A diet enriched in linoleic acid compromises the cryotolerance of embryos from superovulated beef heifers

Reproduction, Fertility and Development

Volumn 26, Issue 4, 2014, Pages 511-520

  Guardieiro, Monique M ^a   Machado, Grazieli M ^b   Bastos, Michele R ^c   Mourão, Gerson B ^a   Carrijo, Luiz H D ^d   Dode, Margot A N ^b   Leroy, Jo L M R ^e   Sartori, Roberto ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b EMBRAPA RECURSOS GENÉTICOS E BIOTECNOLOGIA   (Brazil)

^c SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^d Integral Nutrição Animal ^*  (Brazil)

^e UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

cryopreservation; fatty acid; nutrition

Indexed keywords

LINOLEIC ACID; POLYUNSATURATED FATTY ACID;

ANIMAL EXPERIMENT; ARTICLE; BEEF; CONTROLLED STUDY; CRYOPRESERVATION; DIET SUPPLEMENTATION; EMBRYO; EMBRYO CULTURE; EMBRYO DEVELOPMENT; FEMALE; FREEZING; HATCHING; HEIFER; IN VITRO STUDY; MULTIPLE OVULATION AND EMBRYO TRANSFER; NONHUMAN; SUPEROVULATION; THAWING; VITRIFICATION; WARMING; ANIMAL; ANIMAL EMBRYO; ANIMAL FOOD; BOVINAE; CROSSOVER PROCEDURE; DRUG EFFECTS; FERTILIZATION IN VITRO; METABOLISM; OVULATION INDUCTION; PATHOLOGY; PREGNANCY; TIME; VETERINARY;

ANIMAL FEED; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; CATTLE; CROSS-OVER STUDIES; CRYOPRESERVATION; DIETARY SUPPLEMENTS; EMBRYO CULTURE TECHNIQUES; EMBRYO, MAMMALIAN; FEMALE; FERTILIZATION IN VITRO; LINOLEIC ACIDS; OVULATION INDUCTION; PREGNANCY; SUPEROVULATION; TIME FACTORS; VITRIFICATION;

EID: 84898020786     PISSN: 10313613     EISSN: 14485990     Source Type: Journal    
DOI: 10.1071/RD12403     Document Type: Article

References (71)

