DOI QR코드

DOI QR Code

Production of Cloned Korean Native Goat (Capra hircus) by Somatic Cell Nuclear Transfer

  • Park, H.S. (Department of Animal Science and Biotechnology, Jinju National University) ;
  • Jung, S.Y. (Department of Animal Science and Biotechnology, Jinju National University) ;
  • Kim, T.S. (Department of Animal Science and Biotechnology, Jinju National University) ;
  • Park, J.K. (Gyeongnam Province Advanced Swine Research Institute) ;
  • Moon, T.S. (Department of Animal Science and Biotechnology, Jinju National University) ;
  • Hong, S.P. (Department of Animal Science and Biotechnology, Jinju National University) ;
  • Jin, J.I. (Department of Animal Science and Biotechnology, Jinju National University) ;
  • Lee, J.S. (Department of Animal Science and Biotechnology, Jinju National University) ;
  • Lee, J.H. (EASY BIO System, Inc.) ;
  • Sohn, S.H. (Department of Animal Science and Biotechnology, Jinju National University) ;
  • Lee, C.Y. (Regional Animal Industry Center, Jinju National University) ;
  • Moon, Y.S. (Department of Animal Science and Biotechnology, Jinju National University)
  • Received : 2006.07.25
  • Accepted : 2006.11.17
  • Published : 2007.04.01

Abstract

The objectives of the present study were to initiate cloning of Korean native goat by somatic cell nuclear transfer (NT) and to examine whether unovulated (follicular) oocytes can support the same developmental ability of NT embryos as ovulated (oviductal) oocytes after hCG injection in stimulated cycles of the goat. The in vivo-matured and immature oocytes were collected from the oviducts and follicles of superovulated does, respectively, and the immature oocytes were maturated in vitro. Ear skin fibroblasts derived from a 3-yr-old female Korean native goat were used as the donors of nuclei or karyoplasts. Following fusion, activation and in vitro culture to a 2- to 4-cell stage, 49 in vitro-derived and 105 in vivo-derived embryos were transferred to 6 and 17 recipient does, respectively. One doe and three does of the respective groups were identified as pregnant by ultrasonography on day 30 after embryo transfer. However, only one doe, which had received in vivo-derived embryos, delivered a normal female kid of 1.9 kg on d 149. The cloned kid gained more weight than her age-matched females as much as 87% during the first 4 mo after birth (17.7 vs. $9.4{\pm}0.8$ kg) and reached puberty at 6-mo age a few months earlier than normal female does. The telomere length of the kid, which was similar to that of the donor fibroblast at 2-mo age, decreased 8% between 2- and 7-mo ages. Moreover, at 7-mo age, she had 21% shorter telomere than her age-matched goats. To our knowledge, this is the first case in which a cloned animal born with a normal weight exhibited accelerated growth and development. The unusually rapid growth and development of the cloned goat may have resulted from SCNT-associated epigenetic reprogramming involving telomere shortening.

