Stalled Fork Rescue via Dormant Replication Origins in Unchallenged S Phase Promotes Proper Chromosome Segregation and Tumor Suppression

Molecular Cell

Volumn 41, Issue 5, 2011, Pages 543-553

  Kawabata, Tsuyoshi ^a,b   Luebben, Spencer W ^a   Yamaguchi, Satoru ^a,b,e   Ilves, Ivar ^c   Matise, Ilze ^b,d,f   Buske, Tavanna ^a,g   Botchan, Michael R ^c   Shima, Naoko ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

^e GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^f LATVIA UNIVERSITY OF AGRICULTURE   (Latvia)

^g UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HELICASE; HISTONE H2A; MINICHROMOSOME MAINTENANCE PROTEIN 2; MINICHROMOSOME MAINTENANCE PROTEIN 4; MINICHROMOSOME MAINTENANCE PROTEIN 7; PROTEIN; PROTEIN RAD17; RAD51 PROTEIN; UNCLASSIFIED DRUG;

ALLELE; ANAPHASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CHROMOSOMAL INSTABILITY; CHROMOSOME NUMBER; CHROMOSOME SEGREGATION; CONTROLLED STUDY; FIBROBLAST; HOMOZYGOTE; MICRONUCLEUS; MOLECULAR STABILITY; MOUSE; NONHUMAN; NUMERICAL CHROMOSOME ABERRATION; PROPHASE; PROTEIN STABILITY; STRUCTURAL CHROMOSOME ABERRATION;

ALLELES; ANAPHASE; ANIMALS; CELL CYCLE; CELL DIVISION; CHROMOSOMAL INSTABILITY; CHROMOSOME SEGREGATION; CYTOKINESIS; DNA HELICASES; DNA REPLICATION; FIBROBLASTS; MICE; NEOPLASMS; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; S PHASE;

EUKARYOTA;

EID: 79951970806     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.02.006     Document Type: Article

References (55)

