Breed-specific factors influence embryonic lipid composition: comparison between Jersey and Holstein
Luis Baldoceda A , Isabelle Gilbert A , Dominic Gagné A , Christian Vigneault B , Patrick Blondin B , Christina Ramires Ferreira C and Claude Robert A DA Laboratory of Functional Genomics of Early Embryonic Development, Centre de Recherche en Biologie de la Reproduction, Institut des Nutraceutiques et des Aliments Fonctionnels, Faculté des sciences de l’agriculture et de l’alimentation, Pavillon des services, Université Laval, Québec G1V 0A6, Canada.
B L’Alliance Boviteq Inc., 19320 Grand rang St-François, Saint-Hyacinthe, Québec J2T 5H1, Canada.
C ThoMSon Mass Spectrometry Laboratory, Institute of Chemistry, University of Campinas, São Paulo, Campinas 13083-970, Brazil.
D Corresponding author. Email: claude.robert@fsaa.ulaval.ca
Reproduction, Fertility and Development 28(8) 1185-1196 https://doi.org/10.1071/RD14211
Submitted: 17 June 2014 Accepted: 2 December 2014 Published: 15 January 2015
Abstract
Some embryos exhibit better survival potential to cryopreservation than others. The cause of such a phenotype is still unclear and may be due to cell damage during cryopreservation, resulting from overaccumulation and composition of lipids. In cattle embryos, in vitro culture conditions have been shown to impact the number of lipid droplets within blastomeres. Thus far, the impact of breed on embryonic lipid content has not been studied. In the present study were compared the colour, lipid droplet abundance, lipid composition, mitochondrial activity and gene expression of in vivo-collected Jersey breed embryos, which are known to display poor performance post-freezing, with those of in vivo Holstein embryos, which have good cryotolerance. Even when housed and fed under the same conditions, Jersey embryos were found to be darker and contain more lipid droplets than Holstein embryos, and this was correlated with lower mitochondrial activity. Differential expression of genes associated with lipid metabolism and differences in lipid composition were found. These results show genetic background can impact embryonic lipid metabolism and storage.
Additional keywords: embryo, lipid droplets, lipid profile, mitochondria.
References
Aardema, H., Vos, P. L., Lolicato, F., Roelen, B. A., Knijn, H. M., Vaandrager, A. B., Helms, J. B., and Gadella, B. M. (2011). Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence. Biol. Reprod. 85, 62–69.| Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotFOls74%3D&md5=91c35c1502e6480acc58b76f6a2faff4CAS | 21311036PubMed |
Abe, H., and Hoshi, H. (2003). Evaluation of bovine embryos produced in high performance serum-free media. J. Reprod. Dev. 49, 193–202.
| Evaluation of bovine embryos produced in high performance serum-free media.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmvFSqtLY%3D&md5=1bc26b43a714bf349fc44d256199bc88CAS | 14967928PubMed |
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=f7937ac4f90e986f1bf6436ac8b03c51CAS | 10369393PubMed |
Abe, H., Matsuzaki, S., and Hoshi, H. (2002a). Ultrastructural differences in bovine morulae classified as high and low qualities by morphological evaluation. Theriogenology 57, 1273–1283.
| Ultrastructural differences in bovine morulae classified as high and low qualities by morphological evaluation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD383mvF2itw%3D%3D&md5=e8965e068571dbbc7192377f43ca738dCAS | 12013447PubMed |
Abe, H., Yamashita, S., Satoh, T., and Hoshi, H. (2002b). Accumulation of cytoplasmic lipid droplets in bovine embryos and cryotolerance of embryos developed in different culture systems using serum-free or serum-containing media. Mol. Reprod. Dev. 61, 57–66.
| Accumulation of cytoplasmic lipid droplets in bovine embryos and cryotolerance of embryos developed in different culture systems using serum-free or serum-containing media.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptVejur4%3D&md5=9f309a13a31a61fae851812e002e6e0eCAS | 11774376PubMed |
Baldoceda, L., Gagné, D., Ramires Ferreira, C., and Robert, C. (2016). Genetics influences response to L-carnitine treatment as a mean to reduce lipid content of bovine embryos. Reprod. Fertil. Dev. 28, 1172–1184.
