DOI: 10.1073/pnas.1015739108. Structural basis for scaffolding-mediated assembly and maturation of a dsDNA virus

Structural basis for scaffolding-mediated assembly and maturation of a dsDNA virus

10.1073/pnas.1015739108

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

Formation of many dsDNA viruses begins with the assembly of a procapsid, containing scaffolding proteins and a multisubunit portal but lacking DNA, which matures into an infectious virion. This process, conserved among dsDNA viruses such as herpes viruses and bacteriophages, is key to forming infectious virions. Bacteriophage P22 has served as a model system for this study in the past several decades. However, how capsid assembly is initiated, where and how scaffolding proteins bind to coat proteins in the procapsid, and the conformational changes upon capsid maturation still remain elusive. Here, we report Cα backbone models for the P22 procapsid and infectious virion derived from electron cryomicroscopy density maps determined at 3.8- and 4.0-Å resolution, respectively, and the first procapsid structure at subnanometer resolution without imposing symmetry. The procapsid structures show the scaffolding protein interacting electrostatically with the N terminus (N arm) of the coat protein through its C-terminal helix-loop-helix motif, as well as unexpected interactions between 10 scaffolding proteins and the 12-fold portal located at a unique vertex. These suggest a critical role for the scaffolding proteins both in initiating the capsid assembly at the portal vertex and propagating its growth on a T = 7 icosahedral lattice. Comparison of the procapsid and the virion backbone models reveals coordinated and complex conformational changes. These structural observations allow us to propose a more detailed molecular mechanism for the scaffolding-mediated capsid assembly initiation including portal incorporation, release of scaffolding proteins upon DNA packaging, and maturation into infectious virions.

Bibliography

Chen, D.-H., Baker, M. L., Hryc, C. F., DiMaio, F., Jakana, J., Wu, W., Dougherty, M., Haase-Pettingell, C., Schmid, M. F., Jiang, W., Baker, D., King, J. A., & Chiu, W. (2011). Structural basis for scaffolding-mediated assembly and maturation of a dsDNA virus. Proceedings of the National Academy of Sciences, 108(4), 1355â1360.

Authors 13

Dong-Hua Chen (first)
Matthew L. Baker (additional)
Corey F. Hryc (additional)
Frank DiMaio (additional)
Joanita Jakana (additional)
Weimin Wu (additional)
Matthew Dougherty (additional)
Cameron Haase-Pettingell (additional)
Michael F. Schmid (additional)
Wen Jiang (additional)
David Baker (additional)
Jonathan A. King (additional)
Wah Chiu (additional)

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Dates

Type	When
Created	14 years, 7 months ago (Jan. 10, 2011, 11:55 p.m.)
Deposited	3 years, 2 months ago (June 7, 2022, 4:20 a.m.)
Indexed	4 weeks, 1 day ago (July 25, 2025, 6:01 a.m.)
Issued	14 years, 7 months ago (Jan. 10, 2011)
Published	14 years, 7 months ago (Jan. 10, 2011)
Published Online	14 years, 7 months ago (Jan. 10, 2011)
Published Print	14 years, 6 months ago (Jan. 25, 2011)

Funders 0

None

BibTeX

@article{Chen_2011, title={Structural basis for scaffolding-mediated assembly and maturation of a dsDNA virus}, volume={108}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.1015739108}, DOI={10.1073/pnas.1015739108}, number={4}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Chen, Dong-Hua and Baker, Matthew L. and Hryc, Corey F. and DiMaio, Frank and Jakana, Joanita and Wu, Weimin and Dougherty, Matthew and Haase-Pettingell, Cameron and Schmid, Michael F. and Jiang, Wen and Baker, David and King, Jonathan A. and Chiu, Wah}, year={2011}, month=jan, pages={1355–1360} }

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  "abstract": "<jats:p>\n            Formation of many dsDNA viruses begins with the assembly of a procapsid, containing scaffolding proteins and a multisubunit portal but lacking DNA, which matures into an infectious virion. This process, conserved among dsDNA viruses such as herpes viruses and bacteriophages, is key to forming infectious virions. Bacteriophage P22 has served as a model system for this study in the past several decades. However, how capsid assembly is initiated, where and how scaffolding proteins bind to coat proteins in the procapsid, and the conformational changes upon capsid maturation still remain elusive. Here, we report C\u03b1 backbone models for the P22 procapsid and infectious virion derived from electron cryomicroscopy density maps determined at 3.8- and 4.0-\u212b resolution, respectively, and the first procapsid structure at subnanometer resolution without imposing symmetry. The procapsid structures show the scaffolding protein interacting electrostatically with the N\u00a0terminus (N\u00a0arm) of the coat protein through its C-terminal helix-loop-helix motif, as well as unexpected interactions between 10 scaffolding proteins and the 12-fold portal located at a unique vertex. These suggest a critical role for the scaffolding proteins both in initiating the capsid assembly at the portal vertex and propagating its growth on a\n            <jats:italic>T</jats:italic>\n            \u00a0=\u00a07 icosahedral lattice. Comparison of the procapsid and the virion backbone models reveals coordinated and complex conformational changes. These structural observations allow us to propose a more detailed molecular mechanism for the scaffolding-mediated capsid assembly initiation including portal incorporation, release of scaffolding proteins upon DNA packaging, and maturation into infectious virions.\n          </jats:p>",
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