Replication fork integrity and intra-S phase checkpoint suppress gene amplification

Nucleic Acids Research

Volumn 43, Issue 5, 2015, Pages 2678-2690

  Kondratova, Anna ^a   Watanabe, Takaaki ^a,b   Marotta, Michael ^a   Cannon, Matthew ^a   Segall, Anca M ^c   Serre, David ^a   Tanaka, Hisashi ^a,b  

^a LERNER RESEARCH INSTITUTE   (United States)

^b CEDARS SINAI MEDICAL CENTER   (United States)

^c SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; ATR PROTEIN; MRE11 PROTEIN; MRN COMPLEX; NUCLEIC ACID BINDING PROTEIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; DIHYDROFOLATE REDUCTASE; DNA BINDING PROTEIN; DNA LIGASE; NUCLEAR PROTEIN; PROTEIN P53;

ANIMAL CELL; ARTICLE; CELL CYCLE PROGRESSION; CELL VIABILITY; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; GENE AMPLIFICATION; GENE SILENCING; GENETIC TRANSCRIPTION; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; S PHASE CELL CYCLE CHECKPOINT; SINGLE STRANDED DNA BREAK; TUMOR SUPPRESSOR GENE; ANIMAL; CHO CELL LINE; CRICETULUS; DNA MICROARRAY; DNA REPAIR; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENETICS; HAMSTER; HEK293 CELL LINE; HUMAN; METABOLISM; MUTATION; WESTERN BLOTTING;

MAMMALIA;

ANIMALS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; BLOTTING, WESTERN; CELL CYCLE PROTEINS; CHO CELLS; CRICETINAE; CRICETULUS; DNA BREAKS, DOUBLE-STRANDED; DNA BREAKS, SINGLE-STRANDED; DNA REPAIR; DNA REPAIR ENZYMES; DNA REPLICATION; DNA-BINDING PROTEINS; FLOW CYTOMETRY; GENE AMPLIFICATION; GENE EXPRESSION PROFILING; HEK293 CELLS; HUMANS; MUTATION; NUCLEAR PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; S PHASE CELL CYCLE CHECKPOINTS; TETRAHYDROFOLATE DEHYDROGENASE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84937598041     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv084     Document Type: Article

References (82)

