Inclusion of bovine lipoproteins and the vitamin E analogue, Trolox, during in vitro culture of bovine embryos changes both embryo and fetal development
J. A. Rooke A C , R. G. Watt A , C. J. Ashworth A B and T. G. McEvoy A
+ Author Affiliations
- Author Affiliations
A Sustainable Livestock Systems Group, SAC, West Mains Road, Edinburgh EH9 3JG, UK.
B The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian EH25 9RG, UK.
C Corresponding author. Email: john.rooke@sac.ac.uk
Reproduction, Fertility and Development 24(2) 309-316 https://doi.org/10.1071/RD11034
Submitted: 8 February 2011 Accepted: 28 May 2011 Published: 11 October 2011
Abstract
This experiment investigated effects of lipoproteins and Trolox (vitamin E analogue) on bovine embryo and fetal development. The treatments were: in vitro culture (IVC) in synthetic oviducal fluid alone (SOF); with bovine lipoproteins (2% v/v; SOFLP); with Trolox (100 μM; SOFT); and with lipoproteins and Trolox (SOFLPT). In vitro culture with lipoproteins increased fatty acid content of blastocysts (P < 0.001) whereas inclusion of Trolox had no effect (P > 0.05). Whereas lipoproteins reduced zygote development to blastocysts (P = 0.03), Trolox facilitated increased development (P < 0.001) and counteracted the reduction observed with lipoproteins (interaction, P = 0.009). Lipoproteins also compromised (P < 0.001) but presence of Trolox (P > 0.05) had no effect on blastocyst morphological grade. Pregnancy rates resulting from synchronous transfer of IVP embryos were not affected by IVC treatment. At Day 70 of pregnancy, compared with SOF, fetal weight was lower in SOFLP but not SOFLPT (interaction, P < 0.001). Liver weight (g kg–1 fetal weight) was greater (P = 0.03) in treatments containing Trolox. Placentome numbers were greater in SOF and SOFLPT compared with SOFLP and SOFT (interaction, P = 0.002); superior embryo grades were also associated with increased numbers of placentomes (P = 0.024). In conclusion, the interactive effects of lipoprotein and Trolox inclusion on in vitro embryo development were also evident in fetal development at Day 70.
Additional keywords: antioxidant, embryo culture.
References
Abe, H., Yamashita, S., Itoh, T., Satoh, T., and Hoshi, H. (1999). Ultrastructure of bovine embryos developed from in vitro-matured and -fertilized oocytes: comparative morphological evaluation of embryos cultured either in serum-free medium or in serum-supplemented medium. Mol. Reprod. Dev. 53, 325–335.| Ultrastructure of bovine embryos developed from in vitro-matured and -fertilized oocytes: comparative morphological evaluation of embryos cultured either in serum-free medium or in serum-supplemented medium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjsFGgsr8%3D&md5=f016f6698036c6c035b4d7fbd720ec33CAS | 10369393PubMed |
Adamiak, S. J., Ewen, M., Powell, K., Rooke, J. A., Webb, R., and Sinclair, K. D. (2004). Inclusion of bovine serum from different dietary backgrounds influences embryo viability in vitro. Reproduction 31, 19..
Ali, A. A., Bilodeau, J. F., and Sirard, M. A. (2003). Antioxidant requirements for bovine oocytes varies during in vitro maturation, fertilization and development. Theriogenology 59, 939–949.
| Antioxidant requirements for bovine oocytes varies during in vitro maturation, fertilization and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXotVSh&md5=92134643a54f1fcc6f7bd41a04ce9329CAS | 12517395PubMed |
Barceló-Fimbres, M., and Seidel, G. E. (2007). Effects of either glucose or fructose and metabolic regulators on bovine embryo development and lipid accumulation in vitro. Mol. Reprod. Dev. 74, 1406–1418.
