FANCD2 Facilitates Replication through Common Fragile Sites

Molecular Cell

Volumn 64, Issue 2, 2016, Pages 388-404

  Madireddy, Advaitha ^a   Kosiyatrakul, Settapong T ^a   Boisvert, Rebecca A ^b   Herrera Moyano, Emilia ^c   García Rubio, María L ^c   Gerhardt, Jeannine ^a   Vuono, Elizabeth A ^b   Owen, Nichole ^d   Yan, Zi ^a   Olson, Susan ^d   Aguilera, Andrés ^c   Howlett, Niall G ^b   Schildkraut, Carl L ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF RHODE ISLAND   (United States)

^c UNIVERSITY OF SEVILLE   (Spain)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

cancer; common fragile sites; DNA replication; DNA:RNA hybrids; Fanconi anemia; genomic instability

Indexed keywords

DNA; FANCONI ANEMIA GROUP D2 PROTEIN; REPETITIVE DNA; BRCA2 PROTEIN; BRCA2 PROTEIN, HUMAN; FANCA PROTEIN, HUMAN; FANCD2 PROTEIN, HUMAN; FANCI PROTEIN, HUMAN; FANCONI ANEMIA GROUP A PROTEIN; FANCONI ANEMIA PROTEIN; RNA;

ARTICLE; AT RICH SEQUENCE; COMMON FRAGILE SITE; CONTROLLED STUDY; DNA FLANKING REGION; DNA REPLICATION; DNA REPLICATION ORIGIN; DNA RNA HYBRIDIZATION; DNA SEQUENCE; DNA STRUCTURE; ECTOPIC EXPRESSION; FIBROBLAST; GENOME; LYMPHOBLAST; REPLISOME; CHROMOSOME FRAGILE SITE; CYTOLOGY; EPSTEIN BARR VIRUS; FANCONI ANEMIA; GENE EXPRESSION; GENETICS; GENOMIC INSTABILITY; HUMAN; LYMPHOCYTE; METABOLISM; TRANSFORMED CELL LINE;

BRCA2 PROTEIN; CELL LINE, TRANSFORMED; CHROMOSOME FRAGILE SITES; DNA; DNA REPLICATION; FANCONI ANEMIA; FANCONI ANEMIA COMPLEMENTATION GROUP A PROTEIN; FANCONI ANEMIA COMPLEMENTATION GROUP D2 PROTEIN; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; FIBROBLASTS; GENE EXPRESSION; GENOMIC INSTABILITY; HERPESVIRUS 4, HUMAN; HUMANS; LYMPHOCYTES; RNA;

EID: 84994802487     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.09.017     Document Type: Article

References (65)