1. Engelman, J. A., Zejnullahu, K., Mitsudomi, T., Song, Y., Hyland, C., Park, J. O., Lindeman, N., Gale, C. M., Zhao, X., Christensen, J. et al. (2007) MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science, 316, 1039-1043.
2. Schwab, M., Alitalo, K., Klempnauer, K. H., Varmus, H. E., Bishop, J. M., Gilbert, F., Brodeur, G., Goldstein, M. and Trent, J. (1983) Amplified DNA with limited homology to myc cellular oncogene is shared by human neuroblastoma cell lines and a neuroblastoma tumour. Nature, 305, 245-248.
3. Slamon, D. J., Clark, G. M., Wong, S. G., Levin, W. J., Ullrich, A. and McGuire, W. L. (1987) Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science, 235, 177-182.
4. Sequist, L. V., Waltman, B. A., Dias-Santagata, D., Digumarthy, S., Turke, A. B., Fidias, P., Bergethon, K., Shaw, A. T., Gettinger, S., Cosper, A. K. et al. (2011) Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Sci. Transl. Med., 3, 75ra26.
5. Tlsty, T. D., Brown, P. C. and Schimke, R. T. (1984) UV radiation facilitates methotrexate resistance and amplification of the dihydrofolate reductase gene in cultured 3T6 mouse cells. Mol. Cell. Biol., 4, 1050-1056.
6. Brown, P. C., Tlsty, T. D. and Schimke, R. T. (1983) Enhancement of methotrexate resistance and dihydrofolate reductase gene amplification by treatment of mouse 3T6 cells with hydroxyurea. Mol. Cell. Biol., 3, 1097-1107.
7. Coquelle, A., Pipiras, E., Toledo, F., Buttin, G. and Debatisse, M. (1997) Expression of fragile sites triggers intrachromosomal mammalian gene amplification and sets boundaries to early amplicons. Cell, 89, 215-225.
8. Tanaka, H., Tapscott, S. J., Trask, B. J. and Yao, M. C. (2002) Short inverted repeats initiate gene amplification through the formation of a large DNA palindrome in mammalian cells. Proc. Natl Acad. Sci. U. S. A., 99, 8772-8777.
9. Tanaka, H., Cao, Y., Bergstrom, D. A., Kooperberg, C., Tapscott, S. J. and Yao, M. C. (2007) Intrastrand annealing leads to the formation of a large DNA palindrome and determines the boundaries of genomic amplification in human cancer. Mol. Cell. Biol., 27, 1993-2002.
10. Zeman, M. K. and Cimprich, K. A. (2014) Causes and consequences of replication stress. Nat. Cell Biol., 16, 2-9.
11. Halazonetis, T. D., Gorgoulis, V. G. and Bartek, J. (2008) An oncogene-induced DNA damage model for cancer development. Science, 319, 1352-1355.
12. Bester, A. C., Roniger, M., Oren, Y. S., Im, M. M., Sarni, D., Chaoat, M., Bensimon, A., Zamir, G., Shewach, D. S. and Kerem, B. (2011) Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell, 145, 435-446.
13. Poli, J., Tsaponina, O., Crabbe, L., Keszthelyi, A., Pantesco, V., Chabes, A., Lengronne, A. and Pasero, P. (2012) dNTP pools determine fork progression and origin usage under replication stress. EMBO J., 31, 883-894.
14. Carr, A. M. and Lambert, S. (2013) Replication stress-induced genome instability: the dark side of replication maintenance by homologous recombination. J. Mol. Biol., 425, 4733-4744.
15. Errico, A. and Costanzo, V. (2012) Mechanisms of replication fork protection: a safeguard for genome stability. Crit. Rev. Biochem. Mol. Biol., 47, 222-235.
16. Maser, R. S., Mirzoeva, O. K., Wells, J., Olivares, H., Williams, B. R., Zinkel, R. A., Farnham, P. J. and Petrini, J. H. (2001) Mre11 complex and DNA replication: linkage to E2F and sites of DNA synthesis. Mol. Cell. Biol., 21, 6006-6016.
17. Mirzoeva, O. K. and Petrini, J. H. (2003) DNA replication-dependent nuclear dynamics of the Mre11 complex. Mol. Cancer Res., 1, 207-218.
18. Bryant, H. E., Petermann, E., Schultz, N., Jemth, A. S., Loseva, O., Issaeva, N., Johansson, F., Fernandez, S., McGlynn, P. and Helleday, T. (2009) PARP is activated at stalled forks to mediate Mre11-dependent replication restart and recombination. EMBO J., 28, 2601-2615.
19. Stracker, T. H. and Petrini, J. H. (2011) The MRE11 complex: starting from the ends. Nat. Rev. Mol. Cell Biol., 12, 90-103.
20. Paull, T. T. (2010) Making the best of the loose ends: Mre11/Rad50 complexes and Sae2 promote DNA double-strand break resection. DNA Repair (Amst), 9, 1283-1291.
