Mitochondrial functions on oocytes and preimplantation embryos

Journal of Zhejiang University: Science B

Volumn 10, Issue 7, 2009, Pages 483-492

  Wang, Li Ya ^a,b,c   Wang, Da Hui ^b   Zou, Xiang Yang ^a   Xu, Chen Ming ^c  

^a DALIAN MEDICAL UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c Zhejiang University School of Medicine   (China)

Author keywords

Mitochondria; Oocyte; Preimplantation embryo

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; ADENOSINE TRIPHOSPHATE; CALCIUM; INOSITOL 1,4,5 TRISPHOSPHATE; MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE; RYANODINE RECEPTOR;

APOPTOSIS; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL AGING; CELL FUNCTION; CELL INTERACTION; CUMULUS OOPHORUS; CYTOPLASM; EMBRYO DEVELOPMENT; ENDOPLASMIC RETICULUM; FERTILIZATION IN VITRO; GENE EXPRESSION; GENE MUTATION; HUMAN; MATERNAL AGE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; MITOCHONDRION; OOCYTE; OOCYTE MATURATION; OXIDATIVE STRESS; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; BLASTOCYST; EMBRYONIC DEVELOPMENT; HUMANS; MITOCHONDRIA; MODELS, BIOLOGICAL; OOCYTES;

EID: 67650617645     PISSN: 16731581     EISSN: 18621783     Source Type: Journal    
DOI: 10.1631/jzus.B0820379     Document Type: Review

References (84)