Keywords

References

  1. Baguisi, A., E. Behboodi, D. T. Melican, J. S. Pollock, M. M. Destrempes, C. Cammuso, J. L. Williams, S. D. Nims, C. A. Porter, P. Midura, M. J. Palacios, S. L. Ayres, R. S. Denniston, M. L. Hayes, C. A. Ziomek, H. M. Meade, R. A. Godke, W. G. Gavin, E. W. Overstrom and Y. Echelard. 1999. Production of goats by somtic cell nuclear transfer. Nature Biotechnol. 17:456-461. https://doi.org/10.1038/8632
  2. Behboodi, E., E. Memili, D. T. Melican, M. M. Destrempes, S. A. Overton, J. L. Williams, P. A. Flanagan, R. E. Butler, H. Liem, L. H. Chen, H. M. Meade, W. G. Gavin and Y. Echelard. 2004. Viable transgenic goats derived from skin cells. Transgenic Res. 13:215-224. https://doi.org/10.1023/B:TRAG.0000034620.59250.fd
  3. Betts, D., V. Bordignon, J. Hill, Q. Winger, M. Westhusin, L. Smith and W. King. 2001. Reprogramming of telomere activity and rebuilding of telomere length in cloned cattle. Proc. Natl. Acad. Sci. 98:1077-1082. https://doi.org/10.1073/pnas.031559298
  4. Betts, D. H., S. D. Perrault, J. Petrick, L. Lin, L. A. Favetta, C. L. Keefer and W. A. King. 2005. Telomere length analysis in goat clones and their offspring. Mol. Reprod. Dev. 72:461-470. https://doi.org/10.1002/mrd.20371
  5. Buonomo, F. C. and C. A. Baile. 1991. Influence of nutritional deprivation on insulin-like growth factor I, somatotrophin, and metabolic hormones in swine. J. Anim. Sci. 69:755-760. https://doi.org/10.2527/1991.692755x
  6. Campbell, K. H. S., J. McWhir, W. A. Ritchie and I. Wilmut. 1996. Sheep cloned by nuclear transfer from a cultured cell line. Nature 380:64-66. https://doi.org/10.1038/380064a0
  7. Carroll, J. A., T. A. Veum and R. L. Matteri. 1998. Endocrine responses to weaning and changes in post-weaning diet in the young pig. Domest. Anim. Endocrinol. 15:183-194. https://doi.org/10.1016/S0739-7240(98)00006-X
  8. Chang, Z., X. Fan, M. Luo, Z. Wu and J. Tan. 2006. Factors affecting superovulation and embryo transfer in Boer goats. Asian-Aust. J. Anim. Sci. 19:341-346. https://doi.org/10.5713/ajas.2006.341
  9. Chavatte-Palmer, P., Y. Hayman, C. Richard, P. Monget, D. LeBourhis, G. Kann, Y. Chilliard, X. Vignon and J. P. Renard. 2002. Clinical, hormonal, and hematological characteristics of bovine calves derived from nuclei from somatic cells. Biol. Reprod. 66:1596-1603. https://doi.org/10.1095/biolreprod66.6.1596
  10. Chesne, P., P. G. Adenot, C. Viglietta, M. Baratte, L. Boulanger and J. P. Renard. 2002. Cloned rabbits produced by nuclear transfer from adult somatic cells. Nat. Biotechnol. 20:366-369. https://doi.org/10.1038/nbt0402-366
  11. Choe, S. Y., C. S. Park, D. J. Song and J. H. Kim. 1986. Serum levels of progesterone and estradiol during gestation and peripartum period in Korean native goats. Kor. J. Anim. Sci. 28:400-406.
  12. Dominiko, T., J. Ramalho-Santos, A. Chan, R. D. Moreno, C. M. Luetjens, C. Simerly, L. Hewitson, D. Takahashi, C. Martinovich, J. M. White and G. Schatten. 1999. Optimization strategies for production of mammalian embryos by nuclear transfer. Cloning 1:143-152. https://doi.org/10.1089/15204559950019906
  13. Edwards, J. L., C. M. Dorado, T. J. Wilson and F. N. Schrick. 2001. Development of cloned embryos reconstructed with serum fed or serum starved adult granulose cells. Theriogenol. 55:265.
  14. Edwards, J. L., F. N. Schrick, M. D. McCracken, S. R. Van Amstel, F. M. Hopkins, M. G. Welborn and C. J. Davies. 2003. Cloning adult farm animals: a review of the possibilities and problems associated with somatic cell nuclear transfer. Am. J. Reprod. Immunol. 50:113-123. https://doi.org/10.1034/j.1600-0897.2003.00064.x
