Differentiation-induced Replication-timing Changes Are Restricted to AT-rich/long Interspersed Nuclear Element (LINE)-rich Isochores

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2004 Nov 24

PMID 15557005

Citations 51

Authors

Ichiro Hiratani

Amanda Leskovar

David M Gilbert

Affiliations

Soon will be listed here.

Abstract

The replication timing of some genes is developmentally regulated, but the significance of replication timing to cellular differentiation has been difficult to substantiate. Studies have largely been restricted to the comparison of a few genes in established cell lines derived from different tissues, and most of these genes do not change replication timing. Hence, it has not been possible to predict how many or what types of genes might be subject to such control. Here, we have evaluated the replication timing of 54 tissue-specific genes in mouse embryonic stem cells before and after differentiation to neural precursors. Strikingly, genes residing within isochores rich in GC and poor in long interspersed nuclear elements (LINEs) did not change their replication timing, whereas half of genes within isochores rich in AT and long interspersed nuclear elements displayed programmed changes in replication timing that accompanied changes in gene expression. Our results provide direct evidence that differentiation-induced autosomal replication-timing changes are a significant part of mammalian development, provide a means to predict genes subject to such regulation, and suggest that replication timing may be more related to the evolution of metazoan genomes than to gene function or expression pattern.

Citing Articles

Transcription can be sufficient, but is not necessary, to advance replication timing.

Vouzas A, Sasaki T, Rivera-Mulia J, Turner J, Brown A, Alexander K bioRxiv. 2025; .

PMID: 39975371 PMC: 11838563. DOI: 10.1101/2025.02.04.636516.

Modeling the Dynamics of Eukaryotic DNA Synthesis in Remembrance of Tunde Ogunnaike.

Birtwistle M Ind Eng Chem Res. 2023; 62(5):2288-2298.

PMID: 37441358 PMC: 10338029. DOI: 10.1021/acs.iecr.2c02856.

Replication timing and transcriptional control: beyond cause and effect - part IV.

Vouzas A, Gilbert D Curr Opin Genet Dev. 2023; 79:102031.

PMID: 36905782 PMC: 10035587. DOI: 10.1016/j.gde.2023.102031.

Phylogenetic systematics of and genomes illustrate vast taxonomic diversity, open genomes and an abundance of carbohydrate-active enzyme family isoforms.

Pidcock S, Skvortsov T, Santos F, Courtney S, Sui-Ting K, Creevey C Microb Genom. 2021; 7(10).

PMID: 34605764 PMC: 8627218. DOI: 10.1099/mgen.0.000638.

Low Replicative Stress Triggers Cell-Type Specific Inheritable Advanced Replication Timing.

Courtot L, Bournique E, Maric C, Guitton-Sert L, Madrid-Mencia M, Pancaldi V Int J Mol Sci. 2021; 22(9).

PMID: 34066960 PMC: 8125030. DOI: 10.3390/ijms22094959.

References

Lynch M, Conery J . The origins of genome complexity. Science. 2003; 302(5649):1401-4. DOI: 10.1126/science.1089370. View

Panning M, Gilbert D . Spatio-temporal organization of DNA replication in murine embryonic stem, primary, and immortalized cells. J Cell Biochem. 2005; 95(1):74-82. DOI: 10.1002/jcb.20395. View

Bailey J, Carrel L, Chakravarti A, Eichler E . Molecular evidence for a relationship between LINE-1 elements and X chromosome inactivation: the Lyon repeat hypothesis. Proc Natl Acad Sci U S A. 2000; 97(12):6634-9. PMC: 18684. DOI: 10.1073/pnas.97.12.6634. View

Cimbora D, Schubeler D, Reik A, Hamilton J, Francastel C, Epner E . Long-distance control of origin choice and replication timing in the human beta-globin locus are independent of the locus control region. Mol Cell Biol. 2000; 20(15):5581-91. PMC: 86017. DOI: 10.1128/MCB.20.15.5581-5591.2000. View

