Please wait a minute...
Frontiers of Agricultural Science and Engineering

ISSN 2095-7505

ISSN 2095-977X(Online)

CN 10-1204/S

Postal Subscription Code 80-906

Front. Agr. Sci. Eng.    2014, Vol. 1 Issue (3) : 185-190    https://doi.org/10.15302/J-FASE-2014035
REVIEW
Effects of DNA damage on oocyte meiotic maturation and early embryonic development
Shen YIN,Junyu MA,Wei SHEN()
Key Laboratory of Animal Reproduction and Germplasm Enhancement in Universities of Shandong, College of Animal Science and Technology, Qingdao Agricultural University, Qingdao 266109, China
 Download: PDF(120 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

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.

Keywords DNA damage      double-strand breaks (DSBs)      oocyte      embryo     
Corresponding Author(s): Wei SHEN   
Online First Date: 16 January 2015    Issue Date: 27 January 2015
 Cite this article:   
Shen YIN,Junyu MA,Wei SHEN. Effects of DNA damage on oocyte meiotic maturation and early embryonic development[J]. Front. Agr. Sci. Eng. , 2014, 1(3): 185-190.
 URL:  
https://academic.hep.com.cn/fase/EN/10.15302/J-FASE-2014035
https://academic.hep.com.cn/fase/EN/Y2014/V1/I3/185
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
https://doi.org/10.1093/humrep/des255 pmid: 22786779
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
https://doi.org/10.1016/j.mrgentox.2005.03.008 pmid: 15878304
3 Tease C. X-ray-induced chromosome aberrations in dictyate oocytes of young and old female mice. Mutation Research, 1983, 119(2): 191–194
https://doi.org/10.1016/0165-7992(83)90128-8 pmid: 6828056
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
https://doi.org/10.1093/humupd/dmn063 pmid: 19151106
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
https://doi.org/10.1038/sj.onc.1203283 pmid: 10630641
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
https://doi.org/10.1007/s00412-004-0290-8 pmid: 15235794
7 Grey C, Baudat F, de Massy B. Genome-wide control of the distribution of meiotic recombination. PLoS Biology, 2009, 7(2): e35
https://doi.org/10.1371/journal.pbio.1000035 pmid: 19226188
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
https://doi.org/10.1371/journal.pgen.1000661 pmid: 19763179
9 Lambert J, Hergenr?der R, Suter D, Deckert V. Probing liquid-liquid interfaces with spatially resolved NMR spectroscopy. Angewandte Chemie, 2009, 48(34): 6343–6345
https://doi.org/10.1002/anie.200901389 pmid: 19598187
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
https://doi.org/10.1093/hmg/ddn090 pmid: 18353795
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
https://doi.org/10.1007/BF00330366 pmid: 6180868
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
https://doi.org/10.1007/BF00285618 pmid: 6628083
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
https://doi.org/10.1093/nar/gkn1071 pmid: 19139074
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
https://doi.org/10.1038/35056049 pmid: 11256071
15 Bohgaki T, Bohgaki M, Hakem R. DNA double-strand break signaling and human disorders. Genome Integrity, 2010, 1: 15
https://doi.org/10.1186/2041-9414-1-15 pmid: 21054854
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
https://doi.org/10.1016/S0960-9822(00)00610-2 pmid: 10959836
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
https://doi.org/10.1074/jbc.273.10.5858 pmid: 9488723
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
https://doi.org/10.1038/283593a0 pmid: 6243744
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
pmid: 15959561
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
https://doi.org/10.1093/nar/gkn403 pmid: 18603595
21 Marangos P, Carroll J. Oocytes progress beyond prophase in the presence of DNA damage. Current Biology, 2012, 22(11): 989–994
https://doi.org/10.1016/j.cub.2012.03.063 pmid: 22578416
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
https://doi.org/10.4161/cc.24311 pmid: 23518501
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
https://doi.org/10.1371/journal.pone.0043875 pmid: 22928046
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
pmid: 24036543
25 De Bont R, van Larebeke N. Endogenous DNA damage in humans: a review of quantitative data. Mutagenesis, 2004, 19(3): 169–185
https://doi.org/10.1093/mutage/geh025 pmid: 15123782
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
https://doi.org/10.1210/me.2013-1108 pmid: 24002654
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
https://doi.org/10.1095/biolreprod.113.110692 pmid: 24048577
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
https://doi.org/10.1126/science.1204117 pmid: 21778401
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
pmid: 21677879
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
https://doi.org/10.4161/auto.21484 pmid: 22874562
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
https://doi.org/10.1158/0008-5472.CAN-12-0388 pmid: 22562464
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
https://doi.org/10.1074/jbc.M113.495069 pmid: 23995842
33 Savage J R. A brief survey of aberration origin theories. Mutation Research, 1998, 404(1-2): 139–147
https://doi.org/10.1016/S0027-5107(98)00107-9 pmid: 9729341
