Effect of nucleus transfer on gene expression in bovine embryos during early development

Acta Scientiae Veterinariae

Volumn 38, Issue SUPPL. 2, 2010, Pages

  Rodriguez Alvarez, Lleretny ^a   Castro, Fidel Ovidio ^a  

^a UNIVERSITY OF CONCEPCIÓN   (Chile)

Author keywords

Bovine; Elongation; Embryos; Gene expression; Pre implantation; SNCT

Indexed keywords

ANIMALIA; BOVINAE; MAMMALIA;

EID: 79958764585     PISSN: 16780345     EISSN: 16799216     Source Type: Journal    
DOI: None     Document Type: Article

References (102)

1. Amarnath D., Li X., Kato Y. & Tsunoda Y. 2007. Gene expression in individual bovine somatic cell cloned embryos at the 8-cell and blastocyst stages of preimplantation development. Journal of Reproduction and Development. 53: 1247-1263.
2. Arman E., Haffner-Krausz R., Chen Y., Heath J.K. & Lonai P. 1998. Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proceedings of the National Academy Sciences. 95: 5082-5087.
3. Arnold D.R., Bordignon V., Lefebvre R., Murphy B.D. & Smith L.C. 2006. Somatic cell nuclear transfer alters peri-implantation trophoblast differentiation in bovine embryos. Reproduction. 132: 279-290.
4. Baguisi A., Behboodi E., Melican D.T., Pollocks J.S., Destrempes M.M., Cammuso C., Williams J.L., Nims S.D., Porter C., Midura P., Palacios M.J., Ayres S.L., Denniston R.S., Hayes M.L., Ziomek C.A., Meade H.M., Godke R.A., Gavin W.G., Overström E.W. & Echelard Y. 1999. Production of goats by somatic cell nuclear transfer. Nature Biotechnology. 17: 456- 461.
5. Bertolini M., Beam S.W., Shim H., Bertolini L.R., Moyer A.L., Famula T.R. & Anderson G.B. 2002. Growth, development, and gene expression by in vivo- and in vitro-produced day 7 and 16 bovine embryos. Molecular Reproduction and Development. 63: 318-328.
6. Betteridge K.J. & Flechon J.E. 1988. The anatomy and physiology of preattachment bovine embryos. Theriogenology. 29: 155-187.
7. Beyhan Z., Forsberg E.J., Eilertsen K.J., Kent-First M. & First N.L. 2007. Gene expression in bovine nuclear transfer embryos in relation to donor cell efficiency in producing live offspring. Molecular Reproduction and Development. 74:18-27.
8. Boiani M., Eckardt S., Schöler H. & McLaughlin K.J. 2002. Oct4 distribution and level in mouse clones: consequences for pluripotency. Genes and Development. 16: 1209-1219.
9. Bordignon V., Keyston R., Lazaris A., Bilodeau A.S., Pontes J.H., Arnold D., Fecteau G., Keefer C. & Smith L.C. 2003. Transgene expression of green fluorescent protein and germ line transmission in cloned calves derived from in vitro-transfected somatic cells. Biology of Reproduction. 68: 2013-2023.
10. Bortvin A., Eggan K., Skaletsky H., Akutsu H., Berry D.L., Yanagimachi R., Page D.C. & Jaenisch R. 2003. Incomplete reactivation of Oct4-related genes in mouse embryos cloned from somatic nuclei. Development. 130: 1673-1680.
11. Brem G. & Kuhholzer B. 2002. The recent history of somatic cloning in mammals. Cloning and Stem Cells. 4: 57-63.
12. Campbell K.H., McWhir J., Ritchie W.A. & Wilmut I. 1996. Implications of cloning. Nature. 380: 383.
13. Castro F.O, Sharbati S., Rodríguez-Alvarez LL., Cox J.F., Hultschig C. & Einspanier R. 2010. MicroRNA expression profiling of elongated cloned and in vitro-fertilized bovine embryos. Theriogenology. 73(1): 71-85.
14. Chang M.C. 1952. Development of bovine blastocyst with a note on implantation. The Anatomical Record. 113(2): 143-161.
15. Charpigny G., Reinaud P., Tamby J.P., Créminon C. & Guillomot M. 1997. Cyclooxygenase-2 unlike cyclooxygenase-1 is highly expressed in ovine embryos during the implantation period. Biolology of Reproduction. 57: 1032-1040.
16. Daniels R., Hall V. & Trounson A.O. 2000. Analysis of gene transcription in bovine nuclear transfer embryos reconstructed with granulosa cell nuclei. Biology of Reproduction. 63: 1034- 1040.
