Differential effects of linoleic and alpha-linolenic fatty acids on spatial and temporal mitochondrial distribution and activity in bovine oocytes

Reproduction, Fertility and Development

Volumn 24, Issue 5, 2012, Pages 679-690

  Marei, Waleed F ^a,b   Wathes, D Claire ^a   Fouladi Nashta, Ali A ^a  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

^b Cairo University   (Egypt)

Author keywords

JC 1; mitochondria; MitoTracker; oocyte maturation

Indexed keywords

LINOLEIC ACID; FATTY ACID; HYDROGEN PEROXIDE; LINOLENIC ACID;

ANIMAL CELL; ARTICLE; COW; FEMALE; MITOCHONDRION; NONHUMAN; OOCYTE; ANIMAL; ANIMAL DISEASE; CATTLE; CELL CULTURE; DRUG EFFECT; DRUG SCREENING; IN VITRO OOCYTE MATURATION; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; OOCYTE DEVELOPMENT; PHYSIOLOGY; TISSUE DISTRIBUTION; ULTRASTRUCTURE;

BOVINAE;

ALPHA-LINOLENIC ACID; ANIMALS; CATTLE; CELLS, CULTURED; DRUG EVALUATION, PRECLINICAL; FATTY ACIDS; FEMALE; HYDROGEN PEROXIDE; IN VITRO OOCYTE MATURATION TECHNIQUES; LINOLEIC ACID; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; OOCYTES; OOGENESIS; TISSUE DISTRIBUTION;

EID: 84868282132     PISSN: 10313613     EISSN: 14485990     Source Type: Journal    
DOI: 10.1071/RD11204     Document Type: Article

References (69)

