The role of fatty acids in oocyte and early embryo development

Reproduction, Fertility and Development

Volumn 24, Issue 1, 2012, Pages 59-67

  McKeegan, Paul J ^a   Sturmey, Roger G ^a  

^a UNIVERSITY OF HULL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL COENZYME A DESATURASE; ACYL COENZYME A DESATURASE 2; ARACHIDONIC ACID; COPPER ZINC SUPEROXIDE DISMUTASE; DOCOSAHEXAENOIC ACID; FATTY ACID; ICOSAPENTAENOIC ACID; LINOLEIC ACID; LINOLENIC ACID; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OLEIC ACID; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; PALMITIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHOLIPID; REACTIVE OXYGEN METABOLITE; RETINOID X RECEPTOR ALPHA; RETINOID X RECEPTOR BETA; STEARIC ACID; STEROL REGULATORY ELEMENT BINDING PROTEIN; UNCLASSIFIED DRUG; VERY LONG CHAIN FATTY ACID;

CARBOHYDRATE METABOLISM; EMBRYO DEVELOPMENT; FAT INTAKE; FERTILITY; GENE EXPRESSION; HUMAN; INTRACELLULAR SIGNALING; LIPID METABOLISM; METABOLISM; NONHUMAN; OOCYTE DEVELOPMENT; OOCYTE MATURATION; OXIDATIVE STRESS; REVIEW;

ANIMALS; EMBRYONIC DEVELOPMENT; FATTY ACIDS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MODELS, ANIMAL; OOGENESIS; OXIDATIVE STRESS; PREGNANCY; SIGNAL TRANSDUCTION;

EID: 83155190068     PISSN: 10313613     EISSN: 14485990     Source Type: Journal    
DOI: 10.1071/RD11907     Document Type: Review

References (105)

1. Aardema, H., Vos, P. L. A. M., Lolicato, F., Roelen, B. A. J., 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. doi:10.1095/ BIOLREPROD.110.088815
2. 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. doi:10.1002/ MRD.1131
3. Adamiak, S. J., Powell, K., Rooke, J. A., Webb, R., and Sinclair, K. D.2006). Body composition, dietary carbohydrates and fatty acids determine post-fertilisation development of bovine oocytes in vitro. Reproduction 131, 247-258. doi:10.1530/REP.1.00871
4. Al Darwich, A., Perreau, C., Petit, M. H., Papillier, P., Dupont, J., Guillaume, D., Mermillod, P., and Guignot, F.2010). Effect of PUFA on embryo cryoresistance, gene expression and AMPKa phosphorylation in IVF-derived bovine embryos. Prostaglandins Other Lipid Mediat. 93, 30-36. doi:10.1016/J. PROSTAGLANDINS.2010.06.002
5. Barceló-Fimbres, M., and Seidel, G. E., Jr.2011). Cross-validation of techniques for measuring lipid content of bovine oocytes and blastocysts. Theriogenology 75, 434-444. doi:10.1016/J.THERIOGENOL OGY.2010.09.007
6. Bordoni, A., Di Nunzio, M., Danesi, F., and Biagi, P.2006). Polyunsaturated fatty acids: From diet to binding to PPARs and other nuclear receptors. Genes & Nutrition 1, 95-106.
7. Braissant, O., and Wahli, W.1998). Differential expression of peroxisome proliferator-activated receptor-α, -β and -γ during rat embryonic Dev. Endocrinol. 139, 2748-2754. doi:10.1210/EN.139.6.2748
