The placenta of bovine clones

Acta Scientiae Veterinariae

Volumn 39, Issue SUPPL. 1, 2011, Pages

  Chavatte Palmer, Pascale ^a,b,c   Lee, Rita Sau Fong ^d   Camous, Sylvaine ^a,b   Le Cleac'h, Nicolas ^a,b   Jammes, Hélène ^a,b   Guillomot, Michel ^a,b  

^a INRA Institut National de la Recherche Agronomique   (France)

^b Maisons Alfort ^*  (France)

^c PremUP Foundation   (France)

^d RUAKURA RESEARCH CENTRE   (New Zealand)

Author keywords

Bovine; Cloning; Placenta; SCNT

Indexed keywords

ANIMALIA; BOS; BOVINAE; MAMMALIA; OVIS ARIES;

EID: 84868628360     PISSN: 16780345     EISSN: 16799216     Source Type: Journal    
DOI: None     Document Type: Article

References (98)

1. Adams-Brendemuehl C. & Pipers F.S. 1987. Antepartum evaluations of the equine foetus. Journal of Reproduction and Fertility. 35 (Suppl): 565-573.
2. Agarwal A. & Allamaneni S. 2004. Role of free radicals in female reproductive diseses and assited reproduction. Reproductive BioMedicine Online. 9(3): 338-347.
3. Al-Gubory K.H., Garrel C., Delatouche L., Heyman Y. & Chavatte-Palmer P. 2010. Antioxidant adaptive responses of extraembryonic tissues from cloned and non-cloned bovine conceptuses to oxidative stress during early pregnancy. Reproduction. 140(1): 175-181.
4. Amor D.J. & Halliday J. 2008. A review of known imprinting syndromes and their association with assisted reproduction technologies. Human Reproduction. 23(12): 2826-2834.
5. Apostolidou S., Abu-Amero S., O'donoghue K., Frost J., Olafsdottir O., Chavele K.M., Whittaker J.C., Loughna P., Stanier P. & Moore G.E. 2007. Elevated placental expression of the imprinted PHLDA2 gene is associated with low birth weight. Journal of Molecular Medicine. 85(4): 379-387.
6. Assis Neto A.C., Pereira F.T.V., Santos T.C., Ambrosio C.E., Leiser R. & Miglino M.A. 2010. Morpho-physical recording of bovine conceptus (Bos indicus) and placenta from days 20 to 70 of pregnancy. Reproduction in Domestic Animals. 45(5): 760-772.
7. Barker D.J. 1995. The fetal and infant origins of disease. European Journal of Clinical Investigation. 25(7): 457-463.
8. Batchelder C.A., Bertolini M., Mason J.B., Moyer A.L., Hoffert K.A., Petkov S.G., Famula T.R., Angelos J., George L.W. & Anderson G.B. 2007. Perinatal physiology in cloned and normal calves: hematologic and biochemical profiles. Cloning and Stem Cells. 9(1): 83-96.
9. Batchelder C.A., Bertolini M., Mason J.B., Moyer A.L., Hoffert K.A., Petkov S.G., Famula T.R., Angelos J., George L.W. & Anderson G.B. 2007. Perinatal physiology in cloned and normal calves: physical and clinical characteristics. Cloning and Stem Cells. 9(1): 63-82.
10. Bateson P., Barker D., Clutton-Brock T., Deb D., D'udine B., Foley R.A., Gluckman P., Godfrey K., Kirkwood T., Lahr M.M., Mcnamara J., Metcalfe N.B., Monaghan P., Spencer H.G. & Sultan S.E. 2004. Developmental plasticity and human health. Nature. 430(6998): 419-421.
11. Bertolini M., Mason J.B., Beam S.W., Carneiro G.F., Sween M.L., Kominek D.J., Moyer A.L., Famula T.R., Sainz R.D. & Anderson G.B. 2002. Morphology and morphometry of in vivo- and in vitro-produced bovine concepti from early pregnancy to term and association with high birth weights. Theriogenology. 58(5): 973-994.
