A concomitant loss of dormant origins and FANCC exacerbates genome instability by impairing DNA replication fork progression

Nucleic Acids Research

Volumn 42, Issue 9, 2014, Pages 5605-5615

  Luebben, Spencer W ^a   Kawabata, Tsuyoshi ^a   Johnson, Charles S ^b,c   O'sullivan, M Gerard ^b,c   Shima, Naoko ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FANCONI ANEMIA GROUP C PROTEIN; MINICHROMOSOME MAINTENANCE PROTEIN 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CARCINOGENESIS; CONTROLLED STUDY; DISEASE COURSE; DNA DAMAGE; DNA REPLICATION ORIGIN; EMBRYO; EMBRYO CELL; FANCC GENE; FANCONI ANEMIA; FIBROBLAST; GENETIC MARKER; GENOME ANALYSIS; GENOMIC INSTABILITY; HOMOZYGOTE; MCM4 GENE; MOUSE; NONHUMAN; NULL ALLELE; PERINATAL DEATH; PRIORITY JOURNAL; PROPHASE;

ANIMALS; CELL NUCLEUS; CELLS, CULTURED; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA REPLICATION; DNA-BINDING PROTEINS; FANCONI ANEMIA; FANCONI ANEMIA COMPLEMENTATION GROUP C PROTEIN; GENOMIC INSTABILITY; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRONUCLEUS TESTS; MINICHROMOSOME MAINTENANCE COMPLEX COMPONENT 4; S PHASE CELL CYCLE CHECKPOINTS; SIGNAL TRANSDUCTION;

EID: 84901293712     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku170     Document Type: Article

References (67)

