Histone modifications predispose genome regions to breakage and translocation

Genes and Development

Volumn 29, Issue 13, 2015, Pages 1393-1402

  Burman, Bharat ^a,b   Zhang, Zhuzhu Z ^c,d   Pegoraro, Gianluca ^a   Lieb, Jason D ^c,e   Misteli, Tom ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b TUFTS UNIVERSITY   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^e UNIVERSITY OF CHICAGO   (United States)

Author keywords

Chromatin structure; Chromosome translocations; Histone modifications

Indexed keywords

DNA; ENDONUCLEASE; HISTONE H3K4; NUCLEAR PROTEIN; UNCLASSIFIED DRUG; HISTONE;

ARTICLE; BIOCHEMICAL ANALYSIS; BIOINFORMATICS; CHROMATIN; CHROMOSOME BREAKAGE; CHROMOSOME TRANSLOCATION; DNA METHYLATION; DNA STRAND BREAKAGE; GENE LOCUS; GENETIC PREDISPOSITION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; LARGE CELL LYMPHOMA; PRIORITY JOURNAL; PROTEIN METHYLATION; TRANSIENT TRANSFECTION; U2OS CELL LINE; ANAPLASTIC LARGE CELL LYMPHOMA; BIOLOGY; DOUBLE STRANDED DNA BREAK; GENE TRANSLOCATION; GENETICS; HUMAN GENOME; METABOLISM; METHYLATION; PATHOPHYSIOLOGY; RADIATION RESPONSE; TUMOR CELL LINE;

CELL LINE, TUMOR; CHROMOSOME BREAKAGE; COMPUTATIONAL BIOLOGY; DNA BREAKS, DOUBLE-STRANDED; ENDONUCLEASES; GENOME, HUMAN; HISTONES; HUMANS; LYMPHOMA, LARGE-CELL, ANAPLASTIC; METHYLATION; TRANSLOCATION, GENETIC;

EID: 84936988909     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.262170.115     Document Type: Article

References (39)