  15. Eppig, J. J. 1996. Coordination of nuclear and cytoplasmic oocye maturation in eutherian mammals. Reprod. Fert. Dev. 8:485-489. https://doi.org/10.1071/RD9960485
  16. Govoni, K. E., X. C. Tian, G.. W. Kazmer, M. Taneja, B. P. Enright, A. L. Rivard, X. Yang and S. A. Zinn. 2002. Age related changes of the somatotropic axis in cloned Holstein calves. Biol. Reprod. 66:1293-1298. https://doi.org/10.1095/biolreprod66.5.1293
  17. Heyman, Y. and J. P. Renard. 1996. Cloning of domestic species. Anim. Reprod. Sci. 42:427-436. https://doi.org/10.1016/0378-4320(96)01528-X
  18. Hill, J. R., A. J. Roussel, J. B. Cibelli, J. F. Edwards, R. N. Hooper, M. W. Miller, J. A. Thompson, C. R. Looney, M. E. Westhusin, J. M. Robl and S. L. Stice. 1999. Clinical and pathologic features of cloned transgenic calves and fetuses (13 case studies). Theriogenol. 51:1451-1465. https://doi.org/10.1016/S0093-691X(99)00089-8
  19. Hill, J. R., Q. A. Winger, C. R. Long, C. R. Looney, J. A. Thompson and M. E. Westhusin. 2000. Developmental rates of male bovine nuclear transfer embryos derived from adult and fetal cells. Biol. Reprod. 62:1135-1140. https://doi.org/10.1095/biolreprod62.5.1135
  20. ISCNDB2000. 2001. International System for chromosome nomenclature of domestic bovids (ISCNDB2000). Cytogenet. Cell Genet. 92:283-299. https://doi.org/10.1159/000056917
  21. Jeon, H. Y., S. H. Hyun, G. S. Lee, H. S. Kim, S. Kim, Y. W. Jeong, S. K. Kang, B. C. Lee, J. Y. Han, C. Ahn and W. S. Hwang 2005. The analysis of teleomere length and telomere activity in cloned pigs and cows. Mol. Reprod. Dev. 71:315-320. https://doi.org/10.1002/mrd.20279
  22. Kato, Y., T. Tani, Y. Sotomary, K. Kurokawa, J. Kato, H. Doguchi, H. Yasue and Y. Tsunoda. 1998. Eight calves cloned from somatic cells of a single adult. Sci. 282:2095-2098. https://doi.org/10.1126/science.282.5396.2095
  23. Keefer, C. L., H. Baldassarre, R. Keyston, B. Wang, B. Bhatia, A. S. Bilodeau, J. F. Zhou, M. Leduc, B. R. Downey, A. Lazaris and C. N. Karatzas. 2001. Generation of dwarf goat (Capra hircus) clones following nuclear transfer with transfected and nontransfected fetal fibroblasts and in vitro matured oocytes. Biol. Reprod. 64:849-856. https://doi.org/10.1095/biolreprod64.3.849
  24. Keefer, C. L., R. Keyston, A. Lazzaris, B. Bhatia, I. Begin, A. S. Bioldeau, F. J. Zhou, B. Wang, H. Baldassarre and C. N. Karatzas. 2002. Production of cloned goats after nuclear transfer using adult somatic cells. Biol. Reprod. 66:199-203. https://doi.org/10.1095/biolreprod66.1.199
  25. Kumar, J., J. C. Osborn and A. W. Cameron. 1991. Luteinizing hormone and follicle stimulating hormone induce premature condensation of chromatin in goat (Capra hircus) oocytes. Reprod. Fert. Dev. 3:585-591. https://doi.org/10.1071/RD9910585
  26. Landry, A. M., D. J. Landry, L. R. Gentry, H. L. Green, B. Reggio, K. L. Koonce, Y. Echelard and R. A. Godke. 2005. Endocrine profiles and growth patterns of cloned goats. Cloning Stem Cells 7:214-225. https://doi.org/10.1089/clo.2005.7.214
  27. Lanza, R. P., J. B. Cibelli, C. Blackwall, V. J. Cristofalo, M. K. Francis, G. M. Baerlocher, J. Mak, M. Schertzer, E. A. Chavez, N. Sawyer, P. M. Lansdorp and M. D. West. 2000. Extension of cell life-span and telomere length in animals cloned from senescent somatic cells. Sci. 288:665-669. https://doi.org/10.1126/science.288.5466.665
