Differential effects of linoleic and alpha-linolenic fatty acids on spatial and temporal mitochondrial distribution and activity in bovine oocytes
Waleed F. Marei A B , D. Claire Wathes A and Ali A. Fouladi-Nashta A C
+ Author Affiliations
- Author Affiliations
A Reproduction, Genes and Development Group, Department of Veterinary Basic Sciences, The Royal Veterinary College, Hawkshead Lane, Hatfield, Herts AL9 7TA, UK.
B Department of Theriogenology, Faculty of Veterinary Medicine, Cairo University, Giza 12111, Egypt.
C Corresponding author. Email: afouladi@rvc.ac.uk
Reproduction, Fertility and Development 24(5) 679-690 https://doi.org/10.1071/RD11204
Submitted: 12 August 2011 Accepted: 17 October 2011 Published: 30 November 2011
Abstract
Using specific stains and confocal microscope imaging, the patterns of mitochondrial distribution, mitochondrial inner membrane potential and reactive oxygen species (ROS) levels during bovine oocyte maturation were determined in the presence or absence of physiological concentrations of linoleic acid (LA; 100 µM) or α-linolenic acid (ALA; 50 µM). Mitochondrial distribution in control oocytes at 0 h was mainly peripheral and changed to a diffused pattern after 1 h of culture; this was maintained up to 24 h. Mitochondrial clusters were observed during the early hours of maturation (1–4 h); the majority of these were arranged in perinuclear fashion. LA supplementation resulted in: (1) delayed redistribution of the mitochondria from a peripheral to a diffuse pattern and a decreased percentages of oocytes showing perinuclear mitochondrial clusters, (2) decreased mitochondrial inner membrane potential at 1 and 24 h compared with the control and (3) higher ROS levels, associated with a lower nuclear maturation rate. In contrast, ALA supplementation had no effect on mitochondrial distribution and activity and decreased ROS levels compared with the control; this was associated with an increased nuclear maturation rate. In conclusion, LA induced alterations in mitochondrial distribution and activity as well as increasing ROS levels, which mediate, at least in part, the inhibitory effect on oocyte maturation.
Additional keywords: JC-1, mitochondria, MitoTracker, oocyte maturation.
References
Adamiak, S. J., Ewen, M., Rooke, J. A., Webb, R., and Sinclair, K. D. (2005). Diet and fatty-acid composition of bovine plasma, granulosa cells and cumulus–oocyte complexes. Reprod. Fertil. Dev. 17, 200–201.| Diet and fatty-acid composition of bovine plasma, granulosa cells and cumulus–oocyte complexes.Crossref | GoogleScholarGoogle Scholar |
Adona, P. R., Pires, P. R., Quetglas, M. D., Schwarz, K. R., and Leal, C. L. (2008). Prematuration of bovine oocytes with butyrolactone I: effects on meiosis progression, cytoskeleton, organelle distribution and embryo development. Anim. Reprod. Sci. 108, 49–65.
| Prematuration of bovine oocytes with butyrolactone I: effects on meiosis progression, cytoskeleton, organelle distribution and embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVejtLfO&md5=f226cbecd658717d34fa817f796c385aCAS | 17692479PubMed |
Agnello, M., Morici, G., and Rinaldi, A. M. (2008). A method for measuring mitochondrial mass and activity. Cytotechnology 56, 145–149.
| A method for measuring mitochondrial mass and activity.Crossref | GoogleScholarGoogle Scholar | 19002852PubMed |
Ali, A. A., Bilodeau, J. F., and Sirard, M. A. (2003). Antioxidant requirements for bovine oocytes varies during in vitro maturation, fertilization and development. Theriogenology 59, 939–949.
| Antioxidant requirements for bovine oocytes varies during in vitro maturation, fertilization and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXotVSh&md5=92134643a54f1fcc6f7bd41a04ce9329CAS | 12517395PubMed |
An, W. S., Kim, H. J., Cho, K. H., and Vaziri, N. D. (2009). Omega-3 fatty-acid supplementation attenuates oxidative stress, inflammation and tubulointerstitial fibrosis in the remnant kidney. Am. J. Physiol. Renal Physiol. 297, F895–F903.
