DNA double-strand breaks: Linking gene expression to chromosome morphology and mobility

Chromosoma

Volumn 123, Issue 1-2, 2014, Pages 103-115

  Zhang, Yang ^a   Heermann, Dieter W ^a  

^a INSTITUT FÜR THEORETISCHE PHYSIK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H2AX; MESSENGER RNA;

ARTICLE; CELL NUCLEUS; CHROMOSOME 11; CHROMOSOME STRUCTURE; CONFORMATIONAL TRANSITION; DNA END JOINING REPAIR; DOUBLE STRANDED DNA BREAK; ENTROPY; GENE EXPRESSION; GENOME ANALYSIS; IONIZING RADIATION; MOLECULAR DYNAMICS; NUCLEOTIDE SEQUENCE; RADIATION EXPOSURE;

CHROMATIN; CHROMOSOMES; DNA BREAKS, DOUBLE-STRANDED; ENTROPY; GENE EXPRESSION REGULATION; GENOME, HUMAN; HUMANS; MOVEMENT; RADIATION, IONIZING;

EID: 84897564418     PISSN: 00095915     EISSN: 14320886     Source Type: Journal    
DOI: 10.1007/s00412-013-0432-y     Document Type: Article

References (68)

1. Amundson SA, Do KT, Vinikoor LC, Lee RA, Koch-Paiz CA, Ahn J, Reimers M, Chen Y, Scudiero DA, Weinstein JN, Trent JM, Bittner ML, Meltzer PS, Fornace AJ Jr (2008) Integrating globalgene expression and radiation survival parameters across the 60 cell lines of the national cancer institute anticancer drug screen. Cancer Res 68(2):415-424 (Pubitemid 351380067)
2. Aten JA, Stap J, Krawczyk PM, van Oven CH, Hoebe RA, Essers J, Kanaar R (2004) Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 303(5654):92-95 (Pubitemid 38055778)
3. Bancaud A, Huet S, Daigle N, Mozziconacci J, Beaudouin J, Ellenberg J (2009) Molecular crowding affects diffusion and binding of nuclear proteins in heterochromatin and reveals the fractal organization of chromatin. EMBO J 28(24):37853798
4. Barbieri M, Chotalia M, Fraser J, Lavitas L-M, Dostie J, Pombo A, Nicodemi M (2012) Complexity of chromatin folding is captured by the strings and binders switch model. Proc Natl Acad Sci U S A 109(40):16173-16178
5. Bewersdorf J, Bennett B, Knight K (2006) H2AX chromatin structures and their response to DNA damage revealed by 4Pi microscopy. Proc Natl Acad Sci U S A 103(48):18137-18142 (Pubitemid 44871625)
6. Bohn M, Heermann DW (2010a) Diffusion-driven looping provides a consistent framework for chromatin organization. PLoS One 5(8):e12218
7. Bohn M, Heermann DW (2010b) Topological interactions between ring polymers: implications for chromatin loops. J Chem Phys 132(4):044904
8. Bohn M, Heermann DW (2011) Repulsive forces between looping chromosomes induce entropy-driven segregation. PLoS One 6(1):e14428
9. Carmesin I, Kremer K (1988) The bond fluctuation method: a new effective algorithm for the dynamics of polymers in all spatial dimensions. Macromolecules 21(9):2819-2823
10. Chiolo I, Minoda A, Colmenares SU, Polyzos A, Costes SV, Karpen GH (2011) Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell 144(5):732-744
11. Cook PR (2010) A model for all genomes: the role of transcription factories. J Mol Biol 395(1):1-10
12. Cook P, Marenduzzo D (2009) Entropic organization of interphase chromosomes. J Cell Biol 186(6):825-834
13. Correa CR, Cheung VG (2004) Genetic variation in radiation-induced expression phenotypes. Am J Hum Genet 75(5):885-890 (Pubitemid 39390496)
14. Costes SV, Chiolo I, Pluth JM, Barcellos-Hoff MH, Jakob B (2010) Spatiotemporal characterization of ionizing radiation induced DNA damage foci and their relation to chromatin organization. Mutat Res 704(1-3):7887