1. Ahmad, N., Schrick, F. N., Butcher, R. L., and Inskeep, E. K. (1995). Effect of persistent follicles on early embryonic losses in beef cows. Biol. Reprod. 52, 1129-1135. doi:10.1095/BIOLREPROD52.5.1129
2. 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 AMPKalpha phosphorylation in IVF-derived bovine embryos. Prostaglandins Other Lipid Mediat. 93, 30-36. doi:10.1016/J.PROSTAGLANDINS.2010.06.002
3. Arreseigor, C. J., Sisul, A., Arreseigor, A. E., and Stahringe, R. C. (1998). Effect of cryoprotectant, thawing method, embryo grade and breed on pregnancy rates of cryopreserved bovine embryos. Theriogenology 49, 160. [Abstract] doi:10.1016/S0093-691X(98)90513-1
4. Block, J., Fischer-Brown, A. E., Rodina, T. M., Ealy, A. D., and Hansen, P. J. (2007). The effect of in vitro treatment of bovine embryos with IGF-1 on subsequent development in utero to Day 14 of gestation. Theriogenology 68, 153-161. doi:10.1016/J.THERIOGENOLOGY.2007.04.045
5. Castro Neto, A. S., Sanches, B. V., Binelli, M., Seneda, M. M., Perri, S. H., and Garcia, J. F. (2005). Improvement in embryo recovery using double uterine flushing. Theriogenology 63, 1249-1255. doi:10.1016/J.THERIOGENOLOGY. 2004.03.022
6. Cerri, R. L., Juchem, S. O., Chebel, R. C., Rutigliano, H. M., Bruno, R. G., Galvão, K. N., Thatcher, W. W., and Santos, J. E. (2009). Effect of fat source differing in fatty acid profile on metabolic parameters, fertilization, and embryo quality in high-producing dairy cows. J. Dairy Sci. 92, 1520-1531. doi:10.3168/JDS.2008-1614
7. Childs, S., Carter, F., Lynch, C. O., Sreenan, J. M., Lonergan, P., Hennessy, A. A., and Kenny, D. A. (2008). Embryo yield and quality following dietary supplementation of beef heifers with n-3 polyunsaturated fatty acids (PUFA). Theriogenology 70, 992-1003. doi:10.1016/J.THERIO GENOLOGY.2008.06.008
8. Clandinin, M. T., Cheema, S., Field, C. J., Garg, M. L., Venkatraman, J., and Clandinin, T. R. (1991). Dietary fat: exogenous determination of membrane structure and cell function. FASEB J. 5, 2761-2769.
9. Cuello, C., Berthelot, F., Martinat-Botté, F., Guillouet, P., Furstoss, V., Boisseau, C., Manceau, P., Locatelli, A., and Martínez, E. A. (2004). Transfer of vitrified blastocysts from one or two superovulated Large White Hyperprolific donors to Meishan recipients: reproductive parameters at Day 30 of pregnancy. Theriogenology 61, 843-850. doi:10.1016/S0093-691X(03) 00257-7
10. Dattena, M., Ptak, G., Loi, P., and Cappai, P. (2000). Survival and viability of vitrified in vitro and in vivo produced ovine blastocysts. Theriogenology 53, 1511-1519. doi:10.1016/S0093-691X(00)00293-4
11. Dobrinsky, J. R. (2002). Advancements in cryopreservation of domestic animal embryos. Theriogenology 57, 285-302. doi:10.1016/S0093-691X(01)00672-0
12. El-Gayar, M., Gauly, M., and Holtz, W. (2008). One-step dilution of openpulled-straw (OPS)-vitrified mouse blastocysts in sucrose-free medium. Cryobiology 57, 191-194. doi:10.1016/J.CRYOBIOL.2008.07.012
13. Fenwick, M. A., Llewellyn, S., Fitzpatrick, R., Kenny, D. A., Murphy, J. J., Patton, J., and Wathes, D. C. (2008). Negative energy balance in dairy cows is associatedwith specific changes in IGF-binding protein expression in the oviduct. Reproduction 135, 63-75. doi:10.1530/REP-07-0243
14. 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
15. Gong, J. G. (2002). Influence of metabolic hormones and nutrition on ovarian follicle development in cattle: practical implications. Domest. Anim. Endocrinol. 23, 229-241. doi:10.1016/S0739-7240(02)00159-5
16. Green, M. P., Spate, L. D., Parks, T. E., Kimura, K., Murphy, C. N., Williams, J. E., Kerley, M. S., Green, J. A., Keisler, D. H., and Roberts, R. M. (2008). Nutritional skewing of conceptus sex in sheep: effects of a maternal diet enriched in rumen-protected polyunsaturated fatty acids (PUFA). Reprod. Biol. Endocrinol. 6, 21. doi:10.1186/1477-7827-6-21