| Omega-3 fatty-acid supplementation attenuates oxidative stress, inflammation and tubulointerstitial fibrosis in the remnant kidney.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlent7nF&md5=4663bb80a9bfe125686eb064241531faCAS | 19656915PubMed |
Barbosa, D. S., Cecchini, R., El Kadri, M. Z., Rodriguez, M. A., Burini, R. C., and Dichi, I. (2003). Decreased oxidative stress in patients with ulcerative colitis supplemented with fish oil omega-3 fatty acids. Nutrition 19, 837–842.
| Decreased oxidative stress in patients with ulcerative colitis supplemented with fish oil omega-3 fatty acids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXotVyrs7o%3D&md5=1a91b6806dc37cabbea16e4f1c5ae7d9CAS | 14559317PubMed |
Barzanti, V., Battino, M., Baracca, A., Cavazzoni, M., Cocchi, M., Noble, R., Maranesi, M., Turchetto, E., and Lenaz, G. (1994). The effect of dietary lipid changes on the fatty-acid composition and function of liver, heart and brain mitochondria in the rat at different ages. Br. J. Nutr. 71, 193–202.
| The effect of dietary lipid changes on the fatty-acid composition and function of liver, heart and brain mitochondria in the rat at different ages.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c7ptVymsA%3D%3D&md5=e037ca76ba05eb07d203f7c64538600aCAS | 8142331PubMed |
Bavister, B. D., and Squirrell, J. M. (2000). Mitochondrial distribution and function in oocytes and early embryos. Hum. Reprod. 15, 189–198.
| 11041524PubMed |
Blondin, P., Coenen, K., and Sirard, M. A. (1997). The impact of reactive oxygen species on bovine sperm fertilizing ability and oocyte maturation. J. Androl. 18, 454–460.
| 1:CAS:528:DyaK2sXmtVGisL8%3D&md5=6e9426da2053fe61836ee2d3fbff533fCAS | 9283960PubMed |
Cetica, P. D., Pintos, L. N., Dalvit, G. C., and Beconi, M. T. (2001). Antioxidant enzyme activity and oxidative stress in bovine oocyte in vitro maturation. IUBMB Life 51, 57–64.
| Antioxidant enzyme activity and oxidative stress in bovine oocyte in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktlSmsL8%3D&md5=a5d630805b1136974a4fb72b79fb6753CAS | 11419698PubMed |
Chegary, M., Brinke, H., Ruiter, J. P., Wijburg, F. A., Stoll, M. S., Minkler, P. E., van Weeghel, M., Schulz, H., Hoppel, C. L., Wanders, R. J., and Houten, S. M. (2009). Mitochondrial long-chain fatty-acid beta-oxidation in man and mouse. Biochim. Biophys. Acta 1791, 806–815.
| 1:CAS:528:DC%2BD1MXoslejt7s%3D&md5=627ffd2293d2ea55e413fff5bb232218CAS | 19465148PubMed |
Childs, S., Hennessy, A. A., Sreenan, J. M., Wathes, D. C., Cheng, Z., Stanton, C., Diskin, M. G., and Kenny, D. A. (2008). Effect of level of dietary n-3 polyunsaturated fatty-acid supplementation on systemic and tissue fatty-acid concentrations and on selected reproductive variables in cattle. Theriogenology 70, 595–611.
| Effect of level of dietary n-3 polyunsaturated fatty-acid supplementation on systemic and tissue fatty-acid concentrations and on selected reproductive variables in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpsVCrtbs%3D&md5=a2c4cbfa38819327f6a60c18f903b740CAS | 18514298PubMed |
Combelles, C. M., Gupta, S., and Agarwal, A. (2009). Could oxidative stress influence the in vitro maturation of oocytes? Reprod. Biomed. Online 18, 864–880.
| Could oxidative stress influence the in vitro maturation of oocytes?Crossref | GoogleScholarGoogle Scholar | 19490793PubMed |
Corrêa, G. A., Rumpf, R., Mundim, T. C., Franco, M. M., and Dode, M. A. (2008). Oxygen tension during in vitro culture of bovine embryos: effect in production and expression of genes related to oxidative stress. Anim. Reprod. Sci. 104, 132–142.
