Effects of DNA damage on oocyte meiotic maturation and early embryonic development
Shen YIN, Junyu MA, Wei SHEN
Effects of DNA damage on oocyte meiotic maturation and early embryonic development
DNA damage is one of the most common threats to meiotic cells. It has the potential to induce infertility and genetic abnormalities that may be passed to the embryo. Here, we reviewed exogenous factors which could induce DNA damage. Specially, we addressed the different effects of DNA damage on mouse oocytes and embryonic development. Complex DNA damage, double-strand breaks, represents a more difficult repair process and involves various repair pathways. Understanding the mechanisms involved in DNA damage responses may improve therapeutic strategies for ovarian cancer and fertility preservation.
DNA damage / double-strand breaks (DSBs) / oocyte / embryo
[1] |
Ferraretti A P, Goossens V, de Mouzon J, Bhattacharya S, Castilla J A, Korsak V, Kupka M, Nygren K G, Nyboe Andersen A. Assisted reproductive technology in Europe, 2008: results generated from European registers by ESHRE. Human Reproduction, 2012, 27(9): 2571–2584
CrossRef
Pubmed
Google scholar
|
[2] |
Jacquet P, Adriaens I, Buset J, Neefs M, Vankerkom J. Cytogenetic studies in mouse oocytes irradiated in vitro at different stages of maturation, by use of an early preantral follicle culture system. Mutation Research, 2005, 583(2): 168–177
CrossRef
Pubmed
Google scholar
|
[3] |
Tease C. X-ray-induced chromosome aberrations in dictyate oocytes of young and old female mice. Mutation Research, 1983, 119(2): 191–194
CrossRef
Pubmed
Google scholar
|
[4] |
Adriaens I, Smitz J, Jacquet P. The current knowledge on radio sensitivity of ovarian follicle development stages. Human Reproduction Update, 2009, 15(3): 359–377
CrossRef
Pubmed
Google scholar
|
[5] |
Dasika G K, Lin S C, Zhao S, Sung P, Tomkinson A, Lee E Y. DNA damage-induced cell cycle checkpoints and DNA strand break repair in development and tumorigenesis. Oncogene, 1999, 18(55): 7883–7899
CrossRef
Pubmed
Google scholar
|
[6] |
Roig I, Liebe B, Egozcue J, Cabero L, Garcia M, Scherthan H. Female-specific features of recombinational double-stranded DNA repair in relation to synapsis and telomere dynamics in human oocytes. Chromosoma, 2004, 113(1): 22–33
CrossRef
Pubmed
Google scholar
|
[7] |
Grey C, Baudat F, de Massy B. Genome-wide control of the distribution of meiotic recombination. PLoS Biology, 2009, 7(2): e35
CrossRef
Pubmed
Google scholar
|
[8] |
Cheng E Y, Hunt P A, Naluai-Cecchini T A, Fligner C L, Fujimoto V Y, Pasternack T L, Schwartz J M, Steinauer J E, Woodruff T J, Cherry S M, Hansen T A, Vallente R U, Broman K W, Hassold T J. Meiotic recombination in human oocytes. PLOS Genetics, 2009, 5(9): e1000661
CrossRef
Pubmed
Google scholar
|
[9] |
Lambert J, Hergenröder R, Suter D, Deckert V. Probing liquid-liquid interfaces with spatially resolved NMR spectroscopy. Angewandte Chemie, 2009, 48(34): 6343–6345
CrossRef
Pubmed
Google scholar
|
[10] |
Derijck A, van der Heijden G, Giele M, Philippens M, de Boer P. DNA double-strand break repair in parental chromatin of mouse zygotes, the first cell cycle as an origin of de novo mutation. Human Molecular Genetics, 2008, 17(13): 1922–1937
