A key interaction with RPA orients XPA in NER complexes

Topolska-Woś, Agnieszka M.; Sugitani, Norie; Cordoba, John J.; Le Meur, Kateryna V.; Le Meur, Rémy A.; Kim, Hyun Suk; Yeo, Jung-Eun; Rosenberg, Daniel; Hammel, Michal; Schärer, Orlando D.; Chazin, Walter J.

doi:10.1093/nar/gkz1231

Title: A key interaction with RPA orients XPA in NER complexes

Journal Article · 11 January 2020 · Nucleic Acids Research

DOI: https://doi.org/10.1093/nar/gkz1231 · OSTI ID:1615298

Topolska-Woś, Agnieszka M. ^[1]; Sugitani, Norie ^[2]; Cordoba, John J. ^[1]; Le Meur, Kateryna V. ^[1]; Le Meur, Rémy A. ^[1]; Kim, Hyun Suk ^[3]; Yeo, Jung-Eun ^[3]; Rosenberg, Daniel ^[4]; Hammel, Michal ^[4]; Schärer, Orlando D. ^[5];

^[6]

Vanderbilt Univ., Nashville, TN (United States). Center for Structural Biology, and Dept. of Biochemistry
Vanderbilt Univ., Nashville, TN (United States). Center for Structural Biology, Dept. of Chemistry
Inst. for Basic Science, Ulsan (Korea). Center for Genomic Integrity
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Vanderbilt Univ., Nashville, TN (United States). Dept. of Biochemistry; Inst. for Basic Science, Ulsan (Korea). Center for Genomic Integrity; Ulsan National Inst. of Science and Technology, Ulsan (Korea). School of Life Sciences
Vanderbilt Univ., Nashville, TN (United States). Center for Structural Biology, Dept. of Biochemistry, and Dept. of Chemistry

The XPA protein functions together with the single-stranded DNA (ssDNA) binding protein RPA as the central scaffold to ensure proper positioning of repair factors in multi-protein nucleotide excision repair (NER) machinery. We previously determined the structure of a short motif in the disordered XPA N-terminus bound to the RPA32C domain. However, a second contact between the XPA DNA-binding domain (XPA DBD) and the RPA70AB tandem ssDNA-binding domains, which is likely to influence the orientation of XPA and RPA on the damaged DNA substrate, remains poorly characterized. NMR was used to map the binding interfaces of XPA DBD and RPA70AB. Combining NMR and X-ray scattering data with comprehensive docking and refinement revealed how XPA DBD and RPA70AB orient on model NER DNA substrates. The structural model enabled design of XPA mutations that inhibit the interaction with RPA70AB. These mutations decreased activity in cell-based NER assays, demonstrating the functional importance of XPA DBD–RPA70AB interaction. Our results inform ongoing controversy about where XPA is bound within the NER bubble, provide structural insights into the molecular basis for malfunction of disease-associated XPA missense mutations, and contribute to understanding of the structure and mechanical action of the NER machinery.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1615298

Journal Information:: Nucleic Acids Research, Journal Name: Nucleic Acids Research Journal Issue: 4 Vol. 48; ISSN 0305-1048

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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Implementation and performance of SIBYLS: a dual endstation small-angle X-ray scattering and macromolecular crystallography beamline at the Advanced Light Source Classen, Scott; Hura, Greg L.; Holton, James M. Journal of Applied Crystallography, Vol. 46, Issue 1 https://doi.org/10.1107/S0021889812048698	journal	January 2013
The redefined DNA-binding domain of human xeroderma pigmentosum complementation group A: production, crystallization and structure solution Lian, Fu-Ming; Yang, Xiangwei; Yang, Wancai Acta Crystallographica Section F Structural Biology Communications, Vol. 75, Issue 1 https://doi.org/10.1107/S2053230X18016990	journal	January 2019
Dissection of the Molecular Defects Caused by Pathogenic Mutations in the DNA Repair Factor XPC Bernardes de Jesus, Bruno M.; Bjørås, Magnar; Coin, Frédéric Molecular and Cellular Biology, Vol. 28, Issue 23 https://doi.org/10.1128/MCB.00781-08	journal	September 2008
An interaction between the DNA repair factor XPA and replication protein A appears essential for nucleotide excision repair. Li, L.; Lu, X.; Peterson, C. A. Molecular and Cellular Biology, Vol. 15, Issue 10 https://doi.org/10.1128/MCB.15.10.5396	journal	October 1995
Replication protein A 32 interacts through a similar binding interface with TIPIN, XPA, and UNG2 Ali, Seikh I.; Shin, Jae-Sun; Bae, Sung-Hun Biological Magnetic Resonance Bank https://doi.org/10.13018/bmr17060	dataset	January 2010
Solution Structure of the DNA- and RPA-binding Domain of the Human Repair Factor XPA Ikegami, Takahisa; Kuraoka, Isao; Saijo, Masafumi Biological Magnetic Resonance Bank https://doi.org/10.13018/bmr4249	dataset	January 1999
RosettaRemodel: A Generalized Framework for Flexible Backbone Protein Design Huang, Po-Ssu; Ban, Yih-En Andrew; Richter, Florian PLoS ONE, Vol. 6, Issue 8 https://doi.org/10.1371/journal.pone.0024109	journal	August 2011
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