1. Yekezare, M., Gómez-González, B. and Diffley, J.F.X. (2013) Controlling DNA replication origins in response to DNA damage-inhibit globally, activate locally. J. Cell Sci., 126, 1297-1306
2. Blow, J.J. and Dutta, A. (2005) Preventing re-replication of chromosomal DNA.Nat. Rev. Mol. Cell Biol., 6, 476-486
3. Sclafani, R.A. and Holzen, T.M. (2007) Cell cycle regulation of DNA replication. Annu. Rev. Genet., 41, 237-280
4. Labib, K., Tercero, J.A. and Diffley, J.F.X. (2000) Uninterrupted MCM2-7 function required for DNA replication fork progression. Science, 288, 1643-1647. (Pubitemid 30387430
5. Pacek, M. and Walter, J.C. (2004) A requirement for MCM7 and Cdc45 in chromosome unwinding during eukaryotic DNA replication. EMBO J., 23, 3667-3676. (Pubitemid 39336288
6. Shechter, D., Ying, C.Y. and Gautier, J. (2004) DNA unwinding is an MCM complex-dependent and ATP hydrolysis-dependent process. J. Biol. Chem., 279, 45586-45593
7. Moyer, S.E., Lewis, P.W. and Botchan, M.R. (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, 10236-10241
8. Ilves, I., Petojevic, T., Pesavento, J.J. and Botchan, M.R. (2010) Activation of the MCM2-7 helicase by association with Cdc45 and GINS proteins. Mol. Cell, 37, 247-258
9. Burkhart, R., Schulte, D., Hu, B., Musahl, C., Göhring, F. and Knippers, R. (1995) Interactions of human nuclear proteins P1Mcm3 and P1Cdc46. Eur. J. Biochem., 228, 431-438
10. Rowles, A., Chong, J.P.J., Brown, L., Howell, M., Evan, G.I. and Blow, J.J. (1996) Interaction between the origin recognition complex and the replication licensing system in Xenopus. Cell, 87, 287-296. (Pubitemid 26359006
11. Mahbubani, H.M., Chong, J.P.J., Chevalier, S., Thömmes, P. and Blow, J.J. (1997) Cell cycle regulation of the replication licensing system: Involvement of a Cdk-dependent inhibitor. J. Cell Biol., 136, 125-135. (Pubitemid 27044809
12. Edwards, M.C., Tutter, A.V., Cvetic, C., Gilbert, C.H., Prokhorova, T.A. and Walter, J.C. (2002) MCM2-7 complexes bind chromatin in a distributed pattern surrounding the origin recognition complex in Xenopus egg extracts. J. Biol. Chem., 277, 33049-33057
13. Woodward, A.M., Göhler, T., Luciani, M.G., Oehlmann, M., Ge, X., Gartner, A., Jackson, D.A. and Blow, J.J. (2006) Excess Mcm2-7 license dormant origins of replication that can be used under conditions of replicative stress. J. Cell. Biol., 173, 673-683
14. 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. (Pubitemid 350277759
15. Ibarra, A., Schwob, E. and Ḿendez, 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
16. Kawabata, T., Luebben, S.W., Yamaguchi, S., Ilves, I., Matise, I., Buske, T., Botchan, M.R. and Shima, N. (2011) Stalled fork rescue via dormant replication origins in unchallenged S phase promotes proper chromosome segregation and tumor suppression. Mol. Cell, 41, 543-553
17. Shima, N., Alcaraz, A., Liachko, I., Buske, T.R., Andrews, C.A., Munroe, R.J., Hartford, S.A., Tye, B.K. and Schimenti, J.C. (2007) A viable allele of Mcm4 causes chromosome instability and mammary adenocarcinomas in mice. Nat. Genet., 39, 93-98
18. Blow, J.J., Ge, X.Q. and Jackson, D.A. (2011) How dormant origins promote complete genome replication. Trends Biochem. Sci., 36, 405-414
19. Crossan, G.P. and Patel, K.J. (2012) The Fanconi anaemia pathway orchestrates incisions at sites of crosslinked DNA. J. Pathol., 226, 326-337
20. Kottemann, M.C. and Smogorzewska, A. (2013) Fanconi anaemia and the repair of Watson and Crick DNA crosslinks. Nature, 493, 356-363
21. Kashiyama, K., Nakazawa, Y., Pilz, D.T., Guo, C., Shimada, M., Sasaki, K., Fawcett, H., Wing, J.F., Lewin, S.O., Carr, L. et al. (2013) Malfunction of nuclease ERCC1-XPF results in diverse clinical manifestations and causes Cockayne syndrome, xeroderma pigmentosum, and Fanconi anemia. Am. J. Hum. Genet., 92, 807-819
22. Bogliolo, M., Schuster, B., Stoepker, C., Derkunt, B., Su, Y., Raams, A., Trujillo, J.P., Minguillón, J., Raḿirez, M.J., Pujol, R. et al. (2013) Mutations in ERCC4, encoding the DNA-repair endonuclease XPF, cause Fanconi anemia. Am. J. Hum. Genet., 92, 800-806
23. Constantinou, A. (2012) Rescue of replication failure by Fanconi anaemia proteins. Chromosoma, 121, 21-36
