Replication stress induces micronuclei comprising of aggregated DNA double-strand breaks

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Xu, Bing ^a   Sun, Zhaoliang ^a   Liu, Zhaojian ^a   Guo, Haiyang ^a   Liu, Qiao ^a   Jiang, Haiyan ^a   Zou, Yongxin ^a   Gong, Yaoqin ^a   Tischfield, Jay A ^b   Shao, Changshun ^a,b  

^a Shandong Key Laboratory of Digital Human and Clinical Anatomy   (China)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APHIDICOLIN; CELL PROTEIN; HISTONE H2AX; HYDROXYUREA; PACLITAXEL; PROTEIN CUL4B; REPLICATION FACTOR A; REPLICATION FACTOR A1; THYMIDINE; UNCLASSIFIED DRUG; HISTONE; RPA1 PROTEIN, HUMAN; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CELL CYCLE ARREST; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL STRESS; CONTROLLED STUDY; DEPLETION; DNA DAMAGE; DNA REPLICATION; DNA REPLICATION STRESS; DOUBLE STRANDED DNA BREAK; FLOW CYTOMETRY; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; MAMMAL CELL; MICRONUCLEUS; MICROTUBULE ASSEMBLY; MOUSE; NONHUMAN; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; ANIMAL; CELL LINE; DRUG EFFECT; GENETICS; METABOLISM; MUTATION; PHYSIOLOGICAL STRESS;

MAMMALIA;

ANIMALS; APHIDICOLIN; CELL LINE; DNA BREAKS, DOUBLE-STRANDED; DNA REPLICATION; HISTONES; HUMANS; HYDROXYUREA; MICE; MICRONUCLEI, CHROMOSOME-DEFECTIVE; MUTATION; PACLITAXEL; REPLICATION PROTEIN A; RNA, SMALL INTERFERING; S PHASE; STRESS, PHYSIOLOGICAL; THYMIDINE;

EID: 79954554334     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018618     Document Type: Article

References (45)

