Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Membrane lipid profile of in vitro-produced embryos is affected by vitrification but not by long-term dietary supplementation of polyunsaturated fatty acids for oocyte donor beef heifers

Beatriz C. S. Leão A B , Nathália A. S. Rocha-Frigoni A B , Ériklis Nogueira C , Elaine C. Cabral D , Christina R. Ferreira D , Marcos N. Eberlin D , Mônica F. Accorsi A , Thiago V. Neves A and Gisele Z. Mingoti A B E

A Laboratory of Physiology of Reproduction, School of Veterinary Medicine, UNESP – Universidade Estadual Paulista, Rua Clóvis Pestana 793, 16050-680, Araçatuba, SP, Brazil.

B Post-Graduation Program in Veterinary Medicine, School of Agrarian and Veterinarian Sciences, Department of Animal Reproduction, UNESP – Universidade Estadual Paulista, Via de Acesso Prof.Paulo Donato Castellane s/n, 14884-900 Jaboticabal, SP, Brazil.

C Embrapa Pantanal, Rua 21 de Setembro 1880, 79320-900, Corumbá, MS, Brazil.

D ThoMSon Mass Spectrometry Laboratory, Institute of Chemistry, University of Campinas, Cidade Universitária Zeferino Vaz s/n, CP 6154, bloco A6, sala 111, 13083-970, Distrito de Barão Geraldo, Campinas, SP, Brazil.

E Corresponding author. Email: gmingoti@fmva.unesp.br

Reproduction, Fertility and Development - https://doi.org/10.1071/RD15414
Submitted: 10 October 2015  Accepted: 24 March 2016   Published online: 25 May 2016

Abstract

Dietary rumen-protected polyunsaturated fatty acids (PUFAs) rich in linoleic acid (LA) may affect embryo yield, and LA can modulate the molecular mechanisms of lipid uptake in bovine blastocysts produced in vitro. In embryos, membrane lipids, such as phosphatidylcholines (PCs) and sphingomyelins (SMs), affect cryopreservation success. The aim of the present study was to evaluate embryonic developmental rates after the IVF of oocytes retrieved from Nellore heifers fed for approximately 90 days with rumen-protected PUFAs rich in LA. In addition, we evaluated embryo cryotolerance and the membrane structure lipid composition using matrix-assisted laser desorption ionisation mass spectrometry of fresh and vitrified embryos. Embryo development to the blastocyst stage (mean 43.2%) and embryo survival after vitrification and warming (mean 79.3%) were unaffected by diet. The relative abundance of one lipid species (PC ether (PCe; 38:2, which means that this lipid has 38 carbon atoms and 2 double bonds in the fatty acyl residues) was increased after PUFAs supplementation. However, 10 ions were affected by cryopreservation; ions consistent with PC 32:0, PC 34:1, SM 24:1, PC 40:6 or PC 42:9, PC plasmalogen (PCp) 44:10 or PC 42:7, triacylglycerol (TAG) 54:9 and a not assigned ion (m/z 833.2) were lower in blastocysts that survived to the cryopreservation process compared with fresh blastocysts, whereas the abundance of the ions PC 36:3 or PC 34:0, PCe 38:2 or PC 36:6 and PC 36:5 or PCe 38:1 were increased after cryopreservation. Thus, the results demonstrate that the mass spectrometry profiles of PC, SM and TAG species differ significantly in bovine blastocysts upon cryopreservation. Because the lipid ion abundances of fresh and vitrified–warmed embryos were distinct, they can be used as potential markers of post-cryopreservation embryonic survival.

Additional keywords: bovine, blastocyst, mass spectrometry, Nellore cattle.


References

Aittokallio, T., and Schwikowski, B. (2006). Graph-based methods for analyzing networks in cell biology. Brief. Bioinform. 7, 243–255.
Graph-based methods for analyzing networks in cell biology.CrossRef | 1:CAS:528:DC%2BD28XhtFOnu7jO&md5=cbb734fef78955e1bf8216fd8fe87604CAS | 16880171PubMed | open url image1

Al Darwich, A., Perreau, C., Petit, M. H., Papillier, P., Dupont, J., Guillaume, D., Mermillod, P., and Guignot, F. (2010). Effect of PUFA on embryo cryoresistence, gene expression and AMPKα phosphorylation in IVF-derived bovine embryos. Prostaglandins Other Lipid Mediat. 93, 30–36.
Effect of PUFA on embryo cryoresistence, gene expression and AMPKα phosphorylation in IVF-derived bovine embryos.CrossRef | 1:CAS:528:DC%2BC3cXpvV2ht7Y%3D&md5=09a9453d4a7f8e445fbccf0983c88dd6CAS | 20601073PubMed | open url image1

Almodin, C. G., Minguetti-Camara, V. C., Paixao, C. L., and Pereira, P. C. (2010). Embryo development and gestation using fresh and vitrified oocytes. Hum. Reprod. 25, 1192–1198.
Embryo development and gestation using fresh and vitrified oocytes.CrossRef | 20185514PubMed | open url image1

