Genetic influence on the reduction in bovine embryo lipid content by l-carnitine
Luis Baldoceda A , Dominic Gagné A , Christina Ramires Ferreira B and Claude Robert A C
+ Author Affiliations
- Author Affiliations
A 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 ThoMSon Mass Spectrometry Laboratory, Institute of Chemistry, University of Campinas, São Paulo, Campinas 13083-970, Brazil.
C Corresponding author. Email: claude.robert@fsaa.ulaval.ca
Reproduction, Fertility and Development 28(8) 1172-1184 https://doi.org/10.1071/RD14215
Submitted: 18 June 2014 Accepted: 2 December 2014 Published: 13 January 2015
Abstract
The decreased rate of pregnancy obtained in cattle using frozen in vitro embryos compared with in vivo embryos has been associated with over-accumulation of intracellular lipid, which causes cell damage during cryopreservation. It is believed that the higher lipid content of blastomeres of bovine embryos produced in vitro results in darker-coloured cytoplasm, which could be a consequence of impaired mitochondrial function. In this study, l-carnitine was used as a treatment to reduce embryonic lipid content by increasing metabolism in cultured bovine embryos. We have observed previously that in vivo embryos of different dairy breeds collected from cows housed and fed under the same conditions differed in lipid content and metabolism. As such, breed effects between Holstein and Jersey were also examined in terms of general appearance, lipid composition, mitochondrial activity and gene expression. Adding l-carnitine to the embryo culture medium reduced the lipid content in both breeds due to increased mitochondrial activity. The response to l-carnitine was weaker in Jersey than in Holstein embryos. Our results thus show that genetics influence the response of bovine embryos to stimulation of mitochondrial metabolism.
Additional keywords: dairy breed, in vitro-produced 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., Otoi, T., Tachikawa, S., Yamashita, S., Satoh, T., and Hoshi, H. (1999). Fine structure of bovine morulae and blastocysts in vivo and in vitro. Anat. Embryol. (Berl.) 199, 519–527.
| Fine structure of bovine morulae and blastocysts in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M3nslKgtw%3D%3D&md5=d6390737197b012ab4afff230b271becCAS | 10350132PubMed |
Abe, H., Yamashita, S., Satoh, T., and Hoshi, H. (2002). 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 |
Apparicio, M., Ferreira, C. R., Tata, A., Santos, V. G., Alves, A. E., Mostachio, G. Q., Pires-Butler, E. A., Motheo, T. F., Padilha, L. C., Pilau, E. J., Gozzo, F. C., Eberlin, M. N., Lo Turco, E. G., Luvoni, G. C., and Vicente, W. R. (2012). Chemical composition of lipids present in cat and dog oocytes by matrix-assisted desorption ionisation mass spectrometry (MALDI- MS). Reprod. Domest. Anim. 47, 113–117.
| Chemical composition of lipids present in cat and dog oocytes by matrix-assisted desorption ionisation mass spectrometry (MALDI- MS).Crossref | GoogleScholarGoogle Scholar | 23279478PubMed |
Baldoceda-Baldeon, L. M., Gilbert, I., Gagne, D., Vigneault, C., Blondin, P., Ferrereia, C., and Robert, C. (2016). Breed specific factors influence embryonic lipid composition: comparison between Jersey and Holstein. Reprod. Fertil. Dev. 28, 1185–1196.
| Breed specific factors influence embryonic lipid composition: comparison between Jersey and Holstein.Crossref | GoogleScholarGoogle Scholar |
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., Twagiramungu, H., Morin, N., Brisson, C., Carboneau, G., and Durocher, J. (1999). In vitro embryo production in the cow: an effective alternative to the conventional embryo production approach. Theriogenology 51, 59–70.
| In vitro embryo production in the cow: an effective alternative to the conventional embryo production approach.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7ptFCjtA%3D%3D&md5=59cfef0fd37c314d9df72536c5707451CAS | 10729062PubMed |
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 signalling pathway to regulate lipid metabolism in bovine hepatocytes. J. Steroid Biochem. Mol. Biol. 138, 445–454.
| Adiponectin activates the AMPK signalling pathway to regulate lipid metabolism in bovine hepatocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslerurzJ&md5=f96aba9fa5e7ecb5526b81ef0b8b4b21CAS | 23994141PubMed |
Diez, C., Heyman, Y., Le Bourhis, D., Guyader-Joly, C., Degrouard, J., and Renard, J. P. (2001). Delipidating in vitro-produced bovine zygotes: effect on further development and consequences for freezability. Theriogenology 55, 923–936.
| Delipidating in vitro-produced bovine zygotes: effect on further development and consequences for freezability.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M3kslKnsQ%3D%3D&md5=ad079fb055ff6797e78482200f5fa342CAS | 11291915PubMed |
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.