1. Ayrapetov MK, Gursoy-Yuzugullu O, Xu C, Xu Y, Price BD. 2014. DNA double-strand breaks promote methylation of histone H3 on lysine 9 and transient formation of repressive chromatin. Proc Natl Acad Sci 111: 9169-9174.
2. Bannister AJ, Kouzarides T. 2011. Regulation of chromatin by histone modifications. Cell Res 21: 381-395.
3. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, et al. 2006. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326.
4. Bernt KM, Armstrong SA. 2009. Leukemia stem cells and human acute lymphoblastic leukemia. Semin Hematol 46: 33-38.
5. Bonnet D, Dick JE. 1997. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3: 730-737.
6. Burgess RC, Burman B, Kruhlak MJ, Misteli T. 2014. Activation of DNA damage response signaling by condensed chromatin. Cell Rep 9: 1703-1717.
7. Camphausen K, Tofilon PJ. 2007. Inhibition of histone deacetylation: a strategy for tumor radiosensitization. J Clin Oncol 25: 4051-4056.
8. Chiarle R, ZhangY, Frock RL, Lewis SM, Molinie B, Ho YJ, Myers DR, ChoiVW, Compagno M, Malkin DJ, et al. 2011. Genomewide translocation sequencing reveals mechanisms of chromosome breaks and rearrangements in B cells. Cell 147: 107-119.
9. Daniel JA, Nussenzweig A. 2012. Roles for histone H3K4 methyltransferase activities during immunoglobulin class-switch recombination. Biochim Biophys Acta 1819: 733-738.
10. Falk M, Lukasova E, Kozubek S. 2008. Chromatin structure influences the sensitivity of DNA to γ-radiation. Biochim Biophys Acta 1783: 2398-2414.
11. Fischer P, Nacheva E, Mason DY, Sherrington PD, Hoyle C, Hayhoe FG, Karpas A. 1988. A Ki-1 (CD30)-positive human cell line (Karpas 299) established from a high-grade non-Hodgkin's lymphoma, showing a 2;5 translocation and rearrangement of the T-cell receptor β-chain gene. Blood 72: 234-240.
12. Ji Y, ReschW, Corbett E, Yamane A, Casellas R, Schatz DG. 2010. The in vivo pattern of binding of RAG1 and RAG2 to antigen receptor loci. Cell 141: 419-431.
13. Khurana S, Kruhlak MJ, Kim J, Tran AD, Liu J, Nyswaner K, Shi L, Jailwala P, Sung MH, Hakim O, et al. 2014. A macrohistone variant links dynamic chromatin compaction to BRCA1-dependent genome maintenance. Cell Rep 8: 1049-1062.
14. Klein IA, ReschW, Jankovic M, OliveiraT, Yamane A, Nakahashi H, Di Virgilio M, Bothmer A, Nussenzweig A, Robbiani DF, et al. 2011. Translocation-capture sequencing reveals the extent and nature of chromosomal rearrangements in B lymphocytes. Cell 147: 95-106.
15. Lafon-Hughes L, Di Tomaso MV, Liddle P, Toledo A, Reyes-Abalos AL, Folle GA. 2013. Preferential localization of γH2AXfoci in euchromatin of retina rod cells after DNA damage induction. Chromosome Res 21: 789-803.
16. Lin C, Yang L, Tanasa B, Hutt K, Ju BG, Ohgi K, Zhang J, Rose DW, Fu XD, Glass CK, et al. 2009. Nuclear receptor-induced chromosomal proximity and DNA breaks underlie specific translocations in cancer. Cell 139: 1069-1083.
17. Lin C, Yang L, Rosenfeld MG. 2012. Molecular logic underlying chromosomal translocations, random or non-random? Adv Cancer Res 113: 241-279.
18. Mani RS, Chinnaiyan AM. 2010. Triggers for genomic rearrangements: insights into genomic, cellular and environmental influences. Nat Rev Genet 11: 819-829.
19. Maroschik B, Gurtler A, Kramer A, Rossler U, Gomolka M, Hornhardt S, Mortl S, Friedl AA. 2014. Radiation-induced alterations of histone post-translational modification levels in lymphoblastoid cell lines. Radiat Oncol 9: 15.
20. Mathas S, Kreher S, Meaburn KJ, Johrens K, Lamprecht B, Assaf C, Sterry W, Kadin ME, Daibata M, Joos S, et al. 2009. Gene deregulation and spatial genome reorganization near breakpoints prior to formation of translocations in anaplastic large cell lymphoma. Proc Natl Acad Sci 106: 5831-5836.
21. Mitelman F, Johansson B, Mertens F. 2007. The impact of translocations and gene fusions on cancer causation. Nat Rev Cancer 7: 233-245.
22. Mostoslavsky R, AltFW, Bassing CH. 2003. Chromatin dynamics and locus accessibility in the immune system. Nat Immunol 4: 603-606.
23. Nambiar M, Raghavan SC. 2011. How does DNA break during chromosomal translocations? Nucleic Acids Res 39: 5813-5825.
24. Price BD, D'Andrea AD. 2013. Chromatin remodeling at DNA double-strand breaks. Cell 152: 1344-1354.
25. Roukos V, Misteli T. 2014. The biogenesis of chromosome translocations. Nat Cell Biol 16: 293-300.
26. Roukos V, Burman B, Misteli T. 2013a. The cellular etiology of chromosome translocations. Curr Opin Cell Biol 25: 357-364.
27. Roukos V, Voss TC, Schmidt CK, Lee S, Wangsa D, Misteli T. 2013b. Spatial dynamics of chromosome translocations in living cells. Science 341: 660-664.
28. Seiler DM, Rouquette J, Schmid VJ, Strickfaden H, Ottmann C, Drexler GA, Mazurek B, Greubel C, Hable V, Dollinger G, et al. 2011. Double-strand break-induced transcriptional silencing is associated with loss of tri-methylation at H3K4. Chromosome Res 19: 883-899.
29. Shimazaki N, Tsai AG, Lieber MR. 2009. H3K4me3 stimulates the V(D)J RAG complex for both nicking and hairpinning in trans in addition to tethering in cis: implications for translocations. Mol Cell 34: 535-544.
30. Soutoglou E, Misteli T. 2008. Activation of the cellular DNA damage response in the absence of DNA lesions. Science 320: 1507-1510.
31. Soutoglou E, Dorn JF, Sengupta K, JasinM, Nussenzweig A, Ried T, Danuser G, MisteliT. 2007. Positional stability of single doublestrand breaks in mammalian cells. Nat Cell Biol 9: 675-682.
32. Stanlie A, Aida M, MuramatsuM, Honjo T, BegumNA. 2010. Histone3 lysine4 trimethylationregulated bythefacilitates chromatin transcription complex is critical for DNA cleavage in class switch recombination. Proc Natl Acad Sci 107: 22190-22195.
33. Tabbo F, Ponzoni M, Rabadan R, Bertoni F, Inghirami G. 2013. Beyond NPM-anaplastic lymphoma kinase driven lymphomagenesis: alternative drivers in anaplastic large cell lymphoma. Curr Opin Hematol 20: 374-381.
34. Takata H, Hanafusa T, Mori T, Shimura M, Iida Y, Ishikawa K, Yoshikawa K, Yoshikawa Y, Maeshima K. 2013. Chromatin compaction protects genomic DNA from radiation damage. PLoS One 8: e75622.
35. Talkowski ME, Ernst C, Heilbut A, Chiang C, Hanscom C, Lindgren A, Kirby A, Liu S, Muddukrishna B, Ohsumi TK, et al. 2011. Next-generation sequencing strategies enable routine detection of balanced chromosome rearrangements for clinical diagnostics and genetic research. Am J Hum Genet 88: 469-481.
36. Tumbar T, Sudlow G, Belmont AS. 1999. Large-scale chromatin unfolding and remodeling induced by VP16 acidic activation domain. J Cell Biol 145: 1341-1354.
37. Warters RL, Lyons BW. 1992. Variation in radiation-induced formation of DNA double-strand breaks as a function of chromatin structure. Radiat Res 130: 309-318.
38. Yu J, Mani RS, Cao Q, Brenner CJ, Cao X, Wang X, Wu L, Li J, Hu M, Gong Y, et al. 2010. An integrated network of androgen receptor, polycomb, and TMPRSS2-ERG gene fusions in prostate cancer progression. Cancer Cell 17: 443-454.
39. Zhang Y, Rowley JD. 2006. Chromatin structural elements and chromosomal translocations in leukemia. DNA Repair (Amst) 5: 1282-1297.