Cloning animals by somatic cell nuclear transfer – biological factors

Reproductive Biology and Endocrinology

Xiangzhong Yang²  Brian Enright³  Chikara Kubota¹  X Cindy Tian³ 

[1] Kagoshima Prefectural Cattle Breeding and Genetic Institute, Kagoshima, Japan;Evergen Biotechnologies, Inc. Incubator Program at the University of Connecticut, 1392 Storrs Road, Storrs, CT06269-USA;Center for Regenerative Biology/Department of Animal Science, University of Connecticut, Storrs, Connecticut 06269-4243, USA

关键词: cell passage;    serum starvation;    donor age;    donor cell types;    nuclear transfer;   

Others  :  1156852
DOI  :  10.1186/1477-7827-1-98

 received in 2003-08-08, accepted in 2003-11-13,  发布年份 2003

【 摘 要 】

Cloning by nuclear transfer using mammalian somatic cells has enormous potential application. However, somatic cloning has been inefficient in all species in which live clones have been produced. High abortion and fetal mortality rates are commonly observed. These developmental defects have been attributed to incomplete reprogramming of the somatic nuclei by the cloning process. Various strategies have been used to improve the efficiency of nuclear transfer, however, significant breakthroughs are yet to happen. In this review we will discuss studies conducted, in our laboratories and those of others, to gain a better understanding of nuclear reprogramming. Because cattle are a species widely used for nuclear transfer studies, and more laboratories have succeeded in cloning cattle than any other specie, this review will be focused on somatic cell cloning of cattle.