Arav, A., Zeron, Y., Leslie, S. B., Behboodi, E., Anderson, G. B., and Crowe, J. H. (1996). Phase transition temperature and chilling sensitivity of bovine oocytes. Cryobiology 33, 589–599.
Phase transition temperature and chilling sensitivity of bovine oocytes.CrossRef | 1:STN:280:DyaK2s7jtVyqsQ%3D%3D&md5=5f21d8985e27aaf44538cd86e22e5be5CAS | 8975686PubMed | open url image1

Ashworth, C. J., Toma, L. M., and Hunter, M. G. (2009). Nutritional effects on oocyte and embryo development in mammals: implications for reproductive efficiency and environmental sustainability. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 3351–3361.
Nutritional effects on oocyte and embryo development in mammals: implications for reproductive efficiency and environmental sustainability.CrossRef | 19833647PubMed | open url image1

Bilby, T. R., Block, J., Amaral, B. C., Sá Filho, O., Silvestre, F. T., Hansen, P. J., Staples, C. R., and Thatcher, W. W. (2006). Effects of dietary unsaturated fatty acids on oocyte quality and follicular development in lactating dairy cows in summer. J. Dairy Sci. 89, 3891–3903.
Effects of dietary unsaturated fatty acids on oocyte quality and follicular development in lactating dairy cows in summer.CrossRef | 1:CAS:528:DC%2BD28XhtVWgsb%2FO&md5=9fef7a4bb7c2636cd0a995b15e6979d9CAS | 16960065PubMed | open url image1

Brügger, B., Erben, G., Sandhoff, R., Wieland, F. T., and Lehmann, W. D. (1997). Quantitative analysis of biological membrane lipids at the low picomole level by nano-electrospray ionization tandem mass spectrometry. Proc. Natl Acad. Sci. USA 94, 2339–2344.
Quantitative analysis of biological membrane lipids at the low picomole level by nano-electrospray ionization tandem mass spectrometry.CrossRef | 9122196PubMed | open url image1

Campbell, B. K., Telferb, E. E., Webbc, R., and Bairda, D. T. (2000). Ovarian autografts in sheep as a model for studying folliculogenesis. Mol. Cell. Endocrinol. 163, 131–139.
Ovarian autografts in sheep as a model for studying folliculogenesis.CrossRef | 1:CAS:528:DC%2BD3cXlvV2ms7k%3D&md5=6c7f921e1d48e8b0afb68974740be1ddCAS | 10963885PubMed | open url image1

Carone, B. R., Fauquier, L., Habib, N., Shea, J. M., Hart, C. E., Li, R., Bock, C., Li, C., Gu, H., Zamore, P. D., Meissner, A., Weng, Z., Hofmann, H. A., Friedman, N., and Rando, O. J. (2010). Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143, 1084–1096.
Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals.CrossRef | 1:CAS:528:DC%2BC3cXhs1agtrbE&md5=1e266efe668cf2bd06e76b673a647c6cCAS | 21183072PubMed | open url image1

Cerri, R. L. A., Juchem, S. O., Chebel, R. C., Rutigliano, H., Bruno, R. G. S., Galvão, K. N., Thatcher, W. W., and Santos, J. E. P. (2009). Effect of fat source differing in fatty acid profile on metabolic parameters, fertilization, and embryo quality in high-producing dairy cows. J. Dairy Sci. 92, 1520–1531.
Effect of fat source differing in fatty acid profile on metabolic parameters, fertilization, and embryo quality in high-producing dairy cows.CrossRef | 1:CAS:528:DC%2BD1MXjvFamt78%3D&md5=55a4567d0407406c9fe3241b4f1a0ecbCAS | open url image1

Chapman, J. R. (1993). ‘Practical Organic Mass Spectrometry: A Guide for Chemical and biochemical Analysis.’ (John Wiley: New York.)

Childs, S., Carter, F., Lynch, C. O., Sreenan, J. M., Lonergan, P., Hennessy, A. A., and Kenny, D. A. (2008). Embryo yield and quality following dietary supplementation of beef heifers with n-3 polyunsaturated fatty acids (PUFA). Theriogenology 70, 992–1003.
Embryo yield and quality following dietary supplementation of beef heifers with n-3 polyunsaturated fatty acids (PUFA).CrossRef | 1:CAS:528:DC%2BD1cXhtVKmsLjN&md5=f45bcff925e7bc90591b2aa901959323CAS | 18692227PubMed | open url image1

Dinnyes, A., and Nedambale, T. L. (2009). Cryopreservation of manipulated embryos: tackling the double jeopardy. Reprod. Fertil. Dev. 21, 45–59.
Cryopreservation of manipulated embryos: tackling the double jeopardy.CrossRef | 1:CAS:528:DC%2BD1MXislGgtLs%3D&md5=bc0893622d22811a25c6f43cb4ee5593CAS | 19152745PubMed | open url image1

Fahy, E., Sud, M., Cotter, D., and Subramaniam, S. (2007). LIPID MAPS online tools for lipid research. Nucleic Acids Res. 35, W606–W612.
LIPID MAPS online tools for lipid research.CrossRef | 17584797PubMed | open url image1

