Chronic DNA Replication Stress Reduces Replicative Lifespan of Cells by TRP53-Dependent, microRNA-Assisted MCM2-7 Downregulation

PLoS Genetics

Volumn 12, Issue 1, 2016, Pages

  Bai, Gongshi ^a   Smolka, Marcus B ^a,b   Schimenti, John C ^a  

^a Department of Obstetrics Gynecology   (United States)

^b School of Integrative Plant Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; HELICASE; MINICHROMOSOME MAINTENANCE PROTEIN 2; MINICHROMOSOME MAINTENANCE PROTEIN 4; MINICHROMOSOME MAINTENANCE PROTEIN 7; PROTEIN P53; MICRORNA; MINICHROMOSOME MAINTENANCE PROTEIN; MIRN34 MICRORNA, MOUSE;

ANIMAL CELL; ARTICLE; CELL AGING; CELL CYCLE ARREST; CELL CYCLE S PHASE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DNA REPLICATION; DOWN REGULATION; ENZYME ACTIVITY; FEMALE; GENE OVEREXPRESSION; GENOMIC INSTABILITY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN STABILITY; PROTEIN SYNTHESIS; RNA SEQUENCE; UPREGULATION; ANIMAL; BIOSYNTHESIS; CELL CYCLE CHECKPOINT; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM;

ANIMALS; CELL CYCLE CHECKPOINTS; CELL PROLIFERATION; DNA REPLICATION; FIBROBLASTS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOMIC INSTABILITY; HUMANS; MICE; MICRORNAS; MINICHROMOSOME MAINTENANCE PROTEINS;

EID: 84958729883     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005787     Document Type: Article

References (66)