| Oxygen tension during in vitro culture of bovine embryos: effect in production and expression of genes related to oxidative stress.Crossref | GoogleScholarGoogle Scholar | 17350772PubMed |
Cummins, J. (1998). Mitochondrial DNA in mammalian reproduction. Rev. Reprod. 3, 172–182.
| Mitochondrial DNA in mammalian reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntlaltbk%3D&md5=410c3cb2b397d2b1e24773a68be230e0CAS | 9829552PubMed |
Dalvit, G. C., Cetica, P. D., Pintos, L. N., and Beconi, M. T. (2005). Reactive oxygen species in bovine embryo in vitro production. Biocell 29, 209–212.
| 1:CAS:528:DC%2BD2MXhtFSns73M&md5=1c845978ba504c56c16d5a569be0c893CAS | 16187501PubMed |
Dennery, P. A. (2007). Effects of oxidative stress on embryonic development. Birth Defects Res. C Embryo Today 81, 155–162.
| Effects of oxidative stress on embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlWiur3O&md5=9de7c2da4b04d44ecd13a0e83b580513CAS | 17963268PubMed |
Di Lisa, F., Blank, P. S., Colonna, R., Gambassi, G., Silverman, H. S., Stern, M. D., and Hansford, R. G. (1995). Mitochondrial membrane potential in single living adult rat cardiac myocytes exposed to anoxia or metabolic inhibition. J. Physiol. 486, 1–13.
| 1:CAS:528:DyaK2MXmvFOqtrg%3D&md5=24d0327f07edc5001194eb66f70dd99eCAS | 7562625PubMed |
Downs, S. M., Mosey, J. L., and Klinger, J. (2009). Fatty-acid oxidation and meiotic resumption in mouse oocytes. Mol. Reprod. Dev. 76, 844–853.
| Fatty-acid oxidation and meiotic resumption in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptleht7c%3D&md5=eade76da3a7fc8b2413f655a754df476CAS | 19455666PubMed |
Dumollard, R., Marangos, P., Fitzharris, G., Swann, K., Duchen, M., and Carroll, J. (2004). Sperm-triggered [Ca2+] oscillations and Ca2+ homeostasis in the mouse egg have an absolute requirement for mitochondrial ATP production. Development 131, 3057–3067.
| Sperm-triggered [Ca2+] oscillations and Ca2+ homeostasis in the mouse egg have an absolute requirement for mitochondrial ATP production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtFKlsb0%3D&md5=88653cd7321601c77a26be6c9218b5deCAS | 15163630PubMed |
Dunning, K. R., Cashman, K., Russell, D. L., Thompson, J. G., Norman, R. J., and Robker, R. L. (2010). Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development. Biol. Reprod. 83, 909–918.
| Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFahurfN&md5=1ccb40aa6e9f3c498d9df62ea3805fefCAS | 20686180PubMed |
Eppig, J. J. (1991). Intercommunication between mammalian oocytes and companion somatic cells. Bioessays 13, 569–574.
| Intercommunication between mammalian oocytes and companion somatic cells.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK387is1ShsA%3D%3D&md5=f4e8818ddf8ca51796a545b119b3f763CAS | 1772412PubMed |
Ferreira, E. M., Vireque, A. A., Adona, P. R., Meirelles, F. V., Ferriani, R. A., and Navarro, P. A. (2009). Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence. Theriogenology 71, 836–848.
| Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitVSgs7k%3D&md5=179b674d5a6944e2a68733179da2cf47CAS | 19121865PubMed |
Fouladi-Nashta, A. A., and Campbell, K. H. (2006). Dissociation of oocyte nuclear and cytoplasmic maturation by the addition of insulin in cultured bovine antral follicles. Reproduction 131, 449–460.
| Dissociation of oocyte nuclear and cytoplasmic maturation by the addition of insulin in cultured bovine antral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjs12js7k%3D&md5=1a81580bafcbccb84c6f7afee6fbd98fCAS | 16514188PubMed |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntV2gsb0%3D&md5=ce6fd01f70a6a7a803e2db1a02a11595CAS | 17344470PubMed |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsValt7rI&md5=32ffd347e8bde9db9fe03c4a11fc0d66CAS | 19633135PubMed |
Fulka, J., , First, N. L., and Moor, R. M. (1998). Nuclear and cytoplasmic determinants involved in the regulation of mammalian oocyte maturation. Mol. Hum. Reprod. 4, 41–49.