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. [doi:10.1530/rep.0.1210647]
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. [doi:10.1002/ (SICI)1097-0185(19990601) 255:2<180::AID-AR8>3.3.CO;2-J]
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. [doi:10.1093/nar/26.2.662]
4. Armstrong, J.S., 2007. Mitochondrial medicine: Pharmacological targeting of mitochondria in disease. Br. J. Pharmacol., 151 (8):1154-1165. [doi:10.1038/sj.bjp.0707288]
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. [doi:10.1038/35036035]
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. [doi:10.1016/S0005-2736(97)00175-2]
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. [doi:10.1002/mrd.1080410109]
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. [doi:10.1006/scdb.2000.0211]
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. [doi:10.1016/ S0303-7207(03)00213-2]
10. 2+ homeostasis in peripheral neurones: Implications for changes in function. Aging Cell, 6 (3):285-296. [doi:10.1111/ j.1474-9726.2007.00298.x]
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. [doi:10.1016/S0898-6568(98)00025-4]
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. [doi:10.1093/molehr/4.3.269]
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. [doi:10.1242/dev.00365]
14. Cox, R.T., Spradling, A.C., 2006. Milton controls the early acquisition of mitochondria by Drosophila oocytes. Development, 133 (17):3371-3377. [doi:10.1242/dev.02514]
15. Crompton, M., 1999. The mitochondrial permeability transition pore and its role in cell death. Biochem. J., 341 (2): 233-249. [doi:10.1042/ 0264-6021:3410233]
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. [doi:10.1017/S0967199400003889]
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. [doi:10.1089/rej.2007.0617]
18. Duranthon, V., Renard, J.P., 2001. The developmental competence of mammalian oocytes: A convenient but biologically fuzzy concept. Theriogenology, 55 (6):1277-1289. [doi:10.1016/S0093-691X(01)00482-4]
19. Eichenlaub-Ritter, U., 1998. Genetics of oocyte ageing. Maturitas, 30 (2):143-169. [doi:10.1016/S0378-5122(98) 00070-X]
20. Eppig, J.J., 1996. Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals. Reprod. Fertil. Dev., 8 (4):485-489. [doi:10.1071/RD9960485]
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. [doi:10.1016/ S0531-5565(97)00093-4]
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. [doi:10.1093/molehr/4.1.41]
23. Galat, A., Metcalfe, S.M., 1995. Peptidylproline cis/trans isomerases. Prog. Biophys. Mol. Biol., 63 (1):67-118. [doi:10.1016/ 0079-6107(94)00009-X]
24. 2+ as a key regulator of cell life and death. Cell Death Differ., 14 (7):1267-1274. [doi:10.1038/sj.cdd. 4402147]
25. Gilchrist, R.B., Lane, M., Thompson, J.G., 2008. Oocytesecreted factors: regulators of cumulus cell function and oocyte quality. Hum. Reprod. Update, 14 (2):159-177. [doi:10.1093/humupd/dmm040]
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. 2+ stimulated generation of reactive oxygen species by the respiratory chain. Biochemistry, 38 (40):13279-13287. [doi:10.1021/bi9828674]
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. [doi:10.1080/10715760500043132]
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. [doi:10.1016/S0014-5793(01)03314-2]
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. [doi:10.1016/j.fertnstert.2003.11.013]
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. [doi:10.1242/jcs.02644]
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. [doi:10.1016/ S0092-8674(00)80301-3]
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. [doi:10.1073/pnas.92.10.4542]
34. Kinnally, K.W., Antonsson, B., 2007. A tale of two mitochondrial channels, MAC and PTP, in apoptosis. Apoptosis, 12 (5):857-868. [doi:10.1007/s10495-007-0722-z]
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. [doi:10.1126/ science.1112125]
38. Lonergan, T., Bavister, B., Brenner, C., 2007. Mitochondria in stem cells. Mitochondrion, 7 (5):289-296. [doi:10.1016/j.mito.2007.05.002]
39. López-Lluch, G., Irusta, P.M., Navas, P., de Cabo, R., 2008. Mitochondrial biogenesis and healthy aging. Exp. Gerontol., 43 (9):813-819. [doi:10.1016/j.exger.2008.06.014]
40. 2+ release mechanisms in porcine oocytes. Biol. Reprod., 56 (4): 921-930. [doi:10.1095/biolreprod56.4.921]
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. [doi:10.1006/bbrc.2000.2994]
43. Meiszilig;ner, 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. [doi:10.1007/s004140050089]
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. [doi:10.1111/j.1439-0531.2008.01190.x]
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. [doi:10.1016/ 0002-9378(95)91479-X]
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. [doi:10.1620/ tjem.210.137]
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. [doi:10.1272/jnms.70.408]
48. Ott, M., Gogvadze, V., Orrenius, S., Zhivotovsky, B., 2007. Mitochondria, oxidative stress and cell death. Apoptosis, 12 (5):913-922. [doi:10.1007/s10495-007-0756-2]
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. [doi:10.1196/annals.1335.015]
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. [doi:10.1006/dbio.2000.9656]
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. [doi:10.1074/jbc.M109950200]
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. [doi:10.1023/A:1018431316831]
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. [doi:10.1002/ mrd.20779]
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. [doi:10.1093/molehr/7.5.425]
55. Robertson, J.A., 1998. Oocyte cytoplasm transfers and the ethics of germ-line intervention. J. Law Med. Ethics, 26 (3):211-220, 179. [doi:10.1111/j.1748-720X.1998.tb01422.x]
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. [doi:10.1006/ bbrc.1997.7605]
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. [doi:10.1186/1741-7007-6-24]
58. 2+ signaling and apoptosis. J. Bioenerg. Biomembr., 32 (1):35-46. [doi:10.1023/A:1005508311495]
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. [doi:10.1095/biolreprod.106.054536]
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. [doi:10.1016/ j.brainresbull. 2003.07.009]
61. Tarín, J.J., 1996. Potential effects of age-associated oxidative stress on mammalian oocytes/embryos. Mol. Hum. Reprod., 2 (10):717-724. [doi:10.1093/molehr/2.10.717]
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. [doi:10.1095/ biolreprod.104.033589]
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. [doi:10.1016/j.theriogenology.2003.09.013]
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. [doi:10.1073/pnas.0508886102]
65. Tsujimoto, Y., Shimizu, S., 2007. Role of the mitochondrial membrane permeability transition in cell death. Apoptosis, 12 (5):835-840. [doi:10.1007/s10495-006-0525-7]
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. [doi:10.1073/ pnas.88.11.5031]
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. [doi:10.1093/molehr/ gam068]
70. 2+ levels in metaphase II mouse oocytes. Hum. Reprod., 18 (11):2429-2440. [doi:10.1093/humrep/deg466]
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 Δ m. Reproduction, 131 (5):961-976 [doi:10.1530/rep.1.00458]
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. [doi:10.1093/molehr/gan037]
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. [doi:10.1038/ng.95]
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. [doi:10.1038/ sj.cdd.4400778]
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. [doi:10.1007/s10517-005-0494-9]
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. [doi:10.1098/rstb.2008.2259]
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. [doi:10.1093/humrep/16.5.909]
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. [doi:10.1016/S0015-0282(00)01597-1]
81. 5286) in human oocytes: Correlation with age and IVF outcome. J. Assist. Reprod. Genet., 19 (2):60-66. [doi:10.1023/A:1014439529813]
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. [doi:10.1007/s10815-007-9161-6]
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. [doi:10.1093/mutage/13.6.567]
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. [doi:10.1038/sj.cr.7310095]