Ferreira, C. R., Saraiva, S. A., Catharino, R. R., Garcia, J. S., Gozzo, F. C., Sanvido, G. B., Santos, L. F., Lo Turco, E. G., Pontes, J. H., Basso, A. C., Bertolla, R. P., Sartori, R., Guardieiro, M. M., Perecin, F., Meirelles, F. V., Sangalli, J. R., and Eberlin, M. N. (2010). Single embryo and oocyte lipid fingerprinting by mass spectrometry. J. Lipid Res. 51, 1218–1227.
Single embryo and oocyte lipid fingerprinting by mass spectrometry.CrossRef | 1:CAS:528:DC%2BC3cXltlWktb0%3D&md5=e5937c9801e77527f90a5c66ad148f69CAS | 19965589PubMed | open url image1

Ferreira, C. R., Jarmusch, A. K., Pirro, V., Alfaro, C. M., González-Serrano, A. F., Niemann, H., Wheeler, M. B., Rabel, R. A., Hallett, J. E., Houser, R., Kaufman, A., and Cooks, R. G. (2015). Ambient ionisation mass spectrometry for lipid profiling and structural analysis of mammalian oocytes, preimplantation embryos and stem cells. Reprod. Fertil. Dev. 27, 621–637.
Ambient ionisation mass spectrometry for lipid profiling and structural analysis of mammalian oocytes, preimplantation embryos and stem cells.CrossRef | 1:CAS:528:DC%2BC2MXntVWnurw%3D&md5=3f90109d761cec35483fd09a8e3e4a33CAS | 25763644PubMed | open url image1

Fouladi-Nashta, A. A., Gutierrez, C. G., Gong, J. G., Garnsworthy, P. C., and Webb, R. (2007). Impact of dietary fatty acids on oocyte quality and development in lactating dairy cows. Biol. Reprod. 77, 9–17.
Impact of dietary fatty acids on oocyte quality and development in lactating dairy cows.CrossRef | 1:CAS:528:DC%2BD2sXntV2gsb0%3D&md5=d6c8d5b9ff0b432f19b6ec25aba692abCAS | 17344470PubMed | open url image1

Fouladi-Nashta, A. A., Wonnacott, K. E., Gutierrez, C. G., Gong, J. G., Sinclair, K. D., Garnsworthy, P. C., and Webb, R. (2009). Oocyte quality in lactating dairy cows fed on high levels of n-3 and n-6 fatty acids. Reproduction 138, 771–781.
Oocyte quality in lactating dairy cows fed on high levels of n-3 and n-6 fatty acids.CrossRef | 1:CAS:528:DC%2BD1MXhsValt7rI&md5=f1033fde807dbf7e41a1d97b6a1e9419CAS | 19633135PubMed | open url image1

Funston, R. N. (2004). Fat supplementation and reproduction in beef females. J. Anim. Sci. 82 E-Suppl, E154–E161.
| 1:STN:280:DC%2BD2crjt1CnsQ%3D%3D&md5=a226fde4bf1a370ced2e28e863d9fcaeCAS | 15471795PubMed | open url image1

Gonçalves, R. F., Ferreira, M. S., de Oliveira, D. N., Canevarolo, R., Achilles, M. A., D’Ercole, D. L., Bols, P. E., Visintin, J. A., Killian, G. J., and Catharino, R. R. (2014). Analysis and characterisation of bovine oocyte and embryo biomarkers by matrix-assisted desorption ionisation mass spectrometry imaging. Reprod. Fertil. Dev. , .
Analysis and characterisation of bovine oocyte and embryo biomarkers by matrix-assisted desorption ionisation mass spectrometry imaging.CrossRef | open url image1

González-Serrano, A. F., Ferreira, C. R., Pirro, V., Lucas-Hahn, A., Heinzmann, J., Hadeler, K. G., Baulain, U., Aldag, P., Meyer, U., Piechotta, M., Jahreis, G., Dänicke, S., Cooks, R. G., and Niemann, H. (2015). Effects of long-term dietary supplementation with conjugated linoleic acid on bovine oocyte lipid profile. Reprod. Fertil. Dev. , .
Effects of long-term dietary supplementation with conjugated linoleic acid on bovine oocyte lipid profile.CrossRef | 25763644PubMed | open url image1

Guardieiro, M. M., Machado, G. M., Bastos, M. R., Mourão, G. B., Carrijo, L. H. D., Dode, M. A. N., Leroy, J. L. M. R., and Sartori, R. (2014). A diet enriched in linoleic acid compromises the cryotolerance of embryos from superovulated beef heifers. Reprod. Fertil. Dev. 26, 511–520.
A diet enriched in linoleic acid compromises the cryotolerance of embryos from superovulated beef heifers.CrossRef | 1:CAS:528:DC%2BC2cXmtVWlsr0%3D&md5=e81cd3184264deddb6b2d342610018edCAS | 23657150PubMed | open url image1

Hochi, S., Kimura, K., and Hanada, A. (1999). Effect of linoleic acid–albumin in the culture medium on freezing sensitivity of in vitro-produced bovine morulae. Theriogenology 52, 497–504.
Effect of linoleic acid–albumin in the culture medium on freezing sensitivity of in vitro-produced bovine morulae.CrossRef | 1:CAS:528:DyaK1MXmtlyhuro%3D&md5=31ecf1f1eaa5a89c7e9dcd7cad0aadc6CAS | 10734383PubMed | open url image1