1. 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. doi:10.1071/ RDV17N2AB100
2. 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(1-2), 49-65. doi:10.1016/J.ANIREPROSCI.2007. 07.002
3. Agnello, M., Morici, G., and Rinaldi, A. M. (2008). A method for measuring mitochondrial mass and activity. Cytotechnology 56(3), 145-149. doi:10.1007/S10616-008-9143-2
4. 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(3-4), 939-949. doi:10.1016/S0093-691X(02) 01125-1 (Pubitemid 36117371)
5. An, W.S., Kim, H.J., Cho, K.H., and Vaziri, N.D.(2009). Omega-3 fatty-acid supplementation attenuates oxidative stress, inflammation and tubuloin-terstitial fibrosis in the remnant kidney. Am. J. Physiol. Renal Physiol. 297(4), F895-F903. doi:10.1152/AJPRENAL.00217.2009
6. 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(10), 837-842. doi:10.1016/S0899-9007(03)00162-X (Pubitemid 37244139)
7. 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(2), 193-202. doi:10.1079/BJN19940126 (Pubitemid 24062826)
8. Bavister, B. D., and Squirrell, J. M. (2000). Mitochondrial distribution and function in oocytes and early embryos. Hum. Reprod. 15(Suppl 2), 189-198.
9. 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(4), 454-460. (Pubitemid 27468929)
10. 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(1), 57-64. doi:10.1080/15216540152035073 (Pubitemid 32521204)
11. 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 betaoxidation in man and mouse. Biochim. Biophys. Acta 1791(8), 806-815.
12. 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(4), 595-611. doi:10.1016/J.THERIOGENOLOGY.2008.04.002
13. Combelles, C. M., Gupta, S., and Agarwal, A. (2009). Could oxidative stress influence the in vitro maturation of oocytes? Reprod. Biomed. Online 18(6), 864-880. doi:10.1016/S1472-6483(10)60038-7
14. 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(2-4), 132-142. doi:10.1016/J.ANIREPROSCI.2007. 02.002 (Pubitemid 351163485)
15. Cummins, J. (1998). Mitochondrial DNA in mammalian reproduction. Rev. Reprod. 3(3), 172-182. doi:10.1530/ROR.0.0030172 (Pubitemid 28508648)
16. 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(2), 209-212. (Pubitemid 41297450)
17. Dennery, P. A. (2007). Effects of oxidative stress on embryonic development. Birth Defects Res. C Embryo Today 81(3), 155-162. doi:10.1002/BDRC.20098 (Pubitemid 350086244)
18. 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(Pt 1), 1-13.
19. Downs, S. M., Mosey, J. L., and Klinger, J. (2009). Fatty-acid oxidation and meiotic resumption in mouse oocytes. Mol. Reprod. Dev. 76(9), 844-853. doi:10.1002/MRD.21047
20. 2+ homeo-stasis in the mouse egg have an absolute requirement for mitochondrial ATP production. Development 131(13), 3057-3067. doi:10.1242/DEV. 01181 (Pubitemid 39077431)
21. 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(6), 909-918. doi:10.1095/BIOLREPROD.110.084145
22. Eppig, J. J. (1991). Intercommunication between mammalian oocytes and companion somatic cells. Bioessays 13(11), 569-574. doi:10.1002/BIES.950131105 (Pubitemid 121000533)
23. 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(5), 836-848. doi:10.1016/J. THERIOGENOLOGY.2008.10.023
24. Fouladi-Nashta, A. A., and Campbell, K. H. (2006). Dissociation of oocyte nuclear and cytoplasmic maturationby the addition of insulin in cultured bovine antral follicles. Reproduction 131(3), 449-460. doi:10.1530/REP.1.00581
25. 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(1), 9-17. doi:10.1095/BIOLREPROD.106.058578 (Pubitemid 46986391)
26. 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. doi:10.1530/REP-08-0391
27. Fulka, J., Jr, First, N. L., and Moor, R. M. (1998). Nuclear and cytoplasmic determinants involved in the regulation of mammalian oocyte maturation. Mol. Hum. Reprod. 4(1), 41-49. doi:10.1093/MOLEHR/4.1.41 (Pubitemid 28109159)
28. 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(2), 159-177. doi:10.1093/HUMUPD/DMM040 (Pubitemid 351321110)
29. Goto, Y., Noda, Y., Mori, T., and Nakano, M. (1993). Increased generation of reactive oxygen speciesin embryos culturedin vitro.Free Radic. Biol. Med. 15(1), 69-75. doi:10.1016/0891-5849(93)90126-F (Pubitemid 23171444)
30. 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(5), 1820-1823. doi:10.1016/J.FERTNSTERT.2010.11.021
31. 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(4), 353-360. doi:10.1002/1098-2795(200012)57:4, 353::AID-MRD7.3.0.CO;2-R
32. Hyttel, P., Greve, T., and Callesen, H. (1989). Ultrastructural aspects of oocyte maturation and fertilization in cattle. J. Reprod. Fertil. Suppl. 38, 35-47.
33. 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(7), 1186-1197. doi:10.1016/J.THERIOGENOLOGY.2004.01. 011 (Pubitemid 39123698)
34. Krisher, R. L. (2004). The effect of oocyte quality on development. J Anim. Sci. 82(E-Suppl), E14-E23.
35. 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(1-2), 72-96. doi:10.1016/J.ANIREPROSCI.2006.10.006 (Pubitemid 46223532)
36. 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(2), 119-131. doi:10.1080/ 09540260600581993 (Pubitemid 43791675)
37. 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(6), 1064-1072. doi:10.1095/BIOLREPROD.109.076851
38. 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(6), 979-988. doi:10.1530/REP-09-0503
39. 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(4), 608-614. doi:10.1071/RD08198
40. Nagai, S., Mabuchi, T., Hirata, S., Shoda, T., Kasai, T., Yokota, S., Shitara, H., Yonekawa, H., and Hoshi, K. (2006). Correlation of abnormal mito-chondrial distribution in mouse oocytes with reduced developmental competence. Tohoku J. Exp. Med. 210(2), 137-144. doi:10.1620/TJEM. 210.137 (Pubitemid 44575588)
41. 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(2), 501-507. (Pubitemid 20205588)
42. 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(5), 408-415. doi:10.1272/JNMS.70.408 (Pubitemid 37372857)
43. 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 inmammalian oocytes.J. Cell. Biochem. 111(3), 521-528. doi:10.1002/JCB.22736
44. 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(4), 582-585. doi:10.1095/BIOLREPROD.105.042127 (Pubitemid 41356114)
45. 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. doi:10.1016/0076-6879(95) 60154-6
46. 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(9), 1237-1242. doi:10.1289/EHP.10578
47. 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(3), 623-634.
48. Simopoulos, A. P. (2002). The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed. Pharmacother. 56(8), 365-379. doi:10.1016/S0753-3322(02)00253-6 (Pubitemid 35232740)
49. 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(9), 940-947. doi:10.1038/EJCN.2010.98
50. 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 follicu-lar porcine oocytes. Reprod. Fertil. Dev. 23(7), 912-920. doi:10.1071/RD10339
51. 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(3), 904-909. doi:10.1095/BIOLREPROD64.3.904 (Pubitemid 32174063)
52. 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(1), 5-11. doi:10.1111/J.1439-0531.2006.00615.X
53. 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(6), 1936-1942. doi:10.1095/BIOLREPROD. 104.033589 (Pubitemid 39586939)
54. 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(10), 2155-2167. (Pubitemid 27468023)
55. 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(11), 5031-5035. doi:10.1073/PNAS.88.11.5031 (Pubitemid 21914677)
56. Van Blerkom, J. (2009). Mitochondria in early mammalian development. Semin. Cell Dev. Biol. 20(3), 354-364. doi:10.1016/J.SEMCDB.2008. 12.005
57. Van Blerkom, J., and Davis, P. (2007). Mitochondrial signalling and fertilization. Mol. Hum. Reprod. 13(11), 759-770. doi:10.1093/MOLEHR/GAM068 (Pubitemid 350131349)
58. 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(2), 393-406. doi:10.1093/HUMREP/17.2.393 (Pubitemid 34168448)
59. 2+ levels in metaphase II mouse oocytes. Hum. Reprod. 18(11), 2429-2440. doi:10.1093/HUMREP/DEG466 (Pubitemid 37427827)
60. 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(3), 505-511. doi:10.1530/REP-09-0430
61. 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(2), E425-E434. doi:10.1152/AJPENDO.00409. 2007 (Pubitemid 351231471)
62. 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(7), 483-492. doi:10.1631/JZUS.B0820379
63. Wathes, D.C., Abayasekara, D.R., and Aitken, R.J. (2007). Polyunsaturated fatty acids in male and female reproduction. Biol. Reprod. 77(2), 190-201. doi:10.1095/BIOLREPROD.107.060558 (Pubitemid 47173600)
64. Watson, A. J. (2007). Oocyte cytoplasmic maturation: a key mediator of oocyte and embryo developmental competence. J. Anim. Sci. 85(13, Suppl), E1-E3. doi:10.2527/JAS.2006-432
65. 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(5), 909-917. doi:10.1093/HUMREP/16.5.909 (Pubitemid 32451826)
66. 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(1), 57-69. doi:10.1530/REP-09-0219
67. 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(10), 1457-1467. doi:10.1089/NEU.2004.21.1457 (Pubitemid 39435321)
68. 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(6), e6048. doi:10.1371/JOURNAL.PONE. 0006048
69. 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(10), 841-850. doi:10.1038/SJ.CR.7310095 (Pubitemid 44599797)