DNA Double-Strand Breaks Coupled with PARP1 and HNRNPA2B1 Binding Sites Flank Coordinately Expressed Domains in Human Chromosomes
Genome instability plays a key role in multiple biological processes and diseases, including cancer. Genome-wide mapping of DNA double-strand breaks (DSBs) is important for understanding both chromosomal architecture and specific chromosomal regions at DSBs. We developed a method for precise genome-wide mapping of blunt-ended DSBs in human chromosomes, and observed non-random fragmentation and DSB hot spots. These hot spots are scattered along chromosomes and delimit protected 50–250 kb DNA domains. We found that about 30% of the domains (denoted forum domains) possess coordinately expressed genes and that PARP1 and HNRNPA2B1 specifically bind DNA sequences at the forum domain termini. Thus, our data suggest a novel type of gene regulation: a coordinated transcription or silencing of gene clusters delimited by DSB hot spots as well as PARP1 and HNRNPa2B1 binding sites.
Vyšlo v časopise:
DNA Double-Strand Breaks Coupled with PARP1 and HNRNPA2B1 Binding Sites Flank Coordinately Expressed Domains in Human Chromosomes. PLoS Genet 9(4): e32767. doi:10.1371/journal.pgen.1003429
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1003429
Souhrn
Genome instability plays a key role in multiple biological processes and diseases, including cancer. Genome-wide mapping of DNA double-strand breaks (DSBs) is important for understanding both chromosomal architecture and specific chromosomal regions at DSBs. We developed a method for precise genome-wide mapping of blunt-ended DSBs in human chromosomes, and observed non-random fragmentation and DSB hot spots. These hot spots are scattered along chromosomes and delimit protected 50–250 kb DNA domains. We found that about 30% of the domains (denoted forum domains) possess coordinately expressed genes and that PARP1 and HNRNPA2B1 specifically bind DNA sequences at the forum domain termini. Thus, our data suggest a novel type of gene regulation: a coordinated transcription or silencing of gene clusters delimited by DSB hot spots as well as PARP1 and HNRNPa2B1 binding sites.
Zdroje
1. ArtandiSE, ChangS, LeeSL, AlsonS, GottliebGJ, et al. (2000) Telomere dysfunction promotes non-reciprocal translocations and epithelial cancers in mice. Nature 406: 641–645.
2. GisselssonD, JonsonT, PetersenA, StrombeckB, DalCP, et al. (2001) Telomere dysfunction triggers extensive DNA fragmentation and evolution of complex chromosome abnormalities in human malignant tumors. Proc. Natl. Acad. Sci. USA 98: 12683–12688.
3. BignellGR, GreenmanCD, DaviesH, ButlerAP, EdkinsS, et al. (2010) Signatures of mutation and selection in the cancer genome. Nature 463: 893–898.
4. StephensPJ, GreenmanCD, FuB, YangF, BignellGR, et al. (2011) Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 144: 27–40.
5. StephensPJ, McBrideDJ, LinML, VarelaI, PleasanceED, et al. (2009) Complex landscapes of somatic rearrangement in human breast cancer genomes. Nature 462: 1005–1010.
6. SutherlandGR, RichardsRI (1995) The molecular basis of fragile sites in human chromosomes. Curr. Opin. Genet. Dev. 5: 323–327.
7. SchwartzM, ZlotorynskiE, KeremB (2006) The molecular basis of common and rare fragile sites. Cancer Lett 232: 13–26.
8. NegriniS, GorgoulisVG, HalazonetisTD (2010) Genomic instability—an evolving hallmark of cancer. Nat. Rev. Mol. Cell Biol 11: 220–228.
9. LetessierA, MillotGA, KoundrioukoffS, LachagèsAM, VogtN, et al. (2011) Cell-type-specific replication initiation programs set fragility of the FRA3B fragile site. Nature 470: 120–123.
10. Ozeri-GalaiE, LebofskyR, RahatA, BesterAC, BensimonA, et al. (2011) Failure of origin activation in response to fork stalling leads to chromosomal instability at fragile sites. Mol. Cell 43: 122–131.
11. HelmrichA, BallarinoM, ToraL (2011) Collisions between replication and transcription complexes cause common fragile site instability at the longest human genes. Mol Cell 44: 966–977.
12. HalazonetisTD, GorgoulisVG, BartekJ (2008) An oncogene-induced DNA damage model for cancer development. Science 319: 1352–1355.
13. HuebnerK (2011) DNA fragility put into context. Nature 470: 46–47.
14. LiuP, ErezA, NagamaniSC, DharSU, KołodziejskaKE, et al. (2011) Chromosome catastrophes involve replication mechanisms generating complex genomic rearrangements. Cell 146: 889–903.