Brown K, Amoils S, Horn J, Buckle V, Higgs D, MERKENSCHLAGER M . Expression of alpha- and beta-globin genes occurs within different nuclear domains in haemopoietic cells. Nat Cell Biol. 2001; 3(6):602-6. DOI: 10.1038/35078577. View

Eyre-Walker A, Hurst L . The evolution of isochores. Nat Rev Genet. 2001; 2(7):549-55. DOI: 10.1038/35080577. View

Aladjem M, Rodewald L, Lin C, Bowman S, Cimbora D, Brody L . Replication initiation patterns in the beta-globin loci of totipotent and differentiated murine cells: evidence for multiple initiation regions. Mol Cell Biol. 2002; 22(2):442-52. PMC: 139749. DOI: 10.1128/MCB.22.2.442-452.2002. View

Watanabe Y, Fujiyama A, Ichiba Y, Hattori M, Yada T, Sakaki Y . Chromosome-wide assessment of replication timing for human chromosomes 11q and 21q: disease-related genes in timing-switch regions. Hum Mol Genet. 2002; 11(1):13-21. DOI: 10.1093/hmg/11.1.13. View

Rathjen J, Haines B, Hudson K, Nesci A, Dunn S, Rathjen P . Directed differentiation of pluripotent cells to neural lineages: homogeneous formation and differentiation of a neurectoderm population. Development. 2002; 129(11):2649-61. DOI: 10.1242/dev.129.11.2649. View

10.

Gasser S . Visualizing chromatin dynamics in interphase nuclei. Science. 2002; 296(5572):1412-6. DOI: 10.1126/science.1067703. View

11.

Gilbert D . Replication timing and transcriptional control: beyond cause and effect. Curr Opin Cell Biol. 2002; 14(3):377-83. DOI: 10.1016/s0955-0674(02)00326-5. View

12.

Brockdorff N . X-chromosome inactivation: closing in on proteins that bind Xist RNA. Trends Genet. 2002; 18(7):352-8. DOI: 10.1016/s0168-9525(02)02717-8. View

13.

Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan R, Melton D . "Stemness": transcriptional profiling of embryonic and adult stem cells. Science. 2002; 298(5593):597-600. DOI: 10.1126/science.1072530. View

14.

Ivanova N, Dimos J, Schaniel C, Hackney J, Moore K, Lemischka I . A stem cell molecular signature. Science. 2002; 298(5593):601-4. DOI: 10.1126/science.1073823. View

15.

Schubeler D, Scalzo D, Kooperberg C, van Steensel B, Delrow J, Groudine M . Genome-wide DNA replication profile for Drosophila melanogaster: a link between transcription and replication timing. Nat Genet. 2002; 32(3):438-42. DOI: 10.1038/ng1005. View

16.

Waterston R, Lindblad-Toh K, Birney E, Rogers J, Abril J, Agarwal P . Initial sequencing and comparative analysis of the mouse genome. Nature. 2002; 420(6915):520-62. DOI: 10.1038/nature01262. View

17.

Goren A, Cedar H . Replicating by the clock. Nat Rev Mol Cell Biol. 2003; 4(1):25-32. DOI: 10.1038/nrm1008. View

18.

Ying Q, Stavridis M, Griffiths D, Li M, Smith A . Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat Biotechnol. 2003; 21(2):183-6. DOI: 10.1038/nbt780. View

19.

McNairn A, Gilbert D . Epigenomic replication: linking epigenetics to DNA replication. Bioessays. 2003; 25(7):647-56. DOI: 10.1002/bies.10305. View

20.

Azuara V, Brown K, Williams R, Webb N, Dillon N, Festenstein R . Heritable gene silencing in lymphocytes delays chromatid resolution without affecting the timing of DNA replication. Nat Cell Biol. 2003; 5(7):668-74. DOI: 10.1038/ncb1006. View