1. Sclafani RA, Holzen TM, (2007) Cell cycle regulation of DNA replication. Annu Rev Genet 41: 237–80. doi: 10.1146/annurev.genet.41.110306.130308 17630848
2. Blow JJ, Laskey RA, (1988) A role for the nuclear envelope in controlling DNA replication within the cell cycle. Nature 332(6164): 546–8. doi: 10.1038/332546a0 3357511
3. Bell SP, Stillman B, (1992) ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex. Nature 357(6374): 128–34. doi: 10.1038/357128a0 1579162
4. Bell SP, Dutta A, (2002) DNA replication in eukaryotic cells. Annu Rev Biochem 71: 333–74. doi: 10.1146/annurev.biochem.71.110601.135425 12045100
5. Blow JJ, Dutta A, (2005) Preventing re-replication of chromosomal DNA. Nat Rev Mol Cell Biol 6(6): 476–86. doi: 10.1038/nrm1663 15928711
6. Moyer SE, Lewis PW, Botchan MR, (2006) Isolation of the Cdc45/Mcm2-7/GINS (CMG) complex, a candidate for the eukaryotic DNA replication fork helicase. Proc Natl Acad Sci U S A 103(27): 10236–41. doi: 10.1073/pnas.0602400103 16798881
7. Bochman ML, Schwacha A, (2008) The Mcm2-7 complex has in vitro helicase activity. Mol Cell 31(2): 287–93. doi: 10.1016/j.molcel.2008.05.020 18657510
8. Errico A, Costanzo V, Hunt T, (2007) Tipin is required for stalled replication forks to resume DNA replication after removal of aphidicolin in Xenopus egg extracts. Proc Natl Acad Sci U S A 104(38): 14929–34. doi: 10.1073/pnas.0706347104 17846426
9. Labib K, Tercero JA, Diffley JF, (2000) Uninterrupted MCM2-7 function required for DNA replication fork progression. Science 288(5471): 1643–7. 10834843
10. Bailis JM, Luche DD, Hunter T, Forsburg SL, (2008) Minichromosome maintenance proteins interact with checkpoint and recombination proteins to promote s-phase genome stability. Mol Cell Biol 28(5): 1724–38. doi: 10.1128/MCB.01717-07 18180284
11. Zeman MK, Cimprich KA, (2014) Causes and consequences of replication stress. Nat Cell Biol 16(1): 2–9. doi: 10.1038/ncb2897 24366029
12. Negrini S, Gorgoulis VG, Halazonetis TD, (2010) Genomic instability—an evolving hallmark of cancer. Nat Rev Mol Cell Biol 11(3): 220–8. doi: 10.1038/nrm2858 20177397
13. Allen C, Ashley AK, Hromas R, Nickoloff JA, (2011) More forks on the road to replication stress recovery. J Mol Cell Biol 3(1): 4–12. doi: 10.1093/jmcb/mjq049 21278446
14. Woodward AM, Gohler T, Luciani MG, Oehlmann M, Ge X, Gartner A, et al. (2006) Excess Mcm2-7 license dormant origins of replication that can be used under conditions of replicative stress. J Cell Biol 173(5): 673–83. doi: 10.1083/jcb.200602108 16754955
15. Feng D, Tu Z, Wu W, Liang C, (2003) Inhibiting the expression of DNA replication-initiation proteins induces apoptosis in human cancer cells. Cancer Res 63(21): 7356–64. 14612534
16. Ibarra A, Schwob E, Mendez J, (2008) Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. Proc Natl Acad Sci U S A 105(26): 8956–61. doi: 10.1073/pnas.0803978105 18579778
17. Ge XQ, Jackson DA, Blow JJ, (2007) Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes Dev 21(24): 3331–41. doi: 10.1101/gad.457807 18079179
18. Blow JJ, Ge XQ, Jackson DA, (2011) How dormant origins promote complete genome replication. Trends Biochem Sci 36(8): 405–14. doi: 10.1016/j.tibs.2011.05.002 21641805
19. Blow JJ, Gillespie PJ, (2008) Replication licensing and cancer—a fatal entanglement? Nat Rev Cancer 8(10): 799–806. doi: 10.1038/nrc2500 18756287
20. Shreeram S, Sparks A, Lane DP, Blow JJ, (2002) Cell type-specific responses of human cells to inhibition of replication licensing. Oncogene 21(43): 6624–32. doi: 10.1038/sj.onc.1205910 12242660
21. Campisi J, d'Adda di Fagagna F, (2007) Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol 8(9): 729–40. doi: 10.1038/nrm2233 17667954
22. Kamijo T, Zindy F, Roussel MF, Quelle DE, Downing JR, Ashmun RA, et al. (1997) Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 91(5): 649–59. 9393858
23. d'Adda di Fagagna F, (2008) Living on a break: cellular senescence as a DNA-damage response. Nat Rev Cancer 8(7): 512–22. doi: 10.1038/nrc2440 18574463
24. Feng Z, Zhang C, Wu R, Hu W, (2011) Tumor suppressor p53 meets microRNAs. J Mol Cell Biol 3(1): 44–50. doi: 10.1093/jmcb/mjq040 21278451
25. He L, He X, Lim LP, de Stanchina E, Xuan Z, Liang Y, et al. (2007) A microRNA component of the p53 tumour suppressor network. Nature 447(7148): 1130–4. doi: 10.1038/nature05939 17554337