17. Daniels R., Hall V.J., French A.J., Korfiatis N.A. & Trounson A.O. 2001. Comparison of gene transcription in cloned bovine embryos produced by different nuclear transfer techniques. Molecular Reproduction and Development. 60: 281-288.
18. Degrelle S., Campion E., Cabau C., Piumi F., Reinaud P., Richard C., Renard J-P. & Hue I. 2005. Molecular evidence for a critical period in mural trophoblast development in bovine blastocysts. Developmental Biology. 288: 448-460.
19. Desai N., Scarrow M., Lawson J., Kinzer D. & Goldfarb J. 1999. Evaluation of the effect of interleukin-6 and human extracellular matrix on embryonic development. Human Reproduction. 14: 1588-1592.
20. Donnison M., Beaton A., Davey H.W., Broadhurst R., L'Huillier P. & Pfeffer P.L. 2005. Loss of the extraembryonic ectoderm in Elf5 mutants leads to defects in embryonic patterning. Development. 132: 2299-2308.
21. El-Sayed A., Hoelker M., Rings F., Salilew D., Jennen D., Tholen E., Sirard M.A, Schellander K. & Tesfaye D. 2006. Large-scale transcriptional analysis of bovine embryo biopsies in relation to pregnancy success after transfer to recipients. Physiological Genomics. 28:84-96.
22. Enright B.P., Kubota C., Yang X. & Tian X.C. 2003. Epigenetic characteristics and development of embryos cloned from donor cells treated by Trichostatin A or 5-aza-2'-deoxycytidine. Biology of Reproduction. 69: 896-903.
23. Farin C.E., Imakawa K., Hansen T.R., McDonnell J.J., Murphy C.N., Farin P.W. & Roberts R.M. 1990. Expression of trophoblastic interferon genes in sheep and cattle. Biology of Reproduction. 43: 210-218.
24. Farin P.W., Slenning B.D. & Britt J.H. 1999. Estimates of pregnancy outcomes based on selection of bovine embryos produced in vivo or in vitro. Theriogenology. 52(4): 659-670.
25. Galli C., Duchi R., Crotti G., Turini P., Ponderato N., Colleoni S., Lagutina I. & Lazzari G. 2003. Bovine embryo technologies. Theriogenology. 59:599-616.
26. Garry F.B., Adams R., McCann J.P. & Odde K.G. 1996. Postnatal characteristics of calves produced by nuclear transfer cloning. Theriogenology. 45:141-152.
27. Gibbons J., Arat S., Rzucidlo J., Miyoshi K., Waltenburg R., Respess D., Venable A. & Stice S. 2002. Enhanced survivability of cloned calves derived from roscovitine-treated adult somatic cells. Biology of Reproduction. 66: 895-900.
28. Giraldez A.J., Mishima Y., Rihel J., Grocock R.J., Van Dongen S., Inoue K., Enright A.J. & Schier A.F. 2006. Zebrafish miR-430 promotes deadenylation and clearance of maternal mRNAs. Science. 312(5770): 75-79.
29. Green J.A., Xie S., Quan X., Bao B., Gan X., Mathialagan N., Beckers J.F. & Roberts R.M. 2000. Pregnancy-associated bovine and ovine glycoproteins exhibit spatially and temporally distinct expression patterns during pregnancy. Biolology of Reproduction. 62: 1624-1631.
30. Greenstein J.S, Murray R.W. & Foley R.C. 1958. Observations on the morphogenesis and histochemistry of the bovine preattachment placenta between 16 and 33 days of gestation. Anatomical Record. 132(3): 321-341.
31. Guillomot M. 1995. Cellular interactions during implantation in domestic ruminants. Journal of Reproduction and Fertility Supplement. 49: 39-51.
32. Hall V.J., Ruddock N.T. & French A.J. 2005. Expression profiling of genes crucial for placental and preimplantation development in bovine in vivo, in vitro, and nuclear transfer blastocysts. Molecular Reproduction and Development. 72: 16-24.
33. Hayes O., Ramos B., Rodríguez L.L., Aguilar A., Badía T. & Castro F.O. 2005. Cell confluency is as efficient as serum starvation for inducing arrest in the G0/G1 phase of the cell cycle in granulosa and fibroblast cells of cattle. Animal Reproduction Science. 87: 181-192.