8. Brinster, R. L.1968a). In vitro culture of mammalian embryos. J. Anim. Sci. 27, 1-14.
9. Brinster, R. L.1968b). Lactate dehydrogenase activity in the oocytes of mammals. J. Reprod. Fertil. 17, 139-146. doi:10.1530/JRF.0.0170139
10. Brinster, R. L.1969). Incorporation of carbon from glucose and pyruvate into the preimplantation mouse embryo. Exp. Cell Res. 58, 153-158. doi:10.1016/0014-4827(69)90125-6
11. Brinster, R. L.1971). Oxidation of pyruvate and glucose by oocytes of the mouse and rhesus monkey. J. Reprod. Fertil. 24, 187-191. doi:10.1530/ JRF.0.0240187
12. Brison, D. R., Houghton, F. D., Falconer, D., Roberts, S. A., Hawkhead, J., Humpherson, P. G., Lieberman, B. A., and Leese, H. J.2004). Identification of viable embryos in IVF by non-invasive measurement of amino acid turnover. Hum. Reprod. 19, 2319-2324. doi:10.1093/ HUMREP/DEH409
13. Brown, M. S., and Goldstein, J. L.1997). The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89, 331-340. doi:10.1016/S0092-8674(00) 80213-5
14. Chakravarthy, M. V., Zhu, Y., Wice, M. B., Coleman, T., Pappan, K. L., Marshall, C. A., McDaniel, M. L., and Semenkovich, C. F.2008). Decreased fetal size is associated with bγ-cell hyperfunction in early life and failure with age. Diabetes 57, 2698-2707. doi:10.2337/DB08-0404
15. Chason, R. J., Csokmay, J., Segars, J. H., DeCherney, A. H., and Armant, D. R.2011). Environmental and epigenetic effects upon preimplantation embryo metabolism and development. Trends Endocrinol. Metab. 22, 412-420. doi:10.1016/J.TEM.2011.05.005
16. Conaghan, J., Handyside, A. H., Winston, R. M. L., and Leese, H. J.1993). Effects of pyruvate and glucose on the development of human preimplantation embryos in vitro. J. Reprod. Fertil. 99, 87-95. doi:10.1530/ JRF.0.0990087
17. Coull, G., Speake, B., Staines, M., Broadbent, P., and McEvoy, T.1998). Lipid and fatty acid composition of zona-intact sheep oocytes. Theriogenology 49, 179. doi:10.1016/S0093-691X(98)90532-5
18. Coyne, G. S., Kenny, D. A., Childs, S., Sreenan, J. M., and Waters, S. M.2008). Dietary n-3 polyunsaturated fatty acids alter the expression of genes involved in prostaglandin biosynthesis in the bovine uterus. Theriogenology 70, 772-782. doi:10.1016/J.THERIOGENOLOGY. 2008.05.048
19. Cran, D. G.1985). Qualitative and quantitative structural changes during pig oocyte maturation. J. Reprod. Fertil. 74, 237-245. doi:10.1530/JRF. 0.0740237
20. Cui, Y., Miyoshi, K., Claudio, E., Siebenlist, U. K., Gonzalez, F. J., Flaws, J., Wagner, K.-U., and Hennighausen, L.2002). Loss of the peroxisome proliferation-activated receptor gammaPPARg) does not affect mammary development and propensity for tumor formation but leads to reduced fertility. J. Biol. Chem. 277, 17830-17835. doi:10.1074/JBC. M200186200
21. Desvergne, B., and Wahli, W.1999). Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr. Rev. 20, 649-688. doi:10.1210/ER.20.5.649
22. Downs, S. M.2010). Regulation of the G2/M transition in rodent oocytes. Mol. Reprod. Dev. 77, 566-585. doi:10.1002/MRD.21175
23. 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. doi:10.1002/MRD.21047
24. 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. doi:10.1095/BIOLREPROD.110.084145
25. Duvnjak, M., Lerotić, I., Barsić, N., Tomasić, V., Virović Jukić, L., and Velagić, V.2007). Pathogenesis and management issues for nonalcoholic fatty liver disease. World J. Gastroenterol. 13, 4539-4550
26. Favetta, L. A., St. John, E. J., King, W. A., and Betts, D. H.2007). High levels of p66shc and intracellular ROS in permanently arrested early embryos. Free Radic. Biol. Med. 42, 1201-1210. doi:10.1016/J.FREE RADBIOMED.2007.01.018
27. Ferguson, E. M., and Leese, H. J.1999). Triglyceride content of bovine oocytes and early embryos. J. Reprod. Fertil. 116, 373-378. doi:10.1530/JRF.0. 1160373
28. Ferguson, E. M., and Leese, H. J.2006). A potential role for triglyceride as an energy source during bovine oocyte maturation and early embryo development. Mol. Reprod. Dev. 73, 1195-1201. doi:10.1002/MRD. 20494
29. Ferreira, C. R., Saraiva, S. A., Catharino, R. R., Garcia, J. S., Gozzo, F. C., Sanvido, G. B., Santos, L. F. A., Lo Turco, E. G., Pontes, J. H. F., 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. doi:10.1194/JLR.D001768
30. Flynn, T. J., and Hillman, N.1980). The metabolism of exogenous fatty acids by preimplantation mouse embryos developing in vitro. J. Embryol. Exp. Morphol. 56, 157-168.