15. Cowell IG, Sunter NJ, Singh PB, Austin CA, Durkacz BW, Tilby MJ (2007) gammaH2AX foci form preferentially in euchromatin after ionising-radiation. PLoS One 2(10):e1057
16. Cox MM, Battista JR (2005) Deinococcus radiodurans - the consummate survivor. Nat Rev Microbiol 3(11):882-92 (Pubitemid 41693183)
17. Cremer T, Cremer C (2001) Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet 2(4):292-301 (Pubitemid 33674777)
18. Dasika GK, Lin SC, Zhao S, Sung P, Tomkinson A, Lee EY (1999) DNA damage-induced cell cycle checkpoints and DNA strand break repair in development and tumorigenesis. Oncogene 18(55):7883-99 (Pubitemid 30066234)
19. de Nooijer S, Wellink J, Mulder B, Bisseling T (2009) Non-specific interactions are sufficient to explain the position of heterochromatic chromocenters and nucleoli in interphase nuclei. Nucleic Acids Res 37(11):3558-3568
20. Dekker J (2008) Gene regulation in the third dimension. Science 319(5871):1793-1794
21. Dekker J, Rippe K, Dekker M, Kleckner N (2002) Capturing chromosome conformation. Science 295(5558):1306-1311 (Pubitemid 34157624)
22. Deutsch H, Binder K (1991) Interdiffusion and self-diffusion in polymer mixtures: a Monte Carlo Study. J Chem Phys 94(3):2294-2304
23. Dion V, Kalck V, Horigome C, Towbin BD, Gasser SM (2012) Increased mobility of double-strand breaks requires Mec1, Rad9 and the homologous recombination machinery. Nat Cell Biol 14(5):502-509
24. Downs J, Nussenzweig M, Nussenzweig A (2007) Chromatin dynamics and the preservation of genetic information. Nature 447(7147):951-958 (Pubitemid 46975762)
25. Finan K, Cook PR, Marenduzzo D (2011) Non-specific (entropic) forces as major determinants of the structure of mammalian chromosomes. Chromosome Res 19(1):53-61
26. Goetze S, Mateos-Langerak J, Gierman HJ, Leeuw WD, Giromus O, Indemans MHG, Koster J, Ondrej V, Versteeg R, Driel RV (2007) The three-dimensional structure of human interphase chromosomes is related to the transcriptome map. Mol Cell Biol 27(12):44754487
27. Grenon M, Gilbert C, Lowndes NF (2001) Checkpoint activation in response to double-strand breaks requires the Mre11/Rad50/Xrs2 complex. Nat Cell Biol 3(9):844-7 (Pubitemid 32842691)
28. Grosberg A, Chochlov AR (1994) Statistical physics of macromolecules. AIP series in polymers and complex materials. American Institute of Physics, New York
29. Haffner MC, Aryee MJ, Toubaji A, Esopi DM, Albadine R, Gurel B, Isaacs WB, Bova GS, Liu W, Xu J, Meeker AK, Netto G, De Marzo AM, Nelson WG, Yegnasubramanian S (2010) Androgen-induced TOP2B-mediated double-strand breaks and prostate cancer gene rearrangements. Nat Genet 42(8):668-675
30. Haffner MC, De Marzo AM, Meeker AK, Nelson WG, Yegnasubramanian S (2011) Transcription-induced DNA double strand breaks: both oncogenic force and potential therapeutic target? Clin Cancer Res 17(12):3858-3864
31. Hou C, Corces VG (2012) Throwing transcription for a loop: expression of the genome in the 3D nucleus. Chromosoma 121(2):107-116
32. Jakob B, Splinter J, Conrad S, Voss K-O, Zink D, Durante M, Löbrich M, Taucher-Scholz G (2011) DNA double-strand breaks in heterochromatin elicit fast repair protein recruitment, histone H2AX phosphorylation and relocation to euchromatin. Nucleic Acids Res 39(15):6489-6499