34. Hayes O., Rodríguez L.L., González A., Falcón V., Aguilar A. & Castro F.O. 2005. Effect of cryopreservation on fusion efficiency and in vitro development into blastocysts of bovine cell lines used in somatic cell cloning. Zygote. 13: 277-282.
35. Heyman Y., Chavatte-Palmer P., Berthelot V., Fromentin G., Hocquette J.F., Martignat L. & Renard J.P. 2007. Assessing the quality of products from cloned cattle: an integrative approach. Theriogenology. 67:134-141.
36. Heyman Y., Richard C., Rodriguez-Martinez H., Lazzari G., Chavatte-Palmer P., Vignon X. & Galli C. 2004. Zootechnical performance of cloned cattle and offspring: preliminary results. Cloning and Stem Cells. 6: 111-120.
37. Hill J.R., Roussel A.J., Cibelli J.B., Edwards J.F., Hooper N.L., Miller M.W., Thompson J.A., Looney C.R., Westhusin M.E., Robl J.M. & Stice S.L. 1999. Clinical and pathologic features of cloned transgenic calves and fetuses (13 case studies). Theriogenology. 51: 1451-1465.
38. Hill J.R., Winger Q.A., Long C.R., Looney C.R., Thompson J.A. & Westhusin M.E. 2000. Development rates of male bovine nuclear transfer embryos derived from adult and fetal cells. Biology of Reproduction. 62: 1135-1140.
39. Hodges C.A. & Stice S.L. 2003. Generation of bovine transgenics using somatic cell nuclear transfer. Reproductive Biology and Endocrinology. 7(1): 81.
40. Hue I., Renard J.P. & Viebahn C. 2001. Brachyury is expressed in gastrulating bovine embryos well ahead of implantation. Development. Genes and Evolution. 211:157-159.
41. Kato Y., Tani T. & Tsunoda Y. 2000. Cloning of calves from various somatic cell types of male and female adult, newborn and fetal cows. Journal of Reproduction & Fertility. 120: 231-237.
42. Kato Y., Tani T., Sotomaru Y., Kurokawa K., Kato J., Doguchi H., Yasue H. & Tsunoda Y. 1998. Eight calves cloned from somatic cells of a single adult. Science. 282: 2095-2098.
43. Keefer C.L., Pant D., Blomberg L. & Talbot N.C. 2007. Challenges and prospects for the establishment of embryonic stem cell lines of domesticated ungulates. Animal Reproduction Science. 98: 147-168.
44. Klisch K., Hecht W., Pfarrer C., Schuler G., Hoffmann B. & Leiser R. 1999. DNA content and ploidy level of bovine placentomal trophoblast giant cells. Placenta. 20: 451-458.
45. Kues W.A., Anger M., Carnwath J.W., Paul D., Motlik J. & Niemann H. 2000. Cell cycle synchronization of porcine fetal fibroblasts: effects of serum deprivation and reversible cell cycle inhibitors. Biology of Reproduction. 62: 412-419.
46. Lagutina I., Lazzari G., Duchi R., Turini P., Tessaro I., Brunetti D., Colleoni S., Crotti G. & Galli C. 2007. Comparative aspects of somatic cell nuclear transfer with conventional and zona-free method in cattle, horse, pig and sheep. Theriogenology. 67: 90-98.
47. Lanza R.P., Cibelli J.B. & West MD. 1999. Human therapeutic cloning. Nature Medicine. 5: 975-977.
48. Lanza R.P., Cibelli J.B., Diaz F., Moraes C.T., Farin P.W., Farin C.E., Hammer C.J., West M.D. & Damiani P. 2000. Cloning of an endangered species (Bos gaurus) using interspecies nuclear transfer. Cloning. 2: 79-90.
49. Li J., Du Y., Zhang Y.H., Kragh P.M., Purup S., Bolund L., Yang H., Xue Q.Z. & Vajta G. 2006. Chemically assisted handmade enucleation of porcine oocytes. Cloning and Stem Cells. 8: 241-250.
50. Li J., Svarcova O., Villemoes K., Kragh P.M., Schmidt M., Bøgh I.B., Zhang Y., Du Y., Lin L., Purup S., Xue Q., Bolund L., Yang H., Maddox-Hyttel P. & Vajta G. 2008. High in vitro development after somatic cell nuclear transfer and trichostatin a treatment of reconstructed porcine embryos. Theriogenology. 70(5): 800-808.