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 |
Ferreira, C. R., Eberlin, L. S., Hallett, J. E., and Cooks, R. G. (2012). Single oocyte and single embryo lipid analysis by desorption electrospray ionisation mass spectrometry. J. Mass Spectrom. 47, 29–33.
| Single oocyte and single embryo lipid analysis by desorption electrospray ionisation mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1yms7Y%3D&md5=beab83a6543a046a93a20e4cb8665636CAS | 22282086PubMed |
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 |
Ghanem, N., Ha, A. N., Fakruzzaman, M., Bang, J. I., Lee, S. C., and Kong, I. K. (2014). Differential expression of selected candidate genes in bovine embryos produced in vitro and cultured with chemicals modulating lipid metabolism. Theriogenology 82, 238–250.
| Differential expression of selected candidate genes in bovine embryos produced in vitro and cultured with chemicals modulating lipid metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXnsVeltLc%3D&md5=39d6afb334db3979e4bb4a11e655cdd5CAS | 24786394PubMed |
González-Serrano, A. F., Pirro, V., Ferreira, C. R., Oliveri, P., Eberlin, L. S., Heinzmann, J., Lucas-Hahn, A., Niemann, H., and Cooks, R. G. (2013). Desorption electrospray ionisation mass spectrometry reveals lipid metabolism of individual oocytes and embryos. PLoS ONE 8, e74981.
| Desorption electrospray ionisation mass spectrometry reveals lipid metabolism of individual oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 24073231PubMed |
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 |
Hasler, J. F. (2006). The Holstein cow in embryo transfer today as compared to 20 years ago. Theriogenology 65, 4–16.
| The Holstein cow in embryo transfer today as compared to 20 years ago.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MnjtFSltw%3D%3D&md5=f4aaae7ca49159c620501c1810aff434CAS | 16289326PubMed |
Hong, S., and Pedersen, P. L. (2003). ATP synthases: insights into their motor functions from sequence and structural analyses. J. Bioenerg. Biomembr. 35, 95–120.
| ATP synthases: insights into their motor functions from sequence and structural analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjslWgsLw%3D&md5=1756f62c21b71a6f03f42493f4f5e139CAS | 12887009PubMed |
Hunt, M. C., Rautanen, A., Westin, M. A., Svensson, L. T., and Alexson, S. E. (2006). Analysis of the mouse and human acyl-CoA thioesterase (ACOT) gene clusters shows that convergent, functional evolution results in a reduced number of human peroxisomal ACOTs. FASEB J. 20, 1855–1864.
| Analysis of the mouse and human acyl-CoA thioesterase (ACOT) gene clusters shows that convergent, functional evolution results in a reduced number of human peroxisomal ACOTs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XptlKisLk%3D&md5=227abaa4bdf5ea0ebd62a355cdbaf844CAS | 16940157PubMed |
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 |
Kerner, J., and Hoppel, C. (2000). Fatty-acid import into mitochondria. Biochim. Biophys. Acta 1486, 1–17.
| Fatty-acid import into mitochondria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlt1Snt74%3D&md5=f598115b14d1467de58d8de163b2a2f1CAS | 10856709PubMed |
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 |
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 |
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 |
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 |
Murakami, M., Otoi, T., Sumantri, C., and Suzuki, T. (1998). Effects of centrifugation and lipid removal on the cryopreservation of in vitro-produced bovine embryos at the eight-cell stage. Cryobiology 36, 206–212.
| Effects of centrifugation and lipid removal on the cryopreservation of in vitro-produced bovine embryos at the eight-cell stage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjsVShu78%3D&md5=7c10165acfe31e800d13d117747ba67aCAS | 9597740PubMed |
Park, W. J., Kothapalli, K. S., Lawrence, P., Tyburczy, C., and Brenna, J. T. (2009). An alternate pathway to long-chain polyunsaturates: the FADS2 gene product Delta8-desaturates 20:2n-6 and 20:3n-3. J. Lipid Res. 50, 1195–1202.
| An alternate pathway to long-chain polyunsaturates: the FADS2 gene product Delta8-desaturates 20:2n-6 and 20:3n-3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms1ehtLw%3D&md5=0a843788dcc54a3acea8014c9610a433CAS | 19202133PubMed |
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 |
Phongnimitr, T., Liang, Y., Srirattana, K., Panyawai, K., Sripunya, N., Treetampinich, C., and Parnpai, R. (2013). Effect of l-carnitine on maturation, cryotolerance and embryo developmental competence of bovine oocytes. Anim. Sci. J. 84, 719–725.
| Effect of l-carnitine on maturation, cryotolerance and embryo developmental competence of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1Oku7%2FM&md5=1141638ab58f3e094b8ed88d38d0c9f3CAS | 23634716PubMed |
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 |
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 |
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). Analysing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101–1108.