CrossRef
Pubmed
Google scholar
|
[11] |
Speed R M. Meiosis in the foetal mouse ovary: I. An analysis at the light microscope level using surface-spreading. Chromosoma, 1982, 85(3): 427–437
CrossRef
Pubmed
Google scholar
|
[12] |
Speed R M, Chandley A C. Meiosis in the foetal mouse ovary: II. Oocyte development and age-related aneuploidy. Does a production line exist? Chromosoma, 1983, 88(3): 184–189
CrossRef
Pubmed
Google scholar
|
[13] |
Pandita T K, Richardson C. Chromatin remodeling finds its place in the DNA double-strand break response. Nucleic Acids Research, 2009, 37(5): 1363–1377
CrossRef
Pubmed
Google scholar
|
[14] |
van Gent D C, Hoeijmakers J H, Kanaar R. Chromosomal stability and the DNA double-stranded break connection. Nature Reviews Genetics, 2001, 2(3): 196–206
CrossRef
Pubmed
Google scholar
|
[15] |
Bohgaki T, Bohgaki M, Hakem R. DNA double-strand break signaling and human disorders. Genome Integrity, 2010, 1: 15
CrossRef
Pubmed
Google scholar
|
[16] |
Paull T T, Rogakou E P, Yamazaki V, Kirchgessner C U, Gellert M, Bonner W M. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Current Biology, 2000, 10(15): 886–895
CrossRef
Pubmed
Google scholar
|
[17] |
Rogakou E P, Pilch D R, Orr A H, Ivanova V S, Bonner W M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. Journal of Biological Chemistry, 1998, 273(10): 5858–5868
CrossRef
Pubmed
Google scholar
|
[18] |
Durkacz B W, Omidiji O, Gray D A, Shall S. (ADP-ribose)n participates in DNA excision repair. Nature, 1980, 283(5747): 593–596
CrossRef
Pubmed
Google scholar
|
[19] |
Malanga M, Althaus F R. The role of poly(ADP-ribose) in the DNA damage signaling network. Biochemistry and Cell Biology, 2005, 83(3): 354–364
Pubmed
|
[20] |
Godon C, Cordelières F P, Biard D, Giocanti N, Mégnin-Chanet F, Hall J, Favaudon V. PARP inhibition versus PARP-1 silencing: different outcomes in terms of single-strand break repair and radiation susceptibility. Nucleic Acids Research, 2008, 36(13): 4454–4464
CrossRef
Pubmed
Google scholar
|
[21] |
Marangos P, Carroll J. Oocytes progress beyond prophase in the presence of DNA damage. Current Biology, 2012, 22(11): 989–994
CrossRef
Pubmed
Google scholar
|
[22] |
Ma J Y, Ou Yang Y C, Wang Z W, Wang Z B, Jiang Z Z, Luo S M, Hou Y, Liu Z H, Schatten H, Sun Q Y. The effects of DNA double-strand breaks on mouse oocyte meiotic maturation. Cell Cycle, 2013, 12(8): 1233–1241
CrossRef
Pubmed
Google scholar
|
[23] |
Yuen W S, Merriman J A, O’Bryan M K, Jones K T. DNA double strand breaks but not interstrand crosslinks prevent progress through meiosis in fully grown mouse oocytes. PLoS ONE, 2012, 7(8): e43875
CrossRef
Pubmed
Google scholar
|
[24] |
Wang Z W, Ma X S, Ma J Y, Luo Y B, Lin F, Wang Z B, Fan H Y, Schatten H, Sun Q Y. Laser microbeam-induced DNA damage inhibits cell division in fertilized eggs and early embryos. Cell Cycle, 2013, 12(20): 3336–3344
Pubmed
|
[25] |
De Bont R, van Larebeke N. Endogenous DNA damage in humans: a review of quantitative data. Mutagenesis, 2004, 19(3): 169–185
CrossRef
Pubmed
Google scholar
|