| Effects of either glucose or fructose and metabolic regulators on bovine embryo development and lipid accumulation in vitro.Crossref | GoogleScholarGoogle Scholar | 17342742PubMed |
Barceló-Fimbres, M., Brink, Z., and Seidel, G., (2009). Effects of phenzaine ethosulfate during culture of bovine embryos on pregnancy rate, prenatal and postnatal development. Theriogenology 71, 355–368.
| Effects of phenzaine ethosulfate during culture of bovine embryos on pregnancy rate, prenatal and postnatal development.Crossref | GoogleScholarGoogle Scholar | 18801561PubMed |
Christie, W.W., (2003). ‘Lipid Analysis.’ (The Oily Press: Bridgwater, UK.)
Corrêa, G. A., Rumpf, R., Mundim, T. C. D., Franco, M. M., and Dode, M. A. N. (2008). Oxygen tension during in vitro culture of bovine embryos: effect in production and expression of genes related to oxidative stress. Anim. Reprod. Sci. 104, 132–142.
| Oxygen tension during in vitro culture of bovine embryos: effect in production and expression of genes related to oxidative stress.Crossref | GoogleScholarGoogle Scholar | 17350772PubMed |
Debier, C., and Larondelle, Y. (2005). Vitamins A and E: metabolism, roles and transfer to offspring. Br. J. Nutr. 93, 153–174.
| Vitamins A and E: metabolism, roles and transfer to offspring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivVCksb4%3D&md5=9b22935e4c32a915c6e80523a52b1882CAS | 15788108PubMed |
Eley, R. M., Thatcher, W. W., Bazer, F. W., Wilcox, C. J., Becker, R. B., Head, H. H., and Adkinson, R. W. (1978). Development of conceptus in bovine. J. Dairy Sci. 61, 467–473.
| Development of conceptus in bovine.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1c7psVKrtA%3D%3D&md5=d0eba3fa27bbb4366aa956900bf566adCAS | 659690PubMed |
Farin, P. W., Crosier, A. E., and Farin, C. E. (2001). Influence of in vitro systems on embryo survival and fetal development in cattle. Theriogenology 55, 151–170.
| Influence of in vitro systems on embryo survival and fetal development in cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7nslartg%3D%3D&md5=520effe8af7b6bb5015d74836516d2d3CAS | 11198080PubMed |
Farin, P. W., Piedrahita, J. A., and Farin, C. E. (2006). Errors in development of fetuses and placentas from in vitro-produced bovine embryos. Theriogenology 65, 178–191.
| Errors in development of fetuses and placentas from in vitro-produced bovine embryos.Crossref | GoogleScholarGoogle Scholar | 16266745PubMed |
Farin, C. E., Farmer, W. T., and Farin, P. W. (2010). Pregnancy recognition and abnormal offspring syndrome in cattle. Reprod. Fertil. Dev. 22, 75–87.
| Pregnancy recognition and abnormal offspring syndrome in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitlagurc%3D&md5=68510fbb655befdfbe2df6c22cabcb3bCAS | 20003848PubMed |
Ferguson, E. M., and Leese, H. J. (1999). Triglyceride content of bovine oocytes and early embryos. J. Reprod. Fertil. 116, 373–378.
| Triglyceride content of bovine oocytes and early embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkslOltbc%3D&md5=5534fc675e43007177b78df7750032efCAS | 10615263PubMed |
Ferguson, E. M., and Leese, H. J. (2006). A potential role for triglyceride as an energy source during bovine oocyte maturation and early embryo development. Mol. Reprod. Dev. 73, 1195–1201.
| A potential role for triglyceride as an energy source during bovine oocyte maturation and early embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnvFahtr0%3D&md5=e1849bb61d288c232d9253f14583bc56CAS | 16804881PubMed |
Feugang, J. M., De Roover, R., Moens, A., Leonard, S., Dessy, F., and Donnay, I. (2004). Addition of beta-mercaptoethanol or Trolox (R) at the morula/blastocyst stage improves the quality of bovine blastocysts and prevents induction of apoptosis and degeneration by prooxidant agents. Theriogenology 61, 71–90.
