Similar articles

Abstract: oocyte quality has long been considered as a main limiting factor for in vitro fertilization (IVF). In the past decade, extensive observations demonstrated that the mitochondrion plays a vital role in the oocyte cytoplasm, for it can provide adenosine triphosphate (ATP) for fertilization and preimplantation embryo development and also act as stores of intracellular calcium and proapoptotic factors. During the oocyte maturation, mitochondria are characterized by distinct changes of their distribution pattern from being homogeneous to heterogeneous, which is correlated with the cumulus apoptosis. oocyte quality decreases with the increasing maternal age. Recent studies have shown that low quality oocytes have some age-related dysfunctions, which include the decrease in mitochondrial membrane potential, increase of mitochondrial DNA (mtDNA) damages, chromosomal aneuploidies, the incidence of apoptosis, and changes in mitochondrial gene expression. All these dysfunctions may cause a high level of developmental retardation and arrest of preimplantation embryos. It has been suggested that these mitochondrial changes may arise from excessive reactive oxygen species (ROS) that is closely associated with the oxidative energy production or calcium overload, which may trigger permeability transition pore opening and subsequent apoptosis. Therefore, mitochondria can be seen as signs for oocyte quality evaluation, and it is possible that the oocyte quality can be improved by enhancing the physical function of mitochondria. Here we reviewed recent advances in mitochondrial functions on oocytes.

[1] Albertini, D.F., Combelles, C.M., Benecchi, E., Carabatsos, M.J., 2001. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction, 121(5): 647-653.

[2] Andreuccetti, P., Iodice, M., Prisco, M., Gualtieri, R., 1999. Intercellular bridges between granulosa cells and the oocyte in the elasmobranch Raya asterias. Anat. Rec., 255(2):180-187.

[3] Anson, R.M., Croteau, D.L., Stierum, R.H., Filburn, C., Parsell, R., Bohr, V.A., 1998. Homogenous repair of singlet oxygen-induced DNA damage in differentially transcribed regions and strands of human mitochondrial DNA. Nucleic Acids Res., 26(2):662-668.

[4] Armstrong, J.S., 2007. Mitochondrial medicine: pharmacological targeting of mitochondria in disease. Br. J. Pharmacol., 151(8):1154-1165.

[5] Berridge, M.J., Lipp, P., Bootman, M.D., 2000. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol., 1:11-21.

[6] Beutner, G., Rück, A., Riede, B., Brdiczka, D., 1998. Complexes between porin, hexokinase, mitochondrial creatine kinase and adenylate translocator display properties of the permeability transition pore. Implication for regulation of permeability transition by the kinases. Biochim. Biophys. Acta, 1368:7-18.

[7] Blondin, P., Sirard, M.A., 1995. Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes. Mol. Reprod. Dev., 41(1): 54-62.

[8] Bootman, M.D., Collins, T.J., Peppiatt, C.M., Prothero, L.S., MacKenzie, L., de Smet, P., Travers, M., Tovey, S.C., Seo, J.T., Berridge, M.J., Ciccolini, F., Lipp, P., 2001. Calcium signalling—an overview. Semin. Cell Dev. Biol., 12(1):3-10.

[9] Bu, S., Xia, G., Tao, Y., Lei, L., Zhou, B., 2003. Dual effects of nitric oxide on meiotic maturation of mouse cumulus cell-enclosed oocytes in vitro. Mol. Cell. Endocrinol., 207(1-2):21-30.

[10] Buchholz, J.N., Behringer, E.J., Pottorf, W.J., Pearce, W.J., Vanterpool, C.K., 2007. Age-dependent changes in Ca²⁺ homeostasis in peripheral neurones: implications for changes in function. Aging Cell, 6(3):285-296.

[11] Chakraborti, T., Das, S., Mondal, M., Roychoudhury, S., Chakraborti, S., 1999. Mitochondria and calcium: from cell signalling to cell death. Cell. Signal., 11(2):77-85.

[12] Cohen, J., Scott, R., Alikani, M., Schimmel, T., Munné, S., Levron, J., Wu, L., Brenner, C., Warner, C., Willadsen, S., 1998. Ooplasmic transfer in mature human oocytes. Mol. Hum. Reprod., 4(3):269-280.