21. Williams, G. J., Lees-Miller, S. P. and Tainer, J. A. (2010) Mre11-Rad50-Nbs1 conformations and the control of sensing, signaling, and effector responses at DNA double-strand breaks. DNA Repair (Amst), 9, 1299-1306.
22. Lee, J. H. and Paull, T. T. (2004) Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science, 304, 93-96.
23. Lee, J. H. and Paull, T. T. (2005) ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science, 308, 551-554.
24. Duursma, A. M., Driscoll, R., Elias, J. E. and Cimprich, K. A. (2013) A role for the MRN complex in ATR activation via TOPBP1 recruitment. Mol. Cell, 50, 116-122.
25. Lengsfeld, B. M., Rattray, A. J., Bhaskara, V., Ghirlando, R. and Paull, T. T. (2007) Sae2 is an endonuclease that processes hairpin DNA cooperatively with the Mre11/Rad50/Xrs2 complex. Mol. Cell, 28, 638-651.
26. Sartori, A. A., Lukas, C., Coates, J., Mistrik, M., Fu, S., Bartek, J., Baer, R., Lukas, J. and Jackson, S. P. (2007) Human CtIP promotes DNA end resection. Nature, 450, 509-514.
27. Hopfner, K. P., Karcher, A., Craig, L., Woo, T. T., Carney, J. P. and Tainer, J. A. (2001) Structural biochemistry and interaction architecture of the DNA double-strand break repair Mre11 nuclease and Rad50-ATPase. Cell, 105, 473-485.
28. Williams, R. S., Moncalian, G., Williams, J. S., Yamada, Y., Limbo, O., Shin, D. S., Groocock, L. M., Cahill, D., Hitomi, C., Guenther, G. et al. (2008) Mre11 dimers coordinate DNA end bridging and nuclease processing in double-strand-break repair. Cell, 135, 97-109.
29. Xiao, Y. and Weaver, D. T. (1997) Conditional gene targeted deletion by Cre recombinase demonstrates the requirement for the double-strand break repair Mre11 protein in murine embryonic stem cells. Nucleic Acids Res., 25, 2985-2991.
30. Yamaguchi-Iwai, Y., Sonoda, E., Sasaki, M. S., Morrison, C., Haraguchi, T., Hiraoka, Y., Yamashita, Y. M., Yagi, T., Takata, M., Price, C. et al. (1999) Mre11 is essential for the maintenance of chromosomal DNA in vertebrate cells. EMBO J., 18, 6619-6629.
31. Buis, J., Wu, Y., Deng, Y., Leddon, J., Westfield, G., Eckersdorff, M., Sekiguchi, J. M., Chang, S. and Ferguson, D. O. (2008) Mre11 nuclease activity has essential roles in DNA repair and genomic stability distinct from ATM activation. Cell, 135, 85-96.
32. Trenz, K., Smith, E., Smith, S. and Costanzo, V. (2006) ATM and ATR promote Mre11 dependent restart of collapsed replication forks and prevent accumulation of DNA breaks. EMBO J., 25, 1764-1774.
33. Costanzo, V., Robertson, K., Bibikova, M., Kim, E., Grieco, D., Gottesman, M., Carroll, D. and Gautier, J. (2001) Mre11 protein complex prevents double-strand break accumulation during chromosomal DNA replication. Mol. Cell, 8, 137-147.
34. Livingstone, L. R., White, A., Sprouse, J., Livanos, E., Jacks, T. and Tlsty, T. D. (1992) Altered cell cycle arrest and gene amplification potential accompany loss of wild-type p53. Cell, 70, 923-935.
35. Yin, Y., Tainsky, M. A., Bischoff, F. Z., Strong, L. C. and Wahl, G. M. (1992) Wild-type p53 restores cell cycle control and inhibits gene amplification in cells with mutant p53 alleles. Cell, 70, 937-948.
36. Lopes, M., Cotta-Ramusino, C., Pellicioli, A., Liberi, G., Plevani, P., Muzi-Falconi, M., Newlon, C. S. and Foiani, M. (2001) The DNA replication checkpoint response stabilizes stalled replication forks. Nature, 412, 557-561.
37. Tercero, J. A. and Diffley, J. F. (2001) Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature, 412, 553-557.
38. Couch, F. B., Bansbach, C. E., Driscoll, R., Luzwick, J. W., Glick, G. G., Betous, R., Carroll, C. M., Jung, S. Y., Qin, J., Cimprich, K. A. et al. (2013) ATR phosphorylates SMARCAL1 to prevent replication fork collapse. Genes Dev., 27, 1610-1623.
39. Ragland, R. L., Patel, S., Rivard, R. S., Smith, K., Peters, A. A., Bielinsky, A. K. and Brown, E. J. (2013) RNF4 and PLK1 are required for replication fork collapse in ATR-deficient cells. Genes Dev., 27, 2259-2273.