24. Kee, Y. and D'Andrea, A.D. (2010) Expanded roles of the Fanconi anemia pathway in preserving genomic stability. Genes Dev., 24, 1680-1694
25. Langevin, F., Crossan, G.P., Rosado, I.V., Arends, M.J. and Patel, K.J. (2011) Fancd2 counteracts the toxic effects of naturally produced aldehydes in mice. Nature, 475, 53-58
26. Garcia-Higuera, I., Taniguchi, T., Ganesan, S., Meyn, M.S., Timmers, C., Hejna, J., Grompe, M. and D'Andrea, A.D. (2001) Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol. Cell, 7, 249-262
27. 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. (2007) FANCI is a second monoubiquitinated member of the Fanconi anemia pathway. Nat. Struct. Mol. Biol., 14, 564-567
28. Smogorzewska, A., Matsuoka, S., Vinciguerra, P., McDonald, E.R. III, Hurov, K.E., Luo, J., Ballif, B.A., Gygi, S.P., Hofmann, K., D'Andrea, A.D. et al. (2007) Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell, 129, 289-301. (Pubitemid 46584733
29. Taniguchi, T., Garcia-Higuera, I., Andreassen, P.R., Gregory, R.C., Grompe, M. and D'Andrea, A.D. (2002) S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood, 100, 2414-2420
30. Sobeck, A., Stone, S., Costanzo, V., de Graaf, B., Reuter, T., de Winter, J., Wallisch, M., Akkari, Y., Olson, S., Wang, W. et al. (2006) Fanconi anemia proteins are required to prevent accumulation of replication-Associated DNA double-strand breaks. Mol. Cell. Biol., 26, 425-437
31. Ikegami, S., Taguchi, T., Ohashi, M., Nagano, H. and Mano, Y. (1978) Aphidicolin prevents mitotic cell division by interfering with the activity of DNA polymerase-Alpha. Nature, 275, 458-460. (Pubitemid 9021221
32. Howlett, N.G., Taniguchi, T., Durkin, S.G., D'Andrea, A.D. and Glover, T.W. (2005) The Fanconi anemia pathway is required for the DNA replication stress response and for the regulation of common fragile site stability. Hum. Mol. Genet., 14, 693-701
33. Chan, K.L., Palmai-Pallag, T., Ying, S. and Hickson, I.D. (2009) Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nat. Cell. Biol., 11, 753-760
34. Naim, V. and Rosselli, F. (2009) The FANC pathway and BLM collaborate during mitosis to prevent micro-nucleation and chromosome abnormalities. Nat. Cell. Biol., 11, 761-768
35. Durkin, S.G. and Glover, T.W. (2007) Chromosome fragile sites. Annu. Rev. Genet., 41, 169-192
36. Letessier, A., Millot, G.A., Koundrioukoff, S., Lachages, A-M., Vogt, N., Hansen, R.S., Malfoy, B., Brison, O. and Debatisse, M. (2011) Cell-Type-specific replication initiation programs set fragility of the FRA3B fragile site. Nature, 470, 120-123
37. Ozeri-Galai, E., Lebofsky, R., Rahat, A., Bester, A.C., Bensimon, A. and Kerem, B. (2011) Failure of origin activation in response to fork stalling leads to chromosomal instability at fragile sites. Mol. Cell, 43, 122-131
38. Whitney, M., Royle, G., Low, M., Kelly, M., Axthelm, M., Reifsteck, C., Olson, S., Braun, R., Heinrich, M., Rathbun, R. et al. (1996) Germ cell defects and hematopoietic hypersensitivity to gamma-interferon in mice with a targeted disruption of the Fanconi anemia C gene. Blood, 88, 49-58. (Pubitemid 26230670
39. Kawabata, T., Yamaguchi, S., Buske, T., Luebben, S., Wallace, M., Matise, I., Schimenti, J. and Shima, N. (2011) A reduction of licensed origins reveals strain-specific replication dynamics in mice. Mamm. Genome, 22, 506-517
40. Luebben, S.W., Kawabata, T., Akre, M.K., Lee, W.L., Johnson, C.S., O'Sullivan, M.G. and Shima, N. (2013) Helq acts in parallel to Fancc to suppress replication-Associated genome instability. Nucleic Acids Res, 40, 10283-10297
41. Lukas, C., Savic, V., Bekker-Jensen, S., Doil, C., Neumann, B., Solvhoj Pedersen, R., 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
42. 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
43. Baumann, C., Körner, R., Hofmann, K. and Nigg, E.A. (2007) PICH, a centromere-Associated SNF2 family ATPase, is regulated by Plk1 and required for the spindle checkpoint. Cell, 128, 101-114
44. Carreau, M. (2004) Not-so-novel phenotypes in the Fanconi anemia group D2 mouse model. Blood, 103, 2430
45. Wang, L.C., Stone, S., Hoatlin, M.E. and Gautier, J. (2008) Fanconi anemia proteins stabilize replication forks. DNA Repair, 7, 1973-1981
46. Schlacher, K., Wu, H. and Jasin, M. (2012) A distinct replication fork protection pathway connects Fanconi anemia tumor suppressors to RAD51-BRCA1/2. Cancer Cell, 22, 106-116
