Lin L, Favetta LA, Keefer CL, King WA. Telomere length analysis in goat clones and their offspring. Mol Reprod Dev 2005; 72: 461-470.
24. Alexander B, Coppola G, Perrault SD, Peura TT, Betts DH, King WA. Telomere length status of somatic cell sheep clones and their offspring. Mol Reprod Dev 2007; 74: 1525-1537.
25. Matsumoto S, Okumura K, Nakamura K, Matsumoto M, Kaji Y, Hiramoto A, Aizawa M, Kurome M, Nagashima H, Endo F. Isolation of the swine salivary gland derived endodermal progenitor cells, which differentiate into hepatic lineage by 3D culture. In: Proceedings of the 20th IUBMB International Congress of Biochemistry and Molecular Biology and 11th FAOBMB Congress; 2006; Kyoto, Japan. Abstract 558.
26. Matsumoto S, Okumura K, Ogata A, Hisatomi Y, Sato A, Hattori K, Matsumoto M, Kaji Y, Takahashi M, Yamamoto T, Nakamura K, Endo F. Isolation of tissue progenitor cells from duct-ligated salivary glands of swine. Cloning Stem Cells 2007; 9: 176-190.
27. Kurome M, Tomii R, Ueno S, Hiruma K, Matsumoto S, Okumura K, Nakamura K, Matsumoto M, Kaji Y, Endo F, Nagashima H. Production of cloned pigs from salivary gland-derived progenitor cells. Cloning Stem Cells 2008; 10: 277-285.
28. Okumura K, Nakamura K, Hisatomi Y, Nagano K, Tanaka Y, Terada K, Sugiyama T, Umeyama K, Matsumoto K, Yamamoto T, Endo F. Salivary gland progenitor cells induced by duct ligation differentiate into hepatic and pancreatic lineages. Hepatology 2003; 38: 104-113.
29. Hisatomi Y, Okumura K, Nakamura K, Matsumoto S, Sato A, Nagano K, Yamamoto T, Endo F. Flow cytometric isolation of endodermal progenitors from mouse salivary gland differentiate into hepatic and pancreatic lineages. Hepatology 2004; 39: 667-675.
30. Kurome M, Fujimura T, Murakami H, Takahagi Y, Wako N, Ochiai T, Miyazaki K, Nagashima H. Comparison of electro-fusion and intracytoplasmic nuclear injection methods in pig cloning. Cloning and Stem Cells 2003; 5: 367-378.
31. Kurome M, Ueda H, Tomii R, Naruse K, Nagashima H. Production of transgenicclone pigs by the combination of ICSI-mediated gene transfer with somatic cell nuclear transfer. Transgenic Res 2006; 15: 229-240.
32. 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 tansfer. J Reprod Dev 2008; 54: 156-163.
33. Miyano T, Hiro-oka RE, Kano K, Miyake M, Kusunoki H, Kato S. Effects of hyaluronic acid on the development of 1- and 2-cell porcine embryos to the blastocyst stage in vitro. Theriogenology 1994; 41: 1299-1305.
34. Kikuchi K, Onishi A, Kashiwazaki N, Iwamoto M, Noguchi J, Kaneko H, Akita T, Nagai T. Successful piglet production after transfer of blastocysts produced by a modified in vitro system. Biol Reprod 2002; 66: 1033-1041.
35. Nguyen V, Kure-bayashi S, Harayama H, Nagai T, Miyake M. Stage-specific effects of the osmolarity of a culture medium on the development of parthenogenetic diploids in the pig. Theriogenology 2003; 59: 719-734.
36. Harley CB, Futcher AB, Greider CW. Telomeres shorten during ageing of human fibroblasts. Nature 1990; 31: 458-460.
37. Zhu H, Craig JA, Dyce PW, Sunnen N, Li J. Embryos derived from porcine skinderived stem cells exhibit enhanced preimplantation development. Biol Reprod 2004; 71: 1890-1897.
38. Faast R, Harrison SJ, Beebe LF, McIlfatrick SM, Ashman RJ, Nottle MB. Use of adult mesenchymal stem cells isolated from bone marrow and blood for somatic cell nuclear transfer in pigs. Cloning Stem Cells 2006; 8: 166-173.
39. Inoue K, Ogonuki N, Miki H, Hirose M, Noda S, Kim JM, Aoki F, Miyoshin H, Ogura A. Inefficient reprogramming of the hematopoietic stem cell genome following nuclear transfer. J Cell Sci 2006; 15: 1985-1991.
40. Sung LY, Gao S, Shen H, Yu H, Song Y, Smith SL, Chang CC, Inoue K, Kuo L, Lian J, Li A, Tian XC, Tuck DP, Weissman SM, Yang X, Cheng T. Differentiated cells are more efficient than adult stem cells for cloning by somatic cell nuclear transfer. Nat Genet 2006; 38: 1323-1328.
41. Inoue K, Noda S, Ogonuki N, Miki H, Inoue S, Katayama K, Mekada K, Miyoshi H, Ogura A. Differential developmental ability of embryos cloned from tissue-specific stem cells. Stem Cells 2007; 25: 1279-1285.
42. Jin HF, Kumar BM, Kim JG, Song HJ, Jeong YJ, Cho SK, Balasubramanian S, Choe SY, Rho GJ. Enhanced development of porcine embryos cloned from bone marrow mesenchymal stem cells. Int J Dev Biol 2007; 51: 85-90.
43. Nagashima H, Haruyama E, Ikeda Y, Matsunari H, Kurome M. Application of the designer pigs to fundamental medical research. In: Association of Japanese Agricultural Scientific Societies (ed.), Genetic Engineering of Animals and Microorganisms. Tokyo: Yokendo; 2007: 129-147 (In Japanese).
44. Bourc'his D, Le Bourhis D, Patin D, Niveleau A, Comizzoli P, Renard JP, Viegas-Pequignot E. Delayed and incomplete reprogramming of chromosome methylation patterns in bovine cloned embryos. Curr Biol 2001; 11: 1542-1546.
45. 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.
46. Kozik A, Bradbury EM, Zalensky A. Increased telomere size in sperm cells of mammals with long terminal (TTAGGG)n arrays. Mol Reprod Dev 1998; 51: 98-104.
47. Fradiani PA, Ascenzioni F, Lavitrano M, Donini P. Telomeres and telomerase activity in pig tissues. Biochimie 2004; 86: 7-12.
48. Jiang L, Carter DB, Xu J, Yang X, Prather RS, Tian XC. Telomere lengths in cloned transgenic pigs. Biol Reprod 2004; 70: 1589-1593.
49. Tian XC, Xu J, Yang X. Normal telomere lengths found in cloned cattle. Nat Genet 2000; 26: 272-273.
50. Betts D, Bordignon V, Hill J, Winger Q, Westhusin M, Smith L, King W. Reprogramming of telomerase activity and rebuilding of telomere length in cloned cattle. Proc Natl Acad Sci USA 2001; 98: 1077-1082.
51. Lanza RP, Cibelli JB, Blackwell C, Cristofalo VJ, Francis MK, Baerlocher GM, Mak J, Schertzer M, Chavez EA, Sawyer N, Lansdorp PM, West MD. Extension of cell lifespan and telomere length in animals cloned from senescent somatic cells. Science 2000; 288: 665-669.
52. Jeon HY, Hyun SH, Lee GS, Kim HS, Kim S, Jeong YW, Kang SK, Lee BC, Han JY, Ahn C, Hwang WS. The analysis of telomere length and telomerase activity in cloned pigs and cows. Mol Reprod Dev 2005; 71: 315-320.