31. Gardner, D. K., and Leese, H. J.1986). Non-invasive measurement of nutrient uptake by single cultured pre-implantation mouse embryos. Hum. Reprod. 1, 25-27.
32. Gardner, D. K., Wale, P. L., Collins, R., and Lane, M.2011). Glucose consumption of single post-compaction human embryos is predictive of embryo sex and live birth outcome. Hum. Reprod. doi:10.1093/ HUMREP/DER143
33. Guraya, S. S.1965). A histochemical analysis of lipid yolk deposition in the oocytes of cat and dog. J. Exp. Zool. 160, 123-135. doi:10.1002/ JEZ.1401600111
34. Haggarty, P., Wood, M., Ferguson, E., Hoad, G., Srikantharajah, A., Milne, E., Hamilton, M., and Bhattacharya, S.2006). Fatty acid metabolism in human preimplantation embryos. Hum. Reprod. 21, 766-773. doi:10.1093/HUMREP/ DEI385
35. Hancock, J. T., Desikan, R., and Neill, S. J.2001). Role of reactive oxygen species in cell signalling pathways. Biochem. Soc. Trans. 29, 345-349. doi:10.1042/BST0290345
36. Harvey, K. A., Walker, C. L., Pavlina, T. M., Xu, Z., Zaloga, G. P., and Siddiqui, R. A.2010a). Long-chain saturated fatty acids induce proinflammatory responses and impact endothelial cell growth. Clin. Nutr. 29, 492-500. doi:10.1016/J.CLNU.2009.10.008
37. Harvey, K. A., Walker, C. L., Xu, Z., Whitley, P., Pavlina, T. M., Hise, M., Zaloga, G. P., and Siddiqui, R. A.2010b). Oleic acid inhibits stearic acid-induced inhibition of cell growth and pro-inflammatory responses in human aortic endothelial cells. J. Lipid Res. 51, 3470-3480. doi:10.1194/JLR.M010371
38. Homa, S. T., and Brown, C. A.1992). Changes in linoleic acid during follicular development and inhibition of spontaneous breakdown of germinal vesicles in cumulus-free bovine oocytes. J. Reprod. Fertil. 94, 153-160. doi:10.1530/JRF.0.0940153
39. Homa, S. T., Racowsky, C., and McGaughey, R. W.1986). Lipid analysis of immature pig oocytes. J. Reprod. Fertil. 77, 425-434. doi:10.1530/JRF. 0.0770425
40. Houghton, F. D., Thompson, J. G., Kennedy, C. J., and Leese, H. J.1996). Oxygen consumption and energy metabolism of the early mouse embryo. Mol. Reprod. Dev. 44, 476-485. doi:10.1002/(SICI)1098- 2795(199608)44:4,476::AID-MRD7.3.0. CO;2-I
41. Hugentobler, S. A., Humpherson, P. G., Leese, H. J., Sreenan, J. M., and Morris, D. G.2008). Energy substrates in bovine oviduct and uterine fluid and blood plasma during the oestrous cycle. Mol. Reprod. Dev. 75, 496-503. doi:10.1002/MRD.20760
42. Hughes, J., Kwong, W. Y., Li, D., Salter, A. M., Lea, R. G., and Sinclair, K. D.2011). Effects of omega-3 and -6 polyunsaturated fatty acids on ovine follicular cell steroidogenesis, embryo development and molecular markers of fatty acid metabolism. Reproduction 141, 105-118. doi:10.1530/REP-10-0337
43. Iritani, A., Gomes, W. R., and Vandemark, N. L.1969). Secretion rates and chemical composition of oviduct and uterine fluids in ewes. Biol. Reprod. 1, 72-76. doi:10.1095/BIOLREPROD1.1.72
44. Iritani, A., Nishikawa, Y., Gomes, W. R., and VanDemark, N. L.1971). Secretion rates and chemical composition of oviduct and uterine fluids in rabbits. J. Anim. Sci. 33, 829-835.