| Nuclear and cytoplasmic determinants involved in the regulation of mammalian oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhvV2qtL8%3D&md5=43ce9cd65bcfb7da1a4816b0a59608acCAS |
Gilchrist, R. B., Lane, M., and Thompson, J. G. (2008). Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum. Reprod. Update 14, 159–177.
| Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisVKmurY%3D&md5=ec4994d45ddf61de382a6d71e49eeaa6CAS | 18175787PubMed |
Goto, Y., Noda, Y., Mori, T., and Nakano, M. (1993). Increased generation of reactive oxygen species in embryos cultured in vitro. Free Radic. Biol. Med. 15, 69–75.
| Increased generation of reactive oxygen species in embryos cultured in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlvFOnsL8%3D&md5=6f03a7b07d47aab23ec20122705866bdCAS | 8359711PubMed |
Hammiche, F., Vujkovic, M., Wijburg, W., de Vries, J. H., Macklon, N. S., Laven, J. S., and Steegers-Theunissen, R. P. (2011). Increased preconception omega-3 polyunsaturated fatty-acid intake improves embryo morphology. Fertil. Steril. 95, 1820–1823.
| Increased preconception omega-3 polyunsaturated fatty-acid intake improves embryo morphology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjs1SrurY%3D&md5=4fff3aa8300b8aecc02195bcb7f387b4CAS | 21130435PubMed |
Hashimoto, S., Minami, N., Takakura, R., Yamada, M., Imai, H., and Kashima, N. (2000). Low oxygen tension during in vitro maturation is beneficial for supporting the subsequent development of bovine cumulus–oocyte complexes. Mol. Reprod. Dev. 57, 353–360.
| Low oxygen tension during in vitro maturation is beneficial for supporting the subsequent development of bovine cumulus–oocyte complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotFaiurc%3D&md5=4c6b80387987e737bcf832832b010dbfCAS | 11066064PubMed |
Hyttel, P., Greve, T., and Callesen, H. (1989). Ultrastructural aspects of oocyte maturation and fertilization in cattle. J. Reprod. Fertil. Suppl. 38, 35–47.
| 1:STN:280:DyaK3c%2Fht1ShtA%3D%3D&md5=5ba74f6aa3cae26631ff47f00449b11eCAS | 2677348PubMed |
Kitagawa, Y., Suzuki, K., Yoneda, A., and Watanabe, T. (2004). Effects of oxygen concentration and antioxidants on the in vitro developmental ability, production of reactive oxygen species (ROS) and DNA fragmentation in porcine embryos. Theriogenology 62, 1186–1197.
| Effects of oxygen concentration and antioxidants on the in vitro developmental ability, production of reactive oxygen species (ROS) and DNA fragmentation in porcine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvFCqs7o%3D&md5=e66c8962d91e8d3dd4b9ba5f08b4489bCAS | 15325546PubMed |
Krisher, R. L. (2004). The effect of oocyte quality on development. J Anim. Sci. 82, E14–E23.
| 15471793PubMed |
Krisher, R. L., Brad, A. M., Herrick, J. R., Sparman, M. L., and Swain, J. E. (2007). A comparative analysis of metabolism and viability in porcine oocytes during in vitro maturation. Anim. Reprod. Sci. 98, 72–96.
| A comparative analysis of metabolism and viability in porcine oocytes during in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhs1Sksrw%3D&md5=c68a63c9df9130302b75ca30504e4298CAS | 17110061PubMed |
Mahadik, S. P., Pillai, A., Joshi, S., and Foster, A. (2006). Prevention of oxidative stress-mediated neuropathology and improved clinical outcome by adjunctive use of a combination of antioxidants and omega-3 fatty acids in schizophrenia. Int. Rev. Psychiatry 18, 119–131.
| Prevention of oxidative stress-mediated neuropathology and improved clinical outcome by adjunctive use of a combination of antioxidants and omega-3 fatty acids in schizophrenia.Crossref | GoogleScholarGoogle Scholar | 16777666PubMed |
Marei, W. F., Wathes, D. C., and Fouladi-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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsV2lt7vL&md5=2c022adf7f43186326e1ff335ba24f5cCAS | 19587335PubMed |
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=5979f1e8784809f62beb3c3a9a37de36CAS | 20215338PubMed |
Morado, S. A., Cetica, P. D., Beconi, M. T., and Dalvit, G. C. (2009). Reactive oxygen species in bovine oocyte maturation in vitro. Reprod. Fertil. Dev. 21, 608–614.
