DONSON and FANCM Associate with Different Replisomes Distinguished by Replication Timing and Chromatin Domain

Overview

Journal Nat Commun

Specialty Biology

Date 2020 Aug 10

PMID 32769987

Citations 24

Authors

Jing Zhang

Marina A Bellani

Ryan C James

Durga Pokharel

Yongqing Zhang

John J Reynolds

Gavin S McNee

Andrew P Jackson

Grant S Stewart

Michael M Seidman

Affiliations

Soon will be listed here.

Abstract

Duplication of mammalian genomes requires replisomes to overcome numerous impediments during passage through open (eu) and condensed (hetero) chromatin. Typically, studies of replication stress characterize mixed populations of challenged and unchallenged replication forks, averaged across S phase, and model a single species of "stressed" replisome. Here, in cells containing potent obstacles to replication, we find two different lesion proximal replisomes. One is bound by the DONSON protein and is more frequent in early S phase, in regions marked by euchromatin. The other interacts with the FANCM DNA translocase, is more prominent in late S phase, and favors heterochromatin. The two forms can also be detected in unstressed cells. ChIP-seq of DNA associated with DONSON or FANCM confirms the bias of the former towards regions that replicate early and the skew of the latter towards regions that replicate late.

Citing Articles

Repair of genomic interstrand crosslinks.

Bellani M, Shaik A, Majumdar I, Ling C, Seidman M DNA Repair (Amst). 2024; 141:103739.

PMID: 39106540 PMC: 11423799. DOI: 10.1016/j.dnarep.2024.103739.

Single-molecule imaging reveals the mechanism of bidirectional replication initiation in metazoa.

Terui R, Berger S, Sambel L, Song D, Chistol G Cell. 2024; 187(15):3992-4009.e25.

PMID: 38866019 PMC: 11283366. DOI: 10.1016/j.cell.2024.05.024.

Single-Molecule Imaging Reveals the Mechanism of Bidirectional Replication Initiation in Metazoa.

Terui R, Berger S, Sambel L, Song D, Chistol G bioRxiv. 2024; .

PMID: 38585807 PMC: 10996697. DOI: 10.1101/2024.03.28.587265.

Repli-seq Sample Preparation using Cell Sorting with Cell-Permeant Dyes.

Meyer-Nava S, Shetty A, Rivera-Mulia J Curr Protoc. 2023; 3(11):e945.

PMID: 38009262 PMC: 10838012. DOI: 10.1002/cpz1.945.

The Response of the Replication Apparatus to Leading Template Strand Blocks.

Bellani M, Shaik A, Majumdar I, Ling C, Seidman M Cells. 2023; 12(22).

PMID: 37998342 PMC: 10670059. DOI: 10.3390/cells12222607.

References

Tye B . MCM proteins in DNA replication. Annu Rev Biochem. 2000; 68:649-86. DOI: 10.1146/annurev.biochem.68.1.649. View

Bochman M, Schwacha A . The Mcm2-7 complex has in vitro helicase activity. Mol Cell. 2008; 31(2):287-93. DOI: 10.1016/j.molcel.2008.05.020. View

Bai L, Yuan Z, Sun J, Georgescu R, ODonnell M, Li H . Architecture of the Saccharomyces cerevisiae Replisome. Adv Exp Med Biol. 2018; 1042:207-228. PMC: 5800748. DOI: 10.1007/978-981-10-6955-0_10. View

Mayle R, Langston L, Molloy K, Zhang D, Chait B, ODonnell M . Mcm10 has potent strand-annealing activity and limits translocase-mediated fork regression. Proc Natl Acad Sci U S A. 2019; 116(3):798-803. PMC: 6338834. DOI: 10.1073/pnas.1819107116. View

Yeeles J, Janska A, Early A, Diffley J . How the Eukaryotic Replisome Achieves Rapid and Efficient DNA Replication. Mol Cell. 2016; 65(1):105-116. PMC: 5222725. DOI: 10.1016/j.molcel.2016.11.017. View

