Follicular fluid supplementation during in vitro maturation promotes sperm penetration in bovine oocytes by enhancing cumulus expansion and increasing mitochondrial activity in oocytes

Reproduction, Fertility and Development

Volumn 24, Issue 5, 2012, Pages 743-752

  Somfai, Tams ^a   Inaba, Yasushi ^a   Watanabe, Shinya ^a   Geshi, Masaya ^a   Nagai, Takashi ^a  

^a NATIONAL INSTITUTE OF LIVESTOCK AND GRASSLAND SCIENCE   (Japan)

Author keywords

ATP; fertilisation; follicle fluid; mitochondria.

Indexed keywords

ADENOSINE TRIPHOSPHATE; BOVINE SERUM ALBUMIN; POVIDONE;

ANIMAL CELL; ARTICLE; CELL ACTIVITY; CELL STRESS; CONTROLLED STUDY; CUMULUS CELL; EMBRYO DEVELOPMENT; FEMALE; FERTILIZATION IN VITRO; IN VITRO OOCYTE MATURATION; MITOCHONDRION; NONHUMAN; OVARY FOLLICLE FLUID; REPRODUCTION; SPERMATOZOON PENETRATION;

ANIMALS; CATTLE; CELL PROLIFERATION; CELLS, CULTURED; CULTURE MEDIA; CUMULUS CELLS; FEMALE; FERTILIZATION IN VITRO; FOLLICULAR FLUID; IN VITRO OOCYTE MATURATION TECHNIQUES; MALE; MITOCHONDRIA; OOCYTES; SPERM-OVUM INTERACTIONS;

EID: 84867537515     PISSN: 10313613     EISSN: 14485990     Source Type: Journal    
DOI: 10.1071/RD11251     Document Type: Article

References (44)