12. Bertolini M., Moyer A.L., Mason J.B., Batchelder C.A., Hoffert K.A., Bertolini L.R., Carneiro C., Gargill S.L., Famula T.R., Calvert C.C., Sainz R.D. & Anderson G.B. 2004. Evidence of increased substrate availability to in vitro-derived bovine foetuses and association with accelerated conceptus growth. Reproduction. 128(3): 341-354.
13. Breukelman S., Mulder E.J.H., Oord R.V., Jonker H., Van Der Weijden B.C. & Taverne M.A.M. 2006. Continuous fetal heart rate monitoring during late gestation in cattle by means of Doppler ultrasonography: Reference values obtained by computer-assisted analysis. Theriogenology. 65(3): 486-498.
14. Campos D.B., Papa P.C., Marques Junior J.E.B., Garbelotti F., Fatima L.A., Artoni L.P., Birgel Junior E.H., Meirelles F.V., Buratini Junior J., Leiser R. & Pfarrer C. 2010. Somatic cell nuclear transfer is associated with altered expression of angiogenic factor systems in bovine placentomes at term. Genetics and Molecular Research. 9(1): 309-323.
15. Chae J.-I., Cho S.-K., Seo J.-W., Yoon T.-S., Lee K.-S., Kim J.-H., Lee K.-K., Han Y.-M. & Yu K. 2006. Proteomic analysis of the extraembryonic tissue from cloned porcine embryos. Molecular & Cellular Proteomics. 5(9): 1559-1566.
16. Chavatte-Palmer P. & Lee R.S.F. 2010. Health care and well being of cloned animals. In: IETS Manual. 4.ed. International Embryo Transfer Society, pp.106-113.
17. Chavatte-Palmer P., De Sousa N., Laigre P., Camous S., Ponter A.A., Beckers J.-F. & Heyman Y. 2006. Ultrasound fetal measurements and pregnancy-associated glycoprotein secretion in early pregnancy in cattle recipients carrying somatic clones. Theriogenology. 66(4): 829-840.
18. Chavatte-Palmer P., Remy D., Cordonnier N., Richard C., Issenmann H., Laigre P., Heyman Y. & Mialot J.P. 2004. Health status of cloned cattle at different ages. Cloning and Stem Cells. 6(2): 92-98.
19. Chavatte-Palmer P., Heyman Y., Richard C., Monget P., Lebourhis D., Kann G., Chilliard Y., Vignon X. & Renard J.P. 2002. Clinical, hormonal, and hematologic characteristics of bovine calves derived from nuclei from somatic cells. Biology of Reproduction. 66(6): 1596-1603.
20. Chavatte-Palmer P., Heyman, Y., Renard J.P. 2002. Clonage somatique et physiologies de la gestation associées, In: Martal J. (Ed) L'embryon chez l'homme et l'animal. Paris: INRA, pp.77-88.
21. Cibelli J.B., Stice S., Golueke P.J., Kane J.J., Jerry J., Blackwell C., Ponce De Leon F.A. & Robl J.L. 1998. Cloned transgenic calves produced from non-quiescent fetal fibroblasts. Science. 280(5367): 1256-1258.
22. Conley A.J. & Mason J.I. 1994. Endocrine function of the placenta. In: Textbook of fetal physiology. Oxford: Oxford University Press, pp.16-29.
23. Constant F., Guillomot M., Heyman Y., Vignon X., Laigre P., Servely J.L., Renard J.P. & Chavatte-Palmer P. 2006. Large Offspring or Large Placenta Syndrome? Morphometric Analysis of Late Gestation Bovine Placentomes from Somatic Nuclear Transfer Pregnancies Complicated by Hydrallantois. Biology of Reproduction. 75(1): 122-130.
24. Constant F., Camous S., Chavatte-Palmer P., Heyman Y., De Sousa N., Richard C., Beckers J.F. & Guillomot M. 2011. Altered secretion of pregnancy-associated glycoproteins during gestation in bovine somatic clones. Theriogenology. [in press].
