Follicular fluid supplementation during in vitro maturation promotes sperm penetration in bovine oocytes by enhancing cumulus expansion and increasing mitochondrial activity in oocytes
Tamás Somfai A , Yasushi Inaba A , Shinya Watanabe A , Masaya Geshi A B and Takashi Nagai A
+ Author Affiliations
- Author Affiliations
A NARO Institute of Livestock and Grassland Science, National Agriculture and Food Research Organisation, Tsukuba, Ibaraki 305-0901, Japan.
B Corresponding author. Email: geshi@affrc.go.jp
Reproduction, Fertility and Development 24(5) 743-752 https://doi.org/10.1071/RD11251
Submitted: 28 September 2011 Accepted: 25 November 2011 Published: 6 January 2012
Abstract
The aim of this study was to examine the effects of bovine follicular fluid (bFF) on mitochondrial activity in in vitro-matured (IVM) oocytes and to assess its importance for fertilisation and embryo development. Bovine follicular oocytes were subjected to IVM in medium supplemented either with polyvinylpyrrolidone, bovine serum albumin, calf serum or bFF. Nuclear maturation, cumulus expansion, mitochondrial distribution and ATP content in oocytes were compared between groups along with subsequent in vitro fertilisation (IVF) and embryo development. Compared with other supplements, bFF generated significantly enhanced re-distribution of active mitochondria in oocytes and this effect was associated with elevated intracellular ATP content. Furthermore, bFF significantly improved cumulus expansion, which was associated with improved fertilisation rates when cumulus-enclosed oocytes were subjected to IVF; however, its promoting effect was neutralised when denuded oocytes were inseminated. Elevating ATP content in oocytes by bFF did not affect maturation or embryo development but promoted fertilisation when mitochondrial electron transport was blocked in oocytes before IVF by Rotenone. In conclusion, supplementation of IVM medium with bFF promotes sperm penetration both by the improvement of cumulus expansion and by enhancing ATP levels in oocytes, which maintains their ability to be fertilised after mitochondrial stress.
Additional keywords: ATP, fertilisation, follicle fluid, mitochondria.
References
Abramoff, M. D., Magelhaes, P. J., and Ram, S. J. (2004). Image processing with ImageJ. Biophoton. Int. 11, 36–42.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.
| Effect of the absence or presence of various protein supplements on further development of bovine oocytes during in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitlCltLs%3D&md5=eebc9f0f9295e3f45db4d3ee03108938CAS | 11906907PubMed |
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.
| Origin of bovine follicular fluid and its effect during in vitro maturation on the developmental competence of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 15511547PubMed |
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.
| Identification of potential markers of oocyte competence expressed in bovine cumulus cells matured with follicle-stimulating hormone and/or phorbol myristate acetate in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovFWms7o%3D&md5=febdab62ad9178fa90b61fa272bb4d9eCAS | 18417710PubMed |
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.
| Identification of novel bovine cumulus cell molecular markers predictive of oocyte competence: functional and diagnostic implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovFWmsLo%3D&md5=4306ff16e4a62e04366fd8a5a3dad6e4CAS | 18417713PubMed |
Brackett, B. G., and Oliphant, G. (1975). Capacitation of rabbit spermatozoa in vitro. Biol. Reprod. 12, 260–274.
| Capacitation of rabbit spermatozoa in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28Xnt1WltQ%3D%3D&md5=aaf56920baf0ad059c9c2b3065662c71CAS | 1122333PubMed |
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.
| Role of adenosine triphosphate, active mitochondria and microtubules in the acquisition of developmental competence of parthenogenetically activated pig oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjslSntrc%3D&md5=7c4df6d81dde7ca92fcebffab9c59e59CAS | 15659704PubMed |
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.
| Effect of follicle size and quality on the ability of follicular fluid to support cytoplasmic maturation of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XitVGjs7Y%3D&md5=165807c4f7bfd2ed86a0a357dd1e10f4CAS | 9052939PubMed |
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.
| 1:STN:280:DyaK3M%2FpvFGgug%3D%3D&md5=fe96c81c50b84b7204e0e7e509f7223bCAS | 1986950PubMed |
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.
| Profiling of superoxide dismutase isoenzymes in compartments of the developing bovine antral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmvVCgsLk%3D&md5=2002c3b8180f30c78e4c59ee6ee79b73CAS | 20197373PubMed |
Dumollard, R., Duchen, M., and Carroll, J. (2007). The role of mitochondrial function in the oocyte and embryo. Curr. Top. Dev. Biol. 77, 21–49.
| The role of mitochondrial function in the oocyte and embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmt1Gltb4%3D&md5=399fc81e5dd96afe8b28a999ade3f472CAS | 17222699PubMed |
Edwards, R. G. (1974). Follicular fluid. J. Reprod. Fertil. 37, 189–219.
| Follicular fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXltVait7g%3D&md5=85100bce2af2dda5574f865c3b861d7eCAS | 4274030PubMed |
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.
| Evidence of melatonin synthesis in the cumulus–oocyte complexes and its role in enhancing oocyte maturation in vitro in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkvFajurc%3D&md5=2f874545a0effd756ec831aca500a617CAS | 21381146PubMed |
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.
| Mitochondria directly influence fertilisation outcome in the pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFalsL4%3D&md5=f9a37ec7bfb12652f4929760602aafeaCAS | 16452717PubMed |
Furnus, C. C., de Matos, D. G., and Moses, D. F. (1998). Cumulus expansion during in vitro maturation of bovine oocytes: relationship with intracellular glutathione level and its role in subsequent embryo development. Mol. Reprod. Dev. 51, 76–83.
| Cumulus expansion during in vitro maturation of bovine oocytes: relationship with intracellular glutathione level and its role in subsequent embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXltVGrsLk%3D&md5=136f10b83527ed975fa92e5fb5f23ee9CAS | 9712320PubMed |
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.
| Ultrastructure of in vitro oocyte maturation in cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s7ht1equg%3D%3D&md5=75cee80d377e77c6eb8817a243d6ab0cCAS | 3806520PubMed |
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, 19–29.
