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PMID: 20430782 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Evolutionarily conserved replication timing profiles predict long-range chromatin interactions and distinguish closely related cell types.

Genome research ·Vol. 20 ·No. 6 ·2010-06-00 ·Pages 761-70

Ryba T, Hiratani I, Lu J, Itoh M, Kulik M, Zhang J, Schulz TC, Robins AJ, Dalton S, Gilbert DM

Abstract

To identify evolutionarily conserved features of replication timing and their relationship to epigenetic properties, we profiled replication timing genome-wide in four human embryonic stem cell (hESC) lines, hESC-derived neural precursor cells (NPCs), lymphoblastoid cells, and two human induced pluripotent stem cell lines (hiPSCs), and compared them with related mouse cell types. Results confirm the conservation of coordinately replicated megabase-sized "replication domains" punctuated by origin-suppressed regions. Differentiation-induced replication timing changes in both species occur in 400- to 800-kb units and are similarly coordinated with transcription changes. A surprising degree of cell-type-specific conservation in replication timing was observed across regions of conserved synteny, despite considerable species variation in the alignment of replication timing to isochore GC/LINE-1 content. Notably, hESC replication timing profiles were significantly more aligned to mouse epiblast-derived stem cells (mEpiSCs) than to mouse ESCs. Comparison with epigenetic marks revealed a signature of chromatin modifications at the boundaries of early replicating domains and a remarkably strong link between replication timing and spatial proximity of chromatin as measured by Hi-C analysis. Thus, early and late initiation of replication occurs in spatially separate nuclear compartments, but rarely within the intervening chromatin. Moreover, cell-type-specific conservation of the replication program implies conserved developmental changes in spatial organization of chromatin. Together, our results reveal evolutionarily conserved aspects of developmentally regulated replication programs in mammals, demonstrate the power of replication profiling to distinguish closely related cell types, and strongly support the hypothesis that replication timing domains are spatially compartmentalized structural and functional units of three-dimensional chromosomal architecture.