25. Dalli J. 2011. Statement by Commissioner Dalli on the lack of agreement in the conciliation procedure on the Novel Food Regulation. Available at:.
26. De Laat M.W.M., Manten G.T.R., Nikkels P.G.J. & Stoutenbeek P. 2009. Hydropic placenta as a first manifestation of twintwin transfusion in a monochorionic diamniotic twin pregnancy. Journal of Ultrasound in Medicine. 28(3): 375-378.
27. De Montera B., El Zeihery D., Muller S., Jammes H., Brem G., Reichenbach H.D., Scheipl F., Chavatte-Palmer P., Zakhartchenko V., Schmitz O.J., Wolf E., Renard J.P. & Hiendleder S. 2010. Quantification of Leukocyte Genomic 5-Methylcytosine Levels Reveals Epigenetic Plasticity in Healthy Adult Cloned Cattle. Cellular Reprogramming. 12(2): 175-181.
28. De Sousa P.A., Walker S., King T.J., Young L.E., Harkness L., Ritchie W.A., Travers A., Ferrier P. & Wilmut I. 2001. Evaluation of gestational deficiencies in cloned sheep fetuses and placentae. Biology of Reproduction. 6523-6530.
29. Eggenschwiler J., Ludwig T., Fisher P., Leighton P.A., Tilghman S.M. & Efstratiadis A. 1997. Mouse mutant embryos overexpressing IGF-II exhibit phenotypic features of the Beckwith-Wiedemann and Simpson-Golabi-Behmel syndromes Genes and Devevelopment. 11(23): 3128-3142.
30. European Commission 2010. Report from the commission to the european parliament and the council on animal cloning for food production. Available at: .
31. Everts R.E., Chavatte-Palmer P., Razzak A., Hue I., Green C.A., Oliveira R., Vignon X., Rodriguez-Zas S.L., Tian X.C., Yang X., Renard J.P. & Lewin H.A. 2008. Aberrant gene expression patterns in placentomes is associated with phenotypically normal and abnormal cattle cloned by somatic cell nuclear transfer. Physiological Genomics. 33(1): 65-77.
32. Farin P.W. & Farin C.E. 1995. Transfer of bovine embryos produced in vivo or in vitro: survival and fetal development. Biology of Reproduction. 52(3): 676-682.
33. Farin P.W., Piedrahita J.A. & Farin C.E. 2006. Errors in development of fetuses and placentas from in vitro-produced bovine embryos. Theriogenology. 65(1): 178-191.
34. Fauque P., Leandri R., Merlet F., Juillard J.C., Epelboin S., Guibert J., Jouannet P. & Patrat C. 2007. Pregnancy outcome and live birth after IVF and ICSI according to embryo quality. Journal of Assisted Reproduction and Genetics. 24(5): 159-165.
35. Frank D., Fortino W., Clark L., Musalo R., Wang W., Saxena A., Li C.M., Reik W., Ludwig T. & Tycko B. 2002. Placental overgrowth in mice lacking the imprinted gene Ipl. Proceedings of the National Academy of Sciences of the United States of America. 99(11): 7490-7495.
36. Garry F., Adams R., Holland M.D., Hay W.W., Mccann J.P., Wagner A. & Seidel G.E. 1998. Arterial oxygen, metabolite and energy regulatory hormone concentrations in cloned bovine fetuses. Theriogenology. 49(1): 321-321.
37. Gebert C., Wrenzycki C., Herrmann D., Groger D., Thiel J., Reinhardt R., Lehrach H., Hajkova P., Lucas-Hahn A., Carnwath J.W. & Niemann H. 2009. DNA methylation in the IGF2 intragenic DMR is re-established in a sex-specific manner in bovine blastocysts after somatic cloning. Genomics. 94(1): 63-69.
38. Gluckman P.D. & Hanson M.A. 2004. Living with the past: evolution, development, and patterns of disease. Science. 305(5691): 1733-1736.