40. Matsuoka, S., Ballif, B. A., Smogorzewska, A., McDonald, E. R. III, Hurov, K. E., Luo, J., Bakalarski, C. E., Zhao, Z., Solimini, N., Lerenthal, Y. et al. (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science, 316, 1160-1166.
41. Zou, L. and Elledge, S. J. (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science, 300, 1542-1548.
42. Petermann, E., Woodcock, M. and Helleday, T. (2010) Chk1 promotes replication fork progression by controlling replication initiation. Proc. Natl Acad. Sci. U. S. A., 107, 16090-16095.
43. Petermann, E., Maya-Mendoza, A., Zachos, G., Gillespie, D. A., Jackson, D. A. and Caldecott, K. W. (2006) Chk1 requirement for high global rates of replication fork progression during normal vertebrate S phase. Mol. Cell. Biol., 26, 3319-3326.
44. Canman, C. E., Lim, D. S., Cimprich, K. A., Taya, Y., Tamai, K., Sakaguchi, K., Appella, E., Kastan, M. B. and Siliciano, J. D. (1998) Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science, 281, 1677-1679.
45. Chumakov, S. P., Kravchenko, J. E., Prassolov, V. S., Frolova, E. I. and Chumakov, P. M. (2010) Efficient downregulation of multiple mRNA targets with a single shRNA-expressing lentiviral vector. Plasmid, 63, 143-149.
46. Lee, J. H., Ghirlando, R., Bhaskara, V., Hoffmeyer, M. R., Gu, J. and Paull, T. T. (2003) Regulation of Mre11/Rad50 by Nbs1: effects on nucleotide-dependent DNA binding and association with ataxia-telangiectasia-like disorder mutant complexes. J. Biol. Chem., 278, 45171-45181.
47. Robinson, M. D., McCarthy, D. J. and Smyth, G. K. (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26, 139-140.
48. Stewart, G. S., Maser, R. S., Stankovic, T., Bressan, D. A., Kaplan, M. I., Jaspers, N. G., Raams, A., Byrd, P. J., Petrini, J. H. and Taylor, A. M. (1999) The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell, 99, 577-587.
49. Luria, S. E. and Delbruck, M. (1943) Mutations of bacteria from virus sensitivity to virus resistance. Genetics, 28, 491-511.
50. Utani, K., Kohno, Y., Okamoto, A. and Shimizu, N. (2010) Emergence of micronuclei and their effects on the fate of cells under replication stress. PLoS One, 5, e10089.
51. Marotta, M., Piontkivska, H. and Tanaka, H. (2012) Molecular trajectories leading to the alternative fates of duplicate genes. PLoS One, 7, e38958.
52. Olive, P. L., Wlodek, D., Durand, R. E. and Banath, J. P. (1992) Factors influencing DNA migration from individual cells subjected to gel electrophoresis. Exp. Cell Res., 198, 259-267.
53. Sogo, J. M., Lopes, M. and Foiani, M. (2002) Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science, 297, 599-602.
54. Cotta-Ramusino, C., Fachinetti, D., Lucca, C., Doksani, Y., Lopes, M., Sogo, J. and Foiani, M. (2005) Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells. Mol. Cell, 17, 153-159.
55. Dey, M., Patra, S., Su, L. Y. and Segall, A. M. (2013) Tumor cell death mediated by peptides that recognize branched intermediates of DNA replication and repair. PLoS One, 8, e78751.
56. Kepple, K. V., Boldt, J. L. and Segall, A. M. (2005) Holliday junction-binding peptides inhibit distinct junction-processing enzymes. Proc. Natl Acad. Sci. U. S. A., 102, 6867-6872.
57. Kepple, K. V., Patel, N., Salamon, P. and Segall, A. M. (2008) Interactions between branched DNAs and peptide inhibitors of DNA repair. Nucleic Acids Res., 36, 5319-5334.
58. Harrigan, J. A., Belotserkovskaya, R., Coates, J., Dimitrova, D. S., Polo, S. E., Bradshaw, C. R., Fraser, P. and Jackson, S. P. (2011) Replication stress induces 53BP1-containing OPT domains in G1 cells. J. Cell Biol., 193, 97-108.
59. Lukas, C., Savic, V., Bekker-Jensen, S., Doil, C., Neumann, B., Pedersen, R. S., Grofte, M., Chan, K. L., Hickson, I. D., Bartek, J. et al. (2011) 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat. Cell Biol., 13, 243-253.
60. Liu, S., Shiotani, B., Lahiri, M., Marechal, A., Tse, A., Leung, C. C., Glover, J. N., Yang, X. H. and Zou, L. (2011) ATR autophosphorylation as a molecular switch for checkpoint activation. Mol. Cell, 43, 192-202.