[13] Cox, R.T., Spradling, A.C., 2003. A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development, 130(8):1579-1590.

[14] Cox, R.T., Spradling, A.C., 2006. Milton controls the early acquisition of mitochondria by Drosophila oocytes. Development, 133(17):3371-3377.

[15] Crompton, M., 1999. The mitochondrial permeability transition pore and its role in cell death. Biochem. J., 341(2): 233-249.

[16] Cummins, J.M., Wakayama, T., Yanagimachi, R., 1997. Fate of microinjected sperm components in the mouse oocyte and embryo. Zygote, 5(4):301-308.

[17] Dubec, S.J., Aurora, R., Zassenhaus, H.P., 2008. Mitochondrial DNA mutations may contribute to aging via cell death caused by peptides that induce cytochrome-c release. Rejuvenation Res., 11(3):611-619.

[18] Duranthon, V., Renard, J.P., 2001. The developmental competence of mammalian oocytes: a convenient but biologically fuzzy concept. Theriogenology, 55(6):1277-1289.

[19] Eichenlaub-Ritter, U., 1998. Genetics of oocyte ageing. Maturitas, 30(2):143-169.

[20] Eppig, J.J., 1996. Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals. Reprod. Fertil. Dev., 8(4):485-489.

[21] Fan, W.M., Kou, H., Shen, D.J., LeRoy, E.C., 1998. Identification of altered expression of ADP/ATP translocase during cellular senescence in vitro. Exp. Gerontol., 33(5):457-465.

[22] Fulka, J.J., First, N.L., Moor, R.M., 1998. Nuclear and cytoplasmic determinants involved in the regulation of mammalian oocyte maturation. Mol. Hum. Reprod., 4(1):41-49.

[23] Galat, A., Metcalfe, S.M., 1995. Peptidylproline cis/trans isomerases. Prog. Biophys. Mol. Biol., 63(1):67-118.

[24] Giacomello, M., Drago, I., Pizzo, P., Pozzan, T., 2007. Mitochondrial Ca²⁺ as a key regulator of cell life and death. Cell Death Differ., 14(7):1267-1274.

[25] Gilchrist, R.B., Lane, M., Thompson, J.G., 2008. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum. Reprod. Update, 14(2):159-177.

[26] Golsteyn, R.M., Schultz, S.J., Bartek, J., Ziemiecki, A., Ried, T., Nigg, E.A., 1994. Cell cycle analysis and chromosomal localization of human Plk1, a putative homologue of the mitotic kinases Drosophila polo and Saccharomyces cerevisiae Cdc5. J. Cell Sci., 107(Pt 6):1509-1517.

[27] Grijalba, M.T., Vercesi, A.E., Schreier, S., 1999. Ca²⁺ induced increased lipid packing and domain formation in submitochondrial particles. A possible step in the mechanism of Ca²⁺ stimulated generation of reactive oxygen species by the respiratory chain. Biochemistry, 38(40):13279-13287.

[28] Haghdoost, S., Czene, S., Näslund, I., Skog, S., Harms-Ringdahl, M., 2005. Extracellular 8-oxo-dG as a sensitive parameter for oxidative stress in vivo and in vitro. Free Radic. Res., 39(2):153-162.

[29] He, L., Lemasters, J.J., 2002. Regulated and unregulated mitochondrial permeability transition pores: a new paradigm of pore structure and function? FEBS Lett., 512(1-3):1-7.

[30] Hsieh, R.H., Au, H.K., Yeh, T.S., Chang, S.J., Cheng, Y.F., Tzeng, C.R., 2004. Decreased expression of mitochondrial genes in human unfertilized oocytes and arrested embryos. Fertil. Steril., 81(Suppl. 1):912-918.

[31] Hussein, T.S., Froiland, D.A., Amato, F., Thompson, J.G., Gilchrist, R.B., 2005. Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J. Cell Sci., 118(22):5257-5268.

[32] Ichas, F., Laurence, S., Jouaville, L.S., 1997. Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals. Cell, 89(7):1145-1153.

[33] Kaneda, H., Hayashi, J.I., Takahama, S., Taya, C., Lindahl, K.F., Yonekawa, H., 1995. Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. Proc. Natl. Acad. Sci. USA, 92(10):4542-4546.