Huwiler, A., Kolter, T., Pfeilschifter, J., and Sandhoff, K. (2000). Physiology and pathophysiology of sphingolipid metabolism and signaling. Biochim. Biophys. Acta 1485, 63–99.
Physiology and pathophysiology of sphingolipid metabolism and signaling.CrossRef | 1:CAS:528:DC%2BD3cXjs1Cntbg%3D&md5=69e2f1c7a9a64ab11cfa943fbf638722CAS | 10832090PubMed | open url image1

Kim, J. Y., Kinoshita, M., Ohnishi, M., and Fukui, Y. (2001). Lipid and fatty acid analysis of fresh and frozen–thawed immature and in vitro matured bovine oocytes. Reproduction 122, 131–138.
Lipid and fatty acid analysis of fresh and frozen–thawed immature and in vitro matured bovine oocytes.CrossRef | 1:CAS:528:DC%2BD3MXlsVGis70%3D&md5=f0cf4e744ada4756c8e8e10207580143CAS | 11425337PubMed | open url image1

Lapa, M., Marques, C. C., Alves, S. P., Vasques, M. I., Baptista, M. C., Carvalhais, I., Silva Pereira, M., Horta, A. E., Bessa, R. J., and Pereira, R. M. (2011). Effect of trans-10 cis-12 conjugated linoleic acid on bovine oocyte competence and fatty acid composition. Reprod. Domest. Anim. 46, 904–910.
Effect of trans-10 cis-12 conjugated linoleic acid on bovine oocyte competence and fatty acid composition.CrossRef | 1:CAS:528:DC%2BC3MXhtlemtrvM&md5=4642b8ec9aa7d4b3aa96a8e76a0a716fCAS | 21366717PubMed | open url image1

Leão, B. C. S., Rocha-Frigoni, N. A. S., Cabral, E. C., Coelho, M. B., Ferreira, C. R., Eberlin, M. N., Accorsi, M. F., Nogueira, É., and Mingoti, G. Z. (2015a). Improved embryonic cryosurvival observed after in vitro supplementation with conjugated linoleic acid is related to changes in the membrane lipid profile. Theriogenology 84, 127–136.
Improved embryonic cryosurvival observed after in vitro supplementation with conjugated linoleic acid is related to changes in the membrane lipid profile.CrossRef | open url image1

Leão, B. C. S., Rocha-Frigoni, N. A. S., Cabral, E. C., Franco, M. F., Ferreira, C. R., Eberlin, M. N., Filgueiras, P. R., and Mingoti, G. Z. (2015b). Membrane lipid profile monitored by mass spectrometry detected differences between fresh and vitrified in vitro-produced bovine embryos. Zygote 23, 732–741.
Membrane lipid profile monitored by mass spectrometry detected differences between fresh and vitrified in vitro-produced bovine embryos.CrossRef | open url image1

Leroy, J. L., Van Hoeck, V., Clemente, M., Rizos, D., Gutierrez-Adan, A., Van Soom, A., Uytterhoeven, M., and Bols, P. E. (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 | 1:CAS:528:DC%2BC3cXitFeitr8%3D&md5=87af537b11e8d3d7953e6cd90592f945CAS | 20007613PubMed | open url image1

Leroy, J. L. M. R., Sturmey, R. G., Van Hoeck, V., De Bie, J., McKeegan, P. J., and Bols, P. E. J. (2013). Dietary lipid supplementation on cow reproductive performance and oocyte and embryo viability: a real benefit? In ‘Proceedings of the 27th Annual Meeting of the Brazilian Embryo Technology Society (SBTE)’. (Ed. Brazilian College of Animal Reproduction.) pp. 258–267. (Brazilian Embryo Technology Society.)

Lonergan, P., Rizos, D., Gutierrez-Adan, A., Fair, T., and Boland, M. P. (2003). Oocyte and embryo quality: effect of origin, culture conditions and gene expression patterns. Reprod. Domest. Anim. 38, 259–267.
Oocyte and embryo quality: effect of origin, culture conditions and gene expression patterns.CrossRef | 1:STN:280:DC%2BD3svis1SrsA%3D%3D&md5=c15f7a29da774da5e77ab76c96db5d15CAS | 12887565PubMed | open url image1

Marei, W. F., Wathes, D. C., and Foulad-Nashta, A. A. (2009). The effect of linolenic acid on bovine oocyte maturation and development. Biol. Reprod. 81, 1064–1072.
The effect of linolenic acid on bovine oocyte maturation and development.CrossRef | 1:CAS:528:DC%2BD1MXhsV2lt7vL&md5=63cf73bcfc56be853e4e7e6f8600da2dCAS | 19587335PubMed | open url image1

Marei, W. F., Wathes, D. C., and Foulad-Nashta, A. A. (2010). Impact of linoleic acid on bovine oocyte maturation and embryo development. Reproduction 139, 979–988.
Impact of linoleic acid on bovine oocyte maturation and embryo development.CrossRef | 1:CAS:528:DC%2BC3cXns12qsLY%3D&md5=c7e8bb2e1cc21c723a53bf547c08ae39CAS | 20215338PubMed | open url image1

Mattos, R., Staples, C. R., and Thatcher, W. W. (2000). Effects of dietary fatty acids on reproduction in ruminants. Rev. Reprod. 5, 38–45.
Effects of dietary fatty acids on reproduction in ruminants.CrossRef | 1:CAS:528:DC%2BD3cXotVyisQ%3D%3D&md5=b2616bc03937f37eea0619f201bfa363CAS | 10711734PubMed | open url image1

McEvoy, T. G., Coull, G. D., Broadbent, P. J., Hutchinson, J. S., and Speake, B. K. (2000). Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J. Reprod. Fertil. 118, 163–170.
Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida.CrossRef | 1:CAS:528:DC%2BD3cXpsl2msA%3D%3D&md5=334d2100bbd00638158706e3912bb52eCAS | 10793638PubMed | open url image1

Merrill, A. H., Schmelz, E. M., Dillehay, D. L., Spiegel, S., Shayman, J. A., Schroeder, J. J., Riley, R. T., Voss, K. A., and Wang, E. (1997). Sphingolipids: the enigmatic lipid class: biochemistry, physiology, and pathophysiology. Toxicol. Appl. Pharmacol. 142, 208–225.
Sphingolipids: the enigmatic lipid class: biochemistry, physiology, and pathophysiology.CrossRef | 1:CAS:528:DyaK2sXlt1Gluw%3D%3D&md5=a8a9fb90ea824080c7be52155827b950CAS | 9007051PubMed | open url image1

Milne, S., Ivanova, P., Forrester, J., and Alex Brown, H. (2006). Lipidomics: an analysis of cellular lipids by ESI-MS. Methods 39, 92–103.
Lipidomics: an analysis of cellular lipids by ESI-MS.CrossRef | 1:CAS:528:DC%2BD28XnsFymsbg%3D&md5=73e9d854befa0ada0cefd0bef471fdc4CAS | 16846739PubMed | open url image1

Pariza, M. W., Park, Y., and Cook, M. E. (2001). The biologically active isomers of conjugated linoleic acid. Prog. Lipid Res. 40, 283–298.
The biologically active isomers of conjugated linoleic acid.CrossRef | 1:CAS:528:DC%2BD3MXltFWhurs%3D&md5=2a92b9c45ba7be44c9ee079bb5a3333fCAS | 11412893PubMed | open url image1

Parrish, J. J., Susko-Parrish, J., Winer, M. A., and First, N. L. (1988). Capacitation of bovine sperm by heparin. Biol. Reprod. 38, 1171–1180.
Capacitation of bovine sperm by heparin.CrossRef | 1:CAS:528:DyaL1cXkslWit7g%3D&md5=5f6eee533fe3840b8dccbb5ba5b04cabCAS | 3408784PubMed | open url image1

Pereira, R. M., Baptista, M. C., Vasques, M. I., Horta, A. E., Portugal, P. V., Bessa, R. J., Silva, J. C., Pereira, M. S., and Marques, C. C. (2007). Cryosurvival of bovine blastocysts is enhanced by culture with trans-10 cis-12 conjugated linoleic acid (10t,12c CLA). Anim. Reprod. Sci. 98, 293–301.
Cryosurvival of bovine blastocysts is enhanced by culture with trans-10 cis-12 conjugated linoleic acid (10t,12c CLA).CrossRef | 1:CAS:528:DC%2BD2sXit1Gnu7k%3D&md5=c3da0a8deafaa37a170928a764972c59CAS | 16644149PubMed | open url image1

Pereira, R. M., Carvalhais, I., Pimenta, J., Baptista, M. C., Vasques, M. I., Horta, A. E., Santos, I. C., Marques, M. R., Reis, A., Pereira, M. S., and Marques, C. C. (2008). Biopsied and vitrified bovine embryos viability is improved by trans10, cis12 conjugated linoleic acid supplementation during in vitro embryo culture. Anim. Reprod. Sci. 106, 322–332.
Biopsied and vitrified bovine embryos viability is improved by trans10, cis12 conjugated linoleic acid supplementation during in vitro embryo culture.CrossRef | 1:CAS:528:DC%2BD1cXls1yku78%3D&md5=19fb9b6f451288e7b101837146a3c379CAS | 17580103PubMed | open url image1

Perry, G. (2015). 2013 statistics of embryo collection and transfer in domestic farm animals. Embryo Transfer Newslett. 33, 14–26. open url image1

Petković, M., Schiller, J., Müller, M., Benard, S., Reichl, S., Arnold, K., and Arnhold, J. (2001). Detection of individual phospholipids in lipid mixtures by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry: phosphatidylcholine prevents the detection of further species. Anal. Biochem. 289, 202–216.
Detection of individual phospholipids in lipid mixtures by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry: phosphatidylcholine prevents the detection of further species.CrossRef | 11161314PubMed | open url image1

Picone, O., Laigre, P., Fortun-Lamothe, L., Archilla, C., Peynot, N., Ponter, A. A., Berthelot, V., Cordier, A. G., Duranthon, V., and Chavatte-Palmer, P. (2011). Hyperlipidic hypercholesterolemic diet in prepubertal rabbits affects gene expression in the embryo, restricts fetal growth and increases offspring susceptibility to obesity. Theriogenology 75, 287–299.
Hyperlipidic hypercholesterolemic diet in prepubertal rabbits affects gene expression in the embryo, restricts fetal growth and increases offspring susceptibility to obesity.CrossRef | 1:CAS:528:DC%2BC3cXhsF2isbnK&md5=6c26d93ac3f90ccca6558fbad9ddb6beCAS | 21040967PubMed | open url image1