| Genetics influences response to L-carnitine treatment as a mean to reduce lipid content of bovine embryos.Crossref | GoogleScholarGoogle Scholar | 25568931PubMed |
Beaulieu, A. D., and Palmquist, D. L. (1995). Differential effects of high fat diets on fatty acid composition in milk of Jersey and Holstein cows. J. Dairy Sci. 78, 1336–1344.
| Differential effects of high fat diets on fatty acid composition in milk of Jersey and Holstein cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmsFCnsL8%3D&md5=545f9cbf962dea8a7a8ec668fca7e103CAS | 7673523PubMed |
Bermejo-Alvarez, P., Rizos, D., Rath, D., Lonergan, P., and Gutierrez-Adan, A. (2010). Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts. Proc. Natl Acad. Sci. USA 107, 3394–3399.
| Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtFymtbo%3D&md5=22ce2e70c5491bb48bb12d6c72732255CAS | 20133684PubMed |
Bousquet, D., Burnside, E., and Van Doormaal, B. (2003). Biotechnologies of reproduction applied to dairy cattle production: Embryo transfer and IVF. Can. J. Anim. Sci. 83, 403–407.
| Biotechnologies of reproduction applied to dairy cattle production: Embryo transfer and IVF.Crossref | GoogleScholarGoogle Scholar |
Chen, H., Zhang, L., Li, X., Sun, G., Yuan, X., Lei, L., Liu, J., Yin, L., Deng, Q., Wang, J., Liu, Z., Yang, W., Wang, Z., Zhang, H., and Liu, G. (2013). Adiponectin activates the AMPK signaling pathway to regulate lipid metabolism in bovine hepatocytes. J. Steroid Biochem. Mol. Biol. 138, 445–454.
| Adiponectin activates the AMPK signaling pathway to regulate lipid metabolism in bovine hepatocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslerurzJ&md5=f96aba9fa5e7ecb5526b81ef0b8b4b21CAS | 23994141PubMed |
Crosier, A. E., Farin, P. W., Dykstra, M. J., Alexander, J. E., and Farin, C. E. (2001). Ultrastructural morphometry of bovine blastocysts produced in vivo or in vitro. Biol. Reprod. 64, 1375–1385.
| Ultrastructural morphometry of bovine blastocysts produced in vivo or in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtFKqsrw%3D&md5=32729708550802fe947633a1a43bc883CAS | 11319141PubMed |
Dorland, M., Gardner, D. K., and Trounson, A. O. (1994). Serum in synthetic oviduct fluid causes mitochondrial degeneration in ovine embryos. J. Reprod. Fertil. Abstr. Ser. 13, 70.
Dumollard, R., Duchen, M., and Carroll, J. (2007). The role of mitochondrial function in the oocyte and embryo. Curr. Top. Dev. Biol. 77, 21–49.
| The role of mitochondrial function in the oocyte and embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmt1Gltb4%3D&md5=ef902ce04a34ede18ce030f99570900eCAS | 17222699PubMed |
Fair, T., Lonergan, P., Dinnyes, A., Cottell, D. C., Hyttel, P., Ward, F. A., and Boland, M. P. (2001). Ultrastructure of bovine blastocysts following cryopreservation: effect of method of blastocyst production. Mol. Reprod. Dev. 58, 186–195.
| Ultrastructure of bovine blastocysts following cryopreservation: effect of method of blastocyst production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjslOiug%3D%3D&md5=288b31649d0a53732f7d77f6eb281693CAS | 11139231PubMed |
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=7dcf1ca4e4190921db5a3506b5f051d8CAS | 10615263PubMed |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltlWktb0%3D&md5=7bb1b5e88870c6631e0be3c2eca37682CAS | 19965589PubMed |
Fischer, S., Santos, A. N., Thieme, R., Ramin, N., and Fischer, B. (2010). Adiponectin stimulates glucose uptake in rabbit blastocysts. Biol. Reprod. 83, 859–865.