[34] Kinnally, K.W., Antonsson, B., 2007. A tale of two mitochondrial channels, MAC and PTP, in apoptosis. Apoptosis, 12(5):857-868.

[35] Kong, L.H., Liu, Z., Li, H., Zhu, L., Chen, S.M., Chen, S.L., Xing, F.Q., 2004. Mitochondria transfer from self-granular cells to improve embryos’ quality. Zhonghua Fu Chan Ke Za Zhi, 39(2):105-107 (in Chinese).

[36] Krisher, R.L., 2004. The effect of oocyte quality on development. J. Anim. Sci., 82(E-Suppl):E14-E23.

[37] Kujoth, G.C., Hiona, A., Pugh, T.D., Someya, S., Panzer, K., Wohlgemuth, S.E., Hofer, T., Seo, A.Y., Sullivan, R., Jobling, W.A., et al., 2005. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science, 309(5733):481-484.

[38] Lonergan, T., Bavister, B., Brenner, C., 2007. Mitochondria in stem cells. Mitochondrion, 7(5):289-296.

[39] López-Lluch, G., Irusta, P.M., Navas, P., de Cabo, R., 2008. Mitochondrial biogenesis and healthy aging. Exp. Gerontol., 43(9):813-819.

[40] Machaty, Z., Funahashi, H., Day, B.N., Prather, R.S., 1997. Developmental changes in the intracellular Ca²⁺ release mechanisms in porcine oocytes. Biol. Reprod., 56(4): 921-930.

[41] Malter, H.E., Cohen, J., 2002. Ooplasmic transfer: animal models assist human studies. Reprod. Biomed. Online, 5(1):26-35.

[42] Mather, M., Hagai Rottenberg, H., 2000. Aging enhances the activation of the permeability transition pore in mitochondria. Biochem. Biophys. Res. Commun., 273(2): 603-608.

[43] Meißner, C., von Wurmb, N., Oehmichen, M., 1997. Detection of the age-dependent 4977 bp deletion of mitochondrial DNA. A pilot study. Int. J. Legal Med., 110(5):288-291.

[44] Mermillod, P., Dalbiès-Tran, R., Uzbekova, S., Thélie, A., Traverso, J.M., Perreau, C., Papillier, P., Monget, P., 2008. Factors affecting oocyte quality: who is driving the follicle? Reprod. Domest. Anim., 43(Suppl. 2):393-400.

[45] Munne, S., Sultan, K.M., Weier, H.U.G., Grifo, J.A., Cohen, J., Rosenwaks, Z., 1995. Assessment of numerical abnormalities of X, Y, 18 and 16 chromosomes in preimplantation of human embryos prior to transfer. Am. J. Obstet. Gynecol., 172(4):1191-1201.

[46] Nagai, S., Mabuchi, T., Hirata, S., Shoda, T., Kasai, T., Yokota, S., Shitara, H., Yonekawa, H., Hoshi, K., 2006. Correlation of abnormal mitochondrial distribution in mouse oocytes with reduced developmental competence. Tohoku J. Exp. Med., 210(2):137-144.

[47] Nishi, Y., Takeshita, T., Sato, K., Araki, T., 2003. Change of the mitochondrial distribution in mouse ooplasm during in vitro maturation. J. Nippon Med. Sch., 70(5):408-415.

[48] Ott, M., Gogvadze, V., Orrenius, S., Zhivotovsky, B., 2007. Mitochondria, oxidative stress and cell death. Apoptosis, 12(5):913-922.

[49] Ottolenghi, C., Uda, M., Hamatani, T., Crisponi, L., Garcia, J.E., Ko, M., Pilia, G., Sforza, C., Schlessinger, D., Forabosco, A., 2004. Aging of oocyte, ovary, and human reproduction. Ann. N. Y. Acad. Sci., 1034(1):117-131.

[50] Pahlavan, G., Polanski, Z., Kalab, P., Golsteyn, R., Nigg, E.A., Maro, B., 2000. Characterization of polo-like kinase 1 during meiotic maturation of the mouse oocyte. Dev. Biol., 220(2):392-400.