[26] |
Zhang Y L, Yu C, Ji S Y, Li X M, Zhang Y P, Zhang D, Zhou D, Fan H Y. TOP2β is essential for ovarian follicles that are hypersensitive to chemotherapeutic drugs. Molecular Endocrinology, 2013, 27(10): 1678–1691
CrossRef
Pubmed
Google scholar
|
[27] |
Li X M, Yu C, Wang Z W, Zhang Y L, Liu X M, Zhou D, Sun Q Y, Fan H Y. DNA topoisomerase II is dispensable for oocyte meiotic resumption but is essential for meiotic chromosome condensation and separation in mice. Biology of Reproduction, 2013, 89(5): 118
CrossRef
Pubmed
Google scholar
|
[28] |
Wu C C, Li T K, Farh L, Lin L Y, Lin T S, Yu Y J, Yen T J, Chiang C W, Chan N L. Structural basis of type II topoisomerase inhibition by the anticancer drug etoposide. Science, 2011, 333(6041): 459–462
CrossRef
Pubmed
Google scholar
|
[29] |
Jia L, Li H, Sun Y. Induction of p21-dependent senescence by an NAE inhibitor, MLN4924, as a mechanism of growth suppression. Neoplasia, 2011, 13(6): 561–569
Pubmed
|
[30] |
Luo Z, Pan Y, Jeong L S, Liu J, Jia L. Inactivation of the Cullin (CUL)-RING E3 ligase by the NEDD8-activating enzyme inhibitor MLN4924 triggers protective autophagy in cancer cells. Autophagy, 2012, 8(11): 1677–1679
CrossRef
Pubmed
Google scholar
|
[31] |
Luo Z, Yu G, Lee H W, Li L, Wang L, Yang D, Pan Y, Ding C, Qian J, Wu L, Chu Y, Yi J, Wang X, Sun Y, Jeong L S, Liu J, Jia L. The Nedd8-activating enzyme inhibitor MLN4924 induces autophagy and apoptosis to suppress liver cancer cell growth. Cancer Research, 2012, 72(13): 3360–3371
CrossRef
Pubmed
Google scholar
|
[32] |
Pan W W, Zhou J J, Yu C, Xu Y, Guo L J, Zhang H Y, Zhou D, Song F Z, Fan H Y. Ubiquitin E3 ligase CRL4 (CDT2/DCAF2) as a potential chemotherapeutic target for ovarian surface epithelial cancer. Journal of Biological Chemistry, 2013, 288(41): 29680–29691
CrossRef
Pubmed
Google scholar
|
[33] |
Savage J R. A brief survey of aberration origin theories. Mutation Research, 1998, 404(1-2): 139–147
CrossRef
Pubmed
Google scholar
|
[34] |
Beerman T A, Goldberg I H. The relationship between DNA strand-scission and DNA synthesis inhibition in HeLa cells treated with neocarzinostatin. Biochimica et Biophysica Acta (BBA) - Nucleic Acids and Protein Synthesis, 1977, 475(2): 281–293
Pubmed
|
[35] |
Hatayama T, Goldberg I H. DNA damage and repair in relation to cell killing in neocarzinostatin-treated HeLa cells. Biochimica et Biophysica Acta (BBA) - Nucleic Acids and Protein Synthesis, 1979, 563(1): 59–71
Pubmed
|
[36] |
Bañuelos A, Reyes E, Ocadiz R, Alvarez E, Moreno M, Monroy A, Gariglio P. Neocarzinostatin induces an effective p53-dependent response in human papillomavirus-positive cervical cancer cells. The Journal of Pharmacology and Experimental Therapeutics, 2003, 306(2): 671–680
Pubmed
|
[37] |
Hanoux V, Pairault C, Bakalska M, Habert R, Livera G. Caspase-2 involvement during ionizing radiation-induced oocyte death in the mouse ovary. Cell Death and Differentiation, 2007, 14(4): 671– 681
CrossRef
Pubmed
Google scholar
|
[38] |
Lukas C, Falck J, Bartkova J, Bartek J, Lukas J. Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nature Cell Biology, 2003, 5(3): 255–260
CrossRef
Pubmed