Ponter, A. A., Guyader-Joly, C., Nuttinck, F., Grimard, B., and Humblot, P. (2012). Oocyte and embryo production and quality after OPU-IVF in dairy heifers given diets varying in their n-6/n-3 fatty acid ratio. Theriogenology 78, 632–645.
Oocyte and embryo production and quality after OPU-IVF in dairy heifers given diets varying in their n-6/n-3 fatty acid ratio.CrossRef | 1:CAS:528:DC%2BC38XmtFertrk%3D&md5=ff6299ab942fc16270a5dbff2f1a21b5CAS | 22537996PubMed | open url image1

Rizos, D., Lonergan, P., Boland, M. P., Arroyo-García, R., Pintado, B., de la Fuente, J., and Gutiérrez-Adán, A. (2002a). Analysis of differential mRNA expression between bovine blastocysts produced in different culture systems: implications for blastocyst quality. Biol. Reprod. 66, 589–595.
Analysis of differential mRNA expression between bovine blastocysts produced in different culture systems: implications for blastocyst quality.CrossRef | 1:CAS:528:DC%2BD38XhvVeitLo%3D&md5=3e52e9e316e70f1f138ce22773654801CAS | 11870062PubMed | open url image1

Rizos, D., Lonergan, P., Ward, F., Duffy, P., and Boland, M. P. (2002b). Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol. Reprod. Dev. 61, 234–248.
Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality.CrossRef | 1:CAS:528:DC%2BD38Xlt1Giug%3D%3D&md5=fd530554a4e416cc604ed66ebc4922a4CAS | 11803560PubMed | open url image1

Rizos, D., Gutiérrez-Adán, A., Pérez-Garnelo, S., de la Fuente, J., Boland, M. P., and Lonergan, P. (2003). Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance, and messenger RNA expression. Biol. Reprod. 68, 236–243.
Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance, and messenger RNA expression.CrossRef | 1:CAS:528:DC%2BD3sXjtFWj&md5=32337306805acc917a34f73d5b231a5bCAS | 12493719PubMed | open url image1

Robker, R. L., Akison, L. K., Bennett, B. D., Thrupp, P. N., Chura, L. R., Russell, D. L., Lane, M., and Norman, R. J. (2009). Obese women exhibit differences in ovarian metabolites, hormones and gene expression compared with moderate-weight women. J. Clin. Endocrinol. Metab. 94, 1533–1540.
Obese women exhibit differences in ovarian metabolites, hormones and gene expression compared with moderate-weight women.CrossRef | 1:CAS:528:DC%2BD1MXlvVCqtrw%3D&md5=760ea5af15a944a7834ccc057f620791CAS | 19223519PubMed | open url image1

Rocha-Frigoni, N. A. S., Leão, B. C. S., Nogueira, É., Accorsi, M. F., and Mingoti, G. Z. (2014). Reduced levels of intracellular reactive oxygen species and apoptotic status are not correlated with increases in cryotolerance of bovine embryos produced in vitro in the presence of antioxidants. Reprod. Fertil. Dev. 26, 797–805.
Reduced levels of intracellular reactive oxygen species and apoptotic status are not correlated with increases in cryotolerance of bovine embryos produced in vitro in the presence of antioxidants.CrossRef | 1:CAS:528:DC%2BC2cXhtFynsbnM&md5=55796117adf03e79e0adba01b8e67ed8CAS | open url image1

Sampath, H., and Ntambi, J. M. (2005). Polyunsaturated fatty acid regulation of genes of lipid metabolism. Annu. Rev. Nutr. 25, 317–340.
Polyunsaturated fatty acid regulation of genes of lipid metabolism.CrossRef | 1:CAS:528:DC%2BD2MXpvF2mtrY%3D&md5=51cfdb94ef0c039981cd9a9b25695e0fCAS | 16011470PubMed | open url image1

Santos, J. E. P., Cerri, R. L. A., and Sartori, R. (2008a). Nutritional management of the donor cow. Theriogenology 69, 88–97.
Nutritional management of the donor cow.CrossRef | 1:CAS:528:DC%2BD2sXhsVSmu7nE&md5=706e6beb1c8147f9954591799c5faceeCAS | open url image1

Santos, J. E. P., Bilby, T. R., Thatcher, W. W., Staples, C. R., and Silvestre, F. T. (2008b). Long chain fatty acids of diet as factors influencing reproduction in cattle. Reprod. Domest. Anim. 43, 23–30.
Long chain fatty acids of diet as factors influencing reproduction in cattle.CrossRef | open url image1

Saragusty, J., and Arav, A. (2011). Current progress in oocyte and embryo cryopreservation by slow freezing and vitrification. Reproduction 141, 1–19.
Current progress in oocyte and embryo cryopreservation by slow freezing and vitrification.CrossRef | 1:CAS:528:DC%2BC3MXisVehsrc%3D&md5=b1ab1e2662b60fa6d125db5cb6937876CAS | 20974741PubMed | open url image1

Scaramuzzi, R. J., Baird, D. T., Campbell, B. K., Driancourt, M. A., Dupont, J., Fortune, J. E., Gilchrist, R. B., Martin, G. B., McNatty, K. P., McNeilly, A. S., Monget, P., Monniaux, D., Viñoles, C., and Webb, R. (2011). Regulation of folliculogenesis and the determination of ovulation rate in ruminants. Reprod. Fertil. Dev. 23, 444–467.
Regulation of folliculogenesis and the determination of ovulation rate in ruminants.CrossRef | 1:CAS:528:DC%2BC3MXjt12ntLg%3D&md5=e22ff8ed0c108312648dfb55311dd537CAS | 21426863PubMed | open url image1

Seidel, G. E. (2006). Modifying oocytes and embryos to improve their cryopreservation. Theriogenology 65, 228–235.
Modifying oocytes and embryos to improve their cryopreservation.CrossRef | 1:CAS:528:DC%2BD2MXht1Gitr3O&md5=e0e0448a760c7d2d94eee7fa05ed13feCAS | 16263160PubMed | open url image1

Sinclair, K. D., Kuran, M., Gebbie, F. E., Webb, R., and McEvoy, T. G. (2000). Nitrogen metabolism and fertility in cattle: II. Development of oocytes recovered from heifers offered diets differing in their rate of nitrogen release in the rumen. J. Anim. Sci. 78, 2670–2680.
Nitrogen metabolism and fertility in cattle: II. Development of oocytes recovered from heifers offered diets differing in their rate of nitrogen release in the rumen.CrossRef | 1:CAS:528:DC%2BD3cXnsVarsb0%3D&md5=dd7d6ce8e3ace52f16ac0c08afaf52adCAS | 11048933PubMed | open url image1

Soubry, A., Schildkraut, J. M., Murtha, A., Wang, F., Huang, Z., Bernal, A., Kurtzberg, J., Jirtle, R. L., Murphy, S. K., and Hoyo, C. (2013). Paternal obesity is associated with IGF2 hypomethylation in newborns: results from a Newborn Epigenetics Study (NEST) cohort. BMC Med. 11, 29.
Paternal obesity is associated with IGF2 hypomethylation in newborns: results from a Newborn Epigenetics Study (NEST) cohort.CrossRef | 1:CAS:528:DC%2BC3sXlvVaks7c%3D&md5=6184fc9cf63b6f359a66a9aa7d86e802CAS | 23388414PubMed | open url image1

Staples, C. R., Burke, J. M., and Thatcher, W. W. (1998). Influence of supplemental fats on reproductive tissues and performance of lactating cows. J. Dairy Sci. 81, 856–871.
Influence of supplemental fats on reproductive tissues and performance of lactating cows.CrossRef | 1:CAS:528:DyaK1cXitlyht7c%3D&md5=891e120ab0c7069c0a24c6e9d2b6f82fCAS | 9565891PubMed | open url image1

Stroud, B., and Callesen, H. (2012). IETS statement on worldwide ET statistics for 2010. Anim. Reprod. 9, 210–216. open url image1

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, 50–58.
Role of fatty acids in energy provision during oocyte maturation and early embryo development.CrossRef | 19660080PubMed | open url image1

Sudano, M. J., Santos, V. G., Tata, A., Ferreira, C. R., Paschoal, D. M., Machado, R., Buratini, J., Eberlin, M. N., and Landim-Alvarenga, F. D. (2012). Phosphatidylcholine and sphingomyelin profiles vary in Bos taurus indicus and Bos taurus taurus in vitro- and in vivo-produced blastocysts. Biol. Reprod. 87, 130.
Phosphatidylcholine and sphingomyelin profiles vary in Bos taurus indicus and Bos taurus taurus in vitro- and in vivo-produced blastocysts.CrossRef | 23053436PubMed | open url image1

Sudano, M. J., Caixeta, E. S., Paschoal, D. M., Martins, Jr, A., Machado, R., Buratini, J. J., and Landim-Alvarenga, F. D. C. (2014). Cryotolerance and global gene-expression patterns of Bos taurus indicus and Bos taurus taurus in vitro- and in vivo-produced blastocysts. Reprod. Fertil. Dev. 26, 1129–1141.
Cryotolerance and global gene-expression patterns of Bos taurus indicus and Bos taurus taurus in vitro- and in vivo-produced blastocysts.CrossRef | 1:CAS:528:DC%2BC2cXhslChsbzN&md5=e28f106a460dcfb258eb8606ba3091aaCAS | 24025608PubMed | open url image1

Tata, A., Sudano, M. J., Santos, V. G., Landim-Alvarenga, F. D., Ferreira, C. R., and Eberlin, M. N. (2013). Optimal single-embryo mass spectrometry fingerprinting. J. Mass Spectrom. 48, 844–849.
Optimal single-embryo mass spectrometry fingerprinting.CrossRef | 1:CAS:528:DC%2BC3sXhtVOjtbvL&md5=2befefb1faaf549935217146a385aec6CAS | 23832940PubMed | open url image1