[51] Pastorino, J.G., Shulga, N., Hoek, J.B., 2002. Mitochondrial binding of hexokinase II inhibits Bax-induced cytochrome c release and apoptosis. J. Biol. Chem., 277(9): 7610-7618.

[52] Pinkert, C.A., Irwin, M.H., Johnson, L.W., Moffatt, R.J., 1997. Mitochondria transfer into mouse ova by microinjection. Transgenic Research, 6(6):379-383.

[53] Qiao, T.W., Liu, N., Miao, D.Q., Zhang, X., Han, D., Ge, L., Tan, J.H., 2008. Cumulus cells accelerate aging of mouse oocytes by secreting a soluble factor(s). Mol. Reprod. Dev., 75(3):521-528.

[54] Reynier, P., May-Panloup, P., Chrétien, M.F., Morgan, C.J., Jean, M., Savagner, F., Barrière, P., Malthièry, Y., 2001. Mitochondrial DNA content affects the fertilizability of human oocytes. Mol. Hum. Reprod., 7(5):425-429.

[55] Robertson, J.A., 1998. Oocyte cytoplasm transfers and the ethics of germ-line intervention. J. Law Med. Ethics, 26(3):211-220, 179.

[56] Rottenberg, H., Shaolong, W., 1997. Mitochondrial dysfunction in lymphocytes from old mice: enhanced activation of the permeability transition. Biochem. Biophys. Res. Commun., 240(1):68-74.

[57] Sharov, A.A., Falco, G., Piao, Y., Poosala, S., Becker, K.G., Zonderman, A.B., Longo, D.L., Schlessinger, D., Ko, M.S., 2008. Effects of aging and calorie restriction on the global gene expression profiles of mouse testis and ovary. BMC Biol., 6(1):24.

[58] Smaili, S.S., Hsu, Y.T., Youle, R.J., Russell, J.T., 2000. Mitochondria in Ca²⁺ signaling and apoptosis. J. Bioenerg. Biomembr., 32(1):35-46.

[59] Spikings, E.C., Alderson, J., St. John, J.C., 2007. Regulated mitochondrial DNA replication during oocyte maturation is essential for successful porcine embryonic development. Biol. Reprod., 76(2):327-335.

[60] Takahashi, A., Masuda, A., Sun, M., Centonze, V.E., Herman, B., 2004. Oxidative stress-induced apoptosis is associated with alterations in mitochondrial caspase activity and Bcl-2-dependent alterations in mitochondrial pH (pHm). Brain Res. Bull., 62(6):497-504.

[61] Tarín, J.J., 1996. Potential effects of age-associated oxidative stress on mammalian oocytes/embryos. Mol. Hum. Reprod., 2(10):717-724.

[62] Thouas, G.A., Trounson, A.O., Wolvetang, E.J., Jones, G.M., 2004. Mitochondrial dysfunction in mouse oocytes results in preimplantation embryo arrest in vitro. Biol. Reprod., 71(6):1936-1942.

[63] Torner, H., Brüssow, K.P., Alm, H., Ratky, J., Pöhland, R., Tuchscherer, A., Kanitz, W., 2004. Mitochondrial aggregation patterns and activity in porcine oocytes and apoptosis in surrounding cumulus cells depends on the stage of pre-ovulatory maturation. Theriogenology, 61(9):1675-1689.

[64] Trifunovic, A., Hansson, A., Wredenberg, A., Rovio, A.T., Dufour, E., Khvorostov, I., Spelbrink, J.N., Wibom, R., Jacobs, H.T., Larsson, N.G., 2005. Somatic mtDNA mutations cause aging phenotypes without affecting reactive oxygen species production. Proc. Natl. Acad. Sci. USA, 102(50):17993-17998.

[65] Tsujimoto, Y., Shimizu, S., 2007. Role of the mitochondrial membrane permeability transition in cell death. Apoptosis, 12(5):835-840.

[66] van Blerkom, J., 1991. Microtubule mediation of cytoplasmic and nuclear maturation during the early stages of resumed meiosis in cultured mouse oocyte. Proc. Natl. Acad. Sci. USA, 88(11):5031-5035.

[67] van Blerkom, J., 2008. Mitochondria as regulatory forces in oocytes, preimplantation embryos and stem cells. Reprod. Biomed. Online, 16:553-569.