1. Bao S., Tibbetts R.S., Brumbaugh K.M., Fang Y., Richardson D.A., Ali A., Chen S.M., Abraham R.T., Wang X.F. ATR/ATM-mediated phosphorylation of human Rad17 is required for genotoxic stress responses. Nature 2001, 411:969-974.
2. Blackwell B.N., Bucci T.J., Hart R.W., Turturro A. Longevity, body weight, and neoplasia in ad libitum-fed and diet-restricted C57BL6 mice fed NIH-31 open formula diet. Toxicol. Pathol. 1995, 23:570-582.
3. Blow J.J., Dutta A. Preventing re-replication of chromosomal DNA. Nat. Rev. Mol. Cell Biol. 2005, 6:476-486.
4. Bowers J.L., Randell J.C., Chen S., Bell S.P. ATP hydrolysis by ORC catalyzes reiterative Mcm2-7 assembly at a defined origin of replication. Mol. Cell 2004, 16:967-978.
5. Bugreev D.V., Yu X., Egelman E.H., Mazin A.V. Novel pro- and anti-recombination activities of the Bloom's syndrome helicase. Genes Dev. 2007, 21:3085-3094.
6. Byun T.S., Pacek M., Yee M.C., Walter J.C., Cimprich K.A. Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev. 2005, 19:1040-1052.
7. Casper A.M., Nghiem P., Arlt M.F., Glover T.W. ATR regulates fragile site stability. Cell 2002, 111:779-789.
8. Chan K.L., Hickson I.D. On the origins of ultra-fine anaphase bridges. Cell Cycle 2009, 8:3065-3066.
9. Chan K.L., Palmai-Pallag T., Ying S., Hickson I.D. Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nat. Cell Biol. 2009, 11:753-760.
10. Chuang C.H., Wallace M.D., Abratte C., Southard T., Schimenti J.C. Incremental genetic perturbations to MCM2-7 expression and subcellular distribution reveal exquisite sensitivity of mice to DNA replication stress. PLoS Genet. 2010, 6:e1001110.
11. Cortez D., Glick G., Elledge S.J. Minichromosome maintenance proteins are direct targets of the ATM and ATR checkpoint kinases. Proc. Natl. Acad. Sci. USA 2004, 101:10078-10083.
12. Davies S.L., North P.S., Hickson I.D. Role for BLM in replication-fork restart and suppression of origin firing after replicative stress. Nat. Struct. Mol. Biol. 2007, 14:677-679.
13. Edwards M.C., Tutter A.V., Cvetic C., Gilbert C.H., Prokhorova T.A., Walter J.C. MCM2-7 complexes bind chromatin in a distributed pattern surrounding the origin recognition complex in Xenopus egg extracts. J. Biol. Chem. 2002, 277:33049-33057.
14. Fenech M. Cytokinesis-block micronucleus cytome assay. Nat. Protoc. 2007, 2:1084-1104.
15. Forsburg S.L. Eukaryotic MCM proteins: beyond replication initiation. Microbiol. Mol. Biol. Rev. 2004, 68:109-131.
16. Ge X.Q., Jackson D.A., Blow J.J. Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes Dev. 2007, 21:3331-3341.
17. Gibson S.I., Surosky R.T., Tye B.K. The phenotype of the minichromosome maintenance mutant mcm3 is characteristic of mutants defective in DNA replication. Mol. Cell. Biol. 1990, 10:5707-5720.
18. Gilbert D.M. In search of the holy replicator. Nat. Rev. Mol. Cell Biol. 2004, 5:848-855.
19. Ha S.A., Shin S.M., Namkoong H., Lee H., Cho G.W., Hur S.Y., Kim T.E., Kim J.W. Cancer-associated expression of minichromosome maintenance 3 gene in several human cancers and its involvement in tumorigenesis. Clin. Cancer Res. 2004, 10:8386-8395.
20. Halazonetis T.D., Gorgoulis V.G., Bartek J. An oncogene-induced DNA damage model for cancer development. Science 2008, 319:1352-1355.
21. Hendricks C.A., Almeida K.H., Stitt M.S., Jonnalagadda V.S., Rugo R.E., Kerrison G.F., Engelward B.P. Spontaneous mitotic homologous recombination at an enhanced yellow fluorescent protein (EYFP) cDNA direct repeat in transgenic mice. Proc. Natl. Acad. Sci. USA 2003, 100:6325-6330.
22. Howman E.V., Fowler K.J., Newson A.J., Redward S., MacDonald A.C., Kalitsis P., Choo K.H. Early disruption of centromeric chromatin organization in centromere protein A (Cenpa) null mice. Proc. Natl. Acad. Sci. USA 2000, 97:1148-1153.
23. Ibarra A., Schwob E., Méndez J. Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. Proc. Natl. Acad. Sci. USA 2008, 105:8956-8961.
24. Ilves I., Petojevic T., Pesavento J.J., Botchan M.R. Activation of the MCM2-7 helicase by association with Cdc45 and GINS proteins. Mol. Cell 2010, 37:247-258.
25. Ishimi Y., Okayasu I., Kato C., Kwon H.J., Kimura H., Yamada K., Song S.Y. Enhanced expression of Mcm proteins in cancer cells derived from uterine cervix. Eur. J. Biochem. 2003, 270:1089-1101.
26. Kunnev D., Rusiniak M.E., Kudla A., Freeland A., Cady G.K., Pruitt S.C. DNA damage response and tumorigenesis in Mcm2-deficient mice. Oncogene 2010, 29:3630-3638.
27. Lee J.A., Carvalho C.M., Lupski J.R. A DNA replication mechanism for generating nonrecurrent rearrangements associated with genomic disorders. Cell 2007, 131:1235-1247.
28. Li X.C., Schimenti J.C., Tye B.K. Aneuploidy and improved growth are coincident but not causal in a yeast cancer model. PLoS Biol. 2009, 7:e1000161.