| Analysing 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 |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Gitr3O&md5=02c720c06ddc1ccf639e5b0aa69685ebCAS | 16263160PubMed |
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 |
Somfai, T., Kaneda, M., Akagi, S., Watanabe, S., Haraguchi, S., Mizutani, E., Dang-Nguyen, T. Q., Geshi, M., Kikuchi, K., and Nagai, T. (2011). Enhancement of lipid metabolism with l-carnitine during in vitro maturation improves nuclear maturation and cleavage ability of follicular porcine oocytes. Reprod. Fertil. Dev. 23, 912–920.
| Enhancement of lipid metabolism with l-carnitine during in vitro maturation improves nuclear maturation and cleavage ability of follicular porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVOrtb7M&md5=dcdd4eb03ad167184b957b24fa3acb27CAS | 21871210PubMed |
Smyth, G. K. (2004). Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article3.
| Linear models and empirical bayes methods for assessing differential expression in microarray experiments.Crossref | GoogleScholarGoogle Scholar | 16646809PubMed |
Steel, R., and Hasler, J. F. (2004). 120 Pregnancy rates resulting from transfer of fresh and frozen Holstein and Jersey embryos. Reprod. Fertil. Dev. 16, 182–183.
| 120 Pregnancy rates resulting from transfer of fresh and frozen Holstein and Jersey embryos.Crossref | GoogleScholarGoogle Scholar |
Stoffel, W., Holz, B., Jenke, B., Binczek, E., Gunter, R. H., Kiss, C., Karakesisoglou, I., Thevis, M., Weber, A. A., Arnhold, S., and Addicks, K. (2008). Delta6-desaturase (FADS2) deficiency unveils the role of omega3- and omega6-polyunsaturated fatty acids. EMBO J. 27, 2281–2292.
| Delta6-desaturase (FADS2) deficiency unveils the role of omega3- and omega6-polyunsaturated fatty acids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVGkt7jK&md5=9540b1bd91ebe7727a6be6839aee5db8CAS | 19172737PubMed |
Stroud, C. K., Nara, T. Y., Roqueta-Rivera, M., Radlowski, E. C., Lawrence, P., Zhang, Y., Cho, B. H., Segre, M., Hess, R. A., Brenna, J. T., Haschek, W. M., and Nakamura, M. T. (2009). Disruption of FADS2 gene in mice impairs male reproduction and causes dermal and intestinal ulceration. J. Lipid Res. 50, 1870–1880.
| Disruption of FADS2 gene in mice impairs male reproduction and causes dermal and intestinal ulceration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVCgsrfI&md5=302249b44ab45d44ac961caeaac14ab3CAS | 19351970PubMed |
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 |
Takahashi, T., Inaba, Y., Somfai, T., Kaneda, M., Geshi, M., Nagai, T., and Manabe, N. (2013). Supplementation of culture medium with l-carnitine improves development and cryotolerance of bovine embryos produced in vitro. Reprod. Fertil. Dev. 25, 589–599.
| Supplementation of culture medium with l-carnitine improves development and cryotolerance of bovine embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmt1CgsL0%3D&md5=c029de04617862a09d70dd30bec741ccCAS | 22954232PubMed |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVOjtbvL&md5=78cd553736cbda3d22b518969e204796CAS | 23832940PubMed |
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 utilised during in vitro pre-elongation development of ovine embryos. Biol. Reprod. 53, 1385–1391.
| Lamb birth weight is affected by culture system utilised during in vitro pre-elongation development of ovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpsVeisrs%3D&md5=2d2e16d97ff3c1f2b4422621091e4712CAS | 8562695PubMed |
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 |
Xia, J., Psychogios, N., Young, N., and Wishart, D. S. (2009). MetaboAnalyst: a web server for metabolomic data analysis and interpretation. Nucleic Acids Res. 37, W652–W660.
| MetaboAnalyst: a web server for metabolomic data analysis and interpretation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosFSkt7c%3D&md5=90511f889023612544faddbd2e8e5694CAS | 19429898PubMed |
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., 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 anti-diabetic metabolic effects. Nature 423, 762–769.
| Cloning of adiponectin receptors that mediate anti-diabetic metabolic effects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksV2itL8%3D&md5=b7e433dbe6684cf001314432e81b8ae8CAS | 12802337PubMed |
Yao, D., Mizuguchi, H., Yamaguchi, M., Yamada, H., Chida, J., Shikata, K., and Kido, H. (2008). Thermal instability of compound variants of carnitine palmitoyltransferase II and impaired mitochondrial fuel utilisation in influenza-associated encephalopathy. Hum. Mutat. 29, 718–727.
| Thermal instability of compound variants of carnitine palmitoyltransferase II and impaired mitochondrial fuel utilisation in influenza-associated encephalopathy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsVOnsLc%3D&md5=b2d0990dba0c37b7e2b071622dd6a9d3CAS | 18306170PubMed |
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 |
