[en] Somatic cloning in the bovine species leads to high levels of fetal losses which occur throughout pregnancy. These losses are most often associated with fetal overgrowth, a syndrome known as large offspring syndrome (LOS), and excessive maternal plasma pregnancy serum protein 60 (PSP60), a protein similar to a pregnancy-associated glycoprotein of 67 kDa (PAG 167) produced by the bovine placenta. Predicting the outcome of pregnancies initiated from cloned embryos has become an important issue both to prevent potential harm to the mother because of excessive fetal size at birth and also to get a better understanding of the relationships between growth, differentiation and placental functions in developing cloned fetuses. Here, we report on a systematic analysis of fetal and placental development in the first trimester of pregnancy performed by ultrasonographic imaging and by measurement of the maternal concentrations of pregnancy associated glycoproteins (PAGS), using four different radioimmunoassays (RIA) (two homologous RIA systems with PSP60 and PAG 167; two heterologous RIA systems with PAG 167 as standard and tracer, and antisera anti-caprine PAGs). We showed that crown-rump length (CRL) in clones appeared smaller than controls at 35, 50 and 62 days (P < 0.05). At 62 days of pregnancy, CRL in cloned fetuses that died before 90 days was smaller compared to the other cloned fetuses (P < 0.05) whereas the width of the fetal sack and the biparietal diameter (BPD) was larger in fetuses that developed LOS in late gestation (P < 0.05). Maternal PAGs concentrations were statistically different between controls and all clone recipients as early as Day 34, suggesting early abnormal placental glycoprotein synthesis for clone pregnancies regardless of pregnancy outcome. This work provides a practical, non-invasive tool to follow up clone pregnancies and suggests that primary growth retardation and abnormal placental function precedes excessive fetal and placental growth at later stages of pregnancy. (c) 2006 Elsevier Inc. All rights reserved.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Chavatte-Palmer, P.
Melo de Sousa, Noelita ; Université de Liège - ULiège > Département de sciences fonctionnelles > Physiologie de la reproduction
Laigre, P.
Camous, S.
Ponter, A. A.
Beckers, Jean-François ; Université de Liège - ULiège > Département de sciences fonctionnelles > Physiologie de la reproduction
Heyman, Y.
Language :
English
Title :
Ultrasound fetal measurements and pregnancy associated glycoprotein secretion in early pregnancy in cattle recipients carrying somatic clones
Barker D.J.P., Eriksson J.G., Forsen T., and Osmond C. Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol 31 (2002) 1235-1239
Behboodi E., Anderson G.B., BonDurant R.H., Cargill S.L., Kreuscher B.R., Medrano J.F., et al. Birth of large calves that developed from in vitro-derived embryos. Theriogenology 44 (1995) 227-232
Bertolini M., Mason J.B., Beam S.W., Carneiro G.F., Sween M.L., Kominek D.J., et al. Morphology and morphometry of in vivo- and in vitro-produced bovine concept from early pregnancy to term and association with high birth weights. Theriogenology 58 (2002) 973-994
Breukelman S.P., Reinders J.M.C., Jonker F.H., de Ruigh L., Kaal L.M.T.E., van Wagtendonk-de Leeuw A.M., et al. Fetometry and fetal heart rates between Day 35 and 108 in bovine pregnancies resulting from transfer of either MOET, IVP-co-culture or IVP-SOF embryos. Theriogenology 61 (2004) 867-882
Breukelman S.P., Szenci O., Beckers J.F., Kindahl H., Mulder E.J.H., Jonker F.H., et al. Ultrasonographic appearance of the conceptus, fetal heart rate and profiles of pregnancy-associated glycoproteins (PAG) and prostaglandin F2α-metabolite (PGF2α-metabolite) after induction of fetal death with aglepristone during early gestation in cattle. Theriogenology 64 (2005) 917-933
Butler J.E., Hamilton W.C., Sasser R.G., Ruder C.A., Hass G.M., and Williams R.J. Detection and partial characterization of two bovine pregnancy-specific proteins. Biol Reprod (1982) 26
Chavatte-Palmer P, Constant F, Heyman Y, Laigre P. Images échographiques de gestations pathologiques après clonage. Exemples du syndrome du gros veau. SNGTV, Nantes, France, 2003.