45. Iritani, A., Sato, E., and Nishikawa, Y.1974). Secretion rates and chemical composition of oviduct and uterine fluids in sows. J. Anim. Sci. 39, 582-588.
46. Johnson, M. H., and Nasresfahani, M. H.1994). Radical solutions and cultural problems: Could free oxygen radicals be responsible for the impaired development of preimplantation mammalian embryos in vitro? Bioessays 16, 31-38. doi:10.1002/BIES.950160105
47. Jungheim, E. S., Louden, E. D., Chi, M. M.-Y., Frolova, A. I., Riley, J. K., and Moley, K. H.2011). Preimplantation exposure of mouse embryos to palmitic acid results in fetal growth restriction followed by catch-up growth in the offspring. Biol. Reprod. doi:10.1095/BIOLREPROD. 111.092148
48. Kane, M. T.1979). Fatty acids as energy sources for culture of one-cell rabbit ova to viable morulae. Biol. Reprod. 20, 323-332. doi:10.1095/ BIOLREPROD20.2.323
49. Khandoker, M. A. M. Y., Tsujii, H., and Karasawa, D.1997). Fatty acid compositions of oocytes, follicular, oviductal and uterine fluids of pig and cow. Asian Australas. J. Anim. Sci. 10, 523-527.
50. Khandoker, M. A. M. Y., Tsujii, H., and Karasawa, D.1998). A kinetic study of fatty acid composition of embryos, oviductal and uterine fluids in the rabbit. Asian Australas. J. Anim. Sci. 11, 60-64.
51. Korn, B. S., Shimomura, I., Bashmakov, Y., Hammer, R. E., Horton, J. D., Goldstein, J. L., and Brown, M. S.1998). Blunted feedback suppression of SREBP processing by dietary cholesterol in transgenic mice expressing sterol-resistant SCAP(D443N). J. Clin. Invest. 102, 2050-2060. doi:10.1172/JCI5341
52. 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. doi:10.1002/MRD.1120080105
53. Leese, H. J., Hooper, M. A. K., Edwards, R. G., and Ashwood-Smith, M. J.1986). Uptake of pyruvate by early human embryos determined by a non-invasive technique. Hum. Reprod. 1, 181-182.
54. Leese, H. J., Hugentobler, S. A., Gray, S. M., Morris, D. G., Sturmey, R. G., Whitear, S., and Sreenan, J. M.2008). Female reproductive tract fluids: composition, mechanism of formation and potential role in the developmental origins of health and disease. Reprod. Fertil. Dev. 20, 1-8. doi:10.1071/RD07153
55. Lehmann, J. M., Lenhard, J. M., Oliver, B. B., Ringold, G. M., and Kliewer, S. A.1997). Peroxisome proliferator-activated receptors a and g are activated by indomethacin and other non-steroidal anti-inflammatory drugs. J. Biol. Chem. 272, 3406-3410. doi:10.1074/JBC.272.6.3406
56. Lequarré, A.-S., Feugang, J.-M., Malhomme, O., Donnay, I., Massip, A., Dessy, F., and Van Langendonckt, A.2001). Expression of Cu/Zn and Mn superoxide dismutases during bovine embryo development: Influence of in vitro culture. Mol. Reprod. Dev. 58, 45-53. doi:10.1002/1098- 2795(200101)58:1,45:: AID-MRD7.3.0.CO;2-J
57. Leroy, J. L. M. R., Genicot, G., Donnay, I., and Van Soom, A.2005a). Evaluation of the lipid content in bovine oocytes and embryos with nile red: a practical approach. Reprod. Domest. Anim. 40, 76-78. doi:10.1111/J.1439-0531. 2004.00556.X
58. Leroy, J. L. M. R., Vanholder, T., Mateusen, B., Christophe, A., Opsomer, G., de Kruif, A., Genicot, G., and Van Soom, A.2005b). Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro. Reproduction 130, 485-495. doi:10.1530/REP.1.00735
59. Leroy, J. L. M. R., Opsomer, G., Van Soom, A., Goovaerts, I. G. F., and Bols, P. E. J.2008a). Reduced fertility in high-yielding dairy cows: are the oocyte and embryo in danger? Part I The importance of negative energy balance and altered corpus luteum function to the reduction of oocyte and embryo quality in high-yielding dairy cows. Reprod. Domest. Anim. 43, 612-622. doi:10.1111/J.1439-0531.2007.00960.X
