Structural basis of HMCES interactions with abasic DNA and multivalent substrate recognition

Halabelian, Levon; Ravichandran, Mani; Li, Yanjun; Zeng, Hong; Rao, Anjana; Aravind, L.; Arrowsmith, Cheryl H.

doi:10.1038/s41594-019-0246-6

Title: Structural basis of HMCES interactions with abasic DNA and multivalent substrate recognition

Journal Article · 24 June 2019 · Nature Structural & Molecular Biology

DOI: https://doi.org/10.1038/s41594-019-0246-6 · OSTI ID:1543001

^[1]; Ravichandran, Mani ^[1];

^[1]; Zeng, Hong ^[1]; Rao, Anjana ^[2]; Aravind, L. ^[3];

^[4]

Univ. of Toronto, ON (Canada)
La Jolla Inst. for Immunology, CA (United States); Univ. of San Diego, La Jolla, CA (United States); Sanford Consortium for Regenerative Medicine, La Jolla, CA (United States)
National Inst. of Health (NIH), Bethesda, MD (United States). National Center for Biotechnology Information and National Library of Medicine
Univ. of Toronto, ON (Canada); University Health Network, Toronto, ON (Canada)

Embryonic stem cell-specific 5-hydroxymethylcytosine-binding protein (HMCES) can covalently cross-link to abasic sites in single-stranded DNA at stalled replication forks to prevent genome instability. Here, in this paper, we report crystal structures of the human HMCES SOS response-associated peptidase (SRAP) domain in complex with DNA-damage substrates, including HMCES cross-linked with an abasic site within a 3' overhang DNA. HMCES interacts with both single-strand and duplex segments of DNA, with two independent duplex DNA interaction sites identified in the SRAP domain. The HMCES DNA-protein cross-link structure provides structural insights into a novel thiazolidine covalent interaction between the DNA abasic site and conserved Cys 2 of HMCES. Collectively, our structures demonstrate the capacity for the SRAP domain to interact with a variety of single-strand- and double-strand-containing DNA structures found in DNA-damage sites, including 5' and 3' overhang DNAs and gapped DNAs with short single-strand segments.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institute of General Medical Sciences (NIGMS); National Institutes of Health (NIH); Canadian Institutes of Health Research (CIHR); Natural Sciences and Engineering Research Council of Canada (NSERC); National Library of Medicine (NLM); National Cancer Institute (NCI)

Grant/Contract Number:: AC02-05CH11231; AC02-06CH11357; S10 RR029205

OSTI ID:: 1543001

Journal Information:: Nature Structural & Molecular Biology, Vol. 26, Issue 7; ISSN 1545-9993

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 40 works

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References (34)

