Global organization of replication time zones of the mouse genome.

The division of genomes into distinct replication time zones has long been established. However, an in-depth understanding of their organization and their relationship to transcription is incomplete. Taking advantage of a novel synchronization method ("baby machine") and of genomic DNA microarrays, we have, for the first time, mapped replication times of the entire mouse genome at a high temporal resolution. Our data revealed that although most of the genome has a distinct time of replication either early, middle, or late S phase, a significant portion of the genome is replicated asynchronously. Analysis of the replication map revealed the genomic scale organization of the replication time zones. We found that the genomic regions between early and late replication time zones often consist of extremely large replicons. Analysis of the relationship between replication and transcription revealed that early replication is frequently correlated with the transcription potential of a gene and not necessarily with its actual transcriptional activity. These findings, along with the strong conservation found between replication timing in human and mouse genomes, emphasize the importance of replication timing in transcription regulation.

[1]  David M MacAlpine,et al.  Coordination of replication and transcription along a Drosophila chromosome. , 2004, Genes & development.

[2]  W. Richardson,et al.  A Dynamic Switch in the Replication Timing of Key Regulator Genes in Embryonic Stem Cells upon Neural Induction , 2004, Cell cycle.

[3]  D. Gilbert,et al.  Replication timing and transcriptional control: beyond cause and effect--part II. , 2002, Current opinion in genetics & development.

[4]  Holmquist Gp Role of replication time in the control of tissue-specific gene expression. , 1987 .

[5]  R. D. Little,et al.  Evidence that a single replication fork proceeds from early to late replicating domains in the IgH locus in a non-B cell line. , 1999, Molecular cell.

[6]  Neerja Karnani,et al.  Pan-S replication patterns and chromosomal domains defined by genome-tiling arrays of ENCODE genomic areas. , 2007, Genome research.

[7]  Ian Dunham,et al.  Replication Timing of Human Chromosome 6 , 2005, Cell cycle.

[8]  Michael Ruogu Zhang,et al.  Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. , 1998, Molecular biology of the cell.

[9]  M. A. Goldman,et al.  Replication timing of genes and middle repetitive sequences. , 1984, Science.

[10]  H. Saito,et al.  Novel and quantitative DNA dot-blotting method for assessment of in vivo proliferation. , 2005, American journal of physiology. Gastrointestinal and liver physiology.

[11]  A. Papavassiliou,et al.  Oncogene-induced replication stress preferentially targets common fragile sites in preneoplastic lesions. A genome-wide study , 2008, Oncogene.

[12]  D. Ward,et al.  Delineation of DNA replication time zones by fluorescence in situ hybridization. , 1992, The EMBO journal.

[13]  Alon Goren,et al.  Replicating by the clock , 2003, Nature Reviews Molecular Cell Biology.

[14]  D. J. Driscoll,et al.  Allele-specific replication timing of imprinted gene regions , 1993, Nature.

[15]  C. Ball,et al.  Identification of genes periodically expressed in the human cell cycle and their expression in tumors. , 2002, Molecular biology of the cell.

[16]  Ronald W. Davis,et al.  Replication dynamics of the yeast genome. , 2001, Science.

[17]  Mark Gerstein,et al.  DNA replication-timing analysis of human chromosome 22 at high resolution and different developmental states. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[18]  D. Gilbert,et al.  Differential subnuclear localization and replication timing of histone H3 lysine 9 methylation states. , 2005, Molecular biology of the cell.

[19]  C. Helmstetter,et al.  Synchrony in Human, Mouse and Bacterial Cell Cultures: A Comparison , 2003, Cell cycle.

[20]  R. Hand Eucaryotic DNA: Organization of the genome for replication , 1978, Cell.

[21]  Yonatan Aumann,et al.  Efficient calculation of interval scores for DNA copy number data analysis. , 2006 .

[22]  Stephan Sauer,et al.  Chromatin signatures of pluripotent cell lines , 2006, Nature Cell Biology.

[23]  A. Fisher,et al.  Heritable gene silencing in lymphocytes delays chromatid resolution without affecting the timing of DNA replication , 2003, Nature Cell Biology.