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.
| Effects of follicle size and electrolytes and glucose in maturation medium on nuclear maturation and developmental competence of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXitVWrt7w%3D&md5=0f03839c554b0fcf4b55c69271dd902bCAS | 15056781PubMed |
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.
| Comparison between the characteristics of follicular fluid and the developmental competence of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Gns7jM&md5=68a0a20ec26d5caec65f4462c304dcd5CAS | 15961265PubMed |
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.
| Effect of maternal age on mitochondrial DNA copy number, ATP content and IVF outcome of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjt12nt7s%3D&md5=7e9c27a24f9c921b6e4db3a47e02a02bCAS | 21426860PubMed |
Kadam, A. L., and Koide, S. S. (1990). Identification of hypoxanthine in bovine follicular fluid. J. Pharm. Sci. 79, 1077–1082.
| Identification of hypoxanthine in bovine follicular fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXjvFOlsA%3D%3D&md5=221f509ef3e1995d803ffbaeabc29d2eCAS | 2079654PubMed |
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.
| Characterization of calf follicular fluid and its ability to support cytoplasmic maturation of cow and calf oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlsFertg%3D%3D&md5=fa55a2351efbb6e961a5903d71c60a30CAS | 9462295PubMed |
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=2626cb806f94d99db8b5ddd7b6c003c5CAS | 17110061PubMed |
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.
| Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFent7rJ&md5=70c2d178c77a53da373a14e98e66eedfCAS | 16183866PubMed |
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.
| Melatonin and reproduction revisited.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVChu77F&md5=40931fc7729fe9d12c3c5f210dc50ae0CAS | 19439728PubMed |
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.
| Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xlt1Giug%3D%3D&md5=7e1cd9cffb7fc878404e93f2e0a29d94CAS | 11803560PubMed |
Romero-Arredondo, A., and Seidel, G. E. (1994). Effects of bovine follicular fluid on maturation of bovine oocytes. Theriogenology 41, 383–394.
| Effects of bovine follicular fluid on maturation of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVWmtg%3D%3D&md5=d75b24904bf638bcd6e2067feb4cbbe0CAS | 16727396PubMed |
Romero-Arredondo, A., and Seidel, G. E. (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.
| Effects of follicular fluid during in vitro maturation of bovine oocytes on in vitro fertilization and early embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xmtlalsrg%3D&md5=7745bfb2d5a7ca0bec56dc2b04d7952bCAS | 8902211PubMed |
Rosenkrans, C. F., 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.
| Development of bovine embryos in vitro as affected by energy substrates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlsFWk&md5=a5231f5d00bc660fd97a1a11cc3bcc8aCAS | 8399836PubMed |
Roth, Z., Meidan, R., Shaham-Albalancy, A., Braw-Tal, R., and Wolfenson, D. (2001). Delayed effect of heat stress on steroid production in medium-sized and preovulatory bovine follicles. Reproduction 121, 745–751.
| Delayed effect of heat stress on steroid production in medium-sized and preovulatory bovine follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktVaitrY%3D&md5=1e46fcccff514d9a57ee405837cc138dCAS | 11427162PubMed |
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.
| Concentrations of vitamin A, beta-carotene and vitamin E in individual bovine follicles of different quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXit1Slur4%3D&md5=1d0f87c789cb6092fae30603a5625d2aCAS | 3361492PubMed |
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.
| Origin of the follicular fluid added to the media during bovine IVM influences embryonic development.Crossref | GoogleScholarGoogle Scholar |
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.
| 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=6d2ac9c4e7dc9eb10db34f96f2204365CAS | 11207207PubMed |
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.
| Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsVGis7g%3D&md5=a2a51f2c512c3da8ce3ec6690bc4b53aCAS | 11425340PubMed |
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=725f42909e8a3d51e8163356b10c956aCAS | 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=06c5b4709c665b08682e4c73e34a2e55CAS | 17893093PubMed |
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.
| Mitochondrial reorganization during resumption of arrested meiosis in the mouse oocyte.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2M%2FpsVWhuw%3D%3D&md5=234da96c8edde07611bb93d7f454741bCAS | 6517035PubMed |
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.
| 1:STN:280:DyaK2M3os1OrtQ%3D%3D&md5=da91355e20abcf4da594e929c7419fa3CAS | 7769073PubMed |
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=06de26c3852ccb60655e91a16310184fCAS | 11331637PubMed |
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.
| 1:CAS:528:DyaL2sXhs12gs78%3D&md5=80d09a9e0c11b8cddf836961b50caafbCAS | 3571024PubMed |
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.
| Seasonal and acute heat-stress effects on steroid production by dominant follicles in cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXksVSku7o%3D&md5=b7eb8d08fc80e79659854e2dfadd1874CAS | 9233502PubMed |
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.
| Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXosVWntLo%3D&md5=c7e96b40e0c071c85e1c337000746281CAS | 20578238PubMed |
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.
| Seasonal changes in bovine fertility: relation to developmental competence of oocytes, membrane properties and fatty acid composition of follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXisFWjsrg%3D&md5=34be86524be3d375bf7f4f16283d9160CAS | 11226071PubMed |
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.
| Autologous mature follicular fluid: its role in in vitro maturation of human cumulus-removed oocytes.Crossref | GoogleScholarGoogle Scholar | 18001728PubMed |