39. Guillemot F., Nagy A., Auerbach A., Rossant J. & Joyner A.L. 1994. Essential role of Mash-2 in extraembryonic development. Nature. 371(6495): 333-336.
40. Guillomot M., Taghouti G., Constant F., Degrelle S., Hue I., Chavatte-Palmer P. & Jammes H. 2010. Abnormal expression of the imprinted gene Phlda2 in cloned bovine placenta. Placenta. 31(6): 482-490.
41. Hashizume K., Ishiwata H., Kizaki K., Yamada O., Takahashi T., Imai K., Patel O.V., Akagi S., Shimizu M., Takahashi S., Katsuma S., Shiojima S., Hirasawa A., Tsujimoto G., Todoroki J. & Izaike Y. 2002. Implantation and placental develoment in somatic cell clone recipient cows. Cloning and Stem Cells. 4(3): 197-209.
42. Hemberger M. 2007. Epigenetic landscape required for placental development. Cellular and Molecular Life Sciences. 64(18): 2422-2436.
43. Heyman Y. 2000. Cloning of domestic mammals: recent evolution and potential applications. In: Proceedings IV congress ICEA (Tarragona Spain), pp. 49-76.
44. Heyman Y. 2001. Cloning and transgenesis in cattle: potential applications. In: Duit R., Renaville R. & Burny A. (Eds). Biotechnology in animal husbandry. Norwell: Kluwer Academic Publishers, pp.235-259.
45. Heyman Y., Chavatte-Palmer P., Lebourhis D., Camous S., Vignon X. & Renard J.P. 2002. Frequency and occurrence of late-gestation losses from cattle cloned embryos. Biology of Reproduction. 66(1): 6-13.
46. 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(1): 134-141.
47. Hiendleder S., Mund C., Reichenbach H.-D., Wenigerkind H., Brem G., Zakhartchenko V., Lyko F. & Wolf E. 2004. Tissue-Specific Elevated Genomic Cytosine Methylation Levels Are Associated with an Overgrowth Phenotype of Bovine Fetuses Derived by In Vitro Techniques. Biology of Reproduction. 71(1): 217-223.
48. Hill J.R. & Chavatte-Palmer P. 2002. Pregnancy and neonatal care of cloned animals. In: Cibelli J. (Ed). Principles of cloning. San Diego: Academic Press, pp.247-266.
49. Hill J.R., Long C.R., Looney C.R., Winger Q.A., Spencer T.E., Bazer F.W., Burghardt R.C. & Westhusin M.E. 2000. Placental abnormalities in first trimester somatic cell cloned fetuses. Theriogenology. 53(1): 218.
50. Hill J.R., Burghardt R.C., Jones K., Long C.R., Looney C.R., Shin T., Spencer T.E., Thompson J.A., Winger Q.A. & Westhusin M.E. 2000. Evidence for placental abnormality as the major cause of mortality in first-trimester somatic cell cloned bovine fetuses. Biology of Reproduction. 63(6): 1787-1794.
51. Hirayama H., Sawai K., Hirayama M., Hirai T., Kageyama S., Onoe S., Minamihashi A. & Moriyasu S. 2011. Prepartum maternal plasma glucose concentrations and placental glucose transporter mRNA expression in cows carrying somatic cell clone fetuses. Journal of Reproduction and Development. 57(1): 57-61.
52. Hirayama H., Sawai K., Moriyasu S., Hirayama M., Goto Y., Kaneko E., Miyamoto A., Ushizawa K., Takahashi T. & Minamihashi A. 2008. Excess estrogen sulfoconjugation as the possible cause for a poor sign of parturition in pregnant cows carrying somatic cell clone fetuses. Reproduction. 136(5): 639-647.
53. Hoffmann B. & Schuler G. 2002. The bovine placenta; a source and target of steroid hormones: observations during the second half of gestation. Domestic Animal Endocrinology. 23(1-2): 309-320.