| Addition of beta-mercaptoethanol or Trolox (R) at the morula/blastocyst stage improves the quality of bovine blastocysts and prevents induction of apoptosis and degeneration by prooxidant agents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpt1eqtLs%3D&md5=672167b0349c136b0eed2a263c2da374CAS | 14643863PubMed |
Genicot, G., Leroy, J. L. M. R., Van Soom, A., and Donnay, L. (2005). The use of a fluorescent dye, Nile red, to evaluate the lipid content of single mammalian species. Theriogenology 63, 1181–1194.
| The use of a fluorescent dye, Nile red, to evaluate the lipid content of single mammalian species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlSltb8%3D&md5=01149f1052c7bd68f084ea2e45d21d68CAS | 15710202PubMed |
Goodhand, K. L., Watt, R. G., Staines, M. E., Hutchinson, J. S. M., and Broadbent, P. J. (1999). In vivo oocyte recovery and in vitro embryo production from bovine donors aspirated at different frequencies or following FSH treatment. Theriogenology 51, 951–961.
| In vivo oocyte recovery and in vitro embryo production from bovine donors aspirated at different frequencies or following FSH treatment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjs1ejtr0%3D&md5=9923195b62f2e9df23ba4ee60ba7170dCAS | 10729017PubMed |
Gore, M. T., Young, R. B., Claeys, M. C., Chromiak, J. A., Rahe, C. H., Marple, D. N., Hough, J. D., Griffin, J. L., and Mulvaney, D. R. (1994). Growth and development of bovine fetuses and neonates representing 3 genotypes. J. Anim. Sci. 72, 2307–2318.
| 1:STN:280:DyaK2M%2FpsFOrsw%3D%3D&md5=8806d9368da4feed3e225d8f3553ae4dCAS | 7528193PubMed |
Hiendleder, S., Mund, C., Reichenbach, H. D., Wenigerkind, H., Brem, G., Zakhartchenko, V., Lyko, F., and Wolf, E. (2004). Tissue-specific elevated genomic cytosine methylation levels are associated with an overgrowth phenotype of bovine fetuses derived by in vitro techniques. Biol. Reprod. 71, 217–223.
| Tissue-specific elevated genomic cytosine methylation levels are associated with an overgrowth phenotype of bovine fetuses derived by in vitro techniques.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltFKkurk%3D&md5=c5e1b66096f46c2cdd47d47e3ac02df8CAS | 15028629PubMed |
Hiendleder, S., Wirtz, M., Mund, C., Klempt, M., Reichenbach, H. D., Stojkovic, M., Weppert, M., Wenigerkind, H., Elmlinger, M., Lyko, F., Schmitz, O. J., and Wolf, E. (2006). Tissue-specific effects of in vitro fertilization procedures on genomic cytosine methylation levels in overgrown and normal sized bovine fetuses. Biol. Reprod. 75, 17–23.
| Tissue-specific effects of in vitro fertilization procedures on genomic cytosine methylation levels in overgrown and normal sized bovine fetuses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtlyisL0%3D&md5=546b2d4b1fa33aabdee1e7ad910bb802CAS | 16554415PubMed |
Hubbert, W. T., Booth, G. D., and Stalheim, O. H. (1972). Changes in organ weights and fluid volumes during growth of the bovine fetus. Growth 36, 217–233.
| 1:STN:280:DyaE3s%2FpsV2huw%3D%3D&md5=7f79222707815f56739c927d04663618CAS | 4651636PubMed |
Jorritsma, R., Cesar, M. L., Hermans, J. T., Kruitwagen, C. L. J. J., Vos, P. L. A. M., and Kruip, T. A. M. (2004). Effects of non-esterified fatty acids on bovine granulosa cells and developmental potential of oocytes in vitro. Anim. Reprod. Sci. 81, 225–235.
