Allele-Specific Genome-wide Profiling in Human Primary Erythroblasts Reveal Replication Program Organization

English version České info

DNA replication in mammalian cells proceeds according to a distinct order. Genes that are expressed tend to replicate before genes that are not expressed. We report here that we have developed a method to measure the timing of replication of the maternal and paternal chromosomes separately. We found that the paternal and maternal chromosomes replicate at exactly the same time in the large majority of the genome and that the 12% of the genome that replicated asynchronously was enriched in imprinted genes and in structural variants. Previous experiments have shown that chromosomes could be divided into replication timing domains that are a few hundred thousand to a few megabases in size. We show here that these domains can be divided into sub-domains defined by ripples in the timing profile. These ripples corresponded to clusters of origins of replication. Finally, we show that the frequency of initiation in asynchronous regions was similar in the two homologs.

Vyšlo v časopise: Allele-Specific Genome-wide Profiling in Human Primary Erythroblasts Reveal Replication Program Organization. PLoS Genet 10(5): e32767. doi:10.1371/journal.pgen.1004319
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004319

Souhrn

Zdroje

1. AladjemMI (2007) Replication in context: dynamic regulation of DNA replication patterns in metazoans. Nat Rev Genet 8: 588–600.

2. MasaiH, MatsumotoS, YouZ, Yoshizawa-SugataN, OdaM (2010) Eukaryotic chromosome DNA replication: where, when, and how? Annu Rev Biochem 79: 89–130.

3. LeonardAC, MechaliM (2013) DNA replication origins. Cold Spring Harb Perspect Biol 5: a010116.

4. MechaliM (2010) Eukaryotic DNA replication origins: many choices for appropriate answers. Nat Rev Mol Cell Biol 11: 728–738.

5. MechaliM (2001) DNA replication origins: from sequence specificity to epigenetics. Nat Rev Genet 2: 640–645.

6. WuJR, GilbertDM (1996) A distinct G1 step required to specify the Chinese hamster DHFR replication origin. Science 271: 1270–1272.

7. CourbetS, GayS, ArnoultN, WronkaG, AnglanaM, et al. (2008) Replication fork movement sets chromatin loop size and origin choice in mammalian cells. Nature 455: 557–560.

8. AbdurashidovaG, RadulescuS, SandovalO, ZaharievS, DanailovMB, et al. (2007) Functional interactions of DNA topoisomerases with a human replication origin. EMBO J 26: 998–1009.

9. LemaitreJM, DanisE, PaseroP, VassetzkyY, MechaliM (2005) Mitotic remodeling of the replicon and chromosome structure. Cell 123: 787–801.

10. CayrouC, CoulombeP, PuyA, RialleS, KaplanN, et al. (2012) New insights into replication origin characteristics in metazoans. Cell Cycle 11: 658–667.

11. BechhoeferJ, RhindN (2012) Replication timing and its emergence from stochastic processes. Trends Genet 28: 374–381.

12. GuilbaudG, RappaillesA, BakerA, ChenCL, ArneodoA, et al. (2011) Evidence for sequential and increasing activation of replication origins along replication timing gradients in the human genome. PLoS Comput Biol 7: e1002322.

13. ShawA, Olivares-ChauvetP, Maya-MendozaA, JacksonDA (2010) S-phase progression in mammalian cells: modelling the influence of nuclear organization. Chromosome Res 18: 163–178.

14. DemczukA, GauthierMG, VerasI, KosiyatrakulS, SchildkrautCL, et al. (2012) Regulation of DNA replication within the immunoglobulin heavy-chain locus during B cell commitment. PLoS Biol 10: e1001360.

15. YamazakiS, IshiiA, KanohY, OdaM, NishitoY, et al. (2012) Rif1 regulates the replication timing domains on the human genome. EMBO J 31: 3667–3677.

16. CornacchiaD, DileepV, QuivyJP, FotiR, TiliF, et al. (2012) Mouse Rif1 is a key regulator of the replication-timing programme in mammalian cells. EMBO J 31: 3678–3690.

17. DonleyN, StoffregenEP, SmithL, MontagnaC, ThayerMJ (2013) Asynchronous replication, mono-allelic expression, and long range Cis-effects of ASAR6. PLoS Genet 9: e1003423.

18. PopeBD, GilbertDM (2013) The Replication Domain Model: Regulating Replicon Firing in the Context of Large-Scale Chromosome Architecture. J Mol Biol

19. DelgadoS, GomezM, BirdA, AntequeraF (1998) Initiation of DNA replication at CpG islands in mammalian chromosomes. EMBO J 17: 2426–2435.

20. CadoretJC, MeischF, Hassan-ZadehV, LuytenI, GuilletC, et al. (2008) Genome-wide studies highlight indirect links between human replication origins and gene regulation. Proc Natl Acad Sci U S A 105: 15837–15842.

21. Sequeira-MendesJ, Diaz-UriarteR, ApedaileA, HuntleyD, BrockdorffN, et al. (2009) Transcription initiation activity sets replication origin efficiency in mammalian cells. PLoS Genet 5: e1000446.