| Reactive oxygen species in bovine oocyte maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksF2rtbk%3D&md5=26dbd0f1cedcc52db530faa1f4e9aacaCAS | 19383267PubMed |
Nagai, S., Mabuchi, T., Hirata, S., Shoda, T., Kasai, T., Yokota, S., Shitara, H., Yonekawa, H., and Hoshi, K. (2006). Correlation of abnormal mitochondrial distribution in mouse oocytes with reduced developmental competence. Tohoku J. Exp. Med. 210, 137–144.
| Correlation of abnormal mitochondrial distribution in mouse oocytes with reduced developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtF2rtbjN&md5=674f5ef64475d9d131ede3f9dfef281fCAS | 17023767PubMed |
Nasr-Esfahani, M. H., Aitken, J. R., and Johnson, M. H. (1990). Hydrogen peroxide levels in mouse oocytes and early cleavage-stage embryos developed in vitro or in vivo. Development 109, 501–507.
| 1:CAS:528:DyaK3cXlsV2nsbo%3D&md5=cf2046f101d7a6368f46b999f1cee07aCAS | 2401209PubMed |
Nishi, Y., Takeshita, T., Sato, K., and Araki, T. (2003). Change of the mitochondrial distribution in mouse ooplasm during in vitro maturation. J. Nippon Med. Sch. 70, 408–415.
| Change of the mitochondrial distribution in mouse ooplasm during in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 14578941PubMed |
Pandey, A. N., Tripathi, A., Premkumar, K. V., Shrivastava, T. G., and Chaube, S. K. (2010). Reactive oxygen and nitrogen species during meiotic resumption from diplotene-arrest in mammalian oocytes. J. Cell. Biochem. 111, 521–528.
| Reactive oxygen and nitrogen species during meiotic resumption from diplotene-arrest in mammalian oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtleqs7zI&md5=6104c6ff9dacd57ea76a1e46d65a37d4CAS | 20568115PubMed |
Pangas, S. A., and Matzuk, M. M. (2005). The art and artifact of GDF9 activity: cumulus expansion and the cumulus expansion-enabling factor. Biol. Reprod. 73, 582–585.
| The art and artifact of GDF9 activity: cumulus expansion and the cumulus expansion-enabling factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVCgtrrP&md5=91fcaf4353e19f3c74acf3416e78aec9CAS | 15917343PubMed |
Reers, M., Smiley, S. T., Mottola-Hartshorn, C., Chen, A., Lin, M., and Chen, L. B. (1995). Mitochondrial membrane potential monitored by JC-1 dye. Methods Enzymol. 260, 406–417.
| Mitochondrial membrane potential monitored by JC-1 dye.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjslWlsg%3D%3D&md5=30e7cc34c3c96145b96a472ee44fcacfCAS | 8592463PubMed |
Romieu, I., Garcia-Esteban, R., Sunyer, J., Rios, C., Alcaraz-Zubeldia, M., Velasco, S. R., and Holguin, F. (2008). The effect of supplementation with omega-3 polyunsaturated fatty acids on markers of oxidative stress in elderly exposed to PM(2.5). Environ. Health Perspect. 116, 1237–1242.
| The effect of supplementation with omega-3 polyunsaturated fatty acids on markers of oxidative stress in elderly exposed to PM(2.5).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFOis7fK&md5=4f6c41abf5ecb20b1f46d3e91661ed19CAS | 18795169PubMed |
Santillan, R. M. (2007). Effect of l-arginine, vitamins C and E and omega-3 acids (DHA, EPA) on oxidative stress and endothelial dysfunction in the mouse model of renal insufficiency. An. R. Acad. Nac. Med. (Madr.) 124, 623–634.
