Chromatin remodeller SMARCA4 recruits topoisomerase 1 and suppresses transcription-associated genomic instability

Nature Communications

Volumn 7, Issue , 2016, Pages

  Husain, Afzal ^a   Begum, Nasim A ^a   Taniguchi, Takako ^b   Taniguchi, Hisaaki ^b   Kobayashi, Maki ^a   Honjo, Tasuku ^a  

^a KYOTO UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BRG1 PROTEIN; CHAPERONE; DNA TOPOISOMERASE; FACT PROTEIN; MYC PROTEIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; CHROMATIN; DNA BINDING PROTEIN; DNA HELICASE; HIGH MOBILITY GROUP PROTEIN; NUCLEAR PROTEIN; PROTEOME; SMARCA4 PROTEIN, HUMAN; SMARCA4 PROTEIN, MOUSE; SSRP1 PROTEIN, HUMAN; SSRP1 PROTEIN, MOUSE; SUPT16H PROTEIN, HUMAN; SUPT16H PROTEIN, MOUSE; TRANSCRIPTION ELONGATION FACTOR; TRANSCRIPTION FACTOR;

CHROMOSOME; CYTOGENETICS; DNA; ENZYME; GENOME; NERVOUS SYSTEM DISORDER; PROTEIN; PROTEOMICS;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL LINE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; DNA CLEAVAGE; DNA SEQUENCE; GENE MUTATION; GENETIC TRANSCRIPTION; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN PROTEIN INTERACTION; PROTEOMICS; ANIMAL; CELL PROLIFERATION; CHROMATIN; DOUBLE STRANDED DNA BREAK; FLOW CYTOMETRY; GENE SILENCING; GENE TRANSLOCATION; GENETICS; IMMUNOGLOBULIN HEAVY CHAIN GENE; IMMUNOPRECIPITATION; METABOLISM; ONCOGENE MYC; TUMOR CELL LINE;

ANIMALS; B-LYMPHOCYTES; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELL PROLIFERATION; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; DNA BREAKS, DOUBLE-STRANDED; DNA CLEAVAGE; DNA HELICASES; DNA TOPOISOMERASES, TYPE I; DNA-BINDING PROTEINS; FLOW CYTOMETRY; GENE KNOCKDOWN TECHNIQUES; GENES, IMMUNOGLOBULIN HEAVY CHAIN; GENES, MYC; GENOMIC INSTABILITY; HIGH MOBILITY GROUP PROTEINS; HISTONE CHAPERONES; HUMANS; IMMUNOPRECIPITATION; MICE; NUCLEAR PROTEINS; PROTEOME; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ELONGATION FACTORS; TRANSLOCATION, GENETIC;

EID: 84957603779     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10549     Document Type: Article

References (69)