MeSH Terms
Animals Biological Evolution Cell Line Chromatin/genetics DNA Replication Embryonic Stem Cells/metabolism Humans Mice
Chemicals
Chromatin
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Ryba Tyrone
Department of Biological Science, Florida State University, Tallahassee, Florida 32306, USA.
Hiratani Ichiro
Lu Junjie
Itoh Mari
Kulik Michael
Zhang Jinfeng
Schulz Thomas C
Robins Allan J
Dalton Stephen
Gilbert David M
References (49)
49 references, click to expand
  1. Predictable dynamic program of timing of DNA replication in human cells.
    Genome Res. 2009 Dec;19(12):2288-99 PMID: 19767418
  2. Role of the murine reprogramming factors in the induction of pluripotency.
    Cell. 2009 Jan 23;136(2):364-77 PMID: 19167336
  3. Replication timing and transcriptional control: beyond cause and effect--part II.
    Curr Opin Genet Dev. 2009 Apr;19(2):142-9 PMID: 19345088
  4. Genome-wide DNA replication profile for Drosophila melanogaster: a link between transcription and replication timing.
    Nat Genet. 2002 Nov;32(3):438-42 PMID: 12355067
  5. Genome-wide analysis of the replication program in mammals.
    Chromosome Res. 2010 Jan;18(1):115-25 PMID: 20205353
  6. A chromatin-wide transition to H4K20 monomethylation impairs genome integrity and programmed DNA rearrangements in the mouse.
    Genes Dev. 2008 Aug 1;22(15):2048-61 PMID: 18676810
  7. A shift from reversible to irreversible X inactivation is triggered during ES cell differentiation.
    Mol Cell. 2000 Apr;5(4):695-705 PMID: 10882105
  8. Decreased replication origin activity in temporal transition regions.
    J Cell Biol. 2009 Nov 30;187(5):623-35 PMID: 19951913
  9. Replication timing as an epigenetic mark.
    Epigenetics. 2009 Feb 16;4(2):93-7 PMID: 19242104
  10. A faster circular binary segmentation algorithm for the analysis of array CGH data.
    Bioinformatics. 2007 Mar 15;23(6):657-63 PMID: 17234643
  11. Replication timing and transcriptional control: beyond cause and effect.
    Curr Opin Cell Biol. 2002 Jun;14(3):377-83 PMID: 12067662
  12. Derivation of pluripotent epiblast stem cells from mammalian embryos.
    Nature. 2007 Jul 12;448(7150):191-5 PMID: 17597762
  13. Comprehensive mapping of long-range interactions reveals folding principles of the human genome.
    Science. 2009 Oct 9;326(5950):289-93 PMID: 19815776
  14. Monomethylation of histone H4-lysine 20 is involved in chromosome structure and stability and is essential for mouse development.
    Mol Cell Biol. 2009 Apr;29(8):2278-95 PMID: 19223465
  15. CTCF: master weaver of the genome.
    Cell. 2009 Jun 26;137(7):1194-211 PMID: 19563753
  16. Differentiation of human embryonic stem cells to dopaminergic neurons in serum-free suspension culture.
    Stem Cells. 2004;22(7):1218-38 PMID: 15579641
  17. Amplicons on human chromosome 11q are located in the early/late-switch regions of replication timing.
    Genomics. 2004 Nov;84(5):796-805 PMID: 15475258
  18. Reprogramming of human somatic cells to pluripotency with defined factors.
    Nature. 2008 Jan 10;451(7175):141-6 PMID: 18157115
  19. Identification of higher-order functional domains in the human ENCODE regions.
    Genome Res. 2007 Jun;17(6):917-27 PMID: 17568007
  20. Regional and temporal changes in the pattern of X-chromosome replication during the early post-implantation development of the female mouse.
    Chromosoma. 1982;85(2):275-86 PMID: 6180866
  21. Recombination drives the evolution of GC-content in the human genome.
    Mol Biol Evol. 2004 Jun;21(6):984-90 PMID: 14963104
  22. Core transcriptional regulatory circuitry in human embryonic stem cells.
    Cell. 2005 Sep 23;122(6):947-56 PMID: 16153702
  23. Neural induction promotes large-scale chromatin reorganisation of the Mash1 locus.
    J Cell Sci. 2006 Jan 1;119(Pt 1):132-40 PMID: 16371653
  24. Exploration, normalization, and summaries of high density oligonucleotide array probe level data.
    Biostatistics. 2003 Apr;4(2):249-64 PMID: 12925520
  25. The replication timing program of the Chinese hamster beta-globin locus is established coincident with its repositioning near peripheral heterochromatin in early G1 phase.
    J Cell Biol. 2001 Jul 23;154(2):283-92 PMID: 11470818
  26. Epigenetic aspects of differentiation.
    J Cell Sci. 2004 Sep 1;117(Pt 19):4355-63 PMID: 15331660
  27. Nuclear position leaves its mark on replication timing.
    J Cell Biol. 2001 Jan 22;152(2):F11-5 PMID: 11266441
  28. A genomic view of eukaryotic DNA replication.
    Chromosome Res. 2005;13(3):309-26 PMID: 15868424
  29. Global reorganization of replication domains during embryonic stem cell differentiation.
    PLoS Biol. 2008 Oct 7;6(10):e245 PMID: 18842067
  30. Chromatin state marks cell-type- and gender-specific replication of the Drosophila genome.
    Genes Dev. 2009 Mar 1;23(5):589-601 PMID: 19270159
  31. G9a selectively represses a class of late-replicating genes at the nuclear periphery.
    Proc Natl Acad Sci U S A. 2009 Nov 17;106(46):19363-8 PMID: 19889976
  32. Evolution's cauldron: duplication, deletion, and rearrangement in the mouse and human genomes.
    Proc Natl Acad Sci U S A. 2003 Sep 30;100(20):11484-9 PMID: 14500911
  33. New cell lines from mouse epiblast share defining features with human embryonic stem cells.
    Nature. 2007 Jul 12;448(7150):196-9 PMID: 17597760
  34. ENCODE whole-genome data in the UCSC Genome Browser.
    Nucleic Acids Res. 2010 Jan;38(Database issue):D620-5 PMID: 19920125
  35. Global organization of replication time zones of the mouse genome.
    Genome Res. 2008 Oct;18(10):1562-70 PMID: 18669478
  36. Differential subnuclear localization and replication timing of histone H3 lysine 9 methylation states.
    Mol Biol Cell. 2005 Jun;16(6):2872-81 PMID: 15788566
  37. High-resolution profiling of histone methylations in the human genome.
    Cell. 2007 May 18;129(4):823-37 PMID: 17512414
  38. Sequencing newly replicated DNA reveals widespread plasticity in human replication timing.
    Proc Natl Acad Sci U S A. 2010 Jan 5;107(1):139-44 PMID: 19966280
  39. Self-renewal of human embryonic stem cells requires insulin-like growth factor-1 receptor and ERBB2 receptor signaling.
    Blood. 2007 Dec 1;110(12):4111-9 PMID: 17761519
  40. Genome-wide dynamics of replication timing revealed by in vitro models of mouse embryogenesis.
    Genome Res. 2010 Feb;20(2):155-69 PMID: 19952138
  41. Reflections on the biology of embryonic stem (ES) cells.
    Int J Dev Biol. 1997 Apr;41(2):235-43 PMID: 9184330
  42. Early cell fate decisions of human embryonic stem cells and mouse epiblast stem cells are controlled by the same signalling pathways.
    PLoS One. 2009 Jun 30;4(6):e6082 PMID: 19564924
  43. Gene expression pattern and progression of embryogenesis in the immediate post-implantation period of mouse development.
    Gene Expr Patterns. 2007 Apr;7(5):558-73 PMID: 17331809
  44. ReplicationDomain: a visualization tool and comparative database for genome-wide replication timing data.
    BMC Bioinformatics. 2008 Dec 10;9:530 PMID: 19077204
  45. Klf4 reverts developmentally programmed restriction of ground state pluripotency.
    Development. 2009 Apr;136(7):1063-9 PMID: 19224983
  46. Replication timing of the human genome.
    Hum Mol Genet. 2004 Jan 15;13(2):191-202 PMID: 14645202
  47. The spatial position and replication timing of chromosomal domains are both established in early G1 phase.
    Mol Cell. 1999 Dec;4(6):983-93 PMID: 10635323
  48. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias.
    Bioinformatics. 2003 Jan 22;19(2):185-93 PMID: 12538238
  49. Replication and subnuclear location dynamics of the immunoglobulin heavy-chain locus in B-lineage cells.
    Mol Cell Biol. 2002 Jul;22(13):4876-89 PMID: 12052893
Article Info
Journal
Genome research
Abbr.
Genome Res
ISSN
1549-5469
DOI
10.1101/gr.099655.109
Published
2010-06-00
Epub
2010-00-29
Pages
761-70
Language
English
Region
United States
NLM ID
9518021
PMCID
PMC2877573
Subset
IM
Grants
NIGMS NIH HHS · P01 GM085354 · United States
NICHD NIH HHS · R01 HD049647 · United States
NICHD NIH HHS · HD049647 · United States
NIGMS NIH HHS · GM75334 · United States
Databases
GEO
GSE20027
Corrections
CommentIn
PMID: 23698578
External Links
PubMed source DOI: 10.1101/gr.099655.109 PMC Full Text View journal details
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