1. Abramoff, M. D., Magelhaes, P. J., and Ram, S. J. (2004). Image processing with ImageJ. Biophoton. Int. 11, 36-42.
2. Ali, A., and Sirard, M. A. (2002). Effect of the absence or presence of various protein supplements on further development of bovine oocytes during in vitro maturation. Biol. Reprod. 66, 901-905. doi:10.1095/BIOLREPROD66.4.901 (Pubitemid 34263108)
3. Ali, A., Coenen, K., Bousquet, D., and Sirard, M.A. (2004). Origin of bovine follicular fluid and its effect during in vitro maturation on the developmental competence of bovine oocytes. Theriogenology 62, 1596-1606. doi:10.1016/J.THERIOGENOLOGY.2004.03.011 (Pubitemid 39415749)
4. Assidi, M., Dufort, I., Ali, A., Hamel, M., Algriany, O., Dielemann, S., and Sirard, M. A. (2008). Identification of potential markers of oocyte competence expressed in bovine cumulus cells matured with follicle-stimulating hormone and/or phorbol myristate acetate in vitro. Biol. Reprod. 79, 209-222. doi:10.1095/BIOLREPROD.108.067686
5. Bettegowda, A., Patel, O. V., Lee, K. B., Park, K. E., Salem, M., Yao, J., Ireland, J. J., and Smith, G. W. (2008). Identification of novel bovine cumulus cell molecular markers predictive of oocyte competence: functional and diagnostic implications. Biol. Reprod. 79, 301-309. doi:10.1095/BIOLREPROD.107. 067223
6. Brackett, B. G., and Oliphant, G. (1975). Capacitation of rabbit spermatozoa in vitro. Biol. Reprod. 12, 260-274. doi:10.1095/BIOLREPROD12.2.260
7. Brevini, T. A., Vassena, R., Francisci, C., and Gandolfi, F. (2005). Role of adenosine triphosphate, active mitochondria and microtubules in the acquisition of developmental competence of parthenogenetically activated pig oocytes. Biol. Reprod. 72, 1218-1223. doi:10.1095/BIOLREPROD.104.038141 (Pubitemid 40547986)
8. Carolan, C., Lonergan, P., Monget, P., Monniaux, D., and Mermillod, P. (1996). Effect of follicle size and quality on the ability of follicular fluid to support cytoplasmic maturation of bovine oocytes. Mol. Reprod. Dev. 43, 477-483. doi:10.1002/(SICI)1098-2795(199604)43:4<477::AID-MRD10>3.0.CO;2-X (Pubitemid 26110813)
9. Cha, K. Y., Koo, J. J., Ko, J. J., Choi, D. H., Han, S. Y., and Yoon, T. K. (1991). Pregnancy after in vitro fertilization of human follicular oocytes collected from nonstimulated cycles, their culture in vitro and their transfer in a donor oocyte program. Fertil. Steril. 55, 109-113.
10. Combelles, C. M., Holick, E. A., Paolella, L. J., Walker, D. C., and Wu, Q. (2010). Profiling of superoxide dismutase isoenzymes in compartments of the developing bovine antral follicles. Reproduction 139, 871-881. doi:10.1530/REP-09-0390
11. Dumollard, R., Duchen, M., and Carroll, J. (2007). The roleofmitochondrial function in the oocyte and embryo. Curr. Top. Dev. Biol. 77, 21-49. doi:10.1016/S0070-2153(06)77002-8
12. Edwards, R. G. (1974). Follicular fluid. J. Reprod. Fertil. 37, 189-219. doi:10.1530/JRF.0.0370189
13. El-Raey, M., Geshi, M., Somfai, T., Kaneda, M., Hirako, M., Abdel-Ghaffar, A. E., Sosa, G. A., El-Roos, M. E., and Nagai, T. (2011). Evidence of melatonin synthesis in the cumulus-oocyte complexes and its role in enhancing oocyte maturation in vitro in cattle. Mol. Reprod. Dev. 78, 250-262. doi:10.1002/MRD.21295
14. El Shourbagy, S. H., Spikings, E. C., Freitas, M., and St John, J. C. (2006). Mitochondria directly influence fertilisation outcome in the pig. Reproduction 131, 233-245. doi:10.1530/REP.1.00551 (Pubitemid 43273683)
15. Furnus, C. C., de Matos, D. G., and Moses, D. F. (1998). Cumulus expansion during in vitro maturation of bovine oocytes: relationship with intracel-lular glutathione level and its role in subsequent embryo development. Mol. Reprod. Dev. 51, 76-83. doi:10.1002/(SICI)1098-2795(199809) 51:1<76::AID-MRD9>3.0.CO;2-T (Pubitemid 28372960)
16. Hyttel, P., Xu, K. P., Smith, S., and Greve, T. (1986). Ultrastructure of in vitro oocyte maturation in cattle. J. Reprod. Fertil. 78, 615-625. doi:10.1530/JRF.0.0780615 (Pubitemid 17179863)
17. Imai, K., Tagawa, M., Yoshioka, H., Matoba, S., Narita, M., Inaba, Y., Aikawa, Y., Ohtake, M., and Kobayashi, S. (2006). The efficiency of embryo production by ovum pick-up and in vitro fertilization in cattle. J. Reprod. Dev. 52(Suppl.), 19-29.
18. Iwata, H., Hashimoto, S., Ohota, M., Kimura, K., Shibano, K., and Miyake, M. (2004). Effects of follicle size and electrolytes and glucose in maturation medium on nuclear maturation and developmental competence of bovine oocytes. Reproduction 127, 159-164. doi:10.1530/REP.1. 00084 (Pubitemid 38312786)
19. Iwata, H., Inoue, J., Kimura, K., Kuge, T., Kuwayama, T., and Monji, Y. (2006). Comparison between the characteristics of follicular fluid and the developmental competence of bovine oocytes. Anim. Reprod. Sci. 91, 215-223. doi:10.1016/J.ANIREPROSCI.2005.04.006 (Pubitemid 41674538)
20. Iwata, H., Goto, H., Tanaka, H., Sakaguchi, Y., Kimura, K., Kuwayama, T., and Monji, Y. (2011). Effect of maternal age on mitochondrial DNA copy number, ATP content and IVF outcome of bovine oocytes. Reprod. Fertil. Dev. 23, 424-432. doi:10.1071/RD10133