1. Kerrigan, J. E. & Pilch, D. S. A structural model for the ternary cleavable complex formed between human topoisomerase I, DNA, and camptothecin. Biochemistry 40, 9792-9798 (2001).
2. Pommier, Y. Topoisomerase I inhibitors: camptothecins and beyond. Nat. Rev. Cancer. 6, 789-802 (2006).
3. Tuduri, S. et al. Topoisomerase I suppresses genomic instability by preventing interference between replication and transcription. Nat. Cell Biol. 11, 1315-1324 (2009).
4. Kim, N. & Jinks-Robertson, S. Transcription as a source of genome instability. Nat. Rev. Genet. 13, 204-214 (2012).
5. Miao, Z. H. et al. Nonclassic functions of human topoisomerase I: genome-wide and pharmacologic analyses. Cancer Res. 67, 8752-8761 (2007).
6. Aguilera, A. The connection between transcription and genomic instability. EMBO J. 21, 195-201 (2002).
7. Sordet, O., Nakamura, A. J., Redon, C. E. & Pommier, Y. DNA double-strand breaks and ATM activation by transcription-blocking DNA lesions. Cell Cycle 9, 274-278 (2010).
8. Sordet, O. et al. Ataxia telangiectasia mutated activation by transcription- and topoisomerase I-induced DNA double-strand breaks. EMBO Rep. 10, 887-893 (2009).
9. Napierala, M., Bacolla, A. & Wells, R. D. Increased negative superhelical density in vivo enhances the genetic instability of triplet repeat sequences. J. Biol. Chem. 280, 37366-37376 (2005).
10. Wojciechowska, M., Napierala, M., Larson, J. E. & Wells, R. D. Non-B DNA conformations formed by long repeating tracts of myotonic dystrophy type 1, myotonic dystrophy type 2, and Friedreich's ataxia genes, not the sequences per se, promote mutagenesis in flanking regions. J. Biol. Chem. 281, 24531-24543 (2006).
11. Hubert, Jr L., Lin, Y., Dion, V. & Wilson, J. H. Topoisomerase 1 and single-strand break repair modulate transcription-induced CAG repeat contraction in human cells. Mol. Cell. Biol. 31, 3105-3112 (2011).
12. Takahashi, T., Burguiere-Slezak, G., Van der Kemp, P. A. & Boiteux, S. Topoisomerase 1 provokes the formation of short deletions in repeated sequences upon high transcription in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 108, 692-697 (2011).
13. Lippert, M. J. et al. Role for topoisomerase 1 in transcription-associated mutagenesis in yeast. Proc. Natl Acad. Sci. USA 108, 698-703 (2011).
14. Kim, N. et al. Mutagenic processing of ribonucleotides in DNA by yeast topoisomerase I. Science 332, 1561-1564 (2011).
15. Alagoz, M., Chiang, S. C., Sharma, A. & El-Khamisy, S. F. ATM deficiency results in accumulation of DNA-topoisomerase I covalent intermediates in neural cells. PLoS ONE 8, e58239 (2013).
16. Katyal, S. et al. Aberrant topoisomerase-1 DNA lesions are pathogenic in neurodegenerative genome instability syndromes. Nat. Neurosci. 17, 813-821 (2014).
17. Mosesso, P. et al. The novel human gene aprataxin is directly involved in DNA single-strand-break repair. Cell. Mol. Life Sci. 62, 485-491 (2005).
18. Shen, J. et al. Mutations in PNKP cause microcephaly, seizures and defects in DNA repair. Nat. Genet. 42, 245-249 (2010).
19. Muramatsu, M. et al. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102, 553-563 (2000).
20. Nagaoka, H., Muramatsu, M., Yamamura, N., Kinoshita, K. & Honjo, T. Activation-induced deaminase (AID)-directed hypermutation in the immunoglobulin Smu region: implication of AID involvement in a common step of class switch recombination and somatic hypermutation. J. Exp. Med. 195, 529-534 (2002).
21. Petersen, S. et al. AID is required to initiate Nbs1/gamma-H2AX focus formation and mutations at sites of class switching. Nature 414, 660-665 (2001).
22. Honjo, T. et al. The AID dilemma: infection, or cancer? Adv. Cancer Res. 113, 1-44 (2012).
23. Kobayashi, M. et al. AID-induced decrease in topoisomerase 1 induces DNA structural alteration and DNA cleavage for class switch recombination. Proc. Natl Acad. Sci. USA 106, 22375-22380 (2009).
