Cellular Response to DNA Interstrand Crosslinks: the Fanconi Anemia Pathway

Overview

Journal Cell Mol Life Sci

Publisher Springer

Specialty Biology

Date 2016 Apr 21

PMID 27094386

Citations 73

Authors

David Lopez-Martinez

Chih-Chao Liang

Martin A Cohn

Affiliations

Soon will be listed here.

Abstract

Interstrand crosslinks (ICLs) are a highly toxic form of DNA damage. ICLs can interfere with vital biological processes requiring separation of the two DNA strands, such as replication and transcription. If ICLs are left unrepaired, it can lead to mutations, chromosome breakage and mitotic catastrophe. The Fanconi anemia (FA) pathway can repair this type of DNA lesion, ensuring genomic stability. In this review, we will provide an overview of the cellular response to ICLs. First, we will discuss the origin of ICLs, comparing various endogenous and exogenous sources. Second, we will describe FA proteins as well as FA-related proteins involved in ICL repair, and the post-translational modifications that regulate these proteins. Finally, we will review the process of how ICLs are repaired by both replication-dependent and replication-independent mechanisms.

Citing Articles

Multi-adductomics: Advancing mass spectrometry techniques for comprehensive exposome characterization.

Chao M, Chang Y, Cooke M, Hu C Trends Analyt Chem. 2024; 180.

PMID: 39246549 PMC: 11375889. DOI: 10.1016/j.trac.2024.117900.

Dual role of proliferating cell nuclear antigen monoubiquitination in facilitating Fanconi anemia-mediated interstrand crosslink repair.

Shah R, Aslam M, Spanjaard A, de Groot D, Zurcher L, Altelaar M PNAS Nexus. 2024; 3(7):pgae242.

PMID: 38957451 PMC: 11217772. DOI: 10.1093/pnasnexus/pgae242.

Research progress on the fanconi anemia signaling pathway in non-obstructive azoospermia.

Xu H, Zhang Y, Wang C, Fu Z, Lv J, Yang Y Front Endocrinol (Lausanne). 2024; 15:1393111.

PMID: 38846492 PMC: 11153779. DOI: 10.3389/fendo.2024.1393111.

A minimal Fanconi Anemia complex in early diverging fungi.

Barua D, Plecha M, Muszewska A Sci Rep. 2024; 14(1):9922.

PMID: 38688950 PMC: 11061109. DOI: 10.1038/s41598-024-60318-w.

DoUBLing up: ubiquitin and ubiquitin-like proteases in genome stability.

Foster B, Wang Z, Schmidt C Biochem J. 2024; 481(7):515-545.

PMID: 38572758 PMC: 11088880. DOI: 10.1042/BCJ20230284.

References

Lachaud C, Moreno A, Marchesi F, Toth R, Blow J, Rouse J . Ubiquitinated Fancd2 recruits Fan1 to stalled replication forks to prevent genome instability. Science. 2016; 351(6275):846-9. PMC: 4770513. DOI: 10.1126/science.aad5634. View

Meindl A, Hellebrand H, Wiek C, Erven V, Wappenschmidt B, Niederacher D . Germline mutations in breast and ovarian cancer pedigrees establish RAD51C as a human cancer susceptibility gene. Nat Genet. 2010; 42(5):410-4. DOI: 10.1038/ng.569. View

Ying S, Hickson I . Fanconi anaemia proteins are associated with sister chromatid bridging in mitosis. Int J Hematol. 2011; 93(4):440-445. DOI: 10.1007/s12185-011-0818-7. View

Gibbs-Seymour I, Oka Y, Rajendra E, Weinert B, Passmore L, Patel K . Ubiquitin-SUMO circuitry controls activated fanconi anemia ID complex dosage in response to DNA damage. Mol Cell. 2015; 57(1):150-64. PMC: 4416315. DOI: 10.1016/j.molcel.2014.12.001. View

Brendel M, Ruhland A . Relationships between functionality and genetic toxicology of selected DNA-damaging agents. Mutat Res. 1984; 133(1):51-85. DOI: 10.1016/0165-1110(84)90003-4. View

Shigechi T, Tomida J, Sato K, Kobayashi M, Eykelenboom J, Pessina F . ATR-ATRIP kinase complex triggers activation of the Fanconi anemia DNA repair pathway. Cancer Res. 2012; 72(5):1149-56. DOI: 10.1158/0008-5472.CAN-11-2904. View