33. Jerabek H, Heermann DW (2012) Expression-dependent folding of interphase chromatin. PLoS One 7(5):e37525
34. Ju B-G, Lunyak VV, Perissi V, Garcia-Bassets I, Rose DW, Glass CK, Rosenfeld MG (2006) A topoisomerase IIbeta-mediated dsDNA break required for regulated transcription. Science 312(5781):1798-1802 (Pubitemid 43962898)
35. Junier I, Martin O, Kps F (2010) Spatial and topological organization of DNA chains induced by gene co-localization. PLoS Comput Biol 6(2):e1000678
36. Junier I, Dale RK, Hou C, Képès F, Dean A (2012) CTCF-mediated transcriptional regulation through cell type-specific chromosome organization in the β-globin locus. Nucleic Acids Res 40(16):7718-27
37. Kabacik S, Mackay A, Tamber N, Manning G, Finnon P, Paillier F, Ashworth A, Bouffler S, Badie C (2011) Gene expression following ionising radiation: identification of biomarkers for dose estimation and prediction of individual response. Int J Radiat Biol 87(2):115-29
38. Kinner A, Wu W, Staudt C, Iliakis G (2008) Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res 36(17):56785694
39. Krawczyk PM, Borovski T, Stap J, Cijsouw A, ten Cate R, Medema JP, Kanaar R, Franken NAP, Aten JA (2012) Chromatin mobility is increased at sites of DNA double-strand breaks. J Cell Sci 125(Pt 9):2127-33
40. Kremer K, Grest GS (1990) Dynamics of entangled linear polymer melts: a molecular dynamics simulation. J Chem Phys 92(8):5057-5086
41. Kruhlak M, Celeste A, Dellaire G, Fernandez-Capetillo O, Müller W, McNally J, Bazett-Jones D, Nussenzweig A (2006) Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J Cell Biol 172(6):823-834
42. Lee J-H, Paull TT (2005) ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308(5721):551554
43. Levin-Zaidman S, Englander J, Shimoni E, Sharma AK, Minton KW, Minsky A (2003) Ringlike structure of the Deinococcus radiodurans genome: a key to radioresistance? Science 299(5604):254-6 (Pubitemid 36125212)
44. Lieberman-Aiden E, van Berkum N, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie B, Sabo P, Dorschner M, Sandstrom R, Bernstein B, Bender M, Groudine M, Gnirke A, Stamatoyannopoulos J, Mirny L, Lander E, Dekker J (2009) Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326(5950):289-293
45. Limbach H, Arnold A, Mann B, Holm C (2006) ESPResSo - an extensible simulation package for research on soft matter systems. Comput Phys Commun 174(9):704-727
46. Lukas C, Falck J, Bartkova J, Bartek J, Lukas J (2003) Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nat Cell Biol 5(3):255-260 (Pubitemid 36322254)
47. Mateos-Langerak J, Bohn M, Leeuw WD, Giromus O, Manders EMM, Verschure PJ, Indemans MHG, Gierman HJ, Heermann DW, Driel RV, Goetze S (2009) Spatially conned folding of chromatin in the interphase nucleus. Proc Natl Acad Sci U S A 106(10):38123817
48. Mezentsev A, Amundson SA (2011) Global gene expression responses to low- or high-dose radiation in a human three-dimensional tissue model. Radiat Res 175:677-688
49. Mills KD, Ferguson DO, Alt FW (2003) The role of DNA breaks in genomic instability and tumorigenesis. Immunol Rev 194:7795
50. Min-Hattab J, Rothstein R (2012) Increased chromosome mobility facilitates homology search during recombination. Nat Cell Biol 14(5):510-517