22. CayrouC, CoulombeP, VigneronA, StanojcicS, GanierO, et al. (2011) Genome-scale analysis of metazoan replication origins reveals their organization in specific but flexible sites defined by conserved features. Genome Res 21: 1438–1449.

23. MartinMM, RyanM, KimR, ZakasAL, FuH, et al. (2011) Genome-wide depletion of replication initiation events in highly transcribed regions. Genome Res 21: 1822–1832.

24. BesnardE, BabledA, LapassetL, MilhavetO, ParrinelloH, et al. (2012) Unraveling cell type-specific and reprogrammable human replication origin signatures associated with G-quadruplex consensus motifs. Nat Struct Mol Biol 19: 837–844.

25. MesnerLD, ValsakumarV, CieslikM, PickinR, HamlinJL, et al. (2013) Bubble-seq analysis of the human genome reveals distinct chromatin-mediated mechanisms for regulating early- and late-firing origins. Genome Res

26. AladjemMI, RodewaldLW, KolmanJL, WahlGM (1998) Genetic dissection of a mammalian replicator in the human beta-globin locus. Science 281: 1005–1009.

27. PaixaoS, ColalucaIN, CubellsM, PeveraliFA, DestroA, et al. (2004) Modular structure of the human lamin B2 replicator. Mol Cell Biol 24: 2958–2967.

28. MalottM, LeffakM (1999) Activity of the c-myc replicator at an ectopic chromosomal location. Mol Cell Biol 19: 5685–5695.

29. AltmanAL, FanningE (2001) The Chinese hamster dihydrofolate reductase replication origin beta is active at multiple ectopic chromosomal locations and requires specific DNA sequence elements for activity. Mol Cell Biol 21: 1098–1110.

30. GilbertDM (2002) Replication timing and transcriptional control: beyond cause and effect. Curr Opin Cell Biol 14: 377–383.

31. GondorA, OhlssonR (2009) Replication timing and epigenetic reprogramming of gene expression: a two-way relationship? Nat Rev Genet 10: 269–276.

32. KorenA, McCarrollSA (2013) Random replication of the inactive X chromosome. Genome Res

33. WoodfineK, FieglerH, BeareDM, CollinsJE, McCannOT, et al. (2004) Replication timing of the human genome. Hum Mol Genet 13: 191–202.

34. DespratR, Thierry-MiegD, LaillerN, LajugieJ, SchildkrautC, et al. (2009) Predictable dynamic program of timing of DNA replication in human cells. Genome Res 19: 2288–2299.

35. RoachJC, GlusmanG, SmitAF, HuffCD, HubleyR, et al. (2010) Analysis of genetic inheritance in a family quartet by whole-genome sequencing. Science 328: 636–639.

36. LajugieJ, MukhopadhyayR, SchizasM, LaillerN, FourelN, et al. (2013) Complete genome phasing of family quartet by combination of genetic, physical and population-based phasing analysis. PLoS One 8: e64571.

37. OlivierEQ, C; BouhassiraEE (2012) Novel, High-yield RBC Production Methods from Cells derived from Human ES, Yolk Sac, Fetal Liver, Cord and Peripheral Blood. Stem Cell Translational Medicine 1: 604–614.

38. HirataniI, RybaT, ItohM, YokochiT, SchwaigerM, et al. (2008) Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol 6: e245.

39. SimonI, TenzenT, ReubinoffBE, HillmanD, McCarreyJR, et al. (1999) Asynchronous replication of imprinted genes is established in the gametes and maintained during development. Nature 401: 929–932.

40. AladjemMI, GroudineM, BrodyLL, DiekenES, FournierRE, et al. (1995) Participation of the human beta-globin locus control region in initiation of DNA replication. Science 270: 815–819.

41. SharpA, RobinsonD, JacobsP (2000) Age- and tissue-specific variation of X chromosome inactivation ratios in normal women. Hum Genet 107: 343–349.

42. MossnerM, NolteF, HutterG, ReinsJ, KlaumunzerM, et al. (2013) Skewed X-inactivation patterns in ageing healthy and myelodysplastic haematopoiesis determined by a pyrosequencing based transcriptional clonality assay. J Med Genet 50: 108–117.

43. BeutlerE (1994) G6PD deficiency. Blood 84: 3613–3636.

44. BoggsBA, ChinaultAC (1994) Analysis of replication timing properties of human X-chromosomal loci by fluorescence in situ hybridization. Proc Natl Acad Sci U S A 91: 6083–6087.

45. LyonMF (1972) X-chromosome inactivation and developmental patterns in mammals. Biol Rev Camb Philos Soc 47: 1–35.

46. Farkash-AmarS, LipsonD, PoltenA, GorenA, HelmstetterC, et al. (2008) Global organization of replication time zones of the mouse genome. Genome Res 18: 1562–1570.

47. AuditB, BakerA, ChenCL, RappaillesA, GuilbaudG, et al. (2013) Multiscale analysis of genome-wide replication timing profiles using a wavelet-based signal-processing algorithm. Nat Protoc 8: 98–110.