15. RedonCE, BonnerWM (2011) High salt and DNA double-strand breaks. Proc Natl Acad Sci USA 108: 20281–20282.
16. LindahlT (1993) Instability and decay of the primary structure of DNA. Nature 362: 709–715.
17. NybergKA, Michelson RJ, PutnamCW, WeinertTA (2002) Toward maintaining the genome: DNA damage and replication checkpoints. Annu Rev Genet 36: 617–656.
18. KunkelTA (2004) DNA replication fidelity. J Biol Chem 279: 16895–16898.
19. ZhangL, KimKP, KlecknerNE, StorlazziA (2011) Meiotic double-strand breaks occur once per pair of (sister) chromatids and, via Mec1/ATR and Tel1/ATM, once per quartet of chromatids. Proc Natl Acad Sci USA 108: 20036–200941.
20. TchurikovNA, PonomarenkoNA, AirichLG (1988) Isolation of forum DNA—a specific fraction in human DNA. Doklady Akademii Nauk USSR 303: 491–497.
21. TchurikovNA, PonomarenkoNA (1992) Detection of DNA domains in Drosophila, human and plant chromosomes possessing mainly 50- to 150-kilobase stretches of DNA. Proc Natl Acad Sci USA 89: 6751–6755.
22. TchurikovNA, KretovaOV, SosinDV, ZykovIA, ZhimulevIF, et al. (2011) Genome-wide profiling of forum domains in Drosophila melanogaster. Nucl Acids Res 39: 3667–3685.
23. KaufmannBP (1939) Distribution of induced breaks along the X-chromosome of Drosophila melanogaster. Proc Natl Acad Sci USA 25: 571–577.
24. SpellmanPT, RubinGM (2002) Evidence for large domains of similarly expressed genes in the Drosophila genome. J Biol 1: 5.
25. WeitzmanJB (2002) Transcriptional territories in the genome. J Biol 1: 2.
26. LairdCD, LambMM (1988) Intercalary heterochromatin of Drosophila as a potential model for human fragile sites. Am J Med Genet 30: 689–691.
27. HansenRS, CanfieldTK, LambMM, GartlerSM, LairdCD (1993) Association of fragile X syndrome with delayed replication of the FMR1 gene. Cell 73: 1403–1409.
28. de KoningAPJ, GuW, CastoeTA, BatzerMA, PollockDD (2011) Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet 7: e1002384 doi:10.1371/journal.pgen.1002384.
29. DurkinSG, GloverTW (2007) Chromosome fragile sites. Annu Rev Genet 41: 169–192.
30. ErnstJ, KellisM (2010) Discovery and characterization of chromatin states for systematic annotation of the human genome. Nature Biotechnology 28: 817–825.
31. JacksonSP (2002) Sensing and repairing DNA double-strand breaks. Carcinogenesis 23: 687–696.
32. Lees-MillerSP, MeekK (2003) Repair of DNA double strand breaks by nonhomologous end joining. Biochimie 85: 1161–1173.
33. LieberMR, MaY, PannickeU, SchwarzK (2003) Mechanism and regulation of human non-homologous DNA end-joining. Nat Rev Mol Cell Biol 4: 712–720.
34. Rivera-CalzadaA, SpagnoloL, PearlLH, LlorcaO (2008) Structural model of full-length human Ku70-Ku80 heterodimer and its recognition of DNA and DNA-PKcs. EMBO Rep 8: 56–62.
35. MarconL, BoissonneaultG (2004) Transient DNA strand breaks during mouse and human spermiogenesis: new insights in stage specificity and link to chromatin remodeling. Biol Reprod 70: 910–918.
36. LeducF, MaquennehanV, NkomaGB, BoissonneaultG (2008) DNA damage response during chromatin remodeling in elongating spermatids of mice. Biol Reprod 78: 324–332.
37. BlondetB, Aït-IkhlefA, MurawskyM, RiegerF (2001) Transient massive DNA fragmentation in nervous system during the early course of a murine neurodegenerative disease. Neurosci Lett 305: 202–206.
38. MochizukiK (2010) DNA rearrangements directed by non-coding RNAs in ciliates. Wiley Interdiscip Rev RNA 1: 376–387.
39. RybaT, HirataniI, LuJ, ItohM, KulikM, et al. (2010) Evolutionarily conserved replication timing profiles predict long-range chromatin interactions and distinguish closely related cell types. Genome Res 20: 761–770.
40. RothsteinR, MichelB, GangloffS (2000) Replication fork pausing and recombination or “gimme a break”. Genes Dev 14: 1–10.
41. DebatisseM, Le TallecB, LetessierA, DutrillauxB, BrisonO (2012) Common fragile sites: mechanisms of instability revisited. Trends Genet 28: 22–32.