[24]  Srinka Ghosh,et al.  Temporal profile of replication of human chromosomes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[25]  David M. MacAlpine,et al.  A genomic view of eukaryotic DNA replication , 2005, Chromosome Research.

[26]  R. Drouin,et al.  High-resolution replication bands compared with morphologic G- and R-bands. , 1994, Advances in human genetics.

[27]  T. Canfield,et al.  Role of late replication timing in the silencing of X-linked genes. , 1996, Human molecular genetics.

[28]  T. Hashimshony,et al.  Establishment of transcriptional competence in early and late S phase , 2002, Nature.

[29]  G. Holmquist,et al.  Characterization of Giemsa dark- and light-band DNA , 1982, Cell.

[30]  Ronald Berezney,et al.  Heterogeneity of eukaryotic replicons, replicon clusters, and replication foci , 2000, Chromosoma.

[31]  B. Michel,et al.  When replication forks stop , 1994, Molecular microbiology.

[32]  David Botstein,et al.  Promoter-specific binding of Rap1 revealed by genome-wide maps of protein–DNA association , 2001, Nature Genetics.

[33]  T. Canfield,et al.  Association of fragile X syndrome with delayed replication of the FMR1 gene , 1993, Cell.

[34]  I. Simon,et al.  Allelic inactivation regulates olfactory receptor gene expression , 1994, Cell.

[35]  D. Gilbert Temporal order of replication of Xenopus laevis 5S ribosomal RNA genes in somatic cells. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Y. Yurov Rate of DNA replication fork movement within a single mammalian cell. , 1980, Journal of molecular biology.

[37]  C. Helmstetter,et al.  Production of minimally disturbed synchronous cultures of hematopoietic cells. , 2002, BioTechniques.

[38]  Owen T McCann,et al.  Replication timing of the human genome. , 2004, Human molecular genetics.

[39]  G. Wahl,et al.  Initiation of DNA replication at the human β-globin 3′ enhancer , 2005, Nucleic Acids Research.

[40]  B. Migeon,et al.  Asynchronous replication of homologous loci on human active and inactive X chromosomes. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[41]  S. Gangloff,et al.  Replication fork pausing and recombination or "gimme a break". , 2000, Genes & development.

[42]  C. Schildkraut,et al.  The temporal order of replication of murine immunoglobulin heavy chain constant region sequences corresponds to their linear order in the genome. , 1982, Nucleic acids research.

[43]  A. Chess,et al.  An epigenetic state associated with areas of gene duplication. , 2006, Genome research.

[44]  H. Edenberg,et al.  Eukaryotic chromosome replication. , 1975, Annual review of genetics.

[45]  Doron Lancet,et al.  Genome-wide midrange transcription profiles reveal expression level relationships in human tissue specification , 2005, Bioinform..

[46]  S. Batalov,et al.  A gene atlas of the mouse and human protein-encoding transcriptomes. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[47]  S. Razin,et al.  Mapping of replication origins and termination sites in the Duchenne muscular dystrophy gene. , 1997, Genomics.

[48]  K. Kitada,et al.  Mapping of early firing origins on a replication profile of budding yeast , 2002, Genes to cells : devoted to molecular & cellular mechanisms.

[49]  I. Simon,et al.  Asynchronous replication of imprinted genes is established in the gametes and maintained during development , 1999, Nature.

[50]  Nicola J. Rinaldi,et al.  Control of Pancreas and Liver Gene Expression by HNF Transcription Factors , 2004, Science.

[51]  I. Simon,et al.  Developmental regulation of DNA replication timing at the human β globin locus , 2001 .

[52]  B. Friedlander Gimme a Break! , 2010 .

[53]  Charles Kooperberg,et al.  Genome-wide DNA replication profile for Drosophila melanogaster: a link between transcription and replication timing , 2002, Nature Genetics.

[54]  D. Housman,et al.  Changes in the rate of DNA replication fork movement during S phase in mammalian cells. , 1975, Journal of molecular biology.

[55]  M. Hattori,et al.  Chromosome-wide assessment of replication timing for human chromosomes 11q and 21q: disease-related genes in timing-switch regions. , 2002, Human molecular genetics.

[56]  H. Cedar,et al.  DNA replication timing of the human beta-globin domain is controlled by histone modification at the origin. , 2008, Genes & development.