24. Kobayashi, M. et al. Decrease in topoisomerase I is responsible for activation-induced cytidine deaminase (AID)-dependent somatic hypermutation. Proc. Natl Acad. Sci. USA 108, 19305-19310 (2011).
25. Kato, L. et al. Nonimmunoglobulin target loci of activation-induced cytidine deaminase (AID) share unique features with immunoglobulin genes. Proc. Natl Acad. Sci. USA 109, 2479-2484 (2012).
26. Begum, N. A. & Honjo, T. Evolutionary comparison of the mechanism of DNA cleavage with respect to immune diversity and genomic instability. Biochemistry 51, 5243-5256 (2012).
27. Blackwell, T. K. et al. Recombination between immunoglobulin variable region gene segments is enhanced by transcription. Nature 324, 585-589 (1986).
28. Bachl, J., Carlson, C., Gray-Schopfer, V., Dessing, M. & Olsson, C. Increased transcription levels induce higher mutation rates in a hypermutating cell line. J. Immunol. 166, 5051-5057 (2001).
29. Stanlie, A., Aida, M., Muramatsu, M., Honjo, T. & Begum, N. A. Histone3 lysine4 trimethylation regulated by the facilitates chromatin transcription complex is critical for DNA cleavage in class switch recombination. Proc. Natl Acad. Sci. USA 107, 22190-22195 (2010).
30. Begum, N. A., Stanlie, A., Nakata, M., Akiyama, H. & Honjo, T. The histone chaperone Spt6 is required for activation-induced cytidine deaminase target determination through H3K4me3 regulation. J. Biol. Chem. 287, 32415-32429 (2012).
31. Stanlie, A., Begum, N. A., Akiyama, H. & Honjo, T. The DSIF subunits Spt4 and Spt5 have distinct roles at various phases of immunoglobulin class switch recombination. PLoS Genet. 8, e1002675 (2012).
32. Aida, M., Hamad, N., Stanlie, A., Begum, N. A. & Honjo, T. Accumulation of the FACT complex, as well as histone H3.3, serves as a target marker for somatic hypermutation. Proc. Natl Acad. Sci. USA 110, 7784-7789 (2013).
33. Kato, L. et al. An evolutionary view of the mechanism for immune and genome diversity. J. Immunol. 188, 3559-3566 (2012).
34. Kadoch, C. et al. Proteomic and bioinformatic analysis of mammalian SWI/SNF complexes identifies extensive roles in human malignancy. Nat. Genet. 45, 592-601 (2013).
35. Shain, A. H. & Pollack, J. R. The spectrum of SWI/SNF mutations, ubiquitous in human cancers. PLoS ONE 8, e55119 (2013).
36. Clapier, C. R. & Cairns, B. R. The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 78, 273-304 (2009).
37. Wang, W. et al. Purification and biochemical heterogeneity of the mammalian SWI-SNF complex. EMBO J. 15, 5370-5382 (1996).
38. Franceschini, A. et al. STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res. 41, D808-D815 (2013).
39. Shannon, P. et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504 (2003).
40. Smith, L. M., Willmore, E., Austin, C. A. & Curtin, N. J. The novel poly(ADP-Ribose) polymerase inhibitor, AG14361, sensitizes cells to topoisomerase I poisons by increasing the persistence of DNA strand breaks. Clin. Cancer Res. 11, 8449-8457 (2005).
41. Okazaki, I. M. et al. Histone chaperone Spt6 is required for class switch recombination but not somatic hypermutation. Proc. Natl Acad. Sci. USA 108, 7920-7925 (2011).
42. Okazaki, I. M., Kinoshita, K., Muramatsu, M., Yoshikawa, K. & Honjo, T. The AID enzyme induces class switch recombination in fibroblasts. Nature 416, 340-345 (2002).
43. Faili, A. et al. AID-dependent somatic hypermutation occurs as a DNA single-strand event in the BL2 cell line. Nat. Immunol. 3, 815-821 (2002).
44. Nagaoka, H., Ito, S., Muramatsu, M., Nakata, M. & Honjo, T. DNA cleavage in immunoglobulin somatic hypermutation depends on de novo protein synthesis but not on uracil DNA glycosylase. Proc. Natl Acad. Sci. USA 102, 2022-2027 (2005).
45. French, S. L. et al. Distinguishing the roles of Topoisomerases I and II in relief of transcription-induced torsional stress in yeast rRNA genes. Mol. Cell. Biol. 31, 482-494 (2011).
46. Chiarle, R. et al. Genome-wide translocation sequencing reveals mechanisms of chromosome breaks and rearrangements in B cells. Cell 147, 107-119 (2011).