Google scholar
|
[39] |
Jazayeri A, Falck J, Lukas C, Bartek J, Smith G C, Lukas J, Jackson S P. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nature Cell Biology, 2006, 8(1): 37–45
CrossRef
Pubmed
Google scholar
|
[40] |
Botchway S W, Reynolds P, Parker A W, O’Neill P. Use of near infrared femtosecond lasers as sub-micron radiation microbeam for cell DNA damage and repair studies. Mutation Research, 2010, 704(1-3): 38–44
CrossRef
Pubmed
Google scholar
|
[41] |
Bekker-Jensen S, Lukas C, Kitagawa R, Melander F, Kastan M B, Bartek J, Lukas J. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. The Journal of Cell Biology, 2006, 173(2): 195–206
Pubmed
|
[42] |
Rogakou E P, Boon C, Redon C, Bonner W M. Megabase chromatin domains involved in DNA double-strand breaks in vivo. The Journal of Cell Biology, 1999, 146(5): 905–916
CrossRef
Pubmed
Google scholar
|
[43] |
Carroll J, Marangos P. The DNA damage response in mammalian oocytes. Frontiers in Genetics, 2013, 4: 117
CrossRef
Pubmed
Google scholar
|
[44] |
Aguilera A, Gómez-González B. Genome instability: a mechanistic view of its causes and consequences. Nature Reviews Genetics, 2008, 9(3): 204–217
|
[45] |
Cohn M A, D’Andrea A D. Chromatin recruitment of DNA repair proteins: lessons from the fanconi anemia and double-strand break repair pathways. Molecular Cell, 2008, 32(3): 306–312
CrossRef
Pubmed
Google scholar
|
[46] |
Reinhardt H C, Yaffe M B. Kinases that control the cell cycle in response to DNA damage: Chk1, Chk2, and MK2. Current Opinion in Cell Biology, 2009, 21(2): 245–255
CrossRef
Pubmed
Google scholar
|
[47] |
Smith J, Tho L M, Xu N, Gillespie D A. The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. Advances in Cancer Research, 2010, 108: 73–112
CrossRef
Pubmed
Google scholar
|
[48] |
Lavin M F, Delia D, Chessa L. ATM and the DNA damage response: workshop on ataxia-telangiectasia and related syndromes. EMBO Reports, 2006, 7(2): 154–160
Pubmed
|
[49] |
Shiloh Y. The ATM-mediated DNA-damage response: taking shape. Trends in Biochemical Sciences, 2006, 31(7): 402–410
CrossRef
Pubmed
Google scholar
|
[50] |
Branzei D, Foiani M. Regulation of DNA repair throughout the cell cycle. Nature Reviews Molecular Cell Biology, 2008, 9(4): 297–308
|
[51] |
Bartek J, Lukas J. DNA damage checkpoints: from initiation to recovery or adaptation. Current Opinion in Cell Biology, 2007, 19(2): 238–245
CrossRef
Pubmed
Google scholar
|
[52] |
Ciccia A, Elledge S J. The DNA damage response: making it safe to play with knives. Molecular Cell, 2010, 40(2): 179–204
CrossRef
Pubmed
Google scholar
|
[53] |
Solc P, Schultz R M, Motlik J. Prophase I arrest and progression to metaphase I in mouse oocytes: comparison of resumption of meiosis and recovery from G2-arrest in somatic cells. Molecular Human Reproduction, 2010, 16(9): 654–664
Pubmed
|
[54] |
Lindqvist A, Rodríguez-Bravo V, Medema R H. The decision to enter mitosis: feedback and redundancy in the mitotic entry network. The Journal of Cell Biology, 2009, 185(2): 193–202
Pubmed
|
[55] |
Bassermann F, Frescas D, Guardavaccaro D, Busino L, Peschiaroli A, Pagano M. The Cdc14B-Cdh1-Plk1 axis controls the G2 DNA-damage-response checkpoint. Cell, 2008, 134(2): 256–267