Lewis J, Spenkelink L, Schauer G, Yurieva O, Mueller S, Natarajan V . Tunability of DNA Polymerase Stability during Eukaryotic DNA Replication. Mol Cell. 2019; 77(1):17-25.e5. PMC: 6943181. DOI: 10.1016/j.molcel.2019.10.005. View

Eickhoff P, Kose H, Martino F, Petojevic T, Abid Ali F, Locke J . Molecular Basis for ATP-Hydrolysis-Driven DNA Translocation by the CMG Helicase of the Eukaryotic Replisome. Cell Rep. 2019; 28(10):2673-2688.e8. PMC: 6737378. DOI: 10.1016/j.celrep.2019.07.104. View

Kliszczak A, Rainey M, Harhen B, Boisvert F, Santocanale C . DNA mediated chromatin pull-down for the study of chromatin replication. Sci Rep. 2012; 1:95. PMC: 3216581. DOI: 10.1038/srep00095. View

Wessel S, Mohni K, Luzwick J, Dungrawala H, Cortez D . Functional Analysis of the Replication Fork Proteome Identifies BET Proteins as PCNA Regulators. Cell Rep. 2019; 28(13):3497-3509.e4. PMC: 6878991. DOI: 10.1016/j.celrep.2019.08.051. View

10.

Serizay J, Ahringer J . Genome organization at different scales: nature, formation and function. Curr Opin Cell Biol. 2018; 52:145-153. DOI: 10.1016/j.ceb.2018.03.009. View

11.

Dileep V, Rivera-Mulia J, Sima J, Gilbert D . Large-Scale Chromatin Structure-Function Relationships during the Cell Cycle and Development: Insights from Replication Timing. Cold Spring Harb Symp Quant Biol. 2015; 80:53-63. DOI: 10.1101/sqb.2015.80.027284. View

12.

Marchal C, Sima J, Gilbert D . Control of DNA replication timing in the 3D genome. Nat Rev Mol Cell Biol. 2019; 20(12):721-737. PMC: 11567694. DOI: 10.1038/s41580-019-0162-y. View

13.

Cortez D, Glick G, Elledge S . Minichromosome maintenance proteins are direct targets of the ATM and ATR checkpoint kinases. Proc Natl Acad Sci U S A. 2004; 101(27):10078-83. PMC: 454167. DOI: 10.1073/pnas.0403410101. View

14.

Li Z, Xu X . Post-Translational Modifications of the Mini-Chromosome Maintenance Proteins in DNA Replication. Genes (Basel). 2019; 10(5). PMC: 6563057. DOI: 10.3390/genes10050331. View

15.

Gadaleta M, Noguchi E . Regulation of DNA Replication through Natural Impediments in the Eukaryotic Genome. Genes (Basel). 2017; 8(3). PMC: 5368702. DOI: 10.3390/genes8030098. View

16.

Rickman K, Smogorzewska A . Advances in understanding DNA processing and protection at stalled replication forks. J Cell Biol. 2019; 218(4):1096-1107. PMC: 6446843. DOI: 10.1083/jcb.201809012. View

17.

MARMUR J, Grossman L . Ultraviolet light induced linking of deoxyribonucleic acid strands and its reversal by photoreactivating enzyme. Proc Natl Acad Sci U S A. 1961; 47:778-87. PMC: 221341. DOI: 10.1073/pnas.47.6.778. View

18.

Zhang J, Walter J . Mechanism and regulation of incisions during DNA interstrand cross-link repair. DNA Repair (Amst). 2014; 19:135-42. PMC: 4076290. DOI: 10.1016/j.dnarep.2014.03.018. View

19.

Huang J, Liu S, Bellani M, Thazhathveetil A, Ling C, de Winter J . The DNA translocase FANCM/MHF promotes replication traverse of DNA interstrand crosslinks. Mol Cell. 2013; 52(3):434-46. PMC: 3880019. DOI: 10.1016/j.molcel.2013.09.021. View

20.

Rager P, Cosculluela D, Deviers D . [Drug hepatitis. Possible role of cyamemazine]. Presse Med. 1983; 12(31):1941. View