1. Aguilera, A., García-Muse, T., R loops: from transcription byproducts to threats to genome stability. Mol. Cell 46 (2012), 115–124.
2. Alver, R.C., Chadha, G.S., Blow, J.J., The contribution of dormant origins to genome stability: from cell biology to human genetics. DNA Repair (Amst.) 19 (2014), 182–189.
3. Arlt, M.F., Casper, A.M., Glover, T.W., Common fragile sites. Cytogenet. Genome Res. 100 (2003), 92–100.
4. Bergoglio, V., Boyer, A.S., Walsh, E., Naim, V., Legube, G., Lee, M.Y., Rey, L., Rosselli, F., Cazaux, C., Eckert, K.A., Hoffmann, J.S., DNA synthesis by Pol η promotes fragile site stability by preventing under-replicated DNA in mitosis. J. Cell Biol. 201 (2013), 395–408.
5. Bergsagel, P.L., Kuehl, W.M., Chromosome translocations in multiple myeloma. Oncogene 20 (2001), 5611–5622.
6. Bhatia, V., Barroso, S.I., García-Rubio, M.L., Tumini, E., Herrera-Moyano, E., Aguilera, A., BRCA2 prevents R-loop accumulation and associates with TREX-2 mRNA export factor PCID2. Nature 511 (2014), 362–365.
7. Blow, J.J., Ge, X.Q., A model for DNA replication showing how dormant origins safeguard against replication fork failure. EMBO Rep. 10 (2009), 406–412.
8. Buongiorno-Nardelli, M., Micheli, G., Carri, M.T., Marilley, M., A relationship between replicon size and supercoiled loop domains in the eukaryotic genome. Nature 298 (1982), 100–102.
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. 11 (2009), 753–760.
10. Chaudhury, I., Sareen, A., Raghunandan, M., Sobeck, A., FANCD2 regulates BLM complex functions independently of FANCI to promote replication fork recovery. Nucleic Acids Res. 41 (2013), 6444–6459.
11. Chen, Y.H., Jones, M.J., Yin, Y., Crist, S.B., Colnaghi, L., Sims, R.J. 3rd, Rothenberg, E., Jallepalli, P.V., Huang, T.T., ATR-mediated phosphorylation of FANCI regulates dormant origin firing in response to replication stress. Mol. Cell 58 (2015), 323–338.
12. Chesi, M., Bergsagel, P.L., Shonukan, O.O., Martelli, M.L., Brents, L.A., Chen, T., Schröck, E., Ried, T., Kuehl, W.M., Frequent dysregulation of the c-maf proto-oncogene at 16q23 by translocation to an Ig locus in multiple myeloma. Blood 91 (1998), 4457–4463.
13. Ciullo, M., Debily, M.A., Rozier, L., Autiero, M., Billault, A., Mayau, V., El Marhomy, S., Guardiola, J., Bernheim, A., Coullin, P., et al. Initiation of the breakage-fusion-bridge mechanism through common fragile site activation in human breast cancer cells: the model of PIP gene duplication from a break at FRA7I. Hum. Mol. Genet. 11 (2002), 2887–2894.
14. Courbet, S., Gay, S., Arnoult, N., Wronka, G., Anglana, M., Brison, O., Debatisse, M., Replication fork movement sets chromatin loop size and origin choice in mammalian cells. Nature 455 (2008), 557–560.
15. Durkin, S.G., Glover, T.W., Chromosome fragile sites. Annu. Rev. Genet. 41 (2007), 169–192.
16. Finnis, M., Dayan, S., Hobson, L., Chenevix-Trench, G., Friend, K., Ried, K., Venter, D., Woollatt, E., Baker, E., Richards, R.I., Common chromosomal fragile site FRA16D mutation in cancer cells. Hum. Mol. Genet. 14 (2005), 1341–1349.
17. Fu, D., Dudimah, F.D., Zhang, J., Pickering, A., Paneerselvam, J., Palrasu, M., Wang, H., Fei, P., Recruitment of DNA polymerase eta by FANCD2 in the early response to DNA damage. Cell Cycle 12 (2013), 803–809.
18. Garcia-Higuera, I., Taniguchi, T., Ganesan, S., Meyn, M.S., Timmers, C., Hejna, J., Grompe, M., D'Andrea, A.D., Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol. Cell 7 (2001), 249–262.
19. García-Muse, T., Aguilera, A., Transcription-replication conflicts: how they occur and how they are resolved. Nat. Rev. Mol. Cell Biol. 17 (2016), 553–563.
20. García-Rubio, M.L., Pérez-Calero, C., Barroso, S.I., Tumini, E., Herrera-Moyano, E., Rosado, I.V., Aguilera, A., The Fanconi anemia pathway protects genome integrity from R-loops. PLoS Genet., 11, 2015, e1005674.
21. Gerhardt, J., Zaninovic, N., Zhan, Q., Madireddy, A., Nolin, S.L., Ersalesi, N., Yan, Z., Rosenwaks, Z., Schildkraut, C.L., Cis-acting DNA sequence at a replication origin promotes repeat expansion to fragile X full mutation. J. Cell Biol. 206 (2014), 599–607.
22. Ginno, P.A., Lott, P.L., Christensen, H.C., Korf, I., Chédin, F., R-loop formation is a distinctive characteristic of unmethylated human CpG island promoters. Mol. Cell 45 (2012), 814–825.
23. Glover, T.W., Common fragile sites. Cancer Lett. 232 (2006), 4–12.