51. Li X., Tremoleda J.L. & Allen W.R. 2003. Effect of the number of passages of fetal and adult fibroblasts on nuclear remodelling and first embryonic division in reconstructed horse oocytes after nuclear transfer. Reproduction. 125: 535-542.
52. MacLean II J.A., Chakrabarty A., Xie S., Bixby J.A., Roberts R.M. & Green J.A. 2003. Family of Kunitz proteins from trophoblast: expression of the trophoblast Kunitz domain proteins (TKDP) in cattle and sheep. Molecular Reproduction and Developmental. 65: 30-40.
53. Maddox-Hyttel P., Alexopoulos N.I., Vajta G., Lewis I., Rogers P., Cann L., Callesen H., Tveden-Nyborg P. & Trounson A. 2003. Immunohistochemical and ultrastructural characterization of the initial post-hatching development of bovine embryos. Reproduction. 125: 607-623.
54. Mann M.R., Chung Y.G., Nolen L.D., Verona R.I., Latham K.E. & Bartolomei M.S. 2003. Disruption of imprinted gene methylation and expression in cloned preimplantation stage mouse embryos. Biology of Reproduction. 69: 902-914.
55. Meisser A., Cameo P., Islami D., Campana A. & Bischof P. 1999. Effects of interleukin-6 (IL-6) on cytotrophoblastic cells. Molecular Human Reproduction. 5: 1055-1058.
56. Morris D.G., Diskin M.G. & Sreenan J.M. 2000. Protein synthesis and phosphorylation by elongating 13-15-day-old cattle blastocysts. Reproduction, Fertility and Development. 12: 39-44.
57. Niemann H., Wrenzycki C., Lucas-Hahn A., Brambrink T., Kues W.A. & Carnwath J.W. 2002. Gene expression patterns in bovine in vitro-produced and nuclear transfer-derived embryos and their implications for early development. Cloning and Stem Cells. 4: 29-38.
58. Niwa H., Miyazaki J., Nichols J., Zevnik B., Anastassiadis K., Klewe-Nebenius D. & Smith A.G. 2000. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nature Genetics. 24: 372-376.
59. Ogura A., Inoue K., Ogonuki N., Lee J., Kohda T. & Ishino F. 2002. Phenotypic effects of somatic cell cloning in the mouse. Cloning and Stem Cells. 4: 397-405.
60. Palmieri S.L., Peter W, Hess H. & Schöler H.R. 1994. Oct-4 transcription factor is differentially expressed in the mouse embryo during establishment of the first two extraembryonic cell lineages involved in implantation. Developmental Biology. 166(1): 259-267.
61. Peura T.T. & Vajta G. 2003. A comparison of established and new approaches in ovine and bovine nuclear transfer. Cloning and Stem Cells. 5(4): 257-277.
62. Ranilla M.J., Gebbie F.E., King M.E., Carolan C., Sinclair K.D., Watt R.G., Dolman D.F., Beckers J.F. & Robinson J.J. 1998. The incidence of embryo and fetal loss following the transfer of in vitro-cultured sheep embryos. Theriogenology. 49: 248.
63. Rappolee D.A., Basilico C., Patel Y. & Werb Z. 1994. Expression and function of FGF-4 in peri-implantation development in mouse embryos. Development. 120(8): 2259-2269.
64. Reggio B.C., James A.N., Green H.L., Gavin W.G., Behboodi E., Echelard Y. & Godke R.A. 2001. Cloned transgenic offspring resulting from somatic cell nuclear transfer in the goat: oocytes derived from both follicle-stimulating hormone-stimulated and nonstimulated abattoir-derived ovaries. Biology of Reproduction. 65: 1528-1533.
65. Rexroad, C.E. Jr & Powell, A.M. 1999. The ovine uterus as a host for in vitro-produced bovine embryos. Theriogenology. 15: 351-364.
66. Ribeiro Ede S., Gerger R.P., Ohlweiler L.U., Ortigari I. Jr., Mezzalira J.C., Forell F., Bertolini L.R., Rodrigues J.L., Ambrósio C.E., Miglino M.A., Mezzalira A. & Bertolini M. 2009. Developmental potential of bovine hand-made clone embryos reconstructed by aggregation or fusion with distinct cytoplasmic volumes. Cloning and Stem Cells. 11(3): 377-386.
67. Rieck W. & Dean W. 2002. Epigenetic reprogramming: back to the beginning. Nature. 420: 127.