47. Liu, M. et al. Two levels of protection for the B cell genome during somatic hypermutation. Nature 451, 841-845 (2008).
48. Yamane, A. et al. Deep-sequencing identification of the genomic targets of the cytidine deaminase AID and its cofactor RPA in B lymphocytes. Nat. Immunol. 12, 62-69 (2011).
49. Dykhuizen, E. C. et al. BAF complexes facilitate decatenation of DNA by topoisomerase IIalpha. Nature 497, 624-627 (2013).
50. Bartke, T. et al. Nucleosome-interacting proteins regulated by DNA and histone methylation. Cell 143, 470-484 (2010).
51. Safina, A. et al. Complex mutual regulation of facilitates chromatin transcription (FACT) subunits on both mRNA and protein levels in human cells. Cell Cycle 12, 2423-2434 (2013).
52. Shirakata, M. et al. HMG1-related DNA-binding protein isolated with V-(D)-J recombination signal probes. Mol. Cell. Biol. 11, 4528-4536 (1991).
53. Bruhn, S. L., Pil, P. M., Essigmann, J. M., Housman, D. E. & Lippard, S. J. Isolation and characterization of human cDNA clones encoding a high mobility group box protein that recognizes structural distortions to DNA caused by binding of the anticancer agent cisplatin. Proc. Natl Acad. Sci. USA 89, 2307-2311 (1992).
54. Robbiani, D. F. & Nussenzweig, M. C. Chromosome translocation, B cell lymphoma, and activation-induced cytidine deaminase. Annu. Rev. Pathol. 8, 79-103 (2013).
55. Kuppers, R. & Dalla-Favera, R. Mechanisms of chromosomal translocations in B cell lymphomas. Oncogene 20, 5580-5594 (2001).
56. Leder, P. et al. Translocations among antibody genes in human cancer. Science 222, 765-771 (1983).
57. Wells, R. D. Non-B DNA conformations, mutagenesis and disease. Trends Biochem. Sci. 32, 271-278 (2007).
58. Denepoux, S. et al. Induction of somatic mutation in a human B cell line in vitro. Immunity 6, 35-46 (1997).
59. Smith, A. L., Friedman, D. B., Yu, H., Carnahan, R. H. & Reynolds, A. B. ReCLIP (reversible cross-link immuno-precipitation): an efficient method for interrogation of labile protein complexes. PLoS ONE 6, e16206 (2011).
60. Petritis, B. O., Qian, W. J., Camp, 2nd D. G.& Smith, R. D. A simple procedure for effective quenching of trypsin activity and prevention of 18O-labeling back-exchange. J. Proteome. Res. 8, 2157-2163 (2009).
61. Jorge, I. et al. Statistical model to analyze quantitative proteomics data obtained by 18O/16O labeling and linear ion trap mass spectrometry: application to the study of vascular endothelial growth factor-induced angiogenesis in endothelial cells. Mol. Cell. Proteomics 8, 1130-1149 (2009).
62. Maita, N. et al. Human alpha-L-iduronidase uses its own N-glycan as a substrate-binding and catalytic module. Proc. Natl Acad. Sci. USA 110, 14628-14633 (2013).
63. Kikuchi, M. et al. Proteomic analysis of rat liver peroxisome: presence of peroxisome-specific isozyme of Lon protease. J. Biol. Chem. 279, 421-428 (2004).
64. Boboila, C. et al. Robust chromosomal DNA repair via alternative end-joining in the absence of X-ray repair cross-complementing protein 1 (XRCC1). Proc. Natl Acad. Sci. USA 109, 2473-2478 (2012).
65. Xu, J., Husain, A., Hu, W., Honjo, T. & Kobayashi, M. APE1 is dispensable for S-region cleavage but required for its repair in class switch recombination. Proc. Natl Acad. Sci. USA 111, 17242-17247 (2014).
66. Schrader, C. E., Linehan, E. K., Mochegova, S. N., Woodland, R. T. & Stavnezer, J. Inducible DNA breaks in Ig S regions are dependent on AID and UNG. J. Exp. Med. 202, 561-568 (2005).
67. Kiianitsa, K. & Maizels, N. A rapid and sensitive assay for DNA-protein covalent complexes in living cells. Nucleic Acids Res. 41, e104 (2013).
68. Naughton, C. et al. Transcription forms and remodels supercoiling domains unfolding large-scale chromatin structures. Nat. Struct. Mol. Biol. 20, 387-395 (2013).
69. Stanlie, A., Yousif, A. S., Akiyama, H., Honjo, T. & Begum, N. A. Chromatin reader Brd4 functions in Ig class switching as a repair complex adaptor of nonhomologous end-joining. Mol. Cell. 55, 97-110 (2014).