Chavatte-Palmer P., Heyman Y., Richard C., Monget P., LeBourhis D., Kann G., et al. Clinical, hormonal, and hematologic characteristics of bovine calves derived from nuclei from somatic cells. Biol Reprod 66 (2002) 1596-1603
Chavatte-Palmer P., Rémy D., Cordonnier N., Richard C., Issenmann H., Laigre P., et al. Health status of cloned cattle at different ages. Cloning Stem Cells 6 (2004) 92-98
Constant F., Guillomot M., Chavatte-Palmer P., Heyman Y., Berthelot V., Camous S., et al. Structural and functional studies on placenta of bovine somatic clones. Proceedings of the European Federation studies on placental Associations (2003) 8-9
Curran S., Pierson R.A., and Ginther O.J. Ultrasonographic appearance of the bovine conceptus from day 20 trough 60. J Am Vet Med Assoc 189 (1986) 1295-1302
De Sousa P.A., Walker S., King T.J., Young L.E., Harkness L., Ritchie W.A., et al. Evaluation of gestational deficiencies in cloned sheep fetuses and placentae. Biol Reprod 65 (2001) 23-30
Ectors F.J., Drion P.V., Delval A., Smith L.C., Sulon J., Zaaijer D., et al. Interests of pregnancy follow-up in cows after embryo transfer: special focusing on IVP and NT. 12th Scientific Meeting of the European Embryo Transfer Association. Lyon, France (1996) 95-103
Garbayo J.M., Remy B., Alabart J.L., Folch J., Wattiez R., Falmagne P., et al. Isolation and partial characterization of a pregnancy-associated glycoprotein (PAG) family from the goat placenta. Biol Reprod 58 (1998) 109-115
Green J.A., Xie S.C., Quan X., Bao B.N., Gan X.S., Mathialagan N., et al. Pregnancy-associated bovine and ovine glycoproteins exhibit spatially and temporally distinct expression patterns during pregnancy. Biol Reprod 62 (2000) 1624-1631
Greenwood F.C., Hunter W.M., and Glover J.S. The preparation of 131I-labelled human growth hormone of high specific radioactivity. Biochem J 89 (1963) 114-123
Hansen C., and Delsaux B. Use of transrectal B-mode ultrasound imaging in bovine pregnancy diagnosis. Vet Rec 121 (1987) 200-202
Hashizume K., Ishiwata H., Kizaki K., Yamada O., Takahashi T., Imai K., et al. Implantation and placental development in somatic cell clone recipient cows. Cloning Stem Cells 4 (2002) 197-209
Heyman Y., Chavatte-Palmer P., LeBourhis D., Camous S., Vignon X., and Renard J.P. Frequency and occurrence of late-gestation losses from cattle cloned embryos. Biol Reprod 66 (2002) 6-13
Heyman Y., Richard C., Rodriguez-Martinez H., Lazzari G., Chavatte-Palmer P., Vignon X., et al. Zootechnical performance of cloned cattle and offspring: preliminary results. Cloning Stem Cells 6 (2004) 111-120
Hiendleder S., Mund C., Reichenbach H.-D., Wenigerkind H., Brem G., Zakhartchenko V., et al. Tissue-specific elevated genomic cytosine methylation levels are associated with an overgrowth phenotype of bovine fetuses derived by in vitro techniques. Biol Reprod 71 (2004) 217-223
Hill J.R., Burghardt R.C., Jones K., Long C.R., Looney C.R., Shin T., et al. Evidence for placental abnormality as the major cause of mortality in first-trimester somatic cell cloned bovine fetuses. Biol Reprod 63 (2000) 1787-1794
Hill J.R., and Chavatte-Palmer P. Pregnancy and neonatal care of cloned animals. In: Cibelli J. (Ed). Principles of Cloning (2002), Academic Press, San Diego 247-266
Hill J.R., Long C.R., Looney C.R., Winger Q.A., Spencer T.E., Bazer F.W., et al. Placental abnormalities in first trimester somatic cell cloned fetuses. Theriogenology 53 (2000) 218
Hill J.R., Schlafer D.H., Fisher P.J., and Davies C.J. Abnormal expression of trophoblast major histocompatibility complex class I antigens in cloned bovine pregnancies is associated with a pronounced endometrial lymphocytic response. Biol Reprod 67 (2002) 55-63
Hugues E.A., and Davies D.A.R. Practical uses of ultrasound in early pregnancy in cattle. Vet Rec 136 (1989) 406-410
Kahn W. Sonographic fetometry in the bovine. Theriogenology 31 (1989) 1105-1121
Klisch K., Thomsen P.D., Dantzer V., and Leiser R. Genome multiplication is a generalised phenomenon in placentomal and interplacentomal trophoblast giant cells in cattle. Reprod Fertil Dev 16 (2004) 301-306
Laigre P., Chavatte-Palmer P., Vignon X., and Heyman Y. Suivi échographique de gestations bovines après transfert d'embryons clonés (2004), Rencontres Recherche Ruminants, Paris, France
Lee R.S.F., Peterson A.J., Donnison M.J., Ravelich S., Ledgard A.M., Li N., et al. 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. Biol Reprod 70 (2004) 1-11
Littell R.C., Henry P.R., and Ammerman C.B. Statistical analysis of repeated measures data using SAS procedures. J Anim Sci 76 (1998) 1216-1231