Simopoulos, A. P. (2002). The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed. Pharmacother. 56, 365–379.
| The importance of the ratio of omega-6/omega-3 essential fatty acids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotVKrtbY%3D&md5=b1c2f64d901cf9825f9082113f08c031CAS | 12442909PubMed |
Skouroliakou, M., Konstantinou, D., Koutri, K., Kakavelaki, C., Stathopoulou, M., Antoniadi, M., Xemelidis, N., Kona, V., and Markantonis, S. (2010). A double-blind, randomized clinical trial of the effect of omega-3 fatty acids on the oxidative stress of preterm neonates fed through parenteral nutrition. Eur. J. Clin. Nutr. 64, 940–947.
| A double-blind, randomized clinical trial of the effect of omega-3 fatty acids on the oxidative stress of preterm neonates fed through parenteral nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtV2hurrN&md5=c9a919161798b49467de38cabcec12fbCAS | 20551967PubMed |
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=4cc1bdccde5ffc0a3ef519279f9da889CAS | 21871210PubMed |
Stojkovic, M., Machado, S. A., Stojkovic, P., Zakhartchenko, V., Hutzler, P., Goncalves, P. B., and Wolf, E. (2001). Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol. Reprod. 64, 904–909.
| Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsVKjtrk%3D&md5=1c33fa33a77fabe3ffd8504ad8c8ffc9CAS | 11207207PubMed |
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=d1c05a3e409101ec9bfefd8c2e665958CAS | 16420320PubMed |
Thouas, G. A., Trounson, A. O., Wolvetang, E. J., and Jones, G. M. (2004). Mitochondrial dysfunction in mouse oocytes results in preimplantation embryo arrest in vitro. Biol. Reprod. 71, 1936–1942.
| Mitochondrial dysfunction in mouse oocytes results in preimplantation embryo arrest in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWgsr3O&md5=b477d4a0df34fef026cd34f6896432e7CAS | 15286028PubMed |
Toborek, M., Blanc, E., Kaiser, S., Mattson, M., and Hennig, B. (1997). Linoleic acid potentiates TNF-mediated oxidative stress, disruption of calcium homeostasis and apoptosis of cultured vascular endothelial cells. J. Lipid Res. 38, 2155–2167.
| 1:CAS:528:DyaK2sXntFCnu78%3D&md5=5bea134ebaa50185e52326d8d7757af1CAS | 9374137PubMed |
Van Blerkom, J. (1991). Microtubule mediation of cytoplasmic and nuclear maturation during the early stages of resumed meiosis in cultured mouse oocytes. Proc. Natl. Acad. Sci. USA 88, 5031–5035.
| Microtubule mediation of cytoplasmic and nuclear maturation during the early stages of resumed meiosis in cultured mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M3ntFehtw%3D%3D&md5=e2ff118ebdedb731a561d8358aec90c0CAS | 2052585PubMed |
Van Blerkom, J. (2009). Mitochondria in early mammalian development. Semin. Cell Dev. Biol. 20, 354–364.
| Mitochondria in early mammalian development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltVCmsLs%3D&md5=20a349d277c15879b6634248632f6e70CAS | 19136067PubMed |
Van Blerkom, J., and Davis, P. (2007). Mitochondrial signalling and fertilization. Mol. Hum. Reprod. 13, 759–770.
| Mitochondrial signalling and fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlaqtr3O&md5=3390f8054515df030ad3a0b10f0a01a0CAS | 17893093PubMed |
Van Blerkom, J., Davis, P., Mathwig, V., and Alexander, S. (2002). Domains of high-polarized and low-polarized mitochondria may occur in mouse and human oocytes and early embryos. Hum. Reprod. 17, 393–406.
| Domains of high-polarized and low-polarized mitochondria may occur in mouse and human oocytes and early embryos.Crossref | GoogleScholarGoogle Scholar | 11821285PubMed |
Van Blerkom, J., Davis, P., and Alexander, S. (2003). Inner mitochondrial membrane potential (DeltaPsim), cytoplasmic ATP content and free Ca2+ levels in metaphase II mouse oocytes. Hum. Reprod. 18, 2429–2440.
| Inner mitochondrial membrane potential (DeltaPsim), cytoplasmic ATP content and free Ca2+ levels in metaphase II mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXovVektL8%3D&md5=db4c19db03042e0459e8133b8c086155CAS | 14585897PubMed |
Vandaele, L., Thys, M., Bijttebier, J., Van Langendonckt, A., Donnay, I., Maes, D., Meyer, E., and Van Soom, A. (2010). Short-term exposure to hydrogen peroxide during oocyte maturation improves bovine embryo development. Reproduction 139, 505–511.