21. Kadam, A. L., and Koide, S. S. (1990). Identification of hypoxanthine in bovine follicular fluid. J. Pharm. Sci. 79, 1077-1082. doi:10.1002/JPS. 2600791208
22. Khatir, H., Carolan, C., Lonergan, P., and Mermillod, P. (1997). Characterization of calf follicular fluid and its ability to support cytoplasmic maturation of cow and calf oocytes. J. Reprod. Fertil. 111, 267-275. doi:10.1530/JRF.0.1110267
23. 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. doi:10.1016/J.ANIREPROSCI.2006.10.006 (Pubitemid 46223532)
24. Leroy, J. L., Vanholder, T., Mateusen, B., Christophe, A., Opsomer, G., de Kruif, A., Genicot, G., and Van Soom, A. (2005). 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 (Pubitemid 41472474)
25. Reiter, R. J., Tan, D. X., Manchester, L. C., Paredes, S. D., Mayo, J. C., and Sainz, R. M. (2009). Melatonin and reproduction revisited. Biol. Reprod. 81, 445-456. doi:10.1095/BIOLREPROD.108.075655
26. Rizos, D., Ward, F., Duffy, P., Boland, M. P., and Lonergan, P. (2002). Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol. Reprod. Dev. 61, 234-248. doi:10.1002/MRD.1153 (Pubitemid 34037478)
27. Romero-Arredondo, A., and Seidel, G. E., Jr (1994). Effects of bovine follicular fluid on maturation of bovine oocytes. Theriogenology 41, 383-394. doi:10.1016/0093-691X(94)90074-S (Pubitemid 2040105)
28. Romero-Arredondo, A., and Seidel, G. E., Jr (1996). Effects of follicular fluid during in vitro maturation of bovine oocytes on in vitro fertilization and early embryonic development. Biol. Reprod. 55, 1012-1016. doi:10.1095/BIOLREPROD55.5.1012 (Pubitemid 26346534)
29. Rosenkrans, C. F., Jr, Zeng, G. Q., Mcnamara, G. T., Schoff, P. K., and First, N. L. (1993). Development of bovine embryos in vitro as affected by energy substrates. Biol. Reprod. 49, 459-462. doi:10.1095/BIOLRE PROD49.3.459 (Pubitemid 23259665)
30. Roth, Z., Meidan, R., Shaham-Albalancy, A., Braw-Tal, R., and Wolfenson, D. (2001). Delayed effect of heat stress on steroid production in mediumsized and preovulatory bovine follicles. Reproduction 121, 745-751. doi:10.1530/REP.0.1210745 (Pubitemid 32472060)
31. Schweigert, F. J., and Zucker, H. (1988). Concentrations of vitamin A, beta-carotene and vitamin E in individual bovine follicles of different quality. J. Reprod. Fertil. 82, 575-579. doi:10.1530/JRF.0.0820575 (Pubitemid 18083022)
32. Sirard, M. A., Roy, F., Patrick, B., Mermillod, P., and Guilbault, L. A. (1995). Origin of the follicular fluid added to the media during bovine IVM influences embryonic development. Theriogenology 44, 85-94. doi:10.1016/0093- 691X(95)00150-7
33. Stojkovic, M., Machado, S. A., Stojkovic, P., Zakhartchenko, V., Hutzler, P., Gonçalves, 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. doi:10.1095/BIOLREPROD64.3.904 (Pubitemid 32174063)
34. Sun, Q. Y., Wu, G. M., Lai, L., Park, K. W., Cabot, R., Cheong, H. T., Day, B. N., Prather, R. S., and Schatten, H. (2001). Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro. Reproduction 122, 155-163. doi:10.1530/REP.0.1220155 (Pubitemid 32677159)
35. Van Blerkom, J. (2009). Mitochondria in early mammalian development. Semin. Cell Dev. Biol. 20, 354-364. doi:10.1016/J.SEMCDB.2008. 12.005
36. Van Blerkom, J., and Davis, P. (2007). Mitochondrial signalling and fertilization. Mol. Hum. Reprod. 13, 759-770. doi:10.1093/MOLEHR/GAM068 (Pubitemid 350131349)
37. Van Blerkom, J., and Runner, M. N. (1984). Mitochondrial reorganization during resumption of arrested meiosis in the mouse oocyte. Am. J. Anat. 171, 335-355. doi:10.1002/AJA.1001710309 (Pubitemid 15189965)
38. Van Blerkom, J., Davis, P., and Lee, J. (1995). ATP content of human oocytes and developmental potential and outcome after in vitro fertilization and embryo transfer. Hum. Reprod. 10, 415-424.
39. 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. doi:10.1093/HUMREP/16.5.909 (Pubitemid 32451826)
40. Wise, T. (1987). Biochemical analysis of bovine follicular fluid: albumin, total protein, lysosomal enzymes, ions, steroids and ascorbic acid content in relation to follicular size, rank, atresia classification and day of oestrous cycle. J. Anim. Sci. 64, 1153-1169.
41. Wolfenson, D., Lew, B. J., Thatcher, W. W., Graber, Y., and Meidan, R. (1997). Seasonal and acute heat-stress effects on steroid production by dominant follicles in cows. Anim. Reprod. Sci. 47, 9-19. doi:10.1016/S0378-4320(96) 01638-7 (Pubitemid 27269099)
42. Yu, Y., Dumollard, R., Rossbach, A., Lai, F. A., and Swann, K. (2010). Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation. J. Cell. Physiol. 224, 672-680. doi:10.1002/JCP.22171
43. 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 (Pubitemid 32248669)
44. Zhu, X. M., Zhu, Y. M., Xu, C. M., Qian, Y. L., Jin, F., and Huang, H. F. (2008). Autologous mature follicular fluid: its role in in vitro maturation of human cumulus-removed oocytes. Fertil. Steril. 90, 1094-1102. doi:10.1016/J.FERTNSTERT.2007.07.1323