Lynch K.A., Alexander R.M., and Sasser R.G. The cloning and expression of the bovine pregnancy specific protein B (bPSPB) gene. Biol Reprod 46 Suppl 1 (1992) 73
Marquant-Leguienne B., Humblot P., Thibier M., and Thibault C. Evaluation of bull semen fertility by homologous in vitro fertilization tests. Reprod Nutr Dev 30 (1990) 259-266
Martal J., Chene N., Camous S., Huynh L., Lantier F., Hermier P., et al. Recent developments and potentialities for reducing embryo mortality in ruminants: the role of IFN-tau and other cytokines in early pregnancy. Reprod Fertil Dev (1997) 9
Mialon M.M., Camous S., Renand G., Martal J., and Menissier F. Peripheral concentration of a 60-kDa pregnancy specific protein during gestation and after calving in relationship to embryonic mortality in cattle. Reprod Nutr Dev 33 (1993) 269-282
Moore S.E., Cole T.J., Collinson A.C., Poskitt E.M.E., McGregor I.A., and Prentice A.M. Prenatal or early postnatal events predict infectious deaths in young adulthood in rural Africa. Int J Epidemiol 28 (1999) 1088-1095
Pace M.M., Augenstein M.L., Betthauser J.M., Childs L.A., Eilertsen K.J., Enos J.M., et al. Ontogeny of cloned cattle to lactation. Biol Reprod 67 (2002) 334-339
Patel O.V., Camous S., Takenouchi N., Takahashi T., Hirako M., Sasaki N., et al. Effect of stage of gestation and foetal number on plasma concentrations of a pregnancy serum protein (PSP-60) in cattle. Res Vet Sci 65 (1998) 195-199
Patel O.V., Yamada O., Kizaki K., Takahashi T., Imai K., and Hashizume K. Quantitative analysis throughout pregnancy of placentomal and interplacentomal expression of pregnancy-associated glycoproteins-1 and-9 in the cow. Mol Reprod Dev 67 (2004) 257-263
Patel O.V., Yamada O., Kizaki K., Takahashi T., Imai K., Takahashi S., et al. Expression of trophoblast cell-specific pregnancy-related genes in somatic cell-cloned bovine pregnancies. Biol Reprod 70 (2004) 1114-1120
Perenyi Z.S., Szenci O., Sulon J., Drion P.V., and Beckers J.F. Comparison of the ability of three radioimmunoassay to detect pregnancy-associated glycoproteins in bovine plasma. Reprod Domestic Anim 37 (2002) 100-104
Renard J.P., Chastant S., Chesné P., Richard C., Marchal J., Cordonnier N., et al. Lymphoid hypoplasia and somatic cloning. Lancet 353 (1999) 1489-1491
Sasser R.G., Ruder C.A., Ivani K.A., Butler J.E., and Hamilton W.C. Detection of pregnancy by radioimmunoassay of a novel pregnancy-specific protein in serum of cows and a profile of serum concentrations during gestation. Biol Reprod 35 (1986) 936-942
Sinclair K.D., Young L.E., Wilmut I., and McEvoy T.G. In-utero overgrowth in ruminants following embryo culture: lessons from mice and a warning to men. Human Reprod 15 (2000) 68-86
Skelley D.S., Brown L.P., and Besch P.K. Radioimmunoassay. Clin Chem 19 (1973) 146-186
Vignon X., Chesné P., Lebourhis D., Fléchon J.E., Heyman Y., and Renard J.P. Developmental potential of bovine embryos reconstructed with enucleated matured oocytes fused with cultured somatic cells. C R Acad Sci Paris 321 (1998) 735-745
Vignon X., LeBourhis D., Laloye E., Lavergne Y., Servely J.L., Richard C., et al. A comparison of the development of bovine embryos cloned from fibroblasts of two different genetic origins. 19th AETE 218 (2003) [abstract]
Walker S.K., Hartwich K.M., and Seamark R.F. The production of unusually large offspring following embryo manipulation: concepts and challenges. Theriogenology 45 (1996) 111-120
White I.R., Russel A.J.F., Wright I.A., and Whyte T.K. Realtime ultrasonnic scanning in the diagnosis of pregnancy and the estimation of gestationnal age in cattle. Vet Rec 117 (1985) 5-8
Wilson J.M., Williams J.D., Bondioli K.R., Looney C.R., Westhusin M.E., and McCalla D.F. Comparison of birth weight and growth characteristics of bovine calves produced by nuclear transfer (cloning), embryo transfer and natural mating. Anim Reprod Sci 38 (1995) 73-83
Xie S., Green J.A., Bao B., Bixby J.B., Szafranska B., DeMartini J.C., et al. The diversity and evolutionary relationships of the pregnancy-associated glycoproteins, an aspartic proteinase subfamily consisting of many trophoblast-expressed genes. Proc Natl Acad Sci USA 94 (1997) 12809-12816
Young L.E., Sinclair K.D., and Wilmut I. Large offspring syndrome in cattle and sheep. Rev Reprod 3 (1998) 155-163
Zoli A.P., Beckers J.F., Wouters-Ballman P., Closset J., Falmagne P., and Ectors F. Purification and characterization of a bovine pregnancy-associated glycoprotein. Biol Reprod 45 (1991) 1-10
Zoli A.P., Guilbault L.A., Delahaut P., Benitez Ortiz W., and Beckers J.F. Radioimmunoassay of a bovine pregnancy associated glycoprotein in serum: its application for pregnancy diagnosis. Biol Reprod 46 (1992) 83-92