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
pmid: 139166
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
pmid: 159073
36 Ba?uelos 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
pmid: 12750435
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
https://doi.org/10.1038/sj.cdd.4402052 pmid: 17082817
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
https://doi.org/10.1038/ncb945 pmid: 12598907
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
https://doi.org/10.1038/ncb1337 pmid: 16327781
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
https://doi.org/10.1016/j.mrrev.2010.01.003 pmid: 20079460
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
pmid: 16618811
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
https://doi.org/10.1083/jcb.146.5.905 pmid: 10477747
43 Carroll J, Marangos P. The DNA damage response in mammalian oocytes. Frontiers in Genetics, 2013, 4: 117
https://doi.org/10.3389/fgene.2013.00117 pmid: 23805152
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
https://doi.org/10.1016/j.molcel.2008.10.009 pmid: 18995829
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
https://doi.org/10.1016/j.ceb.2009.01.018 pmid: 19230643
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
https://doi.org/10.1016/B978-0-12-380888-2.00003-0 pmid: 21034966
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
pmid: 16439996
49 Shiloh Y. The ATM-mediated DNA-damage response: taking shape. Trends in Biochemical Sciences, 2006, 31(7): 402–410
https://doi.org/10.1016/j.tibs.2006.05.004 pmid: 16774833
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
https://doi.org/10.1016/j.ceb.2007.02.009 pmid: 17303408
52 Ciccia A, Elledge S J. The DNA damage response: making it safe to play with knives. Molecular Cell, 2010, 40(2): 179–204
https://doi.org/10.1016/j.molcel.2010.09.019 pmid: 20965415
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
pmid: 20453035
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
pmid: 19364923
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
https://doi.org/10.1016/j.cell.2008.05.043 pmid: 18662541
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
pmid: 16715549
57 Schneider M R, Wolf E. The epidermal growth factor receptor ligands at a glance. Journal of Cellular Physiology, 2009, 218(3): 460–466
https://doi.org/10.1002/jcp.21635 pmid: 19006176
58 Mac?rek 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
https://doi.org/10.1073/pnas.0406212102 pmid: 15640358
61 Jackson S P, Bartek J. The DNA-damage response in human biology and disease. Nature, 2009, 461(7267): 1071–1078
https://doi.org/10.1038/nature08467 pmid: 19847258
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
https://doi.org/10.1038/ng856 pmid: 11912493
63 Lindqvist A, K?llstr?m 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
https://doi.org/10.1083/jcb.200503066 pmid: 16216921
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
pmid: 1718679
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
https://doi.org/10.1016/0014-4827(91)90159-R pmid: 1701730
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
https://doi.org/10.1016/0012-1606(91)90218-R pmid: 1850367
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
https://doi.org/10.1006/excr.1996.0262 pmid: 8806464
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
https://doi.org/10.1006/excr.1998.4115 pmid: 9665796
[1] Zachariah MCLEAN, Björn OBACK, Götz LAIBLE. Embryo-mediated genome editing for accelerated genetic improvement of livestock[J]. Front. Agr. Sci. Eng. , 2020, 7(2): 148-160.
[2] Zhengyuan HUANG, Lei GAO, Yunpeng HOU, Shien ZHU, Xiangwei FU. Cryopreservation of farm animal gametes and embryos: recent updates and progress[J]. Front. Agr. Sci. Eng. , 2019, 6(1): 42-53.
[3] Yanna DANG, Kun ZHANG. Factors affecting early embryonic development in cattle: relevance for bovine cloning[J]. Front. Agr. Sci. Eng. , 2019, 6(1): 33-41.
[4] Jianyong HAN, Yi-Liang MIAO, Jinlian HUA, Yan LI, Xue ZHANG, Jilong ZHOU, Na LI, Ying ZHANG, Jinying ZHANG, Zhonghua LIU. Porcine pluripotent stem cells: progress, challenges and prospects[J]. Front. Agr. Sci. Eng. , 2019, 6(1): 8-27.
[5] Xiuchun TIAN. The past, present and future of bovine pluripotent stem cells: a brief overview[J]. Front. Agr. Sci. Eng. , 2019, 6(1): 3-7.
[6] Nan WANG, Jing GAO, Suiqi ZHANG, Feng YAN. Comparison of prechilling stratification and sulfuric acid scarification on seed germination of Panicum virgatum under drought stress[J]. Front. Agr. Sci. Eng. , 2017, 4(2): 220-227.
[7] Yi FANG,Xiangwei FU,Junjie LI,Ming DU,Baoyu JIA,Jinlong ZHANG,Xiaosheng ZHANG,Shien ZHU. Effects of the TLR4 transgene on reproductive traits and DNA methylation pattern of oocytes in ewes[J]. Front. Agr. Sci. Eng. , 2014, 1(4): 314-320.
[8] Hanning WANG,Yangli PEI,Ning LI,Jianyong HAN. Progress, problems and prospects of porcine pluripotent stem cells[J]. Front. Agr. Sci. Eng. , 2014, 1(1): 6-15.
[9] Wanfeng LI,Suying HAN,Liwang QI,Shougong ZHANG. Transcriptome resources and genome-wide marker development for Japanese larch (Larix kaempferi)[J]. Front. Agr. Sci. Eng. , 2014, 1(1): 77-84.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed