A Histone-Fold Complex and FANCM Form a Conserved DNA-Remodeling Complex to Maintain Genome Stability

Zhijiang Yan; Mathieu Delannoy; Chen Ling; Danielle Daee; Fekret Osman; Parameswary A. Muniandy; Xi Shen; Anneke B. Oostra; Hansen Du; Jurgen Steltenpool; Ti Lin; Beatrice Schuster; Chantal Décaillet; Andrzej Stasiak; Alicja Z. Stasiak; Stacie Stone; Maureen E. Hoatlin; Detlev Schindler; Christopher L. Woodcock; Hans Joenje; Ranjan Sen; Johan P. de Winter; Lei Li; Michael M. Seidman; Matthew C. Whitby; Kyungjae Myung; Angelos Constantinou; Weidong Wang

doi:10.1016/j.molcel.2010.01.039

A Histone-Fold Complex and FANCM Form a Conserved DNA-Remodeling Complex to Maintain Genome Stability

Zhijiang Yan, Mathieu Delannoy, Chen Ling, Danielle Daee, Fekret Osman, Parameswary A. Muniandy, Xi Shen, Anneke B. Oostra, Hansen Du, Jurgen Steltenpool, Ti Lin, Beatrice Schuster, Chantal Décaillet, Andrzej Stasiak, Alicja Z. Stasiak, Stacie Stone, Maureen E. Hoatlin, Detlev Schindler, Christopher L. Woodcock, Hans JoenjeRanjan Sen, Johan P. de Winter, Lei Li, Michael M. Seidman, Matthew C. Whitby, Kyungjae Myung, Angelos Constantinou, Weidong Wang

Research output: Contribution to journal › Article › peer-review

174 Scopus citations

Abstract

FANCM remodels branched DNA structures and plays essential roles in the cellular response to DNA replication stress. Here, we show that FANCM forms a conserved DNA-remodeling complex with a histone-fold heterodimer, MHF. We find that MHF stimulates DNA binding and replication fork remodeling by FANCM. In the cell, FANCM and MHF are rapidly recruited to forks stalled by DNA interstrand crosslinks, and both are required for cellular resistance to such lesions. In vertebrates, FANCM-MHF associates with the Fanconi anemia (FA) core complex, promotes FANCD2 monoubiquitination in response to DNA damage, and suppresses sister-chromatid exchanges. Yeast orthologs of these proteins function together to resist MMS-induced DNA damage and promote gene conversion at blocked replication forks. Thus, FANCM-MHF is an essential DNA-remodeling complex that protects replication forks from yeast to human.

Original language	English (US)
Pages (from-to)	865-878
Number of pages	14
Journal	Molecular Cell
Volume	37
Issue number	6
DOIs	https://doi.org/10.1016/j.molcel.2010.01.039
State	Published - Mar 26 2010
Externally published	Yes

Keywords

DNA
PROTEINS

ASJC Scopus subject areas

Molecular Biology
Cell Biology

Access to Document

10.1016/j.molcel.2010.01.039

Cite this

Yan, Z., Delannoy, M., Ling, C., Daee, D., Osman, F., Muniandy, P. A., Shen, X., Oostra, A. B., Du, H., Steltenpool, J., Lin, T., Schuster, B., Décaillet, C., Stasiak, A., Stasiak, A. Z., Stone, S., Hoatlin, M. E., Schindler, D., Woodcock, C. L., ... Wang, W. (2010). A Histone-Fold Complex and FANCM Form a Conserved DNA-Remodeling Complex to Maintain Genome Stability. Molecular Cell, 37(6), 865-878. https://doi.org/10.1016/j.molcel.2010.01.039

Yan, Z, Delannoy, M, Ling, C, Daee, D, Osman, F, Muniandy, PA, Shen, X, Oostra, AB, Du, H, Steltenpool, J, Lin, T, Schuster, B, Décaillet, C, Stasiak, A, Stasiak, AZ, Stone, S, Hoatlin, ME, Schindler, D, Woodcock, CL, Joenje, H, Sen, R, de Winter, JP, Li, L, Seidman, MM, Whitby, MC, Myung, K, Constantinou, A & Wang, W 2010, 'A Histone-Fold Complex and FANCM Form a Conserved DNA-Remodeling Complex to Maintain Genome Stability', Molecular Cell, vol. 37, no. 6, pp. 865-878. https://doi.org/10.1016/j.molcel.2010.01.039

@article{f7ab4ccadee74c3485ffd599782f4146,

title = "A Histone-Fold Complex and FANCM Form a Conserved DNA-Remodeling Complex to Maintain Genome Stability",

abstract = "FANCM remodels branched DNA structures and plays essential roles in the cellular response to DNA replication stress. Here, we show that FANCM forms a conserved DNA-remodeling complex with a histone-fold heterodimer, MHF. We find that MHF stimulates DNA binding and replication fork remodeling by FANCM. In the cell, FANCM and MHF are rapidly recruited to forks stalled by DNA interstrand crosslinks, and both are required for cellular resistance to such lesions. In vertebrates, FANCM-MHF associates with the Fanconi anemia (FA) core complex, promotes FANCD2 monoubiquitination in response to DNA damage, and suppresses sister-chromatid exchanges. Yeast orthologs of these proteins function together to resist MMS-induced DNA damage and promote gene conversion at blocked replication forks. Thus, FANCM-MHF is an essential DNA-remodeling complex that protects replication forks from yeast to human.",

keywords = "DNA, PROTEINS",

author = "Zhijiang Yan and Mathieu Delannoy and Chen Ling and Danielle Daee and Fekret Osman and Muniandy, {Parameswary A.} and Xi Shen and Oostra, {Anneke B.} and Hansen Du and Jurgen Steltenpool and Ti Lin and Beatrice Schuster and Chantal D{\'e}caillet and Andrzej Stasiak and Stasiak, {Alicja Z.} and Stacie Stone and Hoatlin, {Maureen E.} and Detlev Schindler and Woodcock, {Christopher L.} and Hans Joenje and Ranjan Sen and {de Winter}, {Johan P.} and Lei Li and Seidman, {Michael M.} and Whitby, {Matthew C.} and Kyungjae Myung and Angelos Constantinou and Weidong Wang",

note = "Funding Information: We thank Y. Xue for providing recombinant FANCM754 protein, Drs. K.J. Patel for FANCM −/− cells and antibody, M. Takata for chicken FANCD2 antibody, Y. Li for FAAP24 antibody, and D. Schlessinger for critical reading of the manuscript. This work was supported in part by the Intramural Research Program of the National Institute on Aging (grant AG000688-07), NHGRI (grant HG012003-07). National Institute of Health (grants HL007781 and CA112775), and the Fanconi Anemia Research Foundation and Swiss National Science Foundation (grant 3100A0-116275). A.C. was supported by a Swiss National Science Foundation Professorship (grant PP00A-118991). M.C.W. and F.O. were supported by a Wellcome Trust Senior Research Fellowship to M.C.W. ",

year = "2010",

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doi = "10.1016/j.molcel.2010.01.039",

language = "English (US)",

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pages = "865--878",

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TY - JOUR

T1 - A Histone-Fold Complex and FANCM Form a Conserved DNA-Remodeling Complex to Maintain Genome Stability

AU - Yan, Zhijiang

AU - Delannoy, Mathieu

AU - Ling, Chen

AU - Daee, Danielle

AU - Osman, Fekret

AU - Muniandy, Parameswary A.

AU - Shen, Xi

AU - Oostra, Anneke B.

AU - Du, Hansen

AU - Steltenpool, Jurgen

AU - Lin, Ti

AU - Schuster, Beatrice

AU - Décaillet, Chantal

AU - Stasiak, Andrzej

AU - Stasiak, Alicja Z.

AU - Stone, Stacie

AU - Hoatlin, Maureen E.

AU - Schindler, Detlev

AU - Woodcock, Christopher L.

AU - Joenje, Hans

AU - Sen, Ranjan

AU - de Winter, Johan P.

AU - Li, Lei

AU - Seidman, Michael M.

AU - Whitby, Matthew C.

AU - Myung, Kyungjae

AU - Constantinou, Angelos

AU - Wang, Weidong

N1 - Funding Information: We thank Y. Xue for providing recombinant FANCM754 protein, Drs. K.J. Patel for FANCM −/− cells and antibody, M. Takata for chicken FANCD2 antibody, Y. Li for FAAP24 antibody, and D. Schlessinger for critical reading of the manuscript. This work was supported in part by the Intramural Research Program of the National Institute on Aging (grant AG000688-07), NHGRI (grant HG012003-07). National Institute of Health (grants HL007781 and CA112775), and the Fanconi Anemia Research Foundation and Swiss National Science Foundation (grant 3100A0-116275). A.C. was supported by a Swiss National Science Foundation Professorship (grant PP00A-118991). M.C.W. and F.O. were supported by a Wellcome Trust Senior Research Fellowship to M.C.W.

PY - 2010/3/26

Y1 - 2010/3/26

N2 - FANCM remodels branched DNA structures and plays essential roles in the cellular response to DNA replication stress. Here, we show that FANCM forms a conserved DNA-remodeling complex with a histone-fold heterodimer, MHF. We find that MHF stimulates DNA binding and replication fork remodeling by FANCM. In the cell, FANCM and MHF are rapidly recruited to forks stalled by DNA interstrand crosslinks, and both are required for cellular resistance to such lesions. In vertebrates, FANCM-MHF associates with the Fanconi anemia (FA) core complex, promotes FANCD2 monoubiquitination in response to DNA damage, and suppresses sister-chromatid exchanges. Yeast orthologs of these proteins function together to resist MMS-induced DNA damage and promote gene conversion at blocked replication forks. Thus, FANCM-MHF is an essential DNA-remodeling complex that protects replication forks from yeast to human.

AB - FANCM remodels branched DNA structures and plays essential roles in the cellular response to DNA replication stress. Here, we show that FANCM forms a conserved DNA-remodeling complex with a histone-fold heterodimer, MHF. We find that MHF stimulates DNA binding and replication fork remodeling by FANCM. In the cell, FANCM and MHF are rapidly recruited to forks stalled by DNA interstrand crosslinks, and both are required for cellular resistance to such lesions. In vertebrates, FANCM-MHF associates with the Fanconi anemia (FA) core complex, promotes FANCD2 monoubiquitination in response to DNA damage, and suppresses sister-chromatid exchanges. Yeast orthologs of these proteins function together to resist MMS-induced DNA damage and promote gene conversion at blocked replication forks. Thus, FANCM-MHF is an essential DNA-remodeling complex that protects replication forks from yeast to human.

KW - DNA

KW - PROTEINS

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DO - 10.1016/j.molcel.2010.01.039

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