| Effects of non-esterified fatty acids on bovine granulosa cells and developmental potential of oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsleltr0%3D&md5=d8a114e73e824aa7f7713f8fb0a347b5CAS | 14998649PubMed |
Kuran, M., Robinson, J. J., Staines, M. E., and McEvoy, T. G. (2001). Development and de novo protein synthetic activity of bovine embryos produced in vitro in different culture systems. Theriogenology 55, 593–606.
| Development and de novo protein synthetic activity of bovine embryos produced in vitro in different culture systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsFCqu7g%3D&md5=52fc6c0704727fff476eee471f74f1d6CAS | 11233785PubMed |
Lane, M., and Gardner, D. K. (2003). Ammonium induces aberrant blastocyst differentiation, metabolism, pH regulation, gene expression and subsequently alters fetal development in the mouse. Biol. Reprod. 69, 1109–1117.
| Ammonium induces aberrant blastocyst differentiation, metabolism, pH regulation, gene expression and subsequently alters fetal development in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsV2nsr8%3D&md5=978bf448d8584ae5cc82691b22921fc8CAS | 12773416PubMed |
Leese, H. J., Baumann, C. G., Brison, D. R., McEvoy, T. G., and Sturmey, R. G. (2008). Metabolism of the viable mammalian embryo: quietness revisited. Mol. Hum. Reprod. 14, 667–672.
| Metabolism of the viable mammalian embryo: quietness revisited.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltV2gsA%3D%3D&md5=fe9f9412694c80d799aaae5429cbea7dCAS | 19019836PubMed |
Leroy, J. L. M. R., Vanholder, T., Mateusen, B., Christophe, A., Opsomer, G., de Kruif, A., Genicot, G., and Van Soom, A. (2005). Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro. J. Reprod. Fertil. 130, 485–495.
| Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFent7rJ&md5=28b8e4b714ca8128dba0a3e5acb8b0b5CAS |
Leroy, J. L. M. R., Van Hoeck, V., Clemente, M., Rizos, D., Gutierrez-Adan, A., Van Soom, A., Uytterhoeven, M., and Bols, P. E. J. (2010). The effect of nutritionally induced hyperlipidaemia on in vitro bovine embryo quality. Hum. Reprod. 25, 768–778.
| The effect of nutritionally induced hyperlipidaemia on in vitro bovine embryo quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitFeitr8%3D&md5=b0f7e6536db7b75d0e41d7a38ffd1f76CAS |
Lim, J. M., and Hansel, W. (2000). Exogeneous substances affecting development of in vitro-derived bovine embryos before and after embryonic genome activation. Theriogenology 53, 1081–1091.
| Exogeneous substances affecting development of in vitro-derived bovine embryos before and after embryonic genome activation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtl2jtb8%3D&md5=1617532a59555ab542178bc8776f7a1cCAS | 10798486PubMed |
Lindner, G. M., and Wright, R. W. (1983). Bovine embryo morphology and evaluation. Theriogenology 20, 407–416.
| Bovine embryo morphology and evaluation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvVKgsg%3D%3D&md5=14f1e47f228db7c869b649c5a6c35023CAS | 16725857PubMed |
Loureiro, B., Bonilla, L., Block, J., Fear, J. M., Bonilla, A. Q. S., and Hansen, P. J. (2009). Colony-stimulating factor 2 (CSF-2) improves development and posttransfer survival of bovine embryos produced in vitro. Endocrinology 150, 5046–5054.
| Colony-stimulating factor 2 (CSF-2) improves development and posttransfer survival of bovine embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVCht7bF&md5=f0f3285516c074d7aa662a58dcd965e3CAS | 19797121PubMed |
McEvoy, T. G., Robinson, J. J., Aitken, R. P., Findlay, P. A., and Robertson, I. S. (1997). Dietary excesses of urea influence the viability and metabolism of preimplantation sheep embryos and may affect fetal growth among survivors. Anim. Reprod. Sci. 47, 71–90.