  28. Lee, B. C., M. K. Kim, G. Jang, H. J. Oh, F. Yuda, H. J. Kim, M. H. Shamim, J. J. Kim, S. K. Kang, G.. Schatten and W. S. Hwang. 2005a. Dogs cloned from adult somatic cells. Nature 436:641. https://doi.org/10.1038/436641a
  29. Lee, C. Y., S. H. Ha, K. H. Baik, S. H. Sohn, B. C. Park and M. J. Park. 2005b. Effects of estradiol implantation on growth, carcass traits and circulating concentrations of insulin-like growth factors (IGFs) and IGF-binding protein-3 in finishing barrows. Livestock. Prod. Sci. 96:149-155. https://doi.org/10.1016/j.livprodsci.2005.01.007
  30. Matsuzaki, M. and K. Shiga. 2002. Endocrine characteristics of cloned calves. Cloning Stem Cells 4:261-267 https://doi.org/10.1089/15362300260339548
  31. Miyashita, N., K. Shiga, M. Yonai, K. Kaneyama, S. Kobayashi, T. Kojima, Y. Goto, M. Kishi, H. Aso, T. Suzuki, M. Sakaguchi and T. Nagai. 2002. Remarkable differences in telomere lengths among cloned cattle derived from different cell types. Biol. Reprod. 66:1649-1655. https://doi.org/10.1095/biolreprod66.6.1649
  32. Park, C. S., S. Y. Choe, H. J. Lee, J. S. Lee and H. S. Park. 1991. Studies on the technological development of embryo transfer and manipulation in goats. Korean J. Anim. Sci. 33:294-301.
  33. Park, H. S., Y. H. Lee, T. S. Kim, J. K. Park, J. S. Lee, C. H. Lee and J. Y. Jung. 2004. Effects of repeated superovulation on recovery and quality of oocytes in Korean native goats. Kor. J. Emb. Trans. 19:81-87.
  34. Polejaeva, I. A., S. H. Chen, T. D. Vaught, R. L. Page, J. Mullins, S. Ball, Y. Dal, J. Boone, S. Walker, D. L. Ayares, A. Coleman and K. H. S. Campbell. 2000. Cloned pigs produced by nuclear transfer from adult somatic cells. Nature 407:86-90. https://doi.org/10.1038/35024082
  35. Reggio, B. C., A. N. James, H. L. Green, W. G. Gavin, E. Behboodi, Y. Echelard and R. A. Godke. 2001. Cloned transgenic offspring resulting from somatic cell nuclear transfer in the goat: Oocytes derived from both folliclestimulating hormone-stimulated and nonstimulated abattoirderived ovaries. Biol. Reprod. 65:1528-1533. https://doi.org/10.1095/biolreprod65.5.1528
  36. Rideout, W. M., 3rd., K. Eggan and R. Jaenisch. 2001. Nuclear cloning and epigenetic reprogramming of the genome. Sci. 293:1093-1098. https://doi.org/10.1126/science.1063206
  37. Shiels, P. G.., A. J. Kind, K. H. Campbell, D. Waddington, I. Wilmut, A. Coleman and A. E. Schnicke. 1999a. Analysis of telomere lengths in cloned sheep. Nature 399:316-317.
  38. Shiels, P. G., A. J. Kind, K. H. Campbell, I. Wilmut, D. Waddington, A. Coleman and A. E. Schnicke. 1999b. Analysis of telomere length in Dolly, a sheep derived by nuclear transfer. Cloning 1:119-125. https://doi.org/10.1089/15204559950020003
  39. Shin, T., D. Kraemer, J. Pryor, L. Liu, J. Rugila, L. Howe, S. Buck, K. Murphy, L. Lyons and M. Westhusin. 2002. A cat cloned by nuclear transplantation. Nature 415:859 https://doi.org/10.1038/nature00980
  40. Sohn, S. H., C. Y. Lee, E. K. Ryu, J. Y. Han, A. S. Multani and S. Pathak. 2002a. Rapid sex identification of chicken by fluorescence in situ hybridization using a W chromosomespedific DNA prob. Asian-Aust. J. Anim. Sci. 15:1531-1535. https://doi.org/10.5713/ajas.2002.1531
  41. Sohn, S. H., A. S. Muttani, P. K. Gugnani and S. Pathak. 2002b. Telomere erosion-induced mitotic castastrophe in continuously grown Chinese hamster Don cells. Exptle. Cell Res. 279:271-276. https://doi.org/10.1006/excr.2002.5614