【 授权许可】

   
2003 Tian et al; licensee BioMed Central Ltd. This is an Open Access article: verbatim copying and redistribution of this article are permitted in all media for any purpose, provided this notice is preserved along with the article's original URL.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Wilmut I, Schnieke AE, McWhir J, Kind AJ, Campbell KHS: Viable offspring derived from fetal and adult mammalian cells. Nature 1997, 385:810-813.
• [2]Anderson GB, Seidel GE: Cloning for profit. Science 1998, 280:1400-1401.
• [3]Polejaeva IA, Campbell KHS: New advances in somatic cell nuclear transfer: Application in transgenesis. Theriogenology 2000, 53:117-126.
• [4]Robl J: Development and application of technology for large scale cloning of cattle. Theriogenology 1999, 51:499-508.
• [5]Stice SL, Robl JM, Ponce de Leon FA, Jerry J, Golueke PG, Cibelli JB, Kane JJ: Cloning: new breakthroughs leading to commercial opportunities. Theriogenology 1998, 49:129-138.
• [6]Lanza RP, Cibelli JB, West MD: Human therapeutic cloning. Nat Med 1999, 5:975-977.
• [7]Capecchi MR: How close are we to implementing gene targeting in animals other than the mouse? Proc Natl Acad Sci USA 2000, 97:956-957.
• [8]Solter D: Imprinting. Int J Dev Biol 1998, 42:951-954.
• [9]De Sousa PA, Winger Q, Hill JR, Jones K, Watson AJ, Westhusin ME: Reprogramming of fibroblast nuclei after transfer into bovine oocytes. Cloning 1999, 1:63-69.
• [10]Munsie MJ, Michalska AE, O'Brien CM, Trounson AO, Pera MF, Mountford PS: Isolation of pluripotent embryonic stem cells from reprogrammed adult mouse somatic nuclei. Curr Biol 2000, 10:989-992.
• [11]Surani MA: Reprogramming of genome function through epigenetic inheritance. Nature 2001, 414:122-128.
• [12]Winger QA, Hill JR, Shin T, Watson AJ, Kraemer DC, Westhusin ME: Genetic reprogramming of lactate dehydrogenase, citrate synthase, and phosphofructokinase mRNA in bovine nuclear transfer embryos produced using bovine fibroblast cell nuclei. Mol Reprod Dev 2000, 56:458-464.
• [13]Garry FB, Adams R, McCann JP, Odde KG: Postnatal characteristics of calves produced by nuclear transfer cloning. Theriogenology 1996, 45:141-152.
• [14]Hill JR, Roussel AJ, Cibelli JB, Edwards JF, Hooper NL, Miller MW, Thompson JA, Looney CR, Westhusin ME, Robl JM, Stice SL: Clinical and pathologic features of cloned transgenic calves and fetuses (13 case studies). Theriogenology 1999, 51:1451-1465.
• [15]Kato Y, Tani T, Sotomaru Y, Kurokawa K, Kato J, Doguchi H, Yasue H, Tsunoda Y: Eight calves cloned from somatic cells of a single adult. Science 1998, 282:2095-2098.
• [16]Kubota C, Yamakuchi H, Todoroki J, Mizoshita K, Tabara N, Barber M, Yang X: Six cloned calves produced from adult fibroblast cells after long-term culture. Proc Natl Acad Sci USA 2000, 97:990-995.
• [17]Renard J-P, Chastnat S, Chesne P, Richard C, Marchal J, Cordonnier N, Chavatte P, Vignon X: Lymphoid hypoplasia and somatic cloning. Lancet 1999, 353:1489-1491.
• [18]Walker SK, Hartwich KM, Seamark RF: The production of unusually large offspring following embryo manipulation: concepts and changes. Theriogenology 1996, 45:111-120.
• [19]Young LE, Sinclear KD, Wilmut I: Large offspring syndrome in cattle and sheep. Rev Reprod 1998, 3:155-163.
• [20]Bourc'his D, Le Bourhis D, Patin D, Niveleau A, Comizzoli P, Renard J-P, Viegas-Pe'quignot E: Delayed and incomplete reprogramming of chromosome methylation patterns in bovine cloned embryos. Curr Biol 2001, 11:1542-1546.
• [21]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.
• [22]Kang Y-K, Koo D-B, Park J-S, Choi Y-H, Lee K-K, Han Y-M: Aberrant methylation of donor genome in cloned bovine embryos. Nat Genet 2001, 28:173-177.
• [23]Rideout WM III, Eggan K, Jaenisch R: Nuclear cloning and epigenetic reprogramming of the genome. Science 2001, 293:1093-1098.
• [24]Gibbons J, Arat S, Rzucidlo J, Miyoshi K, Waltenburg R, Respess D, Venable A, Stice S: Enhanced survivability of cloned calves derived from roscovitine-treated adult somatic cells. Biol Reprod 2002, 66:895-900.