| Dietary excesses of urea influence the viability and metabolism of preimplantation sheep embryos and may affect fetal growth among survivors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXksVSrt7g%3D&md5=1da6947e6624b66dea3033829344eb7eCAS | 9233507PubMed |
McEvoy, T. G., Reis, A., Ewen, M., McCallum, G. J., and Rooke, J. A. (2004). A water-soluble vitamin E analogue (Trolox) improves ovine embryo development during serum-free culture in the presence of docosahexaneoic acid (C22:6n-3). Reprod. Fertil. Dev. 16, 200–201.
| A water-soluble vitamin E analogue (Trolox) improves ovine embryo development during serum-free culture in the presence of docosahexaneoic acid (C22:6n-3).Crossref | GoogleScholarGoogle Scholar |
Miles, J. R., Farin, C. E., Rodriguez, K. F., Alexander, J. E., and Farin, P. W. (2005). Effects of embryo culture on angiogenesis and morphometry of bovine placentas during early gestation. Biol. Reprod. 73, 663–671.
| Effects of embryo culture on angiogenesis and morphometry of bovine placentas during early gestation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVCgtrvP&md5=d8036a9d0a723849a20e79ac15a4a6c1CAS | 15901637PubMed |
Olson, S. E., and Seidel, G. E. (2000a). Reduced oxygen tension and EDTA improve bovine zygote development in a chemically defined medium. J. Anim. Sci. 78, 152–157.
| 1:CAS:528:DC%2BD3cXhtVansr8%3D&md5=0cac0f480733cd754946d53350ba230cCAS | 10682816PubMed |
Olson, S. E., and Seidel, G. E. (2000b). Culture of in vitro-produced bovine embryos with vitamin E improves development in vitro and after transfer to recipients. Biol. Reprod. 62, 248–252.
| Culture of in vitro-produced bovine embryos with vitamin E improves development in vitro and after transfer to recipients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotVOktA%3D%3D&md5=174c90d236069fa31b9a5f2a422dc265CAS | 10642559PubMed |
Powell, K., Rooke, J. A., McEvoy, T. G., Ashworth, C. J., Robinson, J. J., Wilmut, I., Young, L. E., and Sinclair, K. D. (2006). Zygote donor nitrogen metabolism and in vitro embryo culture perturbs in utero development and IGF2R expression in ovine fetal tissues. Theriogenology 66, 1901–1912.
| Zygote donor nitrogen metabolism and in vitro embryo culture perturbs in utero development and IGF2R expression in ovine fetal tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVGjtLzJ&md5=185e82cd84c36cdca4e2602f8201df4eCAS | 16777210PubMed |
Reis, A., Staines, M. E., McCallum, G. J., Rooke, J. A., Lomax, M. A., and McEvoy, T. G. (2002). Vitamin E supplementation and a low oxygen atmosphere improve ovine embryo development in a serum-supplemented medium. Reprod. Abstr. Ser. 29, 9..
Reis, A., Rooke, J. A., McCallum, G. J., Ewen, M., Lomax, M. A., and McEvoy, T. G. (2003a). Stress-associated developmental arrest following in vitro ovine embryo culture in the presence of docosahexaenoic acid (DHA). Reprod. Abstr. Ser. 30, 48..
Reis, A., Rooke, J. A., McCallum, G. J., Staines, M. E., Ewen, M., Lomax, M. A., and McEvoy, T. G. (2003b). Consequences of exposure to serum, with or without vitamin E supplementation, in terms of the fatty acid content and viability of bovine blastocysts produced in vitro. Reprod. Fertil. Dev. 15, 275–284.
| Consequences of exposure to serum, with or without vitamin E supplementation, in terms of the fatty acid content and viability of bovine blastocysts produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXot1Cgur0%3D&md5=bf1352ea65810ee010cfb864b02c6edbCAS | 14588185PubMed |
Reis, A., Rooke, J. A., McCallum, G. J., Staines, M. E., Ewen, M., Lomax, M. A., and McEvoy, T. G. (2003c). Fatty acid content of polar and neutral lipids from bovine blastocysts produced in vitro in the presence or absence of serum. Reprod. Abstr. Ser. 30, 57–58.