68. Rodríguez LL., Navarrete F., Tovar H., Cox J. & Castro F.O. 2008. High developmental potential in vitro and in vivo of cattle embryos cloned without micromanipulators. Journal of Assisted Reproduction and Genetics. 25(1): 13-16.
69. Rodríguez-Alvarez L., Cox J., Navarrete F., Valdés C., Zamorano T., Einspanier R. & Castro F.O. 2009. Elongation and gene expression in bovine cloned embryos transferred to temporary recipients. Zygote. 8: 1-13.
70. Rodríguez-Alvarez L., Cox J.F., Tovar H., Einspanier R. & Castro F.O. 2010. Changes in the expression of pluripotency-associated genes during pre and peri-implantation stages in bovine cloned and in vitro produced embryos. Zygote. [in press].
71. Rodríguez-Alvarez L., Scholven J., Sharbati S., Einspanier R. & Castro F.O. 2010. Differential gene expression in bovine elongated (Day-17) embryos produced by somatic cell nuclear transfer and in vitro fertilization. Theriogenology. [in press].
72. Rossant J., Guillemot F., Tanaka M., Latham K., Gertenstein M. & Nagy A. 1998. Mash2 is expressed in oogenesis and preimplantation development but is not required for blastocyst formation. Mechanisms of Development. 73: 183-191.
73. Sawai K., Kageyama S., Moriyasu S., Hirayama H., Minamihashi A. & Onoe S. 2007. Changes in the mRNA transcripts of insulinlike growth factor ligand, receptors and binding proteins in bovine blastocysts and elongated embryos derived from somatic cell nuclear transfer. Journal of Reproduction and Development. 53: 77-86.
74. Sawai K., Takahashi M., Moriyasu S., Hirayama H., Minamihashi A., Hashizume T. & Onoe S. 2010. Changes in the DNA methylation status of bovine embryos from the blastocyst to elongated stage derived from somatic cell nuclear transfer. Cloning and Stem Cells. 12(1): 15-22.
75. Schier A.F. & Giraldez A.J. 2006. MicroRNA function and mechanism: insights from zebra fish. Cold Spring Harbor Symposium Quantitative Biology. 71: 195-203.
76. Solter D. 2000. Mammalian cloning: advances and limitations. Nature Reviews Genetics. 1:199-207.
77. Stroband H.W. & Van der Lende T. 1990. Embryonic and uterine development during early pregnancy in pigs. Journal of Reproduction and Fertility Supplement. 40: 261-277.
78. Strumpf D., Mao C.A., Yamanaka Y., Ralston A., Chawengsaksophak K., Beck F. & Rossant J. 2005. Cdx2 is required for correctcell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development. 132: 2093-2102.
79. Ushijima H., Akiyama K. & Tajima T. 2008. Transition of cell numbers in bovine preimplantation embryos: in vivo collected and in vitro produced embryos. Journal of Reproduction and Development. 54: 239-243.
80. Ushizawa K., Herath C.B., Kaneyama K., Shiojima S., Hirasawa A., Takahashi T., Imai K., Ochiai K., Tokunaga T., Tsunoda Y., Tsujimoto G. & Hashizume K. 2004. cDNA microarray analysis of bovine embryo gene expression profiles during the pre-implantation period. Reproductive Biology and Endocrinology. 2: 77.
81. Utsunomiya T., Goto K, Nasu M., Kumasako Y., Araki Y., Yokoo M., Itoh-Sasaki T. & Abe H. 2008. Evaluating the quality of human embryos with a measurement of oxygen consumption by scanning electrochemical microscopy. Journal of Mammalian Ova Research. 25: 1.
82. Vajta G. 2007. Handmade cloning: the future way of nuclear transfer? Trends in Biotechnology. 25: 250-253.
83. Vajta G., Bartels P., Joubert J., de la Rey M., Treadwell R. & Callesen H. 2004. Production of a healthy calf by somatic cell nuclear transfer without micromanipulators and carbon dioxide incubators using the Handmade Cloning (HMC) and the Submarine Incubation System (SIS). Theriogenology. 62:1465-1472.
84. Vajta G., Lewis I.M., Hyttel P., Thouas G.A. & Trounson A.O. 2001. Somatic cell cloning without micromanipulators. Cloning. 3: 89-95.