• [25]Kasinathan P, Knott JG, Wang Z, Jerry DJ, Robl JM: Production of calves from G1 fibroblasts. Nat Biotechnol 2001, 19:1176-1178.
• [26]Wells DN, Laible G, Tucker FC, Miller AL, Oliver JE, Xiang T, Forsyth JT, Berg MC, Cockrem K, L'Huillier PJ, Tervit HR, Oback B: Coordination between donor cell type and cell cycle stage improves nuclear cloning efficiency in cattle. Theriogenology 2003, 59:45-59.
• [27]Campbell KH, Loi P, Cappai P, Wilmut I: Improved development to blastocyst of ovine nuclear transfer embryos reconstructed during the presumptive S-phase of enucleated activated oocytes. Biol Reprod 1994, 50:1385-1393.
• [28]Du F, Sung L-Y, Tian XC, Yang X: Differential Cytoplast Requirement for Embryonic and Somatic Cell Nuclear Transfer in Cattle. Mol Reprod Dev 2002, 63:183-191.
• [29]Hill JR, Winger QA, Long CR, Looney CR, Thompson JA, Westhusin ME: Development rates of male bovine nuclear transfer embryos derived from adult and fetal cells. Biol Reprod 2000, 62:1135-1140.
• [30]Kasinathan P, Knott JG, Moreira PN, Burnside AS, Jerry DJ, Robl JM: Effect of fibroblast donor cell age and cell cycle on development of bovine nuclear transfer embryos in vitro. Biol Reprod 2001, 64:1487-1493.
• [31]Renard JP: Chromatin remodeling and potential for full term development of cloned embryos. In In Proceedings of Transgenic Animals in Research. Conference Proceedings of Transgenic Animal Research Conference: Aug, 1999. Tahoe City, CA; 1999:15.
• [32]Tian XC, Xu J, Yang X: Normal telomere lengths found in cloned cattle. Nat Genet 2000, 26:272-273.
• [33]Xue F, Tian XC, Kubota C, Du F, Taneja M, Dinnyes A, Dai Y, Levine H, Pereira LV, Yang X: Aberrant X-Chromosome inactivation in deceased cattle derived from somatic cloning. Nat Genet 2002, 31:216-220.
• [34]Galli C, Duchi R, Moor RM, Lazzari G: Mammalian leukocytes contain all the genetic information necessary for the development of a new individual. Cloning 1999, 1:161-170.
• [35]Hochedlinger K, Jaenisch R: Monoclonal mice generated by nuclear transfer from mature B and T donor cells. Nature 2002, 415:1035-1038.
• [36]Kato Y, Tani T, Tsunoda Y: Cloning of calves from various somatic cell types of male and female adult, newborn and fetal cows. J Reprod Fertil 2000, 120:231-237.
• [37]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.
• [38]Ogura A, Inoue K, Ogonuki N, Noguchi A, Takano K, Nagano R, Suzuki O, Lee J, Ishino F, Matsuda J: Production of male cloned mice from fresh, cultured, and cryopreserved immature Sertoli cells. Biol Reprod 2000, 62:1579-1584.
• [39]Shiga K, Fujita T, Hirose K, Sasae Y, Nagai T: Production of calves by transfer of nuclei from cultured somatic cells obtained from Japanese black bulls. Theriogenology 1999, 52:527-535.
• [40]Arat S, Rzucidlo SJ, Gibbons J, Miyoshi K, Stice SL: Production of transgenic bovine embryos by transfer of transfected granulosa cells into enucleated oocytes. Mol Reprod Dev 2001, 60:20-26.
• [41]Liu L, Shin T, Pryor JH, Kraemer D, Westhusin M: Regenerated bovine fetal fibroblasts support high blastocyst development following nuclear transfer. Cloning 2001, 3:51-58.
• [42]Zakhartchenko V, Alberio R, Stojkovic M, Prelle K, Schernthaner W, Stojkovic P, Wenigerkind H, Wanke R, Duchler M, Steinborn R, Mueller M, Brem GE: Adult cloning in cattle: potential of nuclei from a permanent cell line and from primary cultures. Mol Reprod Dev 1999, 54:264-272.
• [43]Amano T, Kato Y, Tsunoda Y: Full-term development of enucleated mouse oocytes fused with embryonic stem cells from different cell lines. Reproduction 2001, 121:729-733.
• [44]Eggan K, Akutsu H, Loring J, Jackson-Grusby L, Klemm M, Rideout WM 3rd, Yanagimachi R, Jaenisch R: Hybrid vigor, fetal overgrowth, and viability of mice derived by nuclear cloning and tetraploid embryo complementation. Proc Natl Acad Sci USA 2001, 98:6209-6214.
• [45]Humpherys D, Eggan K, Akutsu H, Hochedlinger K, Rideout WM 3rd, Biniszkiewicz D, Yanagimachi R, Jaenisch R: Epigenetic instability in ES cells and cloned mice. Science 2001, 293:95-97.