60. Leroy, J. L. M. R., Van Soom, A., Opsomer, G., Goovaerts, I. G. F., and Bols, P. E. J.2008b). Reduced fertility in high-yielding dairy cows: are the oocyte and embryo in danger? Part II Mechanisms linking nutrition and reduced oocyte and embryo quality in high-yielding dairy cows. Reprod. Domest. Anim. 43, 623-632. doi:10.1111/J.1439-0531.2007. 00961.X
61. Leroy, J. L. M. R., Van Hoeck, V., Clemente, M., Rizos, D., Gutierrez-Adan, A., Van Soom, A., Uytterhoeven, M., and Bols, P. E. J.2010). The effectof nutritionally induced hyperlipidaemia on in vitro bovine embryo quality. Hum. Reprod. 25, 768-778. doi:10.1093/HUMREP/DEP420
62. Loewenstein, J. E., and Cohen, A. I.1964). Dry mass, lipid content and protein content of the intact and zona-free mouse ovum. J. Embryol. Exp. Morphol. 12, 113-121.
63. Lopes, A. S., Lane, M., and Thompson, J. G.2010). Oxygen consumption and ROS production are increased at the time of fertilization and cell cleavage in bovine zygotes. Hum. Reprod. 25, 2762-2773. doi:10.1093/ HUMREP/DEQ221
64. 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. doi:10.1095/BIOLREPROD.109.076851
65. 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. doi:10.1530/REP-09-0503
66. Matorras, R., Ruiz, J. I., Mendoza, R., Ruiz, N., Sanjurjo, P., and Rodriguez- Escudero, F. J.1998). Fatty acid composition of fertilization-failed human oocytes. Hum. Reprod. 13, 2227-2230. doi:10.1093/HUMREP/ 13.8.2227
67. McEvoy, T., Coull, G., Broadbent, P., Hutchinson, J., and Speake, B.2000). Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J. Reprod. Fertil. 118, 163-170.
68. Menezo, Y., Renard, J. P., Delobel, B., and Pageaux, J. F.1982). Kinetic study of fatty acid composition of day 7 to day 14 cow embryos. Biol. Reprod. 26, 787-790. doi:10.1095/BIOLREPROD26.5.787
69. Miyamoto, K., Sato, E. F., Kasahara, E., Jikumaru, M., Hiramoto, K., Tabata, H., Katsuragi, M., Odo, S., Utsumi, K., and Inoue, M.2010). Effect of oxidative stress during repeated ovulation on the structure and functions of the ovary, oocytes, and their mitochondria. Free Radic. Biol. Med. 49, 674-681. doi:10.1016/J.FREERADBIOMED.2010.05.025
70. Mohan, M., Malayer, J. R., Geisert, R. D., and Morgan, G. L.2002). Expression patterns of retinoid X receptors, retinaldehyde dehydrogenase, and peroxisome proliferator activated receptor gamma in bovine preattachment embryos. Biol. Reprod. 66, 692-700. doi:10.1095/BIOL REPROD66.3.692
71. Moon, Y.-A., Hammer, R. E., and Horton, J. D.2009). Deletion of ELOVL5 leads to fatty liver through activation of SREBP-1c in mice. J. Lipid Res. 50, 412-423. doi:10.1194/JLR.M800383-JLR200
72. Nagashima, H., Kashiwazaki, N., Ashman, R. J., Grupen, C. G., and Nottle, M. B.1995). Cryopreservation of porcine embryos. Nature 374, 416. doi:10.1038/374416A0
73. Nishikimi, A., Mukai, J., and Yamada, M.1999). Nuclear translocation of nuclear factor kappa B in early 1-cell mouse embryos. Biol. Reprod. 60, 1536-1541. doi:10.1095/BIOLREPROD60.6.1536
74. Nonogaki, T., Noda, Y., Goto, Y., Kishi, J., and Mori, T.1994). Developmental blockage of mouse embryos caused by fatty acids. J. Assist. Reprod. Genet. 11, 482-488. doi:10.1007/BF02215713
75. Ntambi, J., and Bené, H.2001). Polyunsaturated fatty acid regulation of gene expression. J. Mol. Neurosci. 16, 273-278. doi:10.1385/ JMN:16:2-3:273
76. Piomelli, D.1993). Arachidonic acid in cell signaling. Curr. Opin. Cell Biol. 5, 274-280. doi:10.1016/0955-0674(93)90116-8
77. Quinn, P., and Whittingham, D. G.1982). Effect of fatty acids on fertilization and development of mouse embryos in vitro. J. Androl. 3, 440-444.