CrossRef
Pubmed
Google scholar
|
[56] |
Reis A, Chang H Y, Levasseur M, Jones K T. APCcdh1 activity in mouse oocytes prevents entry into the first meiotic division. Nature Cell Biology, 2006, 8(5): 539–540
Pubmed
|
[57] |
Schneider M R, Wolf E. The epidermal growth factor receptor ligands at a glance. Journal of Cellular Physiology, 2009, 218(3): 460–466
CrossRef
Pubmed
Google scholar
|
[58] |
Macůrek L, Lindqvist A, Lim D, Lampson M A, Klompmaker R, Freire R, Clouin C, Taylor S S, Yaffe M B, Medema R H. Polo-like kinase-1 is activated by aurora A to promote checkpoint recovery. Nature, 2008, 455(7209): 119–123
|
[59] |
Barlow C, Liyanage M, Moens P B, Tarsounas M, Nagashima K, Brown K, Rottinghaus S, Jackson S P, Tagle D, Ried T, Wynshaw-Boris A. Atm deficiency results in severe meiotic disruption as early as leptonema of prophase I. Development, 1998, 125(20): 4007–4017
|
[60] |
Di Giacomo M, Barchi M, Baudat F, Edelmann W, Keeney S, Jasin M. Distinct DNA-damage-dependent and-independent responses drive the loss of oocytes in recombination-defective mouse mutants. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(3): 737–742
CrossRef
Pubmed
Google scholar
|
[61] |
Jackson S P, Bartek J. The DNA-damage response in human biology and disease. Nature, 2009, 461(7267): 1071–1078
CrossRef
Pubmed
Google scholar
|
[62] |
Lincoln A J, Wickramasinghe D, Stein P, Schultz R M, Palko M E, De Miguel M P, Tessarollo L, Donovan P J. Cdc25b phosphatase is required for resumption of meiosis during oocyte maturation. Nature Genetics, 2002, 30(4): 446–449
CrossRef
Pubmed
Google scholar
|
[63] |
Lindqvist A, Källström H, Lundgren A, Barsoum E, Rosenthal C K. Cdc25B cooperates with Cdc25A to induce mitosis but has a unique role in activating cyclin B1-Cdk1 at the centrosome. The Journal of Cell Biology, 2005, 171(1): 35–45
CrossRef
Pubmed
Google scholar
|
[64] |
Alexandre H, Van Cauwenberge A, Tsukitani Y, Mulnard J. Pleiotropic effect of okadaic acid on maturing mouse oocytes. Development, 1991, 112(4): 971–980
Pubmed
|
[65] |
Gavin A C, Tsukitani Y, Schorderet-Slatkine S. Induction of M-phase entry of prophase-blocked mouse oocytes through microinjection of okadaic acid, a specific phosphatase inhibitor. Experimental Cell Research, 1991, 192(1): 75–81
CrossRef
Pubmed
Google scholar
|
[66] |
Schwartz D A, Schultz R M. Stimulatory effect of okadaic acid, an inhibitor of protein phosphatases, on nuclear envelope breakdown and protein phosphorylation in mouse oocytes and one-cell embryos. Developmental Biology, 1991, 145(1): 119–127
CrossRef
Pubmed
Google scholar
|
[67] |
Ghosh S, Schroeter D, Paweletz N. Okadaic acid overrides the S-phase check point and accelerates progression of G2-phase to induce premature mitosis in HeLa cells. Experimental Cell Research, 1996, 227(1): 165–169
CrossRef
Pubmed
Google scholar
|
[68] |
Ghosh S, Paweletz N, Schroeter D. Cdc2-independent induction of premature mitosis by okadaic acid in HeLa cells. Experimental Cell Research, 1998, 242(1): 1–9
CrossRef
Pubmed
Google scholar
|
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