42. ArltMF, GloverTW (2010) Inhibition of topoisomerase I prevents chromosome breakage at common fragile sites. DNA Repair 9: 678–689.
43. WeiW, BaZ, GaoM, WuY, MaY, et al. (2012) A role for small RNAs in DNA double-strand break repair. Cell 149: 101–112.
44. RazinSV, PetrovP, HancockR (1991) Precise localization of the alpha-globin gene cluster within one of the 20- to 300-kilobase DNA fragments released by cleavage of chicken chromosomal DNA at topoisomerase II sites in vivo: evidence that the fragments are DNA loops or domains. Proc Natl Acad Sci U S A 88: 8515–8519.
45. FosseP, ReneB, Le BretM, PaolettiC, SaucierJM (1991) Sequence requirements for mammalian topoisomerase II mediated DNA cleavage stimulated by an ellipticine derivative. Nucleic Acids Res 19: 2861–2868.
46. ErnstJ, KheradpourP, MikkelsenTS, ShoreshN, WardLD, et al. (2011) Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473: 43–49.
47. KrausWL, LisJT (2003) PARP goes transcription. Cell 113: 677–683.
48. KrishnakumarR, KrausWL (2010) PARP-1 regulates chromatin structure and transcription through a KDM5B-dependent pathway. Mol Cell 39: 736–749.
49. MimoriT, HardinJA (1986) Mechanism of interaction between Ku protein and DNA. J Biol Chem 261: 10375–10379.
50. DownsJA, JacksonSP (2004) A means to a DNA end: the many roles of Ku. Nat Rev Mol Cell Biol 5: 367–378.
51. GuetgC, SantoroR (2012) Noncoding RNAs link PARP1 to heterochromatin. Cell Cycle 11: 2217–2218.
52. GuetgC, ScheifeleF, RosenthalF, HottigerMO, SantoroR (2012) Inheritance of silent rDNA chromatin is mediated by PARP1 via noncoding RNA. Mol Cell 45: 790–800.
53. IsabelleM, GallouziIE, PoirierGG (2012) PARP1 parylation promotes silent locus transmission in the nucleolus: the suspicion confirmed. Mol Cell 45: 706–707.
54. KozuT, HenrichB, SchaferKP (1995) Structure and Expression of the Gene (Hnrpa2b1) Encoding the Human Hnrnp Protein A2/B1. Genomics 25: 365–371.
55. CarpenterB, MacKayC, AlnabulsiA, MacKayM, TelferC, et al. (2006) The roles of heterogeneous nuclear ribonucleoproteins in tumour development and progression. BBA-Rev Cancer 1765: 85–100.
56. YangX, ZouP, YaoJ, YunD, BaoH, et al. (2010) Proteomic dissection of cell type-specific H2AX-interacting protein complex associated with hepatocellular carcinoma. J Proteome Res 9: 1402–1415.
57. SzilardRK, JacquesPE, LaraméeL, ChengB, GaliciaS, et al. (2010) Systematic identification of fragile sites via genome-wide location analysis of gamma-H2AX. Nat Struct Mol Biol 17: 299–305.
58. BuhlerC, BordeV, LichtenM (2007) Mapping meiotic single-strand DNA reveals a new landscape of DNA double-strand breaks in Saccharomyces cerevisiae. PLoS Biol 5: e324 doi:10.1371/journal.pbio.0050324.
59. DoegeCA, InoueK, YamashitaT, RheeDB, TravisS, et al. (2012) Early-stage epigenetic modification during somatic cell reprogramming by Parp1 and Tet2. Nature 488: 652–655.
60. SeabrightM (1971) A rapid banding technique for human chromosomes. Lancet 2: 971–972.
61. YangF, O'BrienPC, MilneBS (1999) A complete comparative chromosome map for the dog, red fox, and human and its integration with canine genetic maps. Genomics 62: 189–202.
62. GraphodatskyAS, SablinamOV, MeyerMN, MalikovVG, IsakovaEA, et al. (2000) Comparative cytogenetics of hamsters of the genus Calomyscus. Cytogenet Cell Genet 88: 296–304.
63. AndrewsNC, FallerDV (1991) A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucl Acids Res 19: 2499.
64. MatsumotoM, NishimuraT (1998) Mersenne Twister: a 623-dimensionally equidistributed uniform pseudo-random number generator. ACM Transactions on Modeling and Computer Simulation 8: 3–30.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2013 Číslo 4
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- The G4 Genome
- Neutral Genomic Microevolution of a Recently Emerged Pathogen, Serovar Agona
- The Histone Demethylase Jarid1b Ensures Faithful Mouse Development by Protecting Developmental Genes from Aberrant H3K4me3
- The Tissue-Specific RNA Binding Protein T-STAR Controls Regional Splicing Patterns of Pre-mRNAs in the Brain