[68] van Blerkom, J., Davis, P., 2006. High-polarized (Delta Psi m(HIGH)) mitochondria are spatially polarized in human oocytes and early embryos in stable subplasmalemmal domains: developmental significance and the concept of vanguard mitochondria. Reprod. Biomed. Online, 13(2): 246-254.

[69] van Blerkom, J., Davis, P., 2007. Mitochondrial signaling and fertilization. Mol. Hum. Reprod., 13(11):759-770.

[70] van Blerkom, J., Davis, P., Alexander, S., 2003. Inner mitochondrial membrane potential (DeltaPsim), cytoplasmic ATP content and free Ca²⁺ levels in metaphase II mouse oocytes. Hum. Reprod., 18(11):2429-2440.

[71] van Blerkom, J., Cox, H., Davis, P., 2006. Regulatory roles for mitochondria in the peri-implantation mouse blastocyst: possible origins and developmental significance of differential ∆ψ_m. Reproduction, 131(5):961-976.

[72] van Blerkom, J., Davis, P., Thalhammer, V., 2008. Regulation of mitochondrial polarity in mouse and human oocytes: the influence of cumulus derived nitric oxide. Mol. Hum. Reprod., 14(8):431-444.

[73] Vermulst, M., Wanagat, J., Kujoth, G.C., Bielas, J.H., Rabinovitch, P.S., Prolla, T.A., Loeb, L.A., 2008. DNA deletions and clonal mutations drive premature aging in mitochondrial mutator mice. Nat. Genet., 40(4):392-394.

[74] Vieira, H.L., Haouzi, D., El Hamel, C., Jacotot, E., Belzacq, A.S., Brenner, C., Kroemer, G., 2000. Permeabilization of the mitochondrial inner membrane during apoptosis: impact of the adenine nucleotide translocator. Cell Death Differ., 7(12):1146-1154.

[75] Voznesenskaya, T.Y., Blashkiv, T.V., 2005. Estradiol-dependent effect of nitric oxide on meiotic maturation of mouse oocytes. Bull. Exp. Biol. Med., 140(4):378-380.

[76] Vyssokikh, M.Y., Brdiczka, D., 2003. The function of complexes between the outer mitochondrial membrane pore (VDAC) and the adenine nucleotide translocase in regulation of energy metabolism and apoptosis. Acta Biochim. Pol., 50(2):389-404.

[77] Wang, J., Lü, Y.Y., 2009. Mitochondrial DNA 4977-bp deletion correlated with reactive oxygen species production and manganese superoxide dismutase expression in gastric tumor cells. Chin. Med. J. (Engl.), 122(4):431-436.

[78] Whitaker, M., 2008. Calcium signalling in early embryos. Philosophical Transactions of The Royal Society B Biological Sciences, 363(1495):1401-1418.

[79] Wilding, M., Dale, B., Marino, M., di Matteo, L., Alviggi, C., Pisaturo, M.L., Lombardi, L., de Placido, G., 2001. Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum. Reprod., 16(5):909-917.

[80] Wu, J., Zhang, L., Wang, X., 2000. Maturation and apoptosis of human oocytes in vitro are age-related. Fertil. Steril., 74(6):1137-1141.

[81] Yesodi, V., Yaron, Y., Lessing, J.B., Amit, A., Ben-Yosef, D., 2002. The mitochondrial DNA mutation (ΔmtDNA⁵²⁸⁶) in human oocytes: correlation with age and IVF outcome. J. Assist. Reprod. Genet., 19(2):60-66.

[82] Yi, Y.C., Chen, M.J., Ho, J.Y., Guu, H.F., Ho, E.S., 2007. Mitochondria transfer can enhance the murine embryo development. J. Assist. Reprod. Genet., 24(10):445-449.

[83] Yin, H., Baart, E., Betzendahl, I., Eichenlaub-Ritter, U., 1998. Diazepam induces meiotic delay, aneuploidy and predivision of homologues and chromatids in mammalian oocytes. Mutagenesis, 13(6):567-580.

[84] Zhang, X., Wu, X.Q., Lu, S., Guo, Y.L., Ma, X., 2006. Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles. Cell Res., 16(10): 841-850.