26. Suzuki HI, Yamagata K, Sugimoto K, Iwamoto T, Kato S, Miyazono K, (2009) Modulation of microRNA processing by p53. Nature 460(7254): 529–33. doi: 10.1038/nature08199 19626115
27. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP, (2008) The impact of microRNAs on protein output. Nature 455(7209): 64–71. doi: 10.1038/nature07242 18668037
28. Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N, (2008) Widespread changes in protein synthesis induced by microRNAs. Nature 455(7209): 58–63. doi: 10.1038/nature07228 18668040
29. Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W, (2006) Stress-induced reversal of microRNA repression and mRNA P-body localization in human cells. Cold Spring Harb Symp Quant Biol 71: 513–21. doi: 10.1101/sqb.2006.71.038 17381334
30. Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W, (2006) Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125(6): 1111–24. doi: 10.1016/j.cell.2006.04.031 16777601
31. Shima N, Alcaraz A, Liachko I, Buske TR, Andrews CA, Munroe RJ, et al. (2007) A viable allele of Mcm4 causes chromosome instability and mammary adenocarcinomas in mice. Nat Genet 39(1): 93–8. doi: 10.1038/ng1936 17143284
32. Chuang CH, Wallace MD, Abratte C, Southard T, Schimenti JC, (2010) Incremental genetic perturbations to MCM2-7 expression and subcellular distribution reveal exquisite sensitivity of mice to DNA replication stress. PLoS Genet 6(9): e1001110. doi: 10.1371/journal.pgen.1001110 20838603
33. Chuang CH, Yang D, Bai G, Freeland A, Pruitt SC, Schimenti JC, (2012) Post-transcriptional homeostasis and regulation of MCM2-7 in mammalian cells. Nucleic Acids Res 40(11): 4914–24. doi: 10.1093/nar/gks176 22362746
34. Kawabata T, Luebben SW, Yamaguchi S, Ilves I, Matise I, Buske T, et al. (2011) Stalled fork rescue via dormant replication origins in unchallenged S phase promotes proper chromosome segregation and tumor suppression. Mol Cell 41(5): 543–53. doi: 10.1016/j.molcel.2011.02.006 21362550
35. Kunnev D, Rusiniak ME, Kudla A, Freeland A, Cady GK, Pruitt SC, (2010) DNA damage response and tumorigenesis in Mcm2-deficient mice. Oncogene 29(25): 3630–8. doi: 10.1038/onc.2010.125 20440269
36. Pruitt SC, Bailey KJ, Freeland A, (2007) Reduced Mcm2 expression results in severe stem/progenitor cell deficiency and cancer. Stem Cells 25(12): 3121–32. doi: 10.1634/stemcells.2007-0483 17717065
37. Parrinello S, Samper E, Krtolica A, Goldstein J, Melov S, Campisi J, (2003) Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat Cell Biol 5(8): 741–7. doi: 10.1038/ncb1024 12855956
38. Flach J, Bakker ST, Mohrin M, Conroy PC, Pietras EM, Reynaud D, et al. (2014) Replication stress is a potent driver of functional decline in ageing haematopoietic stem cells. Nature 512(7513): 198–202. doi: 10.1038/nature13619 25079315
39. Kawabata T, Yamaguchi S, Buske T, Luebben SW, Wallace M, Matise I, et al. (2011) A reduction of licensed origins reveals strain-specific replication dynamics in mice. Mamm Genome 22(9–10): 506–17. doi: 10.1007/s00335-011-9333-7 21611832
40. Kliszczak AE, Rainey MD, Harhen B, Boisvert FM, Santocanale C, (2011) DNA mediated chromatin pull-down for the study of chromatin replication. Sci Rep 1: 95. doi: 10.1038/srep00095 22355613
41. Sirbu BM, Couch FB, Feigerle JT, Bhaskara S, Hiebert SW, Cortez D, (2011) Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev 25(12): 1320–7. doi: 10.1101/gad.2053211 21685366
42. Dungrawala H, Rose KL, Bhat KP, Mohni KN, Glick GG, Couch FB, et al. (2015) The Replication Checkpoint Prevents Two Types of Fork Collapse without Regulating Replisome Stability. Mol Cell. doi: 10.1016/j.molcel.2015.07.030 26365379
43. Byun TS, Pacek M, Yee MC, Walter JC, Cimprich KA, (2005) Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev 19(9): 1040–52. doi: 10.1101/gad.1301205 15833913
44. Groth A, Corpet A, Cook AJ, Roche D, Bartek J, Lukas J, et al. (2007) Regulation of replication fork progression through histone supply and demand. Science 318(5858): 1928–31. 18096807
45. Monasor A, Murga M, Lopez-Contreras AJ, Navas C, Gomez G, Pisano DG, et al. (2013) INK4a/ARF limits the expansion of cells suffering from replication stress. Cell Cycle 12(12): 1948–54. doi: 10.4161/cc.25017 23676215
46. Ahuja D, Saenz-Robles MT, Pipas JM, (2005) SV40 large T antigen targets multiple cellular pathways to elicit cellular transformation. Oncogene 24(52): 7729–45. doi: 10.1038/sj.onc.1209046 16299533