  42. Song, D. J. and C. S. Park. 1984. A study on induction and synchronization of estrus in Korean native goats. Kor. J. Anim. Sci. 26:13-22.
  43. Thomas, R. E., J. G. Thompson, D. T. Armstrong and R. B. Gilchrist. 2004. Effect of specific phosphodiesterase isoenzyme inhibitors during in vitro maturation of bovine oocytes on meiotic and developmental capacity. Biol. Reprod. 71:1142-1149. https://doi.org/10.1095/biolreprod.103.024828
  44. Tian, X. C., J. Xu and X. Yang. 2000. Normal telomere lengths found in cloned cattle. Nat. Genet. 26:272-273. https://doi.org/10.1038/81559
  45. Vajta, G.. and M. Gjerris. 2006. Science and technology of farm animal cloning: state of the art. Anim. Reprod. Sci., Jan. 5; Pub ahead of print.
  46. Vignon, X., P. Chesne, D. LeBourhis, J. E. Flechon, Y. Heyman and J. P. Renard. 1998. Developmental potential of bovine embryos reconstructed from enucleated matured oocytes fused with cultured somatic cells. CR Acad. Sci. Ser. III Life Sci. 321:735-745.
  47. Wakayama, T., A. C. Perry, M. Zuccotti, K. R. Johnson and R. Yanagimachi. 1998. Full term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature 394:369-374. https://doi.org/10.1038/28615
  48. Wakayama, T., I. Rodriguez, A. C. Perry, R. Yanagimachi and P. Mombaerts. 1999. Mice cloned from embryonic stem cells. Proc. Natl. Acad. Sci. USA.
  49. Walker, S. K., K. M. Hartwich and R. F. Seamark. 1996. The production of unusually large offspring following embryo manipulation: concepts and challenges. Theriogenol. 45:111-120. https://doi.org/10.1016/0093-691X(95)00360-K
  50. Wells, D. N., P. M. Misica, A. M. Day and H. R. Tervit. 1997. Production of cloned lambs from an established embryonic cell line: a comparison between in vivo- and in vitro-matured cytoplasts. Biol. Reprod. 57:385-393. https://doi.org/10.1095/biolreprod57.2.385
  51. Wells, D. N., P. M. Misica, H. R. Tervit and W. H. Vivanco. 1998. Adult somatic cell nuclear transfer is used to preserve the last surviving cow of the Enderby Island cattle breed. Reprod. Fertil. Dev. 10:369-378. https://doi.org/10.1071/R98109
  52. Wilmut, I. and K. H. S. Campbell. 1998. Quiescence in nuclear transfer. Sci. 281:1611.
  53. Wilmut, I., A. E. Schnieke, J. McWhir, A. J. Kind and K. H. S. Campbell. 1997. Viable offspring derived from fetal and adult mammalian cells. Nature 385:810-813. https://doi.org/10.1038/385810a0
  54. Young, L. E., K. D. Sinclair and I. Wilmut. 1998. Large offspring syndrome in cattle and sheep. Rev. Reprod. 3:155-163. https://doi.org/10.1530/ror.0.0030155
  55. Zakhartchenko, V., G. Durocova-Hills, M. Stojkovic, W. Schernthaner, K. Prelle, R. Steinborn, M. Muller, G. Brem and E. Wolf. 1999. Effects of serum starvation and re-cloning on the efficiency of nuclear transfer using bovine fetal fibroblasts. J. Reprod. Fertil. 115:325-331. https://doi.org/10.1530/jrf.0.1150325
  56. Zou, X., Y. Wang, Y. Cheng, Y. Yang, H. Ju, H. Tang, Y. Shen, Z. Mu, S. Xu and M. Du. 2002. Generation of cloned goats (Capra hircus) from transfected foetal fibrolbast cells, the effect of donor cell cycle. Mol. Reprod. Dev. 61:164-172. https://doi.org/10.1002/mrd.1143

Cited by

  1. Optimization of Procedure for Efficient Gene Transfer into Porcine Somatic Cells with Lipofection vol.21, pp.5, 2007, https://doi.org/10.5713/ajas.2008.70400
  2. Establishment and Characterization of the Fibroblast Line from Silkie Bantam vol.22, pp.4, 2009, https://doi.org/10.5713/ajas.2009.80480