29. Liang D.T., Hodson J.A., Forsburg S.L. Reduced dosage of a single fission yeast MCM protein causes genetic instability and S phase delay. J. Cell Sci. 1999, 112:559-567.
30. Moyer S.E., Lewis P.W., Botchan M.R. Isolation of the Cdc45/Mcm2-7/GINS (CMG) complex, a candidate for the eukaryotic DNA replication fork helicase. Proc. Natl. Acad. Sci. USA 2006, 103:10236-10241.
31. Naim V., Rosselli F. The FANC pathway and BLM collaborate during mitosis to prevent micro-nucleation and chromosome abnormalities. Nat. Cell Biol. 2009, 11:761-768.
32. Negrini S., Gorgoulis V.G., Halazonetis T.D. Genomic instability-an evolving hallmark of cancer. Nat. Rev. Mol. Cell Biol. 2010, 11:220-228.
33. Orr S.J., Gaymes T., Ladon D., Chronis C., Czepulkowski B., Wang R., Mufti G.J., Marcotte E.M., Thomas N.S. Reducing MCM levels in human primary T cells during the G(0)->G(1) transition causes genomic instability during the first cell cycle. Oncogene 2010, 29:3803-3814.
34. Paulsen R.D., Cimprich K.A. The ATR pathway: fine-tuning the fork. DNA Repair (Amst.) 2007, 6:953-966.
35. Petermann E., Orta M.L., Issaeva N., Schultz N., Helleday T. Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol. Cell 2010, 37:492-502.
36. Pileri S.A., Grogan T.M., Harris N.L., Banks P., Campo E., Chan J.K., Favera R.D., Delsol G., De Wolf-Peeters C., Falini B., et al. Tumours of histiocytes and accessory dendritic cells: an immunohistochemical approach to classification from the International Lymphoma Study Group based on 61 cases. Histopathology 2002, 41:1-29.
37. Prakash S., Johnson R.E., Prakash L. Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu. Rev. Biochem. 2005, 74:317-353.
38. Pruitt S.C., Bailey K.J., Freeland A. Reduced Mcm2 expression results in severe stem/progenitor cell deficiency and cancer. Stem Cells 2007, 25:3121-3132.
39. 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. J. Biol. Chem. 1998, 273:5858-5868.
40. Saleh-Gohari N., Bryant H.E., Schultz N., Parker K.M., Cassel T.N., Helleday T. Spontaneous homologous recombination is induced by collapsed replication forks that are caused by endogenous DNA single-strand breaks. Mol. Cell. Biol. 2005, 25:7158-7169.
41. Sclafani R.A., Holzen T.M. Cell cycle regulation of DNA replication. Annu. Rev. Genet. 2007, 41:237-280.
42. Sherr C.J. The Pezcoller lecture: cancer cell cycles revisited. Cancer Res. 2000, 60:3689-3695.
43. Shi Q., King R.W. Chromosome nondisjunction yields tetraploid rather than aneuploid cells in human cell lines. Nature 2005, 437:1038-1042.
44. Shima N., Alcaraz A., Liachko I., Buske T.R., Andrews C.A., Munroe R.J., Hartford S.A., Tye B.K., Schimenti J.C. A viable allele of Mcm4 causes chromosome instability and mammary adenocarcinomas in mice. Nat. Genet. 2007, 39:93-98.
45. Sims A.E., Spiteri E., Sims R.J., Arita A.G., Lach F.P., Landers T., Wurm M., Freund M., Neveling K., Hanenberg H., et al. FANCI is a second monoubiquitinated member of the Fanconi anemia pathway. Nat. Struct. Mol. Biol. 2007, 14:564-567.
46. Smogorzewska A., Matsuoka S., Vinciguerra P., McDonald E.R., Hurov K.E., Luo J., Ballif B.A., Gygi S.P., Hofmann K., D'Andrea A.D., Elledge S.J. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 2007, 129:289-301.
47. Sugimura K., Takebayashi S., Ogata S., Taguchi H., Okumura K. Non-denaturing fluorescence in situ hybridization to find replication origins in a specific genome region on the DNA fiber. Biosci. Biotechnol. Biochem. 2007, 71:627-632.
48. Todorov I.T., Attaran A., Kearsey S.E. BM28, a human member of the MCM2-3-5 family, is displaced from chromatin during DNA replication. J. Cell Biol. 1995, 129:1433-1445.
49. Tsao C.C., Geisen C., Abraham R.T. Interaction between human MCM7 and Rad17 proteins is required for replication checkpoint signaling. EMBO J. 2004, 23:4660-4669.
50. Tye B.K. MCM proteins in DNA replication. Annu. Rev. Biochem. 1999, 68:649-686.
51. Wang X., Zou L., Lu T., Bao S., Hurov K.E., Hittelman W.N., Elledge S.J., Li L. Rad17 phosphorylation is required for claspin recruitment and Chk1 activation in response to replication stress. Mol. Cell 2006, 23:331-341.
52. Williams B.R., Prabhu V.R., Hunter K.E., Glazier C.M., Whittaker C.A., Housman D.E., Amon A. Aneuploidy affects proliferation and spontaneous immortalization in mammalian cells. Science 2008, 322:703-709.
53. Woodward A.M., Göhler T., Luciani M.G., Oehlmann M., Ge X., Gartner A., Jackson D.A., Blow J.J. Excess Mcm2-7 license dormant origins of replication that can be used under conditions of replicative stress. J. Cell Biol. 2006, 173:673-683.
54. Yan H., Merchant A.M., Tye B.K. Cell cycle-regulated nuclear localization of MCM2 and MCM3, which are required for the initiation of DNA synthesis at chromosomal replication origins in yeast. Genes Dev. 1993, 7:2149-2160.
55. Zou L., Elledge S.J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 2003, 300:1542-1548.