| Adiponectin stimulates glucose uptake in rabbit blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlGls7%2FL&md5=77b15efd077cdbee21feb901ef7c7983CAS | 20686181PubMed |
Gilbert, I., Scantland, S., Sylvestre, E. L., Dufort, I., Sirard, M. A., and Robert, C. (2010). Providing a stable methodological basis for comparing transcript abundance of developing embryos using microarrays. Mol. Hum. Reprod. 16, 601–616.
| Providing a stable methodological basis for comparing transcript abundance of developing embryos using microarrays.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptlegt7Y%3D&md5=a56eeb56ec9c2f67c5c4108849f13ef5CAS | 20479066PubMed |
Gregory, M. K., Gibson, R. A., Cook-Johnson, R. J., Cleland, L. G., and James, M. J. (2011). Elongase reactions as control points in long-chain polyunsaturated fatty acid synthesis. PLoS ONE 6, e29662.
| Elongase reactions as control points in long-chain polyunsaturated fatty acid synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XksFKnsQ%3D%3D&md5=cdcc8b09a1cef1eee58249d0417e6080CAS | 22216341PubMed |
Guignot, F. (2005). Cryoconservation des embryons des espèces domestiques. INRA Prod. Anim. 18, 27–35.
Hasler, J. F. (2001). Factors affecting frozen and fresh embryo transfer pregnancy rates in cattle. Theriogenology 56, 1401–1415.
| Factors affecting frozen and fresh embryo transfer pregnancy rates in cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2Fkt1ektA%3D%3D&md5=82d1e31b1f2cf69aeb462be5406bcdeeCAS | 11768807PubMed |
Hyttel, P., Callesen, H., and Greve, T. (1986). Ultrastructural features of preovulatory oocyte maturation in superovulated cattle. J. Reprod. Fertil. 76, 645–656.
| Ultrastructural features of preovulatory oocyte maturation in superovulated cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL287pvFyrtQ%3D%3D&md5=8296c99176fa9ec87c0627ea5752db2eCAS | 3084771PubMed |
Inagaki, K., Aki, T., Fukuda, Y., Kawamoto, S., Shigeta, S., Ono, K., and Suzuki, O. (2002). Identification and expression of a rat fatty acid elongase involved in the biosynthesis of C18 fatty acids. Biosci. Biotechnol. Biochem. 66, 613–621.
| Identification and expression of a rat fatty acid elongase involved in the biosynthesis of C18 fatty acids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xisl2mur4%3D&md5=97b3348d68aacc9ee8e1d0ca9c7c6083CAS | 12005057PubMed |
Kalo, D., and Roth, Z. (2011). Involvement of the sphingolipid ceramide in heat-shock-induced apoptosis of bovine oocytes. Reprod. Fertil. Dev. 23, 876–888.
| Involvement of the sphingolipid ceramide in heat-shock-induced apoptosis of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVOrtb7O&md5=1fcff06103228557fa0613e086ac6806CAS | 21871207PubMed |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsVGis70%3D&md5=2b5049110598d7946e58d5859cdefa02CAS | 11425337PubMed |
Kruip, T. A. M., Cran, D. G., van Beneden, T. H., and Dieleman, S. J. (1983). Structural changes in bovine oocytes during final maturation in vivo. Gamete Res. 8, 29–47.
| Structural changes in bovine oocytes during final maturation in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXlvVyisLc%3D&md5=fbb3ccdccd16f7d70416030d03e2d31cCAS |
Leonard, A. E., Kelder, B., Bobik, E. G., Chuang, L. T., Lewis, C. J., Kopchick, J. J., Mukerji, P., and Huang, Y. S. (2002). Identification and expression of mammalian long-chain PUFA elongation enzymes. Lipids 37, 733–740.
| Identification and expression of mammalian long-chain PUFA elongation enzymes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsFKgsLk%3D&md5=ebf0d82bfa6df26c35518436416cee77CAS | 12371743PubMed |
Leroy, J. L., Opsomer, G., De Vliegher, S., Vanholder, T., Goossens, L., Geldhof, A., Bols, P. E., de Kruif, A., and Van Soom, A. (2005). Comparison of embryo quality in high-yielding dairy cows, in dairy heifers and in beef cows. Theriogenology 64, 2022–2036.