78. Rees, W. D., McNeil, C. J., and Maloney, C. A.2008). The roles of PPARs in the fetal origins of metabolic health and disease. PPAR Research 2008, pp. 1-8.
79. 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. doi:10.1071/RD03004
80. Ren, B., Thelen, A. P., Peters, J. M., Gonzalez, F. J., and Jump, D. B.1997). Polyunsaturated fatty acid suppression of hepatic fatty acid synthase and S14 gene expression does not require peroxisome proliferator-activated receptor a. J. Biol. Chem. 272, 26827-26832. doi:10.1074/JBC.272.43. 26827
81. Renaville, B., Bacciu, N., Comin, A., Motta, M., Poli, I., Vanini, G., and Prandi, A.2010). Plasma and follicular fluid fatty acid profiles in dairy cows. Reprod. Domest. Anim. 45, 118-121. doi:10.1111/J.1439-0531. 2008.01264.X
82. Rieger, D., McGowan, L. T., Cox, S. F., Pugh, P. A., and Thompson, J. G.2002). Effect of 2,4-dinitrophenol on the energy metabolism of cattle embryos produced by in vitro fertilization and culture. Reprod. Fertil. Dev. 14, 339-343. doi:10.1071/RD02038
83. Sampath, H., and Ntambi, J. M.2005). Polyunsaturated fatty acid regulation of genes of lipid metabolism. Annu. Rev. Nutr. 25, 317-340. doi:10.1146/ANNUREV.NUTR.25.051804.101917
84. Sata, R., Tsujii, H., Abe, H., Yamashita, S., and Hoshi, H.1999). Fatty acid composition of bovine embryos cultured in serum-free and serumcontaining medium during early embryonic development. J. Reprod. Dev. 45, 97-103. doi:10.1262/JRD.45.97
85. Scott, L., Berntsen, J., Davies, D., Gundersen, J., Hill, J., and Ramsing, N.2008). Human oocyte respiration-rate measurement- potential to improve oocyte and embryo selection? Reprod. Biomed. Online 17, 461-469. doi:10.1016/S1472-6483(10)60232-5
86. Seli, E., Botros, L., Sakkas, D., and Burns, D. H.2008). Noninvasive metabolomic profiling of embryo culture media using proton nuclear magnetic resonance correlates with reproductive potential of embryos in women undergoing in vitro fertilization. Fertil. Steril. 90, 2183-2189. doi:10.1016/J.FERTNSTERT. 2008.07.1739
87. Shehab-El-Deen, M. A., Leroy, J. L. M. R., 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. doi:10.1111/J.1439-0531.2008.01084.X
88. Shiku, H., Shiraishi, T., Ohya, H., Matsue, T., Abe, H., Hoshi, H., and Kobayashi, M.2001). Oxygen consumption of single bovine embryos probed by scanning electrochemical microscopy. Anal. Chem. 73, 3751-3758. doi:10.1021/AC010339J
89. Spindler, R. E., Pukazhenthi, B. S., and Wildt, D. E.2000). Oocyte metabolism predicts the development of cat embryos to blastocyst in vitro. Mol. Reprod. Dev. 56, 163-171. doi:10.1002/(SICI)1098-2795200006)56:2,163::AID-MRD7. 3.0.CO;2-3