Thangavelu, G., Colazo, M. G., Ambrose, D. J., Oba, M., Okine, E. K., and Dyck, M. K. (2007). Diets enriched in unsaturated fatty acids enhance early embryonic development in lactating Holstein cows. Theriogenology 68, 949–957.
Diets enriched in unsaturated fatty acids enhance early embryonic development in lactating Holstein cows.CrossRef | 1:CAS:528:DC%2BD2sXhtVOgsb7N&md5=985165fd62aaebe7b8ee83f0a220da6aCAS | 17850856PubMed | open url image1

Vajta, G., Rindom, N., Peura, T. T., Holm, P., Greve, T., and Callesen, H. (1999). The effect of media, serum and temperature on in vitro survival of bovine blastocysts after open pulled straw (OPS) vitrification. Theriogenology 52, 939–948.
The effect of media, serum and temperature on in vitro survival of bovine blastocysts after open pulled straw (OPS) vitrification.CrossRef | 1:STN:280:DC%2BD3c7pvFejtQ%3D%3D&md5=678088c1bf053837a1eec506350ff0ebCAS | 10735132PubMed | open url image1

Viana, J. H. M., and Camargo, L. S. A. (2007). Bovine embryo production in Brazil: a new scenario. Acta Sci. Vet. 35, 915–924. open url image1

Viana, J. H. M., Siqueira, L. G. B., Palhão, M. P., and Camargo, L. S. A. (2010). Use of in vitro fertilization technique in the last decade and its effect on Brazilian embryo industry and animal production. Acta Sci. Vet. 38, 661–674. open url image1

Vinzi, V. E., Chin, W. W., Henseler, J., and Wang, H. (2010). ‘Handbook of Partial Least Squares: Concepts, Methods and Applications (Springer Handbooks of Computational Statistics).’ (Springer Verlag: Berlin, Heidelberg.)

Webb, R., Garnsworthy, P. C., Gong, J. G., and Armstrong, D. G. (2004). Control of follicular growth: local interactions and nutritional influences. J. Anim. Sci. 82 E-Suppl, E63–E74.
| 1:STN:280:DC%2BD2crjt1Cltg%3D%3D&md5=ac0cd3dc081c68f77ff95176454e1808CAS | 15471816PubMed | open url image1

Xia, J., and Wishart, D. S. (2011a). Unit 14.10 metabolomic data processing, analysis, and interpretation using MetaboAnalyst. In ‘Current Protocols in Bioinformatics’. (Eds A. Bateman, W. R. Pearson, L. D. Stein, G. D. Stormo, and J. Yates III.) pp. 14.10.1–14.10.48. (Wiley Online Library: Hoboken, NJ.)

Xia, J., and Wishart, D. S. (2011b). Web-based inference of biological patterns, functions and pathways from metabolomic data using MetaboAnalyst. Nat. Protoc. 6, 743–760.
Web-based inference of biological patterns, functions and pathways from metabolomic data using MetaboAnalyst.CrossRef | 1:CAS:528:DC%2BC3MXmvFyqtL0%3D&md5=b1b37b0a2188e4b89188351ea2ddfa30CAS | 21637195PubMed | open url image1

Xia, J., Mandal, S., Sinelnokov, I. V., Broadhurst, D., and Wishart, D. S. (2012). MetaboAnalyst 2.0: a comprehensive server for metabolomic data analysis. Nucleic Acids Res. 40, W127–W133.
MetaboAnalyst 2.0: a comprehensive server for metabolomic data analysis.CrossRef | 1:CAS:528:DC%2BC3sXjtVCqu7w%3D&md5=bea510bb04e647b09968b99a7ef041c1CAS | 22553367PubMed | open url image1

Zachut, M., Arieli, A., and Moallem, U. (2011). Incorporation of dietary n-3 fatty acids into ovarian compartments in dairy cows and the effects on hormonal and behavioral patterns around estrus. Reproduction 141, 833–840.
Incorporation of dietary n-3 fatty acids into ovarian compartments in dairy cows and the effects on hormonal and behavioral patterns around estrus.CrossRef | 1:CAS:528:DC%2BC3MXovVCktbo%3D&md5=c9a34c76edf02d7a809bea69848fbf1eCAS | 21389076PubMed | open url image1

Zeron, Y., Sklan, D., and Arav, A. (2002). Effect of polyunsaturated fatty acid supplementation on biophysical parameters and chilling sensitivity of ewe oocytes. Mol. Reprod. Dev. 61, 271–278.
Effect of polyunsaturated fatty acid supplementation on biophysical parameters and chilling sensitivity of ewe oocytes.CrossRef | 1:CAS:528:DC%2BD38Xlt1Ghsw%3D%3D&md5=fa41c90744255fef803c04b2b060b785CAS | 11803563PubMed | open url image1

Zhou, Z., Marepally, S. R., Nune, D. S., Pallakollu, P., Ragan, G., Roth, M. R., Wang, L., Lushington, G. H., Visvanathan, M., and Welti, R. (2011). LipidomeDB data calculation environment: online processing of direct-infusion mass spectral data for lipid profiles. Lipids 46, 879–884.
LipidomeDB data calculation environment: online processing of direct-infusion mass spectral data for lipid profiles.CrossRef | 1:CAS:528:DC%2BC3MXptlWis7g%3D&md5=263e63d265f4a12101efac67f01cd84cCAS | 21647782PubMed | open url image1



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