51. Münkel C, Eils R, Dietzel S, Zink D, Mehring C, Wedemann G, Cremer T, Langowski J (1999) Compartmentalization of interphase chromosomes observed in simulation and experiment. J Mol Biol 285(3):1053-1065 (Pubitemid 29054316)
52. Noordermeer D, de Laat W (2008) Joining the loops: beta-globin gene regulation. IUBMB Life 60(12):824-33
53. Oza P, Jaspersen SL, Miele A, Dekker J, Peterson CL (2009) Mechanisms that regulate localization of a DNA double-strand break to the nuclear periphery. Genes Dev 23(8):912927
54. Rogakou E, Pilch D, Orr A, Ivanova V, Bonner W (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273(10):5858-5868 (Pubitemid 28124064)
55. Sachs RK, van den Engh G, Trask B, Yokota H, Hearst JE (1995) A random-walk/giant-loop model for interphase chromosomes. Proc Natl Acad Sci U S A 92(7):2710-2714
56. Schoenfelder S, Sexton T, Chakalova L, Cope NF, Horton A, Andrews S, Kurukuti S, Mitchell JA, Umlauf D, Dimitrova DS, Eskiw CH, Luo Y, Wei C-L, Ruan Y, Bieker JJ, Fraser P (2010) Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat Genet 42(1):53-61
57. Simonis M, Klous P, Splinter E, Moshkin Y, Willemsen R, de Wit E, van Steensel B, de Laat W (2006) Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat Genet 38(11):1348-1354 (Pubitemid 44646300)
58. Slade D, Lindner AB, Paul G, Radman M (2009) Recombination and replication in DNA repair of heavily irradiated Deinococcus radiodurans. Cell 136(6):1044-55
59. Smirnov DA, Morley M, Shin E, Spielman RS, Cheung VG (2009) Genetic analysis of radiation-induced changes in human gene expression. Nature 459(7246):587591
60. Soutoglou E, Misteli T (2007) Mobility and immobility of chromatin in transcription and genome stability. Curr Op Genet Dev 17:435-442 (Pubitemid 350016896)
61. Soutoglou E, Dorn JF, Sengupta K, Jasin M, Nussenzweig A, Ried T, Danuser G, Misteli T (2007) Positional stability of single double strand breaks in mammalian cells. Nat Cell Biol 9(6):675-682 (Pubitemid 47214730)
62. Vasireddy R, Karagiannis T, El-Osta A (2010) Gamma-radiation-induced gammaH2AX formation occurs preferentially in actively transcribing euchromatic loci. Cell Mol Life Sci 67(2):291-294
63. Versteeg R, van Schaik BDC, van Batenburg MF, Roos M, Monajemi R, Caron H, Bussemaker HJ, van Kampen AHC (2003) The human transcriptome map reveals extremes in gene density, intron length, GC content, and repeat pattern for domains of highly and weakly expressed genes. Genome Res 13(9):1998-2004 (Pubitemid 37161757)
64. Weeks JD, Chandler D, Andersen HC (1971) Role of repulsive forces in determining the equilibrium structure of simple liquids. J Chem Phys 54(12):5237-5247
65. Woodbine L, Brunton H, Goodarzi AA, Shibata A, Jeggo PA (2011) Endogenously induced DNA double strand breaks arise in heterochromatic DNA regions and require ataxia telangiectasia mutated and Artemis for their repair. Nucleic Acids Res 39(16):6986-6997
66. Woodcock CL, Ghosh RP (2010) Chromatin higher-order structure and dynamics. Cold Spring Harb Perspect Biol 2(5):a000596
67. Xu M, Cook PR (2008) Similar active genes cluster in specialized transcription factories. J Cell Biol 181(4):615-623 (Pubitemid 351717509)
68. Zhang Y, Heermann DW (2011) Loops determine the mechanical properties of mitotic chromosomes. PLoS One 6(12):e29225