1. Heddle JA, Cimino MC, Hayashi M, Romagna F, Shelby MD, et al. (1991) Micronuclei as an index of cytogenetic damage: past, present, and future. Environ Mol Mutagen 18: 277-291.
2. Bonassi S, Ugolini D, Kirsch-Volders M, Stromberg U, Vermeulen R, et al. (2005) Human population studies with cytogenetic biomarkers: review of the literature and future prospectives. Environ Mol Mutagen 45: 258-270.
3. Norppa H, Falck GC, (2003) What do human micronuclei contain? Mutagenesis 18: 221-233.
4. Grawe J, Zetterberg G, Amneus H, (1992) Flow-cytometric enumeration of micronucleated polychromatic erythrocytes in mouse peripheral blood. Cytometry 13: 750-758.
5. Yasui M, Koyama N, Koizumi T, Senda-Murata K, Takashima Y, et al. (2010) Live cell imaging of micronucleus formation and development. Mutat Res 692: 12-18.
6. Maraschio P, Cortinovis M, Dainotti E, Tupler R, Tiepolo L, (1992) Interphase cytogenetics of the ICF syndrome. Ann Hum Genet 56 (Pt 3): 273-278.
7. Fan T, Yan Q, Huang J, Austin S, Cho E, et al. (2003) Lsh-deficient murine embryonal fibroblasts show reduced proliferation with signs of abnormal mitosis. Cancer Res 63: 4677-4683.
8. Shimizu N, Itoh N, Utiyama H, Wahl GM, (1998) Selective entrapment of extrachromosomally amplified DNA by nuclear budding and micronucleation during S phase. J Cell Biol 140: 1307-1320.
9. Fauth E, Zankl H, (1999) Comparison of spontaneous and idoxuridine-induced micronuclei by chromosome painting. Mutat Res 440: 147-156.
10. Dai W, Wang Q, Liu T, Swamy M, Fang Y, et al. (2004) Slippage of mitotic arrest and enhanced tumor development in mice with BubR1 haploinsufficiency. Cancer Res 64: 440-445.
11. Rosin MP, German J, (1985) Evidence for chromosome instability in vivo in Bloom syndrome: increased numbers of micronuclei in exfoliated cells. Hum Genet 71: 187-191.
12. Wang ZQ, Stingl L, Morrison C, Jantsch M, Los M, et al. (1997) PARP is important for genomic stability but dispensable in apoptosis. Genes Dev 11: 2347-2358.
13. Shima N, Hartford SA, Duffy T, Wilson LA, Schimenti KJ, et al. (2003) Phenotype-based identification of mouse chromosome instability mutants. Genetics 163: 1031-1040.
14. Terradas M, Martin M, Tusell L, Genesca A, (2009) DNA lesions sequestered in micronuclei induce a local defective-damage response. DNA Repair (Amst) 8: 1225-1234.
15. Rogakou EP, Boon C, Redon C, Bonner WM, (1999) Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146: 905-916.
16. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, et al. (2000) A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 10: 886-895.
17. Fernandez-Capetillo O, Lee A, Nussenzweig M, Nussenzweig A, (2004) H2AX: the histone guardian of the genome. DNA Repair (Amst) 3: 959-967.
18. Thiriet C, Hayes JJ, (2005) Chromatin in need of a fix: phosphorylation of H2AX connects chromatin to DNA repair. Mol Cell 18: 617-622.
19. Rothkamm K, Lobrich M, (2003) Evidence for a lack of DNA double-strand break repair in human cells exposed to very low x-ray doses. Proc Natl Acad Sci U S A 100: 5057-5062.
20. Ward IM, Chen J, (2001) Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J Biol Chem 276: 47759-47762.
21. Dmitrieva NI, Cai Q, Burg MB, (2004) Cells adapted to high NaCl have many DNA breaks and impaired DNA repair both in cell culture and in vivo. Proc Natl Acad Sci U S A 101: 2317-2322.
22. Hammond EM, Dorie MJ, Giaccia AJ, (2003) ATR/ATM targets are phosphorylated by ATR in response to hypoxia and ATM in response to reoxygenation. J Biol Chem 278: 12207-12213.
23. Mahadevaiah SK, Turner JM, Baudat F, Rogakou EP, de BP, et al. (2001) Recombinational DNA double-strand breaks in mice precede synapsis. Nat Genet 27: 271-276.
24. Turner JM, Burgoyne PS, Singh PB, (2001) M31 and macroH2A1.2 colocalise at the pseudoautosomal region during mouse meiosis. J Cell Sci 114: 3367-3375.
25. Liu Z, Liu Q, Xu B, Wu J, Guo C, et al. (2009) Berberine induces p53-dependent cell cycle arrest and apoptosis of human osteosarcoma cells by inflicting DNA damage. Mutat Res 662: 75-83.
26. Shao C, Deng L, Henegariu O, Liang L, Raikwar N, et al. (1999) Mitotic recombination produces the majority of recessive fibroblast variants in heterozygous mice. Proc Natl Acad Sci U S A 96: 9230-9235.
27. Timson J, (1975) Hydroxyurea. Mutat Res 32: 115-132.
28. Ikegami S, Taguchi T, Ohashi M, Oguro M, Nagano H, et al. (1978) Aphidicolin prevents mitotic cell division by interfering with the activity of DNA polymerase-alpha. Nature 275: 458-460.
29. Bolderson E, Scorah J, Helleday T, Smythe C, Meuth M, (2004) ATM is required for the cellular response to thymidine induced replication fork stress. Hum Mol Genet 13: 2937-2945.
30. Kurose A, Tanaka T, Huang X, Traganos F, Dai W, et al. (2006) Effects of hydroxyurea and aphidicolin on phosphorylation of ataxia telangiectasia mutated on Ser 1981 and histone H2AX on Ser 139 in relation to cell cycle phase and induction of apoptosis. Cytometry A 69: 212-221.
31. Speicher LA, Barone L, Tew KD, (1992) Combined antimicrotubule activity of estramustine and taxol in human prostatic carcinoma cell lines. Cancer Res 52: 4433-4440.
32. Tinwell H, Ashby J, (1994) Genetic toxicity and potential carcinogenicity of taxol. Carcinogenesis 15: 1499-1501.
33. Zou Y, Mi J, Cui J, Lu D, Zhang X, et al. (2009) Characterization of nuclear localization signal in the N terminus of CUL4B and its essential role in cyclin E degradation and cell cycle progression. J Biol Chem 284: 33320-33332.
34. Wold MS, (1997) Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu Rev Biochem 66: 61-92.
35. Dodson GE, Shi Y, Tibbetts RS, (2004) DNA replication defects, spontaneous DNA damage, and ATM-dependent checkpoint activation in replication protein A-deficient cells. J Biol Chem 279: 34010-34014.
36. Wang Y, Putnam CD, Kane MF, Zhang W, Edelmann L, et al. (2005) Mutation in Rpa1 results in defective DNA double-strand break repair, chromosomal instability and cancer in mice. Nat Genet 37: 750-755.
37. Ishii Y, Bender MA, (1980) Effects of inhibitors of DNA synthesis on spontaneous and ultraviolet light-induced sister-chromatid exchanges in Chinese hamster cells. Mutat Res 79: 19-32.
38. Sorensen CS, Hansen LT, Dziegielewski J, Syljuasen RG, Lundin C, et al. (2005) The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nat Cell Biol 7: 195-201.
39. Kurose A, Tanaka T, Huang X, Halicka HD, Traganos F, et al. (2005) Assessment of ATM phosphorylation on Ser-1981 induced by DNA topoisomerase I and II inhibitors in relation to Ser-139-histone H2AX phosphorylation, cell cycle phase, and apoptosis. Cytometry A 68: 1-9.
40. Decordier I, Dillen L, Cundari E, Kirsch-Volders M, (2002) Elimination of micronucleated cells by apoptosis after treatment with inhibitors of microtubules. Mutagenesis 17: 337-344.
41. Meintieres S, Biola A, Pallardy M, Marzin D, (2001) Apoptosis can be a confusing factor in in vitro clastogenic assays. Mutagenesis 16: 243-250.
42. Aten JA, Stap J, Krawczyk PM, van Oven CH, Hoebe RA, et al. (2004) Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 303: 92-95.
43. Hill AB, Schimke RT, (1985) Increased gene amplification in L5178Y mouse lymphoma cells with hydroxyurea-induced chromosomal aberrations. Cancer Res 45: 5050-5057.
44. Glover TW, Berger C, Coyle J, Echo B, (1984) DNA polymerase alpha inhibition by aphidicolin induces gaps and breaks at common fragile sites in human chromosomes. Hum Genet 67: 136-142.
45. Yang SJ, Hahn GM, Bagshaw MA, (1966) Chromosome aberrations induced by thymidine. Exp Cell Res 42: 130-135.