54. Jauniaux E., Watson A.L., Hempstock J., Bao Y.P., Skepper J.N. & Burton G.J. 2000. Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. American Journal of Pathology. 157(6): 2111-2122.
55. Jonker F.H. 2004. Fetal death: comparative aspects in large domestic animals. Animal Reproduction Science. 82-83: 415-430.
56. Kubota C., Yamakuchi H., Todoroki J., Mizoshita K., Tabara N., Barber M. & Yang X. 2000. Six cloned calves produced from adult fibroblast cells after long-term culture. Proceedings of the National Academy of Sciences of the United States of America. 97(3): 990-995.
57. Ledgard A., Lee R.S.F., Couldrey C. & Peterson J. 2009. Dickkopf-1 Expression During Early Bovine Placentation and Its Downregulation in Somatic Cell Nuclear Transfer (SCNT) Pregnancies. Journal of Reproduction and Development. 55(5): 467-474.
58. Lee R.S.F., Peterson A.J., Donnison M.J., Ravelich S., Ledgard A.M., Li N., Oliver J.E., Miller A.L., Tucker F.C., Breier B.H. & Wells D.N. 2004. Cloned cattle fetuses with the same nuclear genetics are more variable than contemporary half-siblings resulting from artificial insemination and exhibit fetal and placental growth deregulation even in the first trimester. Biology of Reproduction. 70(1): 1-11.
59. Li N., Wells D.N. & Lee R.S.F. 2007. IGF2 and IGFBP-2 expression in bovine somatic cell nuclear transfer (SCNT) conceptuses compared with AI and in vitro produced controls. In: Juengel J.L., Murray J.F. & Smith M.F. (Eds) Reproduction in domestic ruminants. Nottingham: Nottingham University Press, p.554.
60. Li N., Wells D.N., Peterson A.J. & Lee R.S.F. 2005. Perturbations in the biochemical composition of fetal fluids are apparent in surviving bovine somatic cell nuclear transfer pregnancies in the first half of gestation. Biology of Reproduction. 73(1): 139-148.
61. Li Y.H. & Behringer R.R. 1998. Esx1 is an X-chromosome-imprinted regulator of placental development and fetal growth. Nature Genetics. 20(3): 309-311.
62. Long J.E. & Cai X. 2007. Igf-2r expression regulated by epigenetic modification and the locus of gene imprinting disrupted in cloned cattle. Gene. 388(1-2): 125-134.
63. Mann M.R., Lee S.S., Doherty A.S., Verona R.I., Nolen L.D., Schultz R.M. & Bartolomei M.S. 2004. Selective loss of imprinting in the placenta following preimplantation development in culture. Development. 131(15): 3727-3735.
64. Meirelles F.V., Birgel E.H., Perecin F., Bertolini M., Traldi A.S., Pimentel J.R.V., Komninou E.R., Sangalli J.R., Neto P.F., Nunes M.T., Pogliani F.C., Meirelles F.D.P., Kubrusly F.S., Vannucchi C.I. & Silva L.C.G. 2010. Delivery of cloned offspring: experience in Zebu cattle (Bos indicus). Reproduction Fertility and Development. 22(1): 88-97.
65. Mialon M.M., Camous S., Renand G., Martal J. & Menissier F. 1993. Peripheral concentration of a 60-kDa pregnancy serum protein during gestation and after calving in relationship to embryonic mortality in cattle. Reproduction Nutrition Development. 33(3): 269-282.
66. Miglino M.A., Pereira F.T.V., Visintin J.A., Garcia J.M., Meirelles F.V., Rumpf R., Ambrosio C.E., Papa P.C., Santos T.C., Carvalho A.F., Leiser R. & Carter A.M. 2007. Placentation in cloned cattle: Structure and microvascular architecture. Theriogenology. 68(4): 604-617.
67. Morel O., Pachy F., Chavatte-Palmer P., Bonneau M., Gayat E., Laigre P., Evain-Brion D. & Tsatsaris V. 2010. Correlation between utero-placental three-dimensional power Doppler indices and the uterine real blood flow: Evaluation in a pregnant sheep experimental model. Ultrasound in Obstetrics and Gynecology. 36(5): 635-640.
68. Nagel C., Aurich J. & Aurich C. 2010. Determination of heart rate and heart rate variability in the equine fetus by fetomaternal electrocardiography. Theriogenology. 73(7): 973-983.
69. Niemann H., Tian X.C., King W.A. & Lee R.S.F. 2008. Epigenetic reprogramming in embryonic and foetal development upon somatic cell nuclear transfer cloning. Reproduction. 135(2): 151-163.
70. Oback B. & Wells D.N. 2007. Donor cell differentiation, reprogramming, and cloning efficiency: Elusive or illusive correlation? Molecular Reproduction and Development. 74(5): 646-654.
71. Oishi M., Gohma H., Hashizume K., Taniguchi Y., Yasue H., Takahashi S., Yamada T. & Sasaki Y. 2006. Early embryonic death-associated changes in genome-wide gene expression profiles in the fetal placenta of the cow carrying somatic nuclearderived cloned embryo. Molecular Reproduction and Development. 73(4): 404-409.
72. Panarace M., Aguero J.I., Garrote M., Jauregui G., Segovia A., Cane L., Gutierrez J., Marfil M., Rigali F. & Pugliese M. 2007. How healthy are clones and their progeny: 5 years of field experience. Theriogenology. 67(1): 142-151.
73. Qian N., Frank D., Okeefe D., Dao D., Zhao L., Yuan L., Wang Q., Keating M., Walsh C. & Tycko B. 1997. The IPL gene on chromosome 11p15.5 is imprinted in humans and mice and is similar to TDAG51, implicated in Fas expression and apoptosis. Human Molecular Genetics. 6(12): 2021-2029.
74. Ravelich S.R., Breier B.H., Reddy S., Keelan J.A., Wells D.N., Peterson A.J. & Lee R.S.F. 2004. Insulin-Like Growth Factor-I and Binding Proteins 1, 2, and 3 in Bovine Nuclear Transfer Pregnancies. Biology of Reproduction. 70(2): 430-438.
75. Reef V.B., Vaala W.E., Worth L.T., Sertich P.L. & Spencer P.A. 1996. Ultrasonographic assessment of fetal well-being during late gestation: development of an equine biophysical profile. Equine veterinary Journal. 28(3): 200-208.
76. Rici R.E.G., Facciotti P.R., Ambrosio C.E., Maria D.A., Kfoury J.R., Bertolini M. & Miglino M.A. 2009. Cell cycle and apoptosis in normal and cloned bovine near-term placentae. Animal Reproduction Science. 115(1-4): 29-38.
77. Robinson J.S., Kingston E.J., Jones C.T. & Thorburn G.D. 1979. Studies on experimental growth retardation in sheep. The effect of removal of endometrial caruncles on fetal size and metabolism. Journal of Developmental Physiology. 1(5): 379-398.
78. Rodriguez M.M., Chaves F., Romaguera R.L., Ferrer P.L., De La Guardia C. & Bruce J.H. 2002. Value of autopsy in nonimmune hydrops fetalis: Series of 51 stillborn fetuses. Pediatric and Developmental Pathology. 5(4): 365-374.
79. Rossant J. & Cross J.C. 2001. Placental development: Lessons from mouse mutants. Nature Reviews Genetics. 2(7): 538-548.
80. Salas M., John R., Saxena A., Barton S., Frank D., Fitzpatrick G., Higgins M.J. & Tycko B. 2004. Placental growth retardation due to loss of imprinting of Phlda2. Mechanisms of Development. 121(10): 1199-1210.
81. Santos F., Zakhartchenko V., Stojkovic M., Peters A., Jenuwein T., Wolf E., Reik W. & Dean W. 2003. Epigenetic Marking Correlates with Developmental Potential in Cloned Bovine Preimplantation Embryos. Current Biology. 13(13): 1116-1121.
82. Sasser R.G., Ruder C.A., Ivani K.A., Butler J.E. & Hamilton W.C. 1986. Detection of pregnancy by radioimmunoassay of a novel pregnancy-specific protein in serum of cows and a profile of serum concentrations during gestation. Biology of Reproduction. 35(4): 936-942.
83. Stice S.L., Strelchenko N.S., Keefer C.L. & Matthews L. 1996. Pluripotent bovin embryonic cell lines direct embryonic development following nuclear transfer. Biology of Reproduction. 54(1): 100-110.
84. Suzuki J., Therrien J., Filion F., Lefebvre R., Goff A.K. & Smith L.C. 2009. In vitro culture and somatic cell nuclear transfer affect imprinting of SNRPN gene in pre- and post-implantation stages of development in cattle. Bmc Developmental Biology. 9: 9.
85. Takahashi K., Kobayashi T. & Kanayama N. 2000. p57(Kip2) regulates the proper development of labyrinthine and spongiotrophoblasts. Molecular Human Reproduction. 6(11): 1019-1025.
86. Thibault C. & M.-C.Levasseur. 1991. La Reproduction chez les mammifères et chez l'homme. Paris: INRA-Ellipses, 500p.
87. Wang Y. & Walsh S.W. 2001. Increased superoxide generation is associated with decreased superoxide dismutase activity and mRNA expression in placental trophoblast cells in pre-eclampsia. Placenta. 22(2-3): 206-212.
88. Wang Z.Q., Fung M.R., Barlow D.P. & Wagner E.F. 1994. Regulation of embryonic growth and lysosomal targeting by the imprinted IGF2/MPR gene. Nature. 372(6505): 464-467.
89. Wells D., Misica P., Day T. & Tervit H. 1997. Production of cloned lambs from an established embryonic cell line: a comparison between in vivo- and in vitro-matured cytoplasts. Biology of Reproduction. 57(2): 385-393.
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(4): 996-1005.
91. Wells D.N., Forsyth J.T., Mcmillan V. & Oback B. 2004. Review: The health of somatic cell cloned cattle and their offspring. Cloning and Stem Cells. 6(2): 101-110.
92. Wilmut I. & Sales D.I. 1981. Effect of an asynchronous environment on embryonic development in sheep. Journal of Reproduction and Fertility. 61(1): 179-184.
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(6619): 810-813.
94. Wooding F.B.P. 1992. The synepitheliochorial placenta of ruminants - binucleate cell fusions and hormone production. Placenta. 13(2): 101-113
95. Wooding F.B.P. & Beckers J.F. 1987. Triucleate cells and the ultrastructural localization of bovine placental lactogen. Cell and Tissue Research. 247(3): 667-673.
96. Xue F., Tian X.C., Du F., Kubota C., Taneja M., Dinnyes A., Dai Y., Levine H., Pereia L.V. & Yang X. 2002. Aberrant patterns of X chromosome inactivation in bovine clones. Nature Genetics. 31(2): 216-220.
97. Young L.E., Fernandes K., Mcevoy T.G., Butterwith S.C., Gutierrez C.G., Carolan C., Broadbent P.J., Robinson J.J., Wilmut I. & Sinclair K.D. 2001. Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nature Genetics. 27(2): 153-154.
98. Zoli A.P., Guilbault L.A., Delahaut P., Benitez Ortiz W. & Beckers J.F. 1992. Radioimmunoassay of a bovine pregnancyassociated glycoprotein in serum: its application for pregnancy diagnosis. Biology of Reproduction. 46(1): 83-92.