| Short-term exposure to hydrogen peroxide during oocyte maturation improves bovine embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtV2lsb8%3D&md5=97eb0414b47c697e32dee6ecf0194742CAS | 19939885PubMed |
Wakefield, S. L., Lane, M., Schulz, S. J., Hebart, M. L., Thompson, J. G., and Mitchell, M. (2008). Maternal supply of omega-3 polyunsaturated fatty acids alters mechanisms involved in oocyte and early embryo development in the mouse. Am. J. Physiol. Endocrinol. Metab. 294, E425–E434.
| Maternal supply of omega-3 polyunsaturated fatty acids alters mechanisms involved in oocyte and early embryo development in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXit1ykur0%3D&md5=48cabbc11e7e3dee2ef630564122018fCAS | 18073322PubMed |
Wang, L. Y., Wang, D. H., Zou, X. Y., and Xu, C. M. (2009). Mitochondrial functions on oocytes and preimplantation embryos. J. Zhejiang Univ. Sci. B 10, 483–492.
| Mitochondrial functions on oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotV2qtbo%3D&md5=bd3f6b7e90909fe3e36b7bb522553013CAS | 19585665PubMed |
Wathes, D. C., Abayasekara, D. R., and Aitken, R. J. (2007). Polyunsaturated fatty acids in male and female reproduction. Biol. Reprod. 77, 190–201.
| Polyunsaturated fatty acids in male and female reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot1OnsL0%3D&md5=f9f27869c67f75e6ac523b7c248cc21dCAS | 17442851PubMed |
Watson, A. J. (2007). Oocyte cytoplasmic maturation: a key mediator of oocyte and embryo developmental competence. J. Anim. Sci. 85, E1–E3.
| Oocyte cytoplasmic maturation: a key mediator of oocyte and embryo developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2s7ntFensw%3D%3D&md5=d041ebb3f0e95d8fa108e3365ab38293CAS | 17322120PubMed |
Wilding, M., Dale, B., Marino, M., di Matteo, L., Alviggi, C., Pisaturo, M. L., Lombardi, L., and De Placido, G. (2001). Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum. Reprod. 16, 909–917.
| Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvitlCktw%3D%3D&md5=b85d4154f0af9cc86b9b720a1bc5f55dCAS | 11331637PubMed |
Wonnacott, K. E., Kwong, W. Y., Hughes, J., Salter, A. M., Lea, R. G., Garnsworthy, P. C., and Sinclair, K. D. (2010). Dietary omega-3 and -6 polyunsaturated fatty acids affect the composition and development of sheep granulosa cells, oocytes and embryos. Reproduction 139, 57–69.
| Dietary omega-3 and -6 polyunsaturated fatty acids affect the composition and development of sheep granulosa cells, oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXovVWnug%3D%3D&md5=3d2a14200b87ff901dbaa848b8ed96d8CAS | 19789173PubMed |
Wu, A., Ying, Z., and Gomez-Pinilla, F. (2004). Dietary omega-3 fatty acids normalize BDNF levels, reduce oxidative damage and counteract learning disability after traumatic brain injury in rats. J. Neurotrauma 21, 1457–1467.
| Dietary omega-3 fatty acids normalize BDNF levels, reduce oxidative damage and counteract learning disability after traumatic brain injury in rats.Crossref | GoogleScholarGoogle Scholar | 15672635PubMed |
Zhang, H. M., Dang, H., Yeh, C. K., and Zhang, B. X. (2009). Linoleic acid-induced mitochondrial Ca(2+) efflux causes peroxynitrite generation and protein nitrotyrosylation. PLoS ONE 4, e6048.
| Linoleic acid-induced mitochondrial Ca(2+) efflux causes peroxynitrite generation and protein nitrotyrosylation.Crossref | GoogleScholarGoogle Scholar | 19557129PubMed |
Zhang, X., Wu, X. Q., Lu, S., Guo, Y. L., and Ma, X. (2006). Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles. Cell Res. 16, 841–850.
| Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVOmu7fF&md5=67f520f02e547e63c71931641184ace4CAS | 16983401PubMed |
