Assembly and Capsid Expansion Mechanism of Bacteriophage P22 Revealed by High-Resolution Cryo-EM Structures
The formation of many double-stranded DNA viruses, such as herpesviruses and bacteriophages, begins with the scaffolding-protein-mediated assembly of the procapsid. Subsequently, the procapsid undergoes extensive structural rearrangement and expansion to become the mature capsid. Bacteriophage P22 i...
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| Format: | Article |
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MDPI AG
2023-01-01
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| Series: | Viruses |
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| Online Access: | https://www.mdpi.com/1999-4915/15/2/355 |
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| author | Hao Xiao Junquan Zhou Fan Yang Zheng Liu Jingdong Song Wenyuan Chen Hongrong Liu Lingpeng Cheng |
| author_facet | Hao Xiao Junquan Zhou Fan Yang Zheng Liu Jingdong Song Wenyuan Chen Hongrong Liu Lingpeng Cheng |
| author_sort | Hao Xiao |
| collection | DOAJ |
| description | The formation of many double-stranded DNA viruses, such as herpesviruses and bacteriophages, begins with the scaffolding-protein-mediated assembly of the procapsid. Subsequently, the procapsid undergoes extensive structural rearrangement and expansion to become the mature capsid. Bacteriophage P22 is an established model system used to study virus maturation. Here, we report the cryo-electron microscopy structures of procapsid, empty procapsid, empty mature capsid, and mature capsid of phage P22 at resolutions of 2.6 Å, 3.9 Å, 2.8 Å, and 3.0 Å, respectively. The structure of the procapsid allowed us to build an accurate model of the coat protein gp5 and the C-terminal region of the scaffolding protein gp8. In addition, interactions among the gp5 subunits responsible for procapsid assembly and stabilization were identified. Two C-terminal α-helices of gp8 were observed to interact with the coat protein in the procapsid. The amino acid interactions between gp5 and gp8 in the procapsid were consistent with the results of previous biochemical studies involving mutant proteins. Our structures reveal hydrogen bonds and salt bridges between the gp5 subunits in the procapsid and the conformational changes of the gp5 domains involved in the closure of the local sixfold opening and a thinner capsid shell during capsid maturation. |
| first_indexed | 2024-03-11T08:01:16Z |
| format | Article |
| id | doaj.art-f4b9b4c1ef2142239e0765bd158b7d5e |
| institution | Directory Open Access Journal |
| issn | 1999-4915 |
| language | English |
| last_indexed | 2024-03-11T08:01:16Z |
| publishDate | 2023-01-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Viruses |
| spelling | doaj.art-f4b9b4c1ef2142239e0765bd158b7d5e2023-11-16T23:47:53ZengMDPI AGViruses1999-49152023-01-0115235510.3390/v15020355Assembly and Capsid Expansion Mechanism of Bacteriophage P22 Revealed by High-Resolution Cryo-EM StructuresHao Xiao0Junquan Zhou1Fan Yang2Zheng Liu3Jingdong Song4Wenyuan Chen5Hongrong Liu6Lingpeng Cheng7Institute of Interdisciplinary Studies, Key Laboratory for Matter Microstructure and Function of Hunan Province, Key Laboratory of Low-dimensional Quantum Structures and Quantum Control, Hunan Normal University, Changsha 410082, ChinaInstitute of Interdisciplinary Studies, Key Laboratory for Matter Microstructure and Function of Hunan Province, Key Laboratory of Low-dimensional Quantum Structures and Quantum Control, Hunan Normal University, Changsha 410082, ChinaInstitute of Interdisciplinary Studies, Key Laboratory for Matter Microstructure and Function of Hunan Province, Key Laboratory of Low-dimensional Quantum Structures and Quantum Control, Hunan Normal University, Changsha 410082, ChinaKobilka Institute of Innovative Drug Discovery, School of Medicine, Chinese University of Hong Kong, Shenzhen 518172, ChinaState Key Laboratory of Infectious Disease Prevention and Control, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 100052, ChinaInstitute of Interdisciplinary Studies, Key Laboratory for Matter Microstructure and Function of Hunan Province, Key Laboratory of Low-dimensional Quantum Structures and Quantum Control, Hunan Normal University, Changsha 410082, ChinaInstitute of Interdisciplinary Studies, Key Laboratory for Matter Microstructure and Function of Hunan Province, Key Laboratory of Low-dimensional Quantum Structures and Quantum Control, Hunan Normal University, Changsha 410082, ChinaInstitute of Interdisciplinary Studies, Key Laboratory for Matter Microstructure and Function of Hunan Province, Key Laboratory of Low-dimensional Quantum Structures and Quantum Control, Hunan Normal University, Changsha 410082, ChinaThe formation of many double-stranded DNA viruses, such as herpesviruses and bacteriophages, begins with the scaffolding-protein-mediated assembly of the procapsid. Subsequently, the procapsid undergoes extensive structural rearrangement and expansion to become the mature capsid. Bacteriophage P22 is an established model system used to study virus maturation. Here, we report the cryo-electron microscopy structures of procapsid, empty procapsid, empty mature capsid, and mature capsid of phage P22 at resolutions of 2.6 Å, 3