• [46]Kato Y, Rideout III W, Hilton K, Barton SC, Tsunoda Y, Surani MA: Developmental potential of mouse primordial germ cells. Development 1999, 126:1823-1832.
• [47]Wakayama T, Rodriguez I, Perry ACF, Yanagimachi R, Mombaerts P: Mice cloned from embryonic stem cells. Proc Natl Acad Sci USA 1999, 96:14984-14989.
• [48]Zhou Q, Jouneau A, Brochard V, Adenot P, Renard JP: Developmental potential of mouse embryos reconstructed from metaphase embryonic stem cell nuclei. Biol Reprod 2001, 65:412-419.
• [49]Enright BP, Kubota C, Yang X, Tian XC: Epigenetic characteristics and development of embryos cloned from donor cells treated by Trichostatin A or 5-aza-2'-deoxycytidine. Biol Reprod 2003, 69:896-903.
• [50]Jones KL, Hill J, Shin TY, Lui L, Westhusin M: DNA hypomethylation of karyoplasts for bovine nuclear transplantation. Mol Reprod Dev 2001, 60:208-213.
• [51]Zhou Q, Baquir S, Brochard V, Smith LC, Renard JP: Donor nuclei are not well reprogrammed by nuclear transfer procedure. Biol Reprod 2002, 66(suppl 1):237-238. (s345)
• [52]Cibelli P, Stice SL, Golueke PJ, Kane JJ, Jerry J, Blackwell C, deLeon FAP, Robl JM: Cloned transgenic calves produced from non-quiescent fetal fibroblasts. Science 1998, 280:1256-1258.
• [53]Zakhartchenko V, Durcova-Hills G, Stojkovic M, Schernthaner W, Prelle K, Steinborn R, Muller M, Brem G, Wolf E: Effects of serum starvation and re-cloning on the efficiency of nuclear transfer using bovine fetal fibroblasts. J Reprod Fertil 1999, 115:325-331.
• [54]Roh S, Shim H, Hwang WS, Yoon JT: In vitro development of green fluorescent protein (GFP) transgenic bovine embryos after nuclear transfer using different cell cycles and passages of fetal fibroblasts. Reprod Fertil Dev 2000, 12:1-6.
• [55]Cho JK, Lee BC, Park JI, Lim JM, Shin SJ, Kim KY, Lee BD, Hwang WS: Development of bovine oocytes reconstructed with different donor somatic cells with or without serum starvation. Theriogenology 2002, 57:1819-1828.
• [56]Wakayama T, Yanagimachi R: Mouse cloning with nucleus donor cells of different age and type. Mol Reprod Dev 2001, 58:376-383.
• [57]Wakayama T, Perry AC, Zuccotti M, Johnson KR, Yanagimachi R: Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature 1998, 394:369-374.
• [58]Forsberg EJ, Strelchenko NS, Augenstein ML, Betthauser JM, Childs LA, Eilertsen KJ, Enos JM, Forsythe TM, Golueke PJ, Koppang RW, Lange G, Lesmeister TL, Mallon KS, Mell GD, Misica PM, Pace MM, Pfister-Genskow M, Voelker GR, Watt SR, Bishop MD: Production of cloned cattle from in vitro systems. Biol Reprod 2002, 67:327-333.
• [59]Enright BP, Jeong BS, Yang X, Tian XC: Epigenetic Characteristics of Bovine Donor Cells for Nuclear Transfer: Levels of Histone Acetylation. Biol Reprod 2003, in press.
• [60]Hirayu H, Dere WH: Rapoport B. Initiation of normal thyroid cells in primary culture associated with enhanced c-myc messenger ribonucleic acid levels. Endocrinology 1987, 120:924-928.
• [61]Baker TK, Carfagna MA, Gao H, Dow ER, Li Q, Searfoss GH, Ryan TP: Temporal gene expression analysis of monolayer cultured rat hepatocytes. Chem Res Toxicol 2001, 14:1218-1231.
• [62]Hill JR, Winger QA, Burghardt RC, Westhusin ME: Bovine nuclear transfer embryo development using cells derived from a cloned fetus. Anim Reprod Sci 2001, 67:17-26.
• [63]Mayer W, Niveleau A, Walter J, Fundele R, Haaf T: Demethylation of the zygotic paternal genome. Nature 2000, 403:501-502.
• [64]Oswald J, Engemann S, Lane N, Mayer W, Olek A, Fundele R, Dean W, Reik W, Walter J: Active demethylation of the paternal genome in the mouse zygote. Curr Biol 2000, 10:475-478.
• [65]Hoshikawa Y, Kwon HJ, Yoshida M, Horinouchi S, Beppu T: Trichostatin A induces morphological changes and gelsolin expression by inhibiting histone deacetylase in human carcinoma cell lines. Exp Cell Res 1994, 214:189-197.
• [66]Nakajima H, Kim YB, Terano H, Yoshida M, Horinouchi S: FR90 a Potent Antitumor Antibiotic, Is a Novel Histone deacetylase inhibitor. Expt Cell Res 1228, 241:126-133.