Human XPG nuclease structure, assembly, and activities with insights for neurodegeneration and cancer from pathogenic mutations
Abstract
Xeroderma pigmentosum group G (XPG) protein is both a functional partner in multiple DNA damage responses (DDR) and a pathway coordinator and structure-specific endonuclease in nucleotide excision repair (NER). Different mutations in the XPG geneERCC5lead to either of two distinct human diseases: Cancer-prone xeroderma pigmentosum (XP-G) or the fatal neurodevelopmental disorder Cockayne syndrome (XP-G/CS). To address the enigmatic structural mechanism for these differing disease phenotypes and for XPG’s role in multiple DDRs, here we determined the crystal structure of human XPG catalytic domain (XPGcat), revealing XPG-specific features for its activities and regulation. Furthermore, XPG DNA binding elements conserved with FEN1 superfamily members enable insights on DNA interactions. Notably, all but one of the known pathogenic point mutations map to XPGcat, and both XP-G and XP-G/CS mutations destabilize XPG and reduce its cellular protein levels. Mapping the distinct mutation classes provides structure-based predictions for disease phenotypes: Residues mutated in XP-G are positioned to reduce local stability and NER activity, whereas residues mutated in XP-G/CS have implied long-range structural defects that would likely disrupt stability of the whole protein, and thus interfere with its functional interactions. Combined data from crystallography, biochemistry, small angle X-ray scattering, and electron microscopy unveil an XPG homodimermore »
- Authors:
-
[1];
[1];
[1];
[1];
[4];
[1];
[1];
[5]
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- The Scripps Research Inst., La Jolla, CA (United States)
- Univ. of North Carolina, Chapel Hill, NC (United States)
- Univ. of Texas, Houston, TX (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of Texas, Houston, TX (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1756332
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 117; Journal Issue: 25; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; endonuclease; ERCC5; electron microscopy; crystallography; crystal structure
Citation Formats
Tsutakawa, Susan E., Sarker, Altaf H., Ng, Clifford, Arvai, Andrew S., Shin, David S., Shih, Brian, Jiang, Shuai, Thwin, Aye C., Tsai, Miaw-Sheue, Willcox, Alexandra, Her, Mai Zong, Trego, Kelly S., Raetz, Alan G., Rosenberg, Daniel, Bacolla, Albino, Hammel, Michal, Griffith, Jack D., Cooper, Priscilla K., and Tainer, John A. Human XPG nuclease structure, assembly, and activities with insights for neurodegeneration and cancer from pathogenic mutations. United States: N. p., 2020.
Web. doi:10.1073/pnas.1921311117.
Tsutakawa, Susan E., Sarker, Altaf H., Ng, Clifford, Arvai, Andrew S., Shin, David S., Shih, Brian, Jiang, Shuai, Thwin, Aye C., Tsai, Miaw-Sheue, Willcox, Alexandra, Her, Mai Zong, Trego, Kelly S., Raetz, Alan G., Rosenberg, Daniel, Bacolla, Albino, Hammel, Michal, Griffith, Jack D., Cooper, Priscilla K., & Tainer, John A. Human XPG nuclease structure, assembly, and activities with insights for neurodegeneration and cancer from pathogenic mutations. United States. https://doi.org/10.1073/pnas.1921311117
Tsutakawa, Susan E., Sarker, Altaf H., Ng, Clifford, Arvai, Andrew S., Shin, David S., Shih, Brian, Jiang, Shuai, Thwin, Aye C., Tsai, Miaw-Sheue, Willcox, Alexandra, Her, Mai Zong, Trego, Kelly S., Raetz, Alan G., Rosenberg, Daniel, Bacolla, Albino, Hammel, Michal, Griffith, Jack D., Cooper, Priscilla K., and Tainer, John A. Wed .
"Human XPG nuclease structure, assembly, and activities with insights for neurodegeneration and cancer from pathogenic mutations". United States. https://doi.org/10.1073/pnas.1921311117. https://www.osti.gov/servlets/purl/1756332.
@article{osti_1756332,
title = {Human XPG nuclease structure, assembly, and activities with insights for neurodegeneration and cancer from pathogenic mutations},
author = {Tsutakawa, Susan E. and Sarker, Altaf H. and Ng, Clifford and Arvai, Andrew S. and Shin, David S. and Shih, Brian and Jiang, Shuai and Thwin, Aye C. and Tsai, Miaw-Sheue and Willcox, Alexandra and Her, Mai Zong and Trego, Kelly S. and Raetz, Alan G. and Rosenberg, Daniel and Bacolla, Albino and Hammel, Michal and Griffith, Jack D. and Cooper, Priscilla K. and Tainer, John A.},
abstractNote = {Xeroderma pigmentosum group G (XPG) protein is both a functional partner in multiple DNA damage responses (DDR) and a pathway coordinator and structure-specific endonuclease in nucleotide excision repair (NER). Different mutations in the XPG geneERCC5lead to either of two distinct human diseases: Cancer-prone xeroderma pigmentosum (XP-G) or the fatal neurodevelopmental disorder Cockayne syndrome (XP-G/CS). To address the enigmatic structural mechanism for these differing disease phenotypes and for XPG’s role in multiple DDRs, here we determined the crystal structure of human XPG catalytic domain (XPGcat), revealing XPG-specific features for its activities and regulation. Furthermore, XPG DNA binding elements conserved with FEN1 superfamily members enable insights on DNA interactions. Notably, all but one of the known pathogenic point mutations map to XPGcat, and both XP-G and XP-G/CS mutations destabilize XPG and reduce its cellular protein levels. Mapping the distinct mutation classes provides structure-based predictions for disease phenotypes: Residues mutated in XP-G are positioned to reduce local stability and NER activity, whereas residues mutated in XP-G/CS have implied long-range structural defects that would likely disrupt stability of the whole protein, and thus interfere with its functional interactions. Combined data from crystallography, biochemistry, small angle X-ray scattering, and electron microscopy unveil an XPG homodimer that binds, unstacks, and sculpts duplex DNA at internal unpaired regions (bubbles) into strongly bent structures, and suggest how XPG complexes may bind both NER bubble junctions and replication forks. Collective results support XPG scaffolding and DNA sculpting functions in multiple DDR processes to maintain genome stability.},
doi = {10.1073/pnas.1921311117},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 25,
volume = 117,
place = {United States},
year = {Wed Jun 10 00:00:00 EDT 2020},
month = {Wed Jun 10 00:00:00 EDT 2020}
}
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