Yu X, Chini C, He M, Mer G, Chen J . The BRCT domain is a phospho-protein binding domain. Science. 2003; 302(5645):639-42. DOI: 10.1126/science.1088753. View

Kratz K, Schopf B, Kaden S, Sendoel A, Eberhard R, Lademann C . Deficiency of FANCD2-associated nuclease KIAA1018/FAN1 sensitizes cells to interstrand crosslinking agents. Cell. 2010; 142(1):77-88. DOI: 10.1016/j.cell.2010.06.022. View

Drew H, Wing R, Takano T, Broka C, Tanaka S, Itakura K . Structure of a B-DNA dodecamer: conformation and dynamics. Proc Natl Acad Sci U S A. 1981; 78(4):2179-83. PMC: 319307. DOI: 10.1073/pnas.78.4.2179. View

10.

Rajendra E, Oestergaard V, Langevin F, Wang M, Dornan G, Patel K . The genetic and biochemical basis of FANCD2 monoubiquitination. Mol Cell. 2014; 54(5):858-69. PMC: 4051986. DOI: 10.1016/j.molcel.2014.05.001. View

11.

Virts E, Jankowska A, MacKay C, Glaas M, Wiek C, Kelich S . AluY-mediated germline deletion, duplication and somatic stem cell reversion in UBE2T defines a new subtype of Fanconi anemia. Hum Mol Genet. 2015; 24(18):5093-108. PMC: 4550815. DOI: 10.1093/hmg/ddv227. View

12.

Coste F, Malinge J, Serre L, Shepard W, Roth M, Leng M . Crystal structure of a double-stranded DNA containing a cisplatin interstrand cross-link at 1.63 A resolution: hydration at the platinated site. Nucleic Acids Res. 1999; 27(8):1837-46. PMC: 148391. DOI: 10.1093/nar/27.8.1837. View

13.

Machida Y, Machida Y, Chen Y, Gurtan A, Kupfer G, DAndrea A . UBE2T is the E2 in the Fanconi anemia pathway and undergoes negative autoregulation. Mol Cell. 2006; 23(4):589-96. DOI: 10.1016/j.molcel.2006.06.024. View

14.

Wood R . Mammalian nucleotide excision repair proteins and interstrand crosslink repair. Environ Mol Mutagen. 2010; 51(6):520-6. PMC: 3017513. DOI: 10.1002/em.20569. View

15.

Rickman K, Lach F, Abhyankar A, Donovan F, Sanborn E, Kennedy J . Deficiency of UBE2T, the E2 Ubiquitin Ligase Necessary for FANCD2 and FANCI Ubiquitination, Causes FA-T Subtype of Fanconi Anemia. Cell Rep. 2015; 12(1):35-41. PMC: 4497947. DOI: 10.1016/j.celrep.2015.06.014. View

16.

Knipscheer P, Raschle M, Smogorzewska A, Enoiu M, Ho T, Scharer O . The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science. 2009; 326(5960):1698-701. PMC: 2909596. DOI: 10.1126/science.1182372. View

17.

Yan Z, Delannoy M, Ling C, Daee D, Osman F, Muniandy P . A histone-fold complex and FANCM form a conserved DNA-remodeling complex to maintain genome stability. Mol Cell. 2010; 37(6):865-78. PMC: 2847587. DOI: 10.1016/j.molcel.2010.01.039. View

18.

Meetei A, Medhurst A, Ling C, Xue Y, Singh T, Bier P . A human ortholog of archaeal DNA repair protein Hef is defective in Fanconi anemia complementation group M. Nat Genet. 2005; 37(9):958-63. PMC: 2704909. DOI: 10.1038/ng1626. View

19.

Longerich S, Kwon Y, Tsai M, Hlaing A, Kupfer G, Sung P . Regulation of FANCD2 and FANCI monoubiquitination by their interaction and by DNA. Nucleic Acids Res. 2014; 42(9):5657-70. PMC: 4027212. DOI: 10.1093/nar/gku198. View

20.

Sato K, Toda K, Ishiai M, Takata M, Kurumizaka H . DNA robustly stimulates FANCD2 monoubiquitylation in the complex with FANCI. Nucleic Acids Res. 2012; 40(10):4553-61. PMC: 3378891. DOI: 10.1093/nar/gks053. View