24. Hellman, A., Zlotorynski, E., Scherer, S.W., Cheung, J., Vincent, J.B., Smith, D.I., Trakhtenbrot, L., Kerem, B., A role for common fragile site induction in amplification of human oncogenes. Cancer Cell 1 (2002), 89–97.
25. Helmrich, A., Ballarino, M., Tora, L., Collisions between replication and transcription complexes cause common fragile site instability at the longest human genes. Mol. Cell 44 (2011), 966–977.
26. Helmrich, A., Ballarino, M., Nudler, E., Tora, L., Transcription-replication encounters, consequences and genomic instability. Nat. Struct. Mol. Biol. 20 (2013), 412–418.
27. Herrera-Moyano, E., Mergui, X., García-Rubio, M.L., Barroso, S., Aguilera, A., The yeast and human FACT chromatin-reorganizing complexes solve R-loop-mediated transcription-replication conflicts. Genes Dev. 28 (2014), 735–748.
28. Hirsch, B., Shimamura, A., Moreau, L., Baldinger, S., Hag-alshiekh, M., Bostrom, B., Sencer, S., D'Andrea, A.D., Association of biallelic BRCA2/FANCD1 mutations with spontaneous chromosomal instability and solid tumors of childhood. Blood 103 (2004), 2554–2559.
29. Houghtaling, S., Timmers, C., Noll, M., Finegold, M.J., Jones, S.N., Meyn, M.S., Grompe, M., Epithelial cancer in Fanconi anemia complementation group D2 (Fancd2) knockout mice. Genes Dev. 17 (2003), 2021–2035.
30. Howlett, N.G., Taniguchi, T., Olson, S., Cox, B., Waisfisz, Q., De Die-Smulders, C., Persky, N., Grompe, M., Joenje, H., Pals, G., et al. Biallelic inactivation of BRCA2 in Fanconi anemia. Science 297 (2002), 606–609.
31. Howlett, N.G., Taniguchi, T., Durkin, S.G., D'Andrea, A.D., Glover, T.W., 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 (2005), 693–701.
32. Kamath-Loeb, A.S., Johansson, E., Burgers, P.M., Loeb, L.A., Functional interaction between the Werner syndrome protein and DNA polymerase delta. Proc. Natl. Acad. Sci. USA 97 (2000), 4603–4608.
33. Karanja, K.K., Lee, E.H., Hendrickson, E.A., Campbell, J.L., Preventing over-resection by DNA2 helicase/nuclease suppresses repair defects in Fanconi anemia cells. Cell Cycle 13 (2014), 1540–1550.
34. Kutler, D.I., Auerbach, A.D., Satagopan, J., Giampietro, P.F., Batish, S.D., Huvos, A.G., Goberdhan, A., Shah, J.P., Singh, B., High incidence of head and neck squamous cell carcinoma in patients with Fanconi anemia. Arch. Otolaryngol. Head Neck Surg. 129 (2003), 106–112.
35. Lachaud, C., Moreno, A., Marchesi, F., Toth, R., Blow, J.J., Rouse, J., Ubiquitinated Fancd2 recruits Fan1 to stalled replication forks to prevent genome instability. Science 351 (2016), 846–849.
36. Le Beau, M.M., Rassool, F.V., Neilly, M.E., Espinosa, R. 3rd, Glover, T.W., Smith, D.I., McKeithan, T.W., Replication of a common fragile site, FRA3B, occurs late in S phase and is delayed further upon induction: implications for the mechanism of fragile site induction. Hum. Mol. Genet. 7 (1998), 755–761.
37. Le Tallec, B., Dutrillaux, B., Lachages, A.M., Millot, G.A., Brison, O., Debatisse, M., Molecular profiling of common fragile sites in human fibroblasts. Nat. Struct. Mol. Biol. 18 (2011), 1421–1423.
38. Letessier, A., Millot, G.A., Koundrioukoff, S., Lachagès, A.M., Vogt, N., Hansen, R.S., Malfoy, B., Brison, O., Debatisse, M., Cell-type-specific replication initiation programs set fragility of the FRA3B fragile site. Nature 470 (2011), 120–123.
39. Lossaint, G., Larroque, M., Ribeyre, C., Bec, N., Larroque, C., Décaillet, C., Gari, K., Constantinou, A., FANCD2 binds MCM proteins and controls replisome function upon activation of s phase checkpoint signaling. Mol. Cell 51 (2013), 678–690.
40. Lucas, I., Palakodeti, A., Jiang, Y., Young, D.J., Jiang, N., Fernald, A.A., Le Beau, M.M., High-throughput mapping of origins of replication in human cells. EMBO Rep. 8 (2007), 770–777.
41. Madireddy, A., Purushothaman, P., Loosbroock, C.P., Robertson, E.S., Schildkraut, C.L., Verma, S.C., G-quadruplex-interacting compounds alter latent DNA replication and episomal persistence of KSHV. Nucleic Acids Res. 44 (2016), 3675–3694.
42. Mirkin, E.V., Mirkin, S.M., Replication fork stalling at natural impediments. Microbiol. Mol. Biol. Rev. 71 (2007), 13–35.
43. Nadel, J., Athanasiadou, R., Lemetre, C., Wijetunga, N.A., Ó Broin, P., Sato, H., Zhang, Z., Jeddeloh, J., Montagna, C., Golden, A., et al. RNA:DNA hybrids in the human genome have distinctive nucleotide characteristics, chromatin composition, and transcriptional relationships. Epigenetics Chromatin, 8, 2015, 46.