17. Green, R. E., Santos, B. F., Sicherle, C. C., Landim-Alvarenga, F. C., and Bicudo, S. D. (2009). Viability of OPS vitrified sheep embryos after direct transfer. Reprod. Domest. Anim. 44, 406-410. doi:10.1111/J.1439-0531.2008.01088. X
18. Guignot, F., Bouttier, A., Baril, G., Salvetti, P., Pignon, P., Beckers, J. F., Touzé, J. L., Cognié, J., Traldi, A. S., Cognié, Y., and Mermillod, P. (2006). Improved vitrification method allowing direct transfer of goat embryos. Theriogenology 66, 1004-1011. doi:10.1016/J.THERIOGEN OLOGY.2006.02.040
19. Hochi, S., Kimura, K., and Hanada, A. (1999). Effect of linoleic acid-albumin in the culture medium on freezing sensitivity of in vitroproduced bovine morulae. Theriogenology 52, 497-504. doi:10.1016/S0093-691X(99)00146-6
20. Holm, P., Booth, P. J., Schmidt, M. H., Greve, T., and Callesen, H. (1999). High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins. Theriogenology 52, 683-700. doi:10.1016/S0093- 691X(99)00162-4
21. 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
22. Houghton, P. L., Lemenager, R. P., Hendrix, K. S., Moss, G. E., and Stewart, T. S. (1990). Effects of body composition, pre- and postpartum energy intake and stage of production of energy utilization by beef cows. J. Anim. Sci. 68, 1447-1456.
23. 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
24. Jousan, F. D., and Hansen, P. J. (2007). Insulin-like growth factor-I promotes resistance of bovine preimplantation embryos to heat shock through actions independent of its anti-apoptotic actions requiring PI3K signaling. Mol. Reprod. Dev. 74, 189-196. doi:10.1002/MRD.20527
25. Jousan, F. D., Oliveira, L. J., and Hansen, P. J. (2008). Short-term culture of in vitro produced bovine preimplantation embryos with insulin-like growth factor-i prevents heat shock-induced apoptosis through activation of the phosphatidylinositol 3-kinase/Akt pathway. Mol. Reprod. Dev. 75, 681-688. doi:10.1002/MRD.20830
26. 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. doi:10.1530/REP.0. 1220131
27. Kojima, T., Zeniya, Y., Aoyama, T., Kondo, A., and Yoshino, J. (1997). Dietary administration of fatty acids-enriched mold dried cell containing γ-linolenic acid to female pigs improves ovulation rate and embryo quality in summer. J. Reprod. Dev. 43, 121-127. doi:10.1262/JRD.43.121
28. Kong, I. K., Lee, S. I., Cho, S. G., Cho, S. K., and Park, C. S. (2000). Comparison of open pulled straw (OPS) vs glass micropipette (GMP) vitrification in mouse blastocysts. Theriogenology 53, 1817-1826. doi:10.1016/S0093-691X(00) 00317-4
29. Kurzawa, R., Głabowski, W., Baczkowski, T., and Brelik, P. (2002). Evaluation of mouse preimplantation embryos exposed to oxidative stress cultured with insulin-like growth factor I and II, epidermal growth factor, insulin, transferrin and selenium. Reprod. Biol. 2, 143-162.
30. Lapa, M., Marques, C. C., Alves, S. P., Vasques, M. I., Baptista, M. C., Carvalhais, I., Silva Pereira, M., Horta, A. E., Bessa, R. J., and Pereira, R. M. (2011). Effect of trans-10 cis-12 conjugated linoleic acid on bovine oocyte competence and fatty acid composition. Reprod. Domest. Anim. 46, 904-910. doi:10.1111/J.1439-0531.2011.01762.X
31. Leroy, J., Van Hoeck, V., Clemente, M., Rizos, D., Gutierrez-Adan, A., Van Soom, A., Uytterhoeven, M., and Bols, P. E. J. (2010). The effect of nutritionally induced hyperlipidaemia on in vitro bovine embryo quality. Hum. Reprod. 25, 768-778. doi:10.1093/HUMREP/DEP420
32. Leroy, J. L. M. R., Rizos, D., Sturmey, R., Bossaert, P., Gutierrez-Adan, A., Van Hoeck, V., Valckx, S., and Bols, P. E. J. (2012). Intrafollicular conditions as a major link between maternal metabolism and oocyte quality: a focus on dairy cow fertility. Reprod. Fertil. Dev. 24, 1-12. doi:10.1071/RD11901
