Structural and Functional Studies of the Phage Sf6 Terminase Small Subunit Reveal a DNA-Spooling Device Facilitated by Structural Plasticity |
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| Authors: | Haiyan Zhao Yvonne N. Kamau Theodore E. Christensen Liang Tang |
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| Affiliation: | 1. Department of Biological Sciences, Laboratory for Molecular Biology (M/C 567), University of Illinois at Chicago, 900 South Ashland Avenue, Molecular Biology Research Building, Room 4318, Chicago, IL 60607, USA;2. Institut für Biologie, Humboldt Universität zu Berlin, Invalidenstraße 43, D-10115 Berlin, Germany;3. From the Division of Rheumatology, Immunology, and Allergy, Brigham and Women''s Hospital, and the Department of Medicine, Harvard Medical School, Boston, Massachusetts 02115 and;4. the National Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China;3. Departments of Molecular Biology of Archaea, Karl-von-Frisch-Strasse 10, 35043 Marburg, Germany;5. Departments of Ecophysiology, Max Planck Institute for terrestrial Microbiology, Karl-von-Frisch-Strasse 10, 35043 Marburg, Germany;4. Department of Structural Biology, Max Planck Institute of Biophysics, Max-von-Laue-Strasse 3, 60438 Frankfurt, Germany;3. Live Cell Molecular Imaging Research Team, RIKEN Center for Advanced Photonics, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan;4. Chemical Biology Laboratory, RIKEN, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan;5. Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo, Tokyo 113-0033, Japan;3. Department of Biochemistry, Duke University School of Medicine, Durham, North Carolina 27710;4. Department of Biochemistry and Molecular Biology, The University of Texas MD Anderson Cancer Center, Houston, Texas 77030;5. Department of Biology, University of York, York YO10 5DD, United Kingdom;6. Faculty of Life Sciences and Manchester Interdisciplinary Biocentre, The University of Manchester, Manchester M1 7DN, United Kingdom;1. Department of Chemistry and Biochemistry, University of Denver, Denver, CO 80208, USA;2. Virus and Prion Research Unit, USDA-ARS-National Animal Disease Center, Ames, IA 50010, USA;3. Department of Pharmaceutical and Biomedical Sciences, University of Georgia, Athens, GA 30602, USA |
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| Abstract: | In many DNA viruses, genome packaging is initiated by the small subunit of the packaging terminase, which specifically binds to the packaging signal on viral DNA and directs assembly of the terminase holoenzyme. We have experimentally mapped the DNA-interacting region on Shigella virus Sf6 terminase small subunit gp1, which occupies extended surface areas encircling the gp1 octamer, indicating that DNA wraps around gp1 through extensive contacts. High‐resolution structures reveal large-scale motions of the gp1 DNA-binding domain mediated by the curved helix formed by residues 54–81 and an intermolecular salt bridge formed by residues Arg67 and Glu73, indicating remarkable structural plasticity underlying multivalent, pleomorphic gp1:DNA interactions. These results provide spatial restraints for protein:DNA interactions, which enable construction of a three-dimensional pseudo-atomic model for a DNA-packaging initiation complex assembled from the terminase small subunit and the packaging region on viral DNA. Our results suggest that gp1 functions as a DNA-spooling device, which may transform DNA into a specific architecture appropriate for interaction with and cleavage by the terminase large subunit prior to DNA translocation into viral procapsid. This may represent a common mechanism for the initiation step of DNA packaging in tailed double‐stranded DNA bacterial viruses. |
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