47. Chaudhury, I., Sareen, A., Raghunandan, M. and Sobeck, A. (2013) FANCD2 regulates BLM complex functions independently of FANCI to promote replication fork recovery. Nucleic Acids Res., 41, 6444-6459
48. Zou, L. and Elledge, S.J. (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science, 300, 1542-1548. (Pubitemid 36682880
49. 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. (Pubitemid 40632450
50. Rogakou, E.P., Pilch, D.R., Orr, A.H., Ivanova, V.S. and Bonner, W.M. (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem., 273, 5858-5868
51. Chuang, C-H., Wallace, M.D., Abratte, C., Southard, T. and Schimenti, J.C. (2010) Incremental genetic perturbations to MCM2-7 expression and subcellular distribution reveal exquisite sensitivity of mice to DNA replication stress. PLoS Genet., 6, e1001110
52. Bergoglio, V., Boyer, A-S., Walsh, E., Naim, V., Legube, G., Lee, M.Y.W.T., Rey, L., Rosselli, F., Cazaux, C., Eckert, K.A. et al. (2013) DNA synthesis by Pol - promotes fragile site stability by preventing under-replicated DNA in mitosis. J. Cell Biol., 201, 395-408
53. Naim, V., Wilhelm, T., Debatisse, M. and Rosselli, F. (2013) ERCC1 and MUS81-EME1 promote sister chromatid separation by processing late replication intermediates at common fragile sites during mitosis. Nat. Cell Biol., 15, 1008-1015
54. Casper, A.M., Nghiem, P., Arlt, M.F. and Glover, T.W. (2002) ATR regulates fragile site stability. Cell, 111, 779-789. (Pubitemid 36106400
55. Fenech, M. (2007) Cytokinesis-block micronucleus cytome assay. Nat. Protocols, 2, 1084-1104
56. Freie, B., Li, X., Ciccone, S.L.M., Nawa, K., Cooper, S., Vogelweid, C., Schantz, L., Haneline, L.S., Orazi, A., Broxmeyer, H.E. et al. (2003) Fanconi anemia type C and p53 cooperate in apoptosis and tumorigenesis. Blood, 102, 4146-4152. (Pubitemid 37487001
57. Wallace, M.D., Southard, T.L., Schimenti, K.J. and Schimenti, J.C. (2013) Role of DNA damage response pathways in preventing carcinogenesis caused by intrinsic replication stress. Oncogene
58. Niedzwiedz, W., Mosedale, G., Johnson, M., Ong, C.Y., Pace, P. and Patel, K.J. (2004) The Fanconi anaemia gene FANCC promotes homologous recombination and error-prone DNA repair. Mol. Cell, 15, 607-620
59. Mirchandani, K.D., McCaffrey, R.M. and D'Andrea, A.D. (2008) The Fanconi anemia core complex is required for efficient point mutagenesis and Rev1 foci assembly. DNA Repair, 7, 902-911
60. Kim, H., Yang, K., Dejsuphong, D. and D'Andrea, A.D. (2012) Regulation of Rev1 by the Fanconi anemia core complex. Nat. Struct. Mol. Biol., 19, 164-170
61. Lossaint, G., Larroque, M., Ribeyre, C., Bec, N., Larroque, C., D́ecaillet, C., Gari, K. and Constantinou, A. (2013) FANCD2 binds MCM proteins and controls replisome function upon activation of S phase checkpoint signaling. Mol. Cell, 51, 678-690
62. Ying, S., Minocherhomji, S., Chan, K.L., Palmai-Pallag, T., Chu, W.K., Wass, T., Mankouri, H.W., Liu, Y. and Hickson, I.D. (2013) MUS81 promotes common fragile site expression. Nat. Cell Biol., 15, 1001-1007
63. Parmar, K., D'Andrea, A. and Niedernhofer, L.J. (2009) Mouse models of Fanconi anemia. Mutat. Res./Fundam. Mol. Mech. Mutagen., 668, 133-140
64. Tischkowitz, M. and Winqvist, R. (2011) Using mouse models to investigate the biological and physiological consequences of defects in the Fanconi anaemia/breast cancer DNA repair signalling pathway. J. Pathol., 224, 301-305
65. Hughes, C.R., Guasti, L., Meimaridou, E., Chuang, C-H., Schimenti, J.C., King, P.J., Costigan, C., Clark, A.J.L. and Metherell, L.A. (2012) MCM4 mutation causes adrenal failure, short stature, and natural killer cell deficiency in humans. J. Clin. Invest., 122, 814-820
66. Gineau, L., Cognet, C., Kara, N., Lach, F.P., Dunne, J., Veturi, U., Picard, C., Trouillet, C., Eidenschenk, C., Aoufouchi, S. et al. (2012) Partial MCM4 deficiency in patients with growth retardation, adrenal insufficiency, and natural killer cell deficiency. J. Clin. Invest., 122, 821-832
67. Hendzel, M.J., Wei, Y., Mancini, M.A., Van Hooser, A., Ranalli, T., Brinkley, B.R., Bazett-Jones, D.P. and Allis, C.D. (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma, 106, 348-360. (Pubitemid 27510848