85. Vajta G., Lewis I.M., Trounson A.O., Purup S., Maddox-Hyttel P., Schmidt M., Pedersen H.G., Greve T. & Callesen H. 2003. Handmade somatic cell cloning in cattle: analysis of factors contributing to high efficiency in vitro. Biology of Reproduction. 68: 571-578.
86. van Eijk M.J., van Rooijen M.A., Modina S., Scesi L., Folkers G., van Tol H.T., Bevers M.M., Fisher S.R., Lewin H.A., Rakacolli D, Galli C., de Vaureix C., Trounson A.O., Mummery C.L. & Gandolfi F. 1999. Molecular cloning, genetic mapping, and developmental expression of bovine POU5F1. Biology of Reproduction. 60: 1093-1103.
87. Viebahn C. 1999. The anterior margin of the mammalian gastrula: comparative and phylogenetic aspects of its role in axis formation and head induction. Current Topics in Developmental Biology. 46: 63-103.
88. Wakayama T., Perry A.C., Zuccotti M, Johnson K.R. & Yanagimachi R. 1998. Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature. 394: 369-374.
89. Walker S.K., Hartwich K.M. & Seamark R.F. 1996. The production of unusually large offspring following embryo manipulation: concepts and changes. Theriogenology. 45: 111-120.
90. Wells D.N, Misica P.M. & Tervit H.R. 1999. Production of cloned calves following nuclear transfer with cultured adult mural granulosa cells. Biology of Reproduction. 60: 996-1005.
91. Wells DN, Laible G, Tucker FC, Miller AL, Oliver JE, Xiang T, Forsyth JT, Berg MC, Cockrem K., L'Huillier P.J., Tervit H.R. & Oback B. 2003. Coordination between donor cell type and cell cycle stage improves nuclear cloning efficiency in cattle. Theriogenology. 59: 45-59.
92. Willadsen S.M. 1986. Nuclear transplantation in sheep embryos. Nature. 320: 63-65.
93. Wilmut I., Schnieke A.E., McWhir J., Kind A.J. & Campbell K.H.S. 1997. Viable offspring derived from fetal and adult mammalian cells. Nature. 385: 810-813.
94. Wooding F.B. 1992. Current topic: the synepitheliochorial placenta of ruminants: binucleate cell fusions and hormone production. Placenta. 13(2): 101-113.
95. Wrenzycki C. & Niemann H. 2003. Epigenetic reprogramming in early embryonic development: Effects of in-vitro production and somatic nuclear transfer. Reproduction Biomedicine Online. 7: 649-656.
96. Wrenzycki C., Wells D., Herrmann D., Miller A., Oliver J., Tervit R. & Niemann H. 2001. Nuclear transfer protocol affects messenger RNA expression patterns in cloned bovine blastocysts. Biology of Reproduction. 65: 309-317.
97. Wu G.M., Lai L., Mao J., McCauley T.C., Caamaño J.N., Cantley T., Rieke A., Murphy C.N., Prather R.S., Didion B.A. & Day B.N. 2004. Birth of piglets by in vitro fertilization of zona-free porcine oocytes. Theriogenology. 62(8): 1544-1556.
98. Yao N., Wan P.C., Hao Z.D., Gao F.F., Yang L., Cui M.S., Wu Y., Liu J.H., Liu S., Chen H. & Zeng S.M. 2008. Expression of Interferontau mRNA in Bovine Embryos Derived from Different Procedures. Reproduction in Domestic Animals. 44(1): 132-139.
99. Yu X.S., Sun X.S., Jiang H.N., Han Y., Zhao C.B. & Tan J.H. 2003. Studies of the cell cycle of in vitro cultured skin fibroblasts in goats. Theriogenology. 59: 1277-1289.
100. Yu Z., Jian Z., Shen S.H., Purisima E. & Wang E. 2007. Global analysis of microRNA target gene expression reveals that miRNA targets are lower expressed in mature mouse and Drosophila tissues than in the embryos. Nucleic Acids Research. 35: 152-64.
101. Zakhartchenko V., Alberio R., Stojkovic M., Prelle K., Schernthaner W., Stojkovic P., Wenigerkind H., Wanke R., Duchler M., Steinborn R., Mueller M., Brem G. & Wolf E. 1999. Adult cloning in cattle: potential of nuclei from a permanent cell line and from primary cultures. Molecular Reproduction and Development. 54(3): 264-272.
102. Zhan S., Kubota C., Yang L., Zhang Y., Page R. & O'Neill M. 2004. Genomic Imprinting of H19 in Naturally Reproduced and Cloned Cattle. Biology of Reproduction. 71: 1540-1544.