90. Stadtman, E. R., and Levine, R. L.2000). Protein oxidation. Ann. N. Y. Acad. Sci. 899, 191-208.
91. Sturmey, R., and Leese, H.2003). Energy metabolism in pig oocytes and early embryos. Reproduction 126, 197-204. doi:10.1530/REP.0. 1260197
92. 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. doi:10.1530/REP- 06-0073
93. Sturmey, R. G., Hawkhead, J. A., Barker, E. A., and Leese, H. J.2009a). DNA damage and metabolic activity in the preimplantation embryo. Hum. Reprod. 24, 81-91. doi:10.1093/HUMREP/DEN346
94. Sturmey, R. G., Reis, A., Leese, H. J., and McEvoy, T. G.2009b). Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reprod. Domest. Anim. 44(Suppl 3), 50-58. doi:10.1111/J.1439-0531. 2009.01402.X
95. Tabor, D. E., Kim, J. B., Spiegelman, B. M., and Edwards, P. A.1998). Transcriptional activation of the stearoyl-CoA desaturase 2 gene by sterol regulatory element-binding protein/adipocyte determination and differentiation factor 1. J. Biol. Chem. 273, 22052-22058. doi:10.1074/ JBC.273.34.22052
96. Takahashi, M., Keicho, K., Takahashi, H., Ogawa, H., Schulte, R. M., and Okano, A.2000). Effect of oxidative stress on development and DNA damage in in-vitro cultured bovine embryos by comet assay. Theriogenology 54, 137-145. doi:10.1016/S0093-691X(00)00332-0
97. Thompson, J. G., Partridge, R. J., Houghton, F. D., Cox, C. I., and Leese, H. J.1996). Oxygen uptake and carbohydrate metabolism by in vitro derived bovine embryos. J. Reprod. Fertil. 106, 299-306. doi:10.1530/ JRF.0.1060299
98. Tsujii, H., Khandoker, M. A. M. Y., and Hamano, K.-i.2001). Lipid in mammalian embryo development. J. Mamm. Ova Res. 18, 73-80. doi:10.1274/JMOR.18. 73
99. Van Hoeck, V., Sturmey, R. G., Bermejo-Alvarez, P., Rizos, D., Gutierrez- Adan, A., Leese, H. J., Bols, P. E. J., and Leroy, J. L. M. R.2011). Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology. PLoS ONE 6, e23183. doi:10.1371/JOURNAL. PONE.0023183
100. Vanholder, T., Leroy, J. L. M. R., Soom, A. V., Opsomer, G., Maes, D., Coryn, M., and Kruif, A. d.2005). Effect of non-esterified fatty acids on bovine granulosa cell steroidogenesis and proliferation in vitro. Anim. Reprod. Sci. 87, 33-44. doi:10.1016/J.ANIREPROSI.2004.09.006
101. 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 alter mechanisms involved in oocyte and early embryo development in the mouse. Am. J. Physiol. Endocrinol. Metab. 294, E425-E434. doi:10.1152/AJPENDO. 00409.2007
102. 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. doi:10.1530/REP-09-0219
103. Wu, G. Q., Jia, B. Y., Li, J. J., Fu, X. W., Zhou, G. B., Hou, Y. P., and Zhu, S. E.2011). L-Carnitine enhances oocyte maturation and development of parthenogenetic embryos in pigs. Theriogenology. doi:10.1016/ J.THERIOGENOLOGY.2011.04.011
104. Yang, H. W., Hwang, K. J., Kwon, H. C., Kim, H. S., Choi, K. W., and Oh, K. S.1998). Detection of reactive oxygen speciesROS) and apoptosis in human fragmented embryos. Hum. Reprod. 13, 998-1002. doi:10.1093/HUMREP/13.4.998
105. Zeron, Y., Sklan, D., and Arav, A.2002). Effect of polyunsaturated fatty acid supplementation on biophysical parameters and chilling sensitivity of ewe oocytes. Mol. Reprod. Dev. 61, 271-278. doi:10.1002/ MRD.1156