| Comparison of embryo quality in high-yielding dairy cows, in dairy heifers and in beef cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MnitlejtQ%3D%3D&md5=cd5ecb4d6c1a85b58600bc93d1fd755aCAS | 15936067PubMed |
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=7617679a6efca9a3c2534e0fac863978CAS | 16725857PubMed |
Liu, Q., Yuan, B., Lo, K. A., Patterson, H. C., Sun, Y., and Lodish, H. F. (2012). Adiponectin regulates expression of hepatic genes critical for glucose and lipid metabolism. Proc. Natl Acad. Sci. USA 109, 14 568–14 573.
| Adiponectin regulates expression of hepatic genes critical for glucose and lipid metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVaqu7%2FE&md5=a6add44e6d0aaa1a46b1e9bf98b9d90cCAS |
Lucy, M. C. (2001). Reproductive loss in high-producing dairy cattle: where will it end? J. Dairy Sci. 84, 1277–1293.
| Reproductive loss in high-producing dairy cattle: where will it end?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktlKhu7Y%3D&md5=cf556fffd11c0b2e8d9de1dae13cadb1CAS | 11417685PubMed |
Marei, W. F., Wathes, D. C., and Fouladi-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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXns12qsLY%3D&md5=f1453b3876f400dafb2548712582ab31CAS | 20215338PubMed |
Massip, A. (2001). Cryopreservation of embryos of farm animals. Reprod. Domest. Anim. 36, 49–55.
| Cryopreservation of embryos of farm animals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3Mzhs12rtA%3D%3D&md5=d093f57bec67073fda67ec19e0d23014CAS | 11328556PubMed |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit1Gnu7k%3D&md5=4754b56fbdef4d43831f3b08e33ee359CAS | 16644149PubMed |
Plourde, D., Vigneault, C., Lemay, A., Breton, L., Gagne, D., Laflamme, I., Blondin, P., and Robert, C. (2012). Contribution of oocyte source and culture conditions to phenotypic and transcriptomic variation in commercially produced bovine blastocysts. Theriogenology 78, 116–131e3.
| Contribution of oocyte source and culture conditions to phenotypic and transcriptomic variation in commercially produced bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 22494684PubMed |
Poot, M., Zhang, Y. Z., Kramer, J. A., Wells, K. S., Jones, L. J., Hanzel, D. K., Lugade, A. G., Singer, V. L., and Haugland, R. P. (1996). Analysis of mitochondrial morphology and function with novel fixable fluorescent stains. J. Histochem. Cytochem. 44, 1363–1372.
| Analysis of mitochondrial morphology and function with novel fixable fluorescent stains.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhvVyrtw%3D%3D&md5=3e565a4b57915b378ef3001b43d55637CAS | 8985128PubMed |
Reis, A., Rooke, J. A., McCallum, G. J., Staines, M. E., Ewen, M., Lomax, M. A., and McEvoy, T. G. (2003). 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=074a230cd93f0e1eeb70f427916e92b1CAS | 14588185PubMed |
Reue, K., and Zhang, P. (2008). The lipin protein family: dual roles in lipid biosynthesis and gene expression. FEBS Lett. 582, 90–96.
| The lipin protein family: dual roles in lipid biosynthesis and gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVOltbrM&md5=b5f003f514c4360e53108cce7e96f7e9CAS | 18023282PubMed |
Rizos, D., Gutierrez-Adan, A., Perez-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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtFWj&md5=7eac6d4191c91ddad2567e3bfaf367f2CAS | 12493719PubMed |
Robert, C., Nieminen, J., Dufort, I., Gagne, D., Grant, J. R., Cagnone, G., Plourde, D., Nivet, A. L., Fournier, E., Paquet, E., Blazejczyk, M., Rigault, P., Juge, N., and Sirard, M. A. (2011). Combining resources to obtain a comprehensive survey of the bovine embryo transcriptome through deep sequencing and microarrays. Mol. Reprod. Dev. 78, 651–664.
| Combining resources to obtain a comprehensive survey of the bovine embryo transcriptome through deep sequencing and microarrays.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFGns7vK&md5=4ef8f3dc9ceca3d36f42017fe8717fb4CAS | 21812063PubMed |
Robertson, I., and Nelson, R. (1998). Certification and identification of the embryo. In ‘Manual of the International Embryo Transfer Society (IETS), 3rd edn’. (Eds D. A. Stringfellow and S. M. Seidel.) pp. 103–116. (IETS: Savoy, IL, USA)
Sata, R., Tsuji, H., Abe, H., Yamashita, S., and Hoshi, H. (1999). Fatty acid composition of bovine embryos cultured in serum-free and serum-containing medium during early embryonic development. J. Reprod. Dev. 45, 97–103.
| Fatty acid composition of bovine embryos cultured in serum-free and serum-containing medium during early embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXisFentb4%3D&md5=27a5a4a3ae762d43fedbebe15eeba240CAS |
Schmittgen, T. D., and Livak, K. J. (2008). Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101–1108.
| Analyzing real-time PCR data by the comparative C(T) method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmvVemt7c%3D&md5=2631c2b2b1241a121f40c7c7f9c099ceCAS | 18546601PubMed |
Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675.
| NIH Image to ImageJ: 25 years of image analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVKntb7P&md5=b185f20c8797a84cfbb62751d93dfd7cCAS | 22930834PubMed |
Sembongi, H., Miranda, M., Han, G. S., Fakas, S., Grimsey, N., Vendrell, J., Carman, G. M., and Siniossoglou, S. (2013). Distinct roles of the phosphatidate phosphatases lipin 1 and 2 during adipogenesis and lipid droplet biogenesis in 3T3-L1 cells. J. Biol. Chem. 288, 34 502–34 513.
| Distinct roles of the phosphatidate phosphatases lipin 1 and 2 during adipogenesis and lipid droplet biogenesis in 3T3-L1 cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVKnsLfJ&md5=f0988c9deb655af710f210c5b121d950CAS |
Shehab-El-Deen, M. A., Leroy, J. L., Maes, D., and Van Soom, A. (2009). Cryotolerance of bovine blastocysts is affected by oocyte maturation in media containing palmitic or stearic acid. Reprod. Domest. Anim. 44, 140–142.
| Cryotolerance of bovine blastocysts is affected by oocyte maturation in media containing palmitic or stearic acid.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M%2Fnslyqtg%3D%3D&md5=5e88e37028395b22a67b42cbeee94bf3CAS | 18992093PubMed |
Steel, R., and Hasler, J. F. (2004). Pregnancy rates resulting from transfer of fresh and frozen Holstein and Jersey embryos. Reprod. Fertil. Dev. 16, 182–183.
| Pregnancy rates resulting from transfer of fresh and frozen Holstein and Jersey embryos.Crossref | GoogleScholarGoogle Scholar |
Stroud, B. (2011). IETS 2011 statistics and data retrieval committee report: the year 2010 worldwide statistics of embryo transfer in domestic farm animals. Embryo Trans. Newsl. 29, 1–23.
Sturmey, R. G., O’Toole, P. J., and Leese, H. J. (2006). Fluorescence resonance energy transfer analysis of mitochondrial:lipid association in the porcine oocyte. Reproduction 132, 829–837.
| Fluorescence resonance energy transfer analysis of mitochondrial:lipid association in the porcine oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsF2isw%3D%3D&md5=41804fc5d2cbb5f9dfe8f86c072f1501CAS | 17127743PubMed |
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 | GoogleScholarGoogle Scholar | 23053436PubMed |
Tarazona, A. M., Rodriguez, J. I., Restrepo, L. F., and Olivera-Angel, M. (2006). Mitochondrial activity, distribution and segregation in bovine oocytes and in embryos produced in vitro. Reprod. Domest. Anim. 41, 5–11.
| Mitochondrial activity, distribution and segregation in bovine oocytes and in embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28%2FjsVWnuw%3D%3D&md5=038bd7348b9750f05387b04b8c268b62CAS | 16420320PubMed |
Thompson, J. G., Gardner, D. K., Pugh, P. A., McMillan, W. H., and Tervit, H. R. (1995). Lamb birth weight is affected by culture system utilized during in vitro pre-elongation development of ovine embryos. Biol. Reprod. 53, 1385–1391.