Novel autoproteolytic and DNA-damage sensing components in the bacterial SOS response and oxidized methylcytosine-induced eukaryotic DNA demethylation systems Aravind, L.; Anand, Swadha; Iyer, Lakshminarayan M. Biology Direct, Vol. 8, Issue 1 https://doi.org/10.1186/1745-6150-8-20	journal	August 2013
Dynamic Readers for 5-(Hydroxy)Methylcytosine and Its Oxidized Derivatives Spruijt, Cornelia G.; Gnerlich, Felix; Smits, Arne H. Cell, Vol. 152, Issue 5 https://doi.org/10.1016/j.cell.2013.02.004	journal	February 2013
The Curious Chemical Biology of Cytosine: Deamination, Methylation,and Oxidation as Modulators of Genomic Potential Nabel, Christopher S.; Manning, Sara A.; Kohli, Rahul M. ACS Chemical Biology, Vol. 7, Issue 1 https://doi.org/10.1021/cb2002895	journal	October 2011
Improvements to the APBS biomolecular solvation software suite: Improvements to the APBS Software Suite Jurrus, Elizabeth; Engel, Dave; Star, Keith Protein Science, Vol. 27, Issue 1 https://doi.org/10.1002/pro.3280	journal	October 2017
How good are my data and what is the resolution? Evans, Philip R.; Murshudov, Garib N. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7 https://doi.org/10.1107/S0907444913000061	journal	June 2013
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures Landau, M.; Mayrose, I.; Rosenberg, Y. Nucleic Acids Research, Vol. 33, Issue Web Server https://doi.org/10.1093/nar/gki370	journal	July 2005
Replisome Dynamics and Their Functional Relevance upon DNA Damage through the PCNA Interactome Srivastava, Mrinal; Chen, Zhen; Zhang, Huimin Cell Reports, Vol. 25, Issue 13 https://doi.org/10.1016/j.celrep.2018.11.099	journal	December 2018
HMCES Maintains Genome Integrity by Shielding Abasic Sites in Single-Strand DNA Mohni, Kareem N.; Wessel, Sarah R.; Zhao, Runxiang Cell, Vol. 176, Issue 1-2 https://doi.org/10.1016/j.cell.2018.10.055	journal	January 2019
Fisher's information in maximum-likelihood macromolecular crystallographic refinement Steiner, Roberto A.; Lebedev, Andrey A.; Murshudov, Garib N. Acta Crystallographica Section D Biological Crystallography, Vol. 59, Issue 12 https://doi.org/10.1107/S0907444903018675	journal	November 2003
Protection Against Acetaminophen Hepatotoxicity by Ribose-Cysteine (RibCys) Roberts, Jeanette C.; Charyulu, Rajeev L.; Zera, Richard T. Pharmacology & Toxicology, Vol. 70, Issue 4 https://doi.org/10.1111/j.1600-0773.1992.tb00472.x	journal	April 1992
Comparison of sequence profiles. Strategies for structural predictions using sequence information Rychlewski, Leszek; Li, Weizhong; Jaroszewski, Lukasz Protein Science, Vol. 9, Issue 2 https://doi.org/10.1110/ps.9.2.232	journal	January 2000
Computational identification of novel biochemical systems involved in oxidation, glycosylation and other complex modifications of bases in DNA Iyer, Lakshminarayan M.; Zhang, Dapeng; Maxwell Burroughs, A. Nucleic Acids Research, Vol. 41, Issue 16 https://doi.org/10.1093/nar/gkt573	journal	June 2013
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Base excision repair of oxidative DNA damage and association with cancer and aging Maynard, S.; Schurman, S. H.; Harboe, C. Carcinogenesis, Vol. 30, Issue 1 https://doi.org/10.1093/carcin/bgn250	journal	September 2008
MolProbity: More and better reference data for improved all-atom structure validation: PROTEIN SCIENCE.ORG Williams, Christopher J.; Headd, Jeffrey J.; Moriarty, Nigel W. Protein Science, Vol. 27, Issue 1 https://doi.org/10.1002/pro.3330	journal	November 2017
Extent of N-terminal methionine excision from Escherichia coli proteins is governed by the side-chain length of the penultimate amino acid. Hirel, P. H.; Schmitter, M. J.; Dessen, P. Proceedings of the National Academy of Sciences, Vol. 86, Issue 21 https://doi.org/10.1073/pnas.86.21.8247	journal	November 1989
The mouse ortholog of NEIL3 is a functional DNA glycosylase in vitro and in vivo Liu, M.; Bandaru, V.; Bond, J. P. Proceedings of the National Academy of Sciences, Vol. 107, Issue 11 https://doi.org/10.1073/pnas.0908307107	journal	February 2010
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
DNA N-glycosidases: properties of uracil-DNA glycosidase from Escherichia coli. Lindahl, T.; Ljungquist, S.; Siegert, W. Journal of Biological Chemistry, Vol. 252, Issue 10 https://doi.org/10.1016/S0021-9258(17)40386-3	journal	May 1977
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13641-0	journal	December 2019
Overview of the CCP4 suite and current developments. Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.52322	text	January 2011
Liquid chromatography mass spectrometry data of HMCES SRAP domain Halabelian, Levon Zenodo https://doi.org/10.5281/zenodo.2662531	dataset	January 2019
Improvements to the APBS biomolecular solvation software suite Jurrus, Elizabeth; Engel, Dave; Star, Keith arXiv https://doi.org/10.48550/arxiv.1707.00027	text	January 2017
HMCES Maintains Genome Integrity by Shielding Abasic Sites in Single-Strand DNA Mohni, Kareem N.; Wessel, Sarah R.; Zhao, Runxiang Cell, Vol. 176, Issue 1-2 https://doi.org/10.1016/j.cell.2018.10.055	journal	January 2019
Replisome Dynamics and Their Functional Relevance upon DNA Damage through the PCNA Interactome Srivastava, Mrinal; Chen, Zhen; Zhang, Huimin Cell Reports, Vol. 25, Issue 13 https://doi.org/10.1016/j.celrep.2018.11.099	journal	December 2018
The mouse ortholog of NEIL3 is a functional DNA glycosylase in vitro and in vivo Liu, M.; Bandaru, V.; Bond, J. P. Proceedings of the National Academy of Sciences, Vol. 107, Issue 11 https://doi.org/10.1073/pnas.0908307107	journal	February 2010
Extent of N-terminal methionine excision from Escherichia coli proteins is governed by the side-chain length of the penultimate amino acid. Hirel, P. H.; Schmitter, M. J.; Dessen, P. Proceedings of the National Academy of Sciences, Vol. 86, Issue 21 https://doi.org/10.1073/pnas.86.21.8247	journal	November 1989
Base excision repair of oxidative DNA damage and association with cancer and aging Maynard, S.; Schurman, S. H.; Harboe, C. Carcinogenesis, Vol. 30, Issue 1 https://doi.org/10.1093/carcin/bgn250	journal	September 2008
Comparison of sequence profiles. Strategies for structural predictions using sequence information Rychlewski, Leszek; Li, Weizhong; Jaroszewski, Lukasz Protein Science, Vol. 9, Issue 2 https://doi.org/10.1110/ps.9.2.232	journal	January 2000
Protection Against Acetaminophen Hepatotoxicity by Ribose-Cysteine (RibCys) Roberts, Jeanette C.; Charyulu, Rajeev L.; Zera, Richard T. Pharmacology & Toxicology, Vol. 70, Issue 4 https://doi.org/10.1111/j.1600-0773.1992.tb00472.x	journal	April 1992
Improvements to the APBS biomolecular solvation software suite Jurrus, Elizabeth; Engel, Dave; Star, Keith arXiv https://doi.org/10.48550/arxiv.1707.00027	text	January 2017
Liquid chromatography mass spectrometry data of HMCES SRAP domain Halabelian, Levon Zenodo https://doi.org/10.5281/zenodo.2662532	dataset	January 2019

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Molecular basis of abasic site sensing in single-stranded DNA by the SRAP domain of E. coli yedK Wang, Na; Bao, Hongyu; Chen, Liu Nucleic Acids Research, Vol. 47, Issue 19 https://doi.org/10.1093/nar/gkz744	journal	August 2019
Molecular basis of abasic site sensing in single-stranded DNA by the SRAP domain of E. coli yedK Wang, Na; Bao, Hongyu; Chen, Liu Nucleic Acids Research, Vol. 47, Issue 19 https://doi.org/10.1093/nar/gkz744	journal	August 2019