47. Lal A, Thomas MP, Altschuler G, Navarro F, O'Day E, Li XL, et al. (2011) Capture of microRNA-bound mRNAs identifies the tumor suppressor miR-34a as a regulator of growth factor signaling. PLoS Genet 7(11): e1002363. doi: 10.1371/journal.pgen.1002363 22102825
48. Kaller M, Liffers ST, Oeljeklaus S, Kuhlmann K, Roh S, Hoffmann R, et al. (2011) Genome-wide characterization of miR-34a induced changes in protein and mRNA expression by a combined pulsed SILAC and microarray analysis. Mol Cell Proteomics 10(8): M111.010462. doi: 10.1074/mcp.M111.010462 21566225
49. Wallace MD, Pfefferle AD, Shen L, McNairn AJ, Cerami EG, Fallon BL, et al. (2012) Comparative oncogenomics implicates the neurofibromin 1 gene (NF1) as a breast cancer driver. Genetics 192(2): 385–96. doi: 10.1534/genetics.112.142802 22851646
50. Madine MA, Swietlik M, Pelizon C, Romanowski P, Mills AD, Laskey RA, (2000) The roles of the MCM, ORC, and Cdc6 proteins in determining the replication competence of chromatin in quiescent cells. J Struct Biol 129(2–3): 198–210. doi: 10.1006/jsbi.2000.4218 10806069
51. Lau E, Tsuji T, Guo L, Lu SH, Jiang W, (2007) The role of pre-replicative complex (pre-RC) components in oncogenesis. FASEB J 21(14): 3786–94. doi: 10.1096/fj.07-8900rev 17690155
52. Freeman A, Morris LS, Mills AD, Stoeber K, Laskey RA, Williams GH, et al. (1999) Minichromosome maintenance proteins as biological markers of dysplasia and malignancy. Clin Cancer Res 5(8): 2121–32. 10473096
53. Gineau L, Cognet C, Kara N, Lach FP, Dunne J, Veturi U, et al. (2012) Partial MCM4 deficiency in patients with growth retardation, adrenal insufficiency, and natural killer cell deficiency. J Clin Invest 122(3): 821–32. doi: 10.1172/JCI61014 22354167
54. Hughes CR, Guasti L, Meimaridou E, Chuang CH, Schimenti JC, King PJ, et al. (2012) MCM4 mutation causes adrenal failure, short stature, and natural killer cell deficiency in humans. J Clin Invest 122(3): 814–20. doi: 10.1172/JCI60224 22354170
55. Das M, Singh S, Pradhan S, Narayan G, (2014) MCM Paradox: Abundance of Eukaryotic Replicative Helicases and Genomic Integrity. Mol Biol Int 2014: 574850. doi: 10.1155/2014/574850 25386362
56. Cortez D, Glick G, Elledge SJ, (2004) Minichromosome maintenance proteins are direct targets of the ATM and ATR checkpoint kinases. Proc Natl Acad Sci U S A 101(27): 10078–83. doi: 10.1073/pnas.0403410101 15210935
57. Ishimi Y, Komamura-Kohno Y, Kwon HJ, Yamada K, Nakanishi M, (2003) Identification of MCM4 as a target of the DNA replication block checkpoint system. J Biol Chem 278(27): 24644–50. doi: 10.1074/jbc.M213252200 12714602
58. Sabatinos SA, Green MD, Forsburg SL, (2012) Continued DNA synthesis in replication checkpoint mutants leads to fork collapse. Mol Cell Biol 32(24): 4986–97. doi: 10.1128/MCB.01060-12 23045396
59. Rufini A, Tucci P, Celardo I, Melino G, (2013) Senescence and aging: the critical roles of p53. Oncogene 32(43): 5129–43. doi: 10.1038/onc.2012.640 23416979
60. Nevis KR, Cordeiro-Stone M, Cook JG, (2009) Origin licensing and p53 status regulate Cdk2 activity during G(1). Cell Cycle 8(12): 1952–63. 19440053
61. Cheng CY, Hwang CI, Corney DC, Flesken-Nikitin A, Jiang L, Oner GM, et al. (2014) miR-34 cooperates with p53 in suppression of prostate cancer by joint regulation of stem cell compartment. Cell Rep 6(6): 1000–7. doi: 10.1016/j.celrep.2014.02.023 24630988
62. Concepcion CP, Han YC, Mu P, Bonetti C, Yao E, D'Andrea A, et al. (2012) Intact p53-dependent responses in miR-34-deficient mice. PLoS Genet 8(7): e1002797. doi: 10.1371/journal.pgen.1002797 22844244
63. Li XC, Schimenti JC, Tye BK, (2009) Aneuploidy and improved growth are coincident but not causal in a yeast cancer model. PLoS Biol 7(7): e1000161. doi: 10.1371/journal.pbio.1000161 19636358
64. Alabert C, Bukowski-Wills JC, Lee SB, Kustatscher G, Nakamura K, de Lima Alves F, et al. (2014) Nascent chromatin capture proteomics determines chromatin dynamics during DNA replication and identifies unknown fork components. Nat Cell Biol 16(3): 281–93. doi: 10.1038/ncb2918 24561620
65. Debacq-Chainiaux F, Erusalimsky JD, Campisi J, Toussaint O, (2009) Protocols to detect senescence-associated beta-galactosidase (SA-betagal) activity, a biomarker of senescent cells in culture and in vivo. Nat Protoc 4(12): 1798–806. doi: 10.1038/nprot.2009.191 20010931
66. Anders S, Huber W, (2010) Differential expression analysis for sequence count data. Genome Biol 11(10): R106. doi: 10.1186/gb-2010-11-10-r106 20979621