33. Lopatářová, M., Čech, S., Havlíček, V., and Holý, L. (2002). Effect of vitrification in open pulled straws on survival of bovine embryos from superovulated cows. Acta Vet. 71, 93-99. doi:10.2754/AVB200271010093
34. Lopatarova, M., Cech, S., Holy, L., and Dolezel, R. (2006). The effect of vitrification in open pulled straws on pregnancy rates after transfer of in vivo produced bovine embryos. Vet. Med. (Praha) 51, 454-460.
35. 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
36. 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
37. Marei, W. F., Wathes, D. C., and Fouladi-Nashta, A. A. (2012). Differential effects of linoleic and alpha-linolenic fatty acids on spatial and temporal mitochondrial distribution and activity in bovine oocytes. Reprod. Fertil. Dev. 24, 679-690. doi:10.1071/RD11204
38. Mattos, M. C. C., Bastos, M. R., Oliveira, A.C. S., Gonçalves, J.R., Lima, L.G., Sousa, R. V., Pires, A. V., Mourão, G. B., and Sartori, R. (2010). Cryotolerance of morulae and blastocysts produced in vivo in Bos indicus. In 'Proceedings of the 24th Reunião Anual da SBTE', 19 August 2010. (Ed. Universidade Federal do Rio Grande do Sul) p. 815. (Acta Scientiae Veterinariae: Porto de Galinhas.)
39. McEvoy, T. G., Coull, G. D., Broadbent, P. J., Hutchinson, J. S., and Speake, B. K. (2000). Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J. Reprod. Fertil. 118, 163-170.
40. Miller, R. R., Cornett, C. L., Waterhouse, K. E., and Farstad, W. (2005). Comparative aspects of sperm membrane fatty acid composition in silver (Vulpes vulpes) and blue (Alopex lagopus) foxes, and their relationship to cell cryopreservation. Cryobiology 51, 66-75. doi:10.1016/J.CRYO BIOL.2005.04.009
41. Nelder, J. A., and Wedderburn, R. W. M. (1972). Generalized linear models. J. R. Stat. Soc. [Ser. A] 135, 370-384. doi:10.2307/2344614
42. Nogueira, M. F., Fragnito, P. S., Trinca, L. A., and Barros, C. M. (2007). The effect of type of vaginal insert and dose of pLH on embryo production, following fixed-time AI in a progestin-based superstimulatory protocol in Nelore cattle. Theriogenology 67, 655-660. doi:10.1016/J.THERIO GENOLOGY.2006.10.001
43. 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
44. Papadopoulos, S., Rizos, D., Duffy, P., Wade, M., Quinn, K., Boland, M. P., and Lonergan, P. (2002). Embryo survival and recipient pregnancy rates after transfer of fresh or vitrified, in vivo or in vitro produced ovine blastocysts. Anim. Reprod. Sci. 74, 35-44. doi:10.1016/S0378-4320(02) 00162-8
45. Parrish, J. J., Krogenaes, A., and Susko-Parrish, J. L. (1995). Effect of bovine sperm separation by either swim-up or Percoll method on success of in vitro fertilization and early embryonic development. Theriogenology 44, 859-869. doi:10.1016/0093-691X(95)00271-9
46. 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. doi:10.1016/J.ANIREPROSCI.2006.03.015
47. Pereira, R. M., Carvalhais, I., Pimenta, J., Baptista, M. C., Vasques, M. I., Horta, A. E., Santos, I. C., Marques, M. R., Reis, A., Pereira, M. S., and Marques, C. C. (2008). Biopsied and vitrified bovine embryos viability is improved by trans 10, cis 12 conjugated linoleic acid supplementation during in vitro embryo culture. Anim. Reprod. Sci. 106, 322-332. doi:10.1016/J. ANIREPROSCI.2007.05.008
48. Petit, H. V., and Twagiramungu, H. (2006). Conception rate and reproductive function of dairy cows fed different fat sources. Theriogenology 66, 1316-1324. doi:10.1016/J.THERIOGENOLOGY.2006.04.029
49. Petit, H. V., Cavalieri, F. B., Santos, G. T., Morgan, J., and Sharpe, P. (2008). Quality of embryos produced from dairy cows fed whole flaxseed and the success of embryo transfer. J. Dairy Sci. 91, 1786-1790. doi:10.3168/JDS.2007- 0782
50. 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