44. Naim, V., Wilhelm, T., Debatisse, M., Rosselli, F., ERCC1 and MUS81-EME1 promote sister chromatid separation by processing late replication intermediates at common fragile sites during mitosis. Nat. Cell Biol. 15 (2013), 1008–1015.
45. Norio, P., Schildkraut, C.L., Visualization of DNA replication on individual Epstein-Barr virus episomes. Science 294 (2001), 2361–2364.
46. O'Keefe, L.V., Richards, R.I., Common chromosomal fragile sites and cancer: focus on FRA16D. Cancer Lett. 232 (2006), 37–47.
47. Palumbo, E., Matricardi, L., Tosoni, E., Bensimon, A., Russo, A., Replication dynamics at common fragile site FRA6E. Chromosoma 119 (2010), 575–587.
48. Panneerselvam, J., Pickering, A., Han, B., Li, L., Zheng, J., Zhang, J., Zhang, Y., Fei, P., Basal level of FANCD2 monoubiquitination is required for the maintenance of a sufficient number of licensed-replication origins to fire at a normal rate. Oncotarget 5 (2014), 1326–1337.
49. Pellicioli, A., Muzi-Falconi, M., A blooming resolvase at chromosomal fragile sites. Nat. Cell Biol. 15 (2013), 883–885.
50. 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 37 (2010), 492–502.
51. Raghunandan, M., Chaudhury, I., Kelich, S.L., Hanenberg, H., Sobeck, A., FANCD2, FANCJ and BRCA2 cooperate to promote replication fork recovery independently of the Fanconi anemia core complex. Cell Cycle 14 (2015), 342–353.
52. Rajendra, E., Oestergaard, V.H., Langevin, F., Wang, M., Dornan, G.L., Patel, K.J., Passmore, L.A., The genetic and biochemical basis of FANCD2 monoubiquitination. Mol. Cell 54 (2014), 858–869.
53. Rey, L., Sidorova, J.M., Puget, N., Boudsocq, F., Biard, D.S., Monnat, R.J. Jr., Cazaux, C., Hoffmann, J.S., Human DNA polymerase eta is required for common fragile site stability during unperturbed DNA replication. Mol. Cell. Biol. 29 (2009), 3344–3354.
54. Rosenberg, P.S., Greene, M.H., Alter, B.P., Cancer incidence in persons with Fanconi anemia. Blood 101 (2003), 822–826.
55. Sato, K., Ishiai, M., Toda, K., Furukoshi, S., Osakabe, A., Tachiwana, H., Takizawa, Y., Kagawa, W., Kitao, H., Dohmae, N., et al. Histone chaperone activity of Fanconi anemia proteins, FANCD2 and FANCI, is required for DNA crosslink repair. EMBO J. 31 (2012), 3524–3536.
56. Schlacher, K., Wu, H., Jasin, M., A distinct replication fork protection pathway connects Fanconi anemia tumor suppressors to RAD51-BRCA1/2. Cancer Cell 22 (2012), 106–116.
57. Schwab, R.A., Nieminuszczy, J., Shah, F., Langton, J., Lopez Martinez, D., Liang, C.C., Cohn, M.A., Gibbons, R.J., Deans, A.J., Niedzwiedz, W., The Fanconi anemia pathway maintains genome stability by coordinating replication and transcription. Mol. Cell 60 (2015), 351–361.
58. Shah, S.N., Opresko, P.L., Meng, X., Lee, M.Y., Eckert, K.A., DNA structure and the Werner protein modulate human DNA polymerase delta-dependent replication dynamics within the common fragile site FRA16D. Nucleic Acids Res. 38 (2010), 1149–1162.
59. Siprashvili, Z., Sozzi, G., Barnes, L.D., McCue, P., Robinson, A.K., Eryomin, V., Sard, L., Tagliabue, E., Greco, A., Fusetti, L., et al. Replacement of Fhit in cancer cells suppresses tumorigenicity. Proc. Natl. Acad. Sci. USA 94 (1997), 13771–13776.
60. Sutherland, G.R., Richards, R.I., The molecular basis of fragile sites in human chromosomes. Curr. Opin. Genet. Dev. 5 (1995), 323–327.
61. Taniguchi, T., Garcia-Higuera, I., Andreassen, P.R., Gregory, R.C., Grompe, M., D'Andrea, A.D., S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood 100 (2002), 2414–2420.
62. Walsh, E., Wang, X., Lee, M.Y., Eckert, K.A., Mechanism of replicative DNA polymerase delta pausing and a potential role for DNA polymerase kappa in common fragile site replication. J. Mol. Biol. 425 (2013), 232–243.
63. Ying, S., Minocherhomji, S., Chan, K.L., Palmai-Pallag, T., Chu, W.K., Wass, T., Mankouri, H.W., Liu, Y., Hickson, I.D., MUS81 promotes common fragile site expression. Nat. Cell Biol. 15 (2013), 1001–1007.
64. Yunis, J.J., Soreng, A.L., Bowe, A.E., Fragile sites are targets of diverse mutagens and carcinogens. Oncogene 1 (1987), 59–69.
65. Zhang, H., Freudenreich, C.H., An AT-rich sequence in human common fragile site FRA16D causes fork stalling and chromosome breakage in S. cerevisiae. Mol. Cell 27 (2007), 367–379.