61. Abe, T., Harashima, A., Xia, T., Konno, H., Konno, K., Morales, A., Ahn, J., Gutman, D. and Barber, G. N. (2013) STING recognition of cytoplasmic DNA instigates cellular defense. Mol. Cell, 50, 5-15.
62. Moreau, S., Ferguson, J. R. and Symington, L. S. (1999) The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol. Cell. Biol., 19, 556-566.
63. Doksani, Y., Bermejo, R., Fiorani, S., Haber, J. E. and Foiani, M. (2009) Replicon dynamics, dormant origin firing, and terminal fork integrity after double-strand break formation. Cell, 137, 247-258.
64. Walter, J. and Newport, J. (2000) Initiation of eukaryotic DNA replication: origin unwinding and sequential chromatin association of Cdc45, RPA, and DNA polymerase alpha. Mol. Cell, 5, 617-627.
65. Byun, T. S., Pacek, M., Yee, M. C., Walter, J. C. and Cimprich, K. A. (2005) Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev., 19, 1040-1052.
66. Tittel-Elmer, M., Alabert, C., Pasero, P. and Cobb, J. A. (2009) The MRX complex stabilizes the replisome independently of the S phase checkpoint during replication stress. EMBO J., 28, 1142-1156.
67. Tittel-Elmer, M., Lengronne, A., Davidson, M. B., Bacal, J., Francois, P., Hohl, M., Petrini, J. H., Pasero, P. and Cobb, J. A. (2012) Cohesin association to replication sites depends on rad50 and promotes fork restart. Mol. Cell, 48, 98-108.
68. Hashimoto, Y., Puddu, F. and Costanzo, V. (2012) RAD51- and MRE11-dependent reassembly of uncoupled CMG helicase complex at collapsed replication forks. Nat. Struct. Mol. Biol., 19, 17-24.
69. Sirbu, B. M., Couch, F. B., Feigerle, J. T., Bhaskara, S., Hiebert, S. W. and Cortez, D. (2011) Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev., 25, 1320-1327.
70. Mimitou, E. P. and Symington, L. S. (2008) Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature, 455, 770-774.
71. Eid, W., Steger, M., El-Shemerly, M., Ferretti, L. P., Pena-Diaz, J., Konig, C., Valtorta, E., Sartori, A. A. and Ferrari, S. (2010) DNA end resection by CtIP and exonuclease 1 prevents genomic instability. EMBO Rep., 11, 962-968.
72. Tsang, E., Miyabe, I., Iraqui, I., Zheng, J., Lambert, S. A. and Carr, A. M. (2014) The extent of error-prone replication restart by homologous recombination is controlled by Exo1 and checkpoint proteins. J. Cell Sci., 127, 2983-2994.
73. Brown, E. J. and Baltimore, D. (2000) ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev., 14, 397-402.
74. Ge, X. Q., Jackson, D. A. and Blow, J. J. (2007) Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes Dev., 21, 3331-3341.
75. Ibarra, A., Schwob, E. and 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, 8956-8961.
76. Green, B. M., Finn, K. J. and Li, J. J. (2010) Loss of DNA replication control is a potent inducer of gene amplification. Science, 329, 943-946.
77. Watanabe, T., Tanabe, H. and Horiuchi, T. (2011) Gene amplification system based on double rolling-circle replication as a model for oncogene-type amplification. Nucleic Acids Res., 39, e106.
78. Narayanan, V., Mieczkowski, P. A., Kim, H. M., Petes, T. D. and Lobachev, K. S. (2006) The pattern of gene amplification is determined by the chromosomal location of hairpin-capped breaks. Cell, 125, 1283-1296.
79. Marotta, M., Chen, X., Watanabe, T., Faber, P. W., Diede, S. J., Tapscott, S., Tubbs, R., Kondratova, A., Stephens, R. and Tanaka, H. (2013) Homology-mediated end-capping as a primary step of sister chromatid fusion in the breakage-fusion-bridge cycles. Nucleic Acids Res., 41, 9732-9740.
80. Lobachev, K. S., Gordenin, D. A. and Resnick, M. A. (2002) TheMre11 complex is required for repair of hairpin-capped double-strand breaks and prevention of chromosome rearrangements. Cell, 108, 183-193.
81. Rattray, A. J., Shafer, B. K., Neelam, B. and Strathern, J. N. (2005) A mechanism of palindromic gene amplification in Saccharomyces cerevisiae. Genes Dev., 19, 1390-1399.
82. Mizuno, K., Miyabe, I., Schalbetter, S. A., Carr, A. M. and Murray, J. M. (2013) Recombination-restarted replication makes inverted chromosome fusions at inverted repeats. Nature, 493, 246-249.