51. Ryan, D. P., Spoon, R. A., and Williams, G. L. (1992). Ovarian follicular characteristics, embryo recovery, and embryo viability in heifers fed high-fat diets and treated with follicle-stimulating hormone. J. Anim. Sci. 70, 3505-3513.
52. Sartori, R., Sartor-Bergfelt, R., Mertens, S. A., Guenther, J. N., Parrish, J. J., and Wiltbank, M. C. (2002). Fertilization and early embryonic development in heifers and lactating cows in summer and lactating and dry cows in winter. J. Dairy Sci. 85, 2803-2812. doi:10.3168/JDS.S0022-0302 (02)74367-1
53. Seidel, G. E. (2006). Modifying oocytes and embryos to improve their cryopreservation. Theriogenology 65, 228-235. doi:10.1016/J.THERIO GENOLOGY.2005.09.025
54. Souza, A. H., Sartori, R., Guenther, J. N., Caraviello, D., Monson, R., and Wiltbank, M. C. (2007). Effect of semen source and dose of FSH on superovulatory response and embryo production in Holstein heifers. Anim. Reprod. 4, 70-76.
55. Stringfellow, D. A., and Seidel, S. M. (1998). 'Manual of the International Embryo Transfer Society. 3rd edn.' (IETS: Savoy, IL).
56. Stroud, B., and Callesen, H. (2012). IETS statement on worldwide ET statistics for 2010. Anim. Reprod. 9, 210-216.
57. Sturmey, R. G., Reis, A., Leese, H. J., and McEvoy, T. G. (2009). Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reprod. Domest. Anim. 44, 50-58. doi:10.1111/J.1439-0531.2009. 01402.X
58. 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. doi:10.1095/BIOLREPROD.112.102897
59. Thangavelu, G., Colazo, M. G., Ambrose, D. J., Oba, M., Okine, E. K., and Dyck, M. K. (2007). Diets enriched in unsaturated fatty acids enhance early embryonic development in lactating Holstein cows. Theriogenology 68, 949-957. doi:10.1016/J.THERIOGENOLOGY.2007.07.002
60. Tominaga, K., Hamada, Y., Yabuue, T., and Ariyoshi, T. (2000). Effect of linoleic acid-albumin on post-thaw survival of in vitro-produced bovine embryos at the 16-cell stage. J. Vet. Med. Sci. 62, 465-467. doi:10.1292/JVMS.62.465
61. Vajta, G., Holm, P., Kuwayama, M., Booth, P. J., Jacobsen, H., Greve, T., and Callesen, H. (1998). Open pulled straw (OPS) vitrification: a new way to reduce cryoinjuries of bovine ova and embryos. Mol. Reprod. Dev. 51, 53-58. doi:10.1002/(SICI)1098-2795(199809)51:1,53::AIDMRD6.3.0. CO;2-V
62. 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. doi:10.1371/JOURNAL. PONE.0023183
63. Van Wagtendonk-De Leeuw, A. M., Den Daas, J. H., Kruip, T. A., and Rall, W. F. (1995). Comparison of the efficacy of conventional slow freezing and rapid cryopreservation methods for bovine embryos. Cryobiology 32, 157-167. doi:10.1006/CRYO.1995.1014
64. Viana, J. H. M., and Camargo, L. S. A. (2007). Bovine embryo production in Brazil: a new scenario. Acta Sci. Vet. 35, 915-924.
65. Visintin, J. A., Martins, J. F., Bevilacqua, E. M., Mello, M. R., Nicácio, A. C., and Assumpção, M. E. (2002). Cryopreservation of Bos taurus vs Bos indicus embryos: are they really different? Theriogenology 57, 345-359. doi:10.1016/S0093-691X(01)00675-6
66. 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
67. Walter, B. M. T., and Sampaio, A. B. (1998). 'A vegetação da fazenda Sucupira.' (Embrapa Recursos Genéticos e Biotecnologia: Brasília.)
68. Wathes, D. C., Abayasekara, D. R., and Aitken, R. J. (2007). Polyunsaturated fatty acids in male and female reproduction. Biol. Reprod. 77, 190-201. doi:10.1095/BIOLREPROD.107.060558
69. 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
70. Zeron, Y., Ocheretny, A., Kedar, O., Borochov, A., Sklan, D., and Arav, A. (2001). Seasonal changes in bovine fertility: relation to developmental competence of oocytes, membrane properties and fatty acid composition of follicles. Reproduction 121, 447-454. doi:10.1530/REP.0.1210447
71. 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