48. 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.

49. KorenA, PolakP, NemeshJ, MichaelsonJJ, SebatJ, et al. (2012) Differential relationship of DNA replication timing to different forms of human mutation and variation. Am J Hum Genet 91: 1033–1040.

50. RaghuramanMK, WinzelerEA, CollingwoodD, HuntS, WodickaL, et al. (2001) Replication dynamics of the yeast genome. Science 294: 115–121.

51. VassilevL, JohnsonEM (1989) Mapping initiation sites of DNA replication in vivo using polymerase chain reaction amplification of nascent strand segments. Nucleic Acids Res 17: 7693–7705.

52. YoonY, SanchezJA, BrunC, HubermanJA (1995) Mapping of replication initiation sites in human ribosomal DNA by nascent-strand abundance analysis. Mol Cell Biol 15: 2482–2489.

53. AladjemMI, RodewaldLW, LinCM, BowmanS, CimboraDM, et al. (2002) Replication initiation patterns in the beta-globin loci of totipotent and differentiated murine cells: evidence for multiple initiation regions. Mol Cell Biol 22: 442–452.

54. ZhangY, LiuT, MeyerCA, EeckhouteJ, JohnsonDS, et al. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol 9: R137.

55. ToledoF, BaronB, FernandezMA, LachagesAM, MayauV, et al. (1998) oriGNAI3: a narrow zone of preferential replication initiation in mammalian cells identified by 2D gel and competitive PCR replicon mapping techniques. Nucleic Acids Res 26: 2313–2321.

56. AbdurashidovaG, DeganutoM, KlimaR, RivaS, BiamontiG, et al. (2000) Start sites of bidirectional DNA synthesis at the human lamin B2 origin. Science 287: 2023–2026.

57. VassilevLT, BurhansWC, DePamphilisML (1990) Mapping an origin of DNA replication at a single-copy locus in exponentially proliferating mammalian cells. Mol Cell Biol 10: 4685–4689.

58. LadenburgerEM, KellerC, KnippersR (2002) Identification of a binding region for human origin recognition complex proteins 1 and 2 that coincides with an origin of DNA replication. Mol Cell Biol 22: 1036–1048.

59. DePamphilisML (1999) Replication origins in metazoan chromosomes: fact or fiction? Bioessays 21: 5–16.

60. CostantiniM, BernardiG (2008) Replication timing, chromosomal bands, and isochores. Proc Natl Acad Sci U S A 105: 3433–3437.

61. LopesJ, PiazzaA, BermejoR, KriegsmanB, ColosioA, et al. (2011) G-quadruplex-induced instability during leading-strand replication. EMBO J 30: 4033–4046.

62. FuH, MaunakeaAK, MartinMM, HuangL, ZhangY, et al. (2013) Methylation of histone H3 on lysine 79 associates with a group of replication origins and helps limit DNA replication once per cell cycle. PLoS Genet 9: e1003542.

63. HaaseSB, HeinzelSS, CalosMP (1994) Transcription inhibits the replication of autonomously replicating plasmids in human cells. Mol Cell Biol 14: 2516–2524.

64. MesnerLD, HamlinJL (2005) Specific signals at the 3′ end of the DHFR gene define one boundary of the downstream origin of replication. Genes Dev 19: 1053–1066.

65. SasakiT, RamanathanS, OkunoY, KumagaiC, ShaikhSS, et al. (2006) The Chinese hamster dihydrofolate reductase replication origin decision point follows activation of transcription and suppresses initiation of replication within transcription units. Mol Cell Biol 26: 1051–1062.

66. ErmakovaOV, NguyenLH, LittleRD, ChevillardC, RibletR, et al. (1999) Evidence that a single replication fork proceeds from early to late replicating domains in the IgH locus in a non-B cell line. Mol Cell 3: 321–330.

67. NorioP, KosiyatrakulS, YangQ, GuanZ, BrownNM, et al. (2005) Progressive activation of DNA replication initiation in large domains of the immunoglobulin heavy chain locus during B cell development. Mol Cell 20: 575–587.

68. DimitrovaDS, GilbertDM (1998) Regulation of mammalian replication origin usage in Xenopus egg extract. J Cell Sci 111(Pt 19): 2989–2998.

69. LiH, DurbinR (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760.

70. McKennaA, HannaM, BanksE, SivachenkoA, CibulskisK, et al. (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20: 1297–1303.

71. LajugieJ, BouhassiraEE (2011) GenPlay, a multipurpose genome analyzer and browser. Bioinformatics 27: 1889–1893.

72. ZangC, SchonesDE, ZengC, CuiK, ZhaoK, et al. (2009) A clustering approach for identification of enriched domains from histone modification ChIP-Seq data. Bioinformatics 25: 1952–1958.

73. HuppertJL, BalasubramanianS (2005) Prevalence of quadruplexes in the human genome. Nucleic Acids Res 33: 2908–2916.