Reis, A., McCallum, G. J., and McEvoy, T. G. (2005). Accumulation and distribution of neutral lipid droplets is non-uniform in ovine blastocysts produced in vitro in either the presence or absence of serum. Reprod. Fertil. Dev. 17, 815–823.
| Accumulation and distribution of neutral lipid droplets is non-uniform in ovine blastocysts produced in vitro in either the presence or absence of serum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlSntLvI&md5=9718be105aa7968c7a7123aac567bdb5CAS | 16476209PubMed |
Richardson, C., Barnard, V., Jones, P. C., and Hebert, C. N. (1991). Growth-rates and patterns of organs and tissues in the bovine fetus. Br. Vet. J. 147, 197–206.
| 1:STN:280:DyaK3MzkslSqtQ%3D%3D&md5=4abb46d3b9de2e8e1475c39e52f93baeCAS | 1878766PubMed |
Rooke, J. A., Carmichael, S., Talbot, R. T., and McEvoy, T. G. (2006). Effects of IVC on bovine cotyledon gene expression. Reprod. Abstr. Ser. 33, 51–52.
Sato, N., Kawamura, K., Fukuda, J., Honda, Y., Sato, T., Tanikawa, H., Kodama, H., and Tanaka, T. (2003). Expression of LDL receptor and uptake of LDL in mouse preimplantation embryos. Mol. Cell. Endocrinol. 202, 191–194.
| Expression of LDL receptor and uptake of LDL in mouse preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktFSntr0%3D&md5=c6e6f8c9a77bc28033c6cd55ab0f9b02CAS | 12770750PubMed |
Sinclair, K. D., McEvoy, T. G., Maxfield, E. K., Maltin, C. A., Young, L. E., Wilmut, I., Broadbent, P. J., and Robinson, J. J. (1999). Aberrant fetal growth and development after in vitro culture of sheep zygotes. J. Reprod. Fertil. 116, 177–186.
| Aberrant fetal growth and development after in vitro culture of sheep zygotes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjvVemtr4%3D&md5=b3c03f7b5056d66ead887960eab2b9deCAS | 10505068PubMed |
Sturmey, R. G., Reis, A., Leese, H. J., and McEvoy, T. G. (2009). Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reprod. Domest. Anim. 44(Suppl. 3), 50–58.
| Role of fatty acids in energy provision during oocyte maturation and early embryo development.Crossref | GoogleScholarGoogle Scholar |
Thompson, J. G., Mitchell, M., and Kind, K. L. (2007). Embryo culture and long-term consequences. Reprod. Fertil. Dev. 19, 43–52.
| Embryo culture and long-term consequences.Crossref | GoogleScholarGoogle Scholar | 17389134PubMed |
Young, L. E., Fernandes, K., McEvoy, T. G., Butterwith, S. C., Gutierrez, C. G., Carolan, C., Broadbent, P. J., Robinson, J. J., Wilmut, I., and Sinclair, K. D. (2001). Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat. Genet. 27, 153–154.
| Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtFGktL8%3D&md5=2077e1e455edac4e7e3dc16f0fc255adCAS | 11175780PubMed |
Zander, D. L., Thompson, J. G., and Lane, M. (2006). Perturbations in mouse embryo development and viability caused by ammonium are more severe after exposure at the cleavage stages. Biol. Reprod. 74, 288–294.
| Perturbations in mouse embryo development and viability caused by ammonium are more severe after exposure at the cleavage stages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xot1KlsA%3D%3D&md5=9bcf371ab42fda8e13e9877887515b21CAS | 16221986PubMed |