| Lamb birth weight is affected by culture system utilized during in vitro pre-elongation development of ovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpsVeisrs%3D&md5=2d2e16d97ff3c1f2b4422621091e4712CAS | 8562695PubMed |
Valdearcos, M., Esquinas, E., Meana, C., Pena, L., Gil-de-Gomez, L., Balsinde, J., and Balboa, M. A. (2012). Lipin-2 reduces proinflammatory signaling induced by saturated fatty acids in macrophages. J. Biol. Chem. 287, 10 894–10 904.
| Lipin-2 reduces proinflammatory signaling induced by saturated fatty acids in macrophages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvVWlsr8%3D&md5=01fa647e158af3ad1f99b2120eafb9bfCAS |
Van Hoeck, V., Sturmey, R. G., Bermejo-Alvarez, P., Rizos, D., Gutierrez-Adan, A., Leese, H. J., Bols, P. E., and Leroy, J. L. (2011). Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology. PLoS ONE 6, e23183.
| Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFKmsLjM&md5=b6eb69e3072d782b967fdaef51eb2625CAS | 21858021PubMed |
Van Soom, A., Mateusen, B., Leroy, J., and De Kruif, A. (2003). Assessment of mammalian embryo quality: what can we learn from embryo morphology? Reprod. Biomed. Online 7, 664–670.
| Assessment of mammalian embryo quality: what can we learn from embryo morphology?Crossref | GoogleScholarGoogle Scholar | 14748965PubMed |
Visintin, J. A., Martins, J. F., Bevilacqua, E. M., Mello, M. R., Nicacio, A. C., and Assumpcao, M. E. (2002). Cryopreservation of Bos taurus vs Bos indicus embryos: are they really different? Theriogenology 57, 345–359.
| Cryopreservation of Bos taurus vs Bos indicus embryos: are they really different?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktFyltQ%3D%3D&md5=ed1ce5bde71854c8c8c1a71e555b33b7CAS | 11775979PubMed |
Yamashita, S., Abe, H., Itoh, T., Satoh, T., and Hoshi, H. (1999). A serum-free culture system for efficient in vitro production of bovine blastocysts with improved viability after freezing and thawing. Cytotechnology 31, 123–131.
| A serum-free culture system for efficient in vitro production of bovine blastocysts with improved viability after freezing and thawing.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38bitF2jtg%3D%3D&md5=b3cc93f846333b1baeb1e3bb05a01b83CAS | 19003132PubMed |
Yamauchi, T., Kamon, J., Minokoshi, Y., Ito, Y., Waki, H., Uchida, S., Yamashita, S., Noda, M., Kita, S., Ueki, K., Eto, K., Akanuma, Y., Froguel, P., Foufelle, F., Ferre, P., Carling, D., Kimura, S., Nagai, R., Kahn, B. B., and Kadowaki, T. (2002). Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat. Med. 8, 1288–1295.
| Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotlWlsrg%3D&md5=809368b32d1da6a2ed9af50dc90929e6CAS | 12368907PubMed |
Yamauchi, T., Kamon, J., Ito, Y., Tsuchida, A., Yokomizo, T., Kita, S., Sugiyama, T., Miyagishi, M., Hara, K., Tsunoda, M., Murakami, K., Ohteki, T., Uchida, S., Takekawa, S., Waki, H., Tsuno, N. H., Shibata, Y., Terauchi, Y., Froguel, P., Tobe, K., Koyasu, S., Taira, K., Kitamura, T., Shimizu, T., Nagai, R., and Kadowaki, T. (2003). Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 423, 762–769.
| Cloning of adiponectin receptors that mediate antidiabetic metabolic effects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksV2itL8%3D&md5=b7e433dbe6684cf001314432e81b8ae8CAS | 12802337PubMed |
Zhou, M., Xu, A., Tam, P. K., Lam, K. S., Chan, L., Hoo, R. L., Liu, J., Chow, K. H., and Wang, Y. (2008). Mitochondrial dysfunction contributes to the increased vulnerabilities of adiponectin knockout mice to liver injury. Hepatology 48, 1087–1096.
| Mitochondrial dysfunction contributes to the increased vulnerabilities of adiponectin knockout mice to liver injury.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Khu77J&md5=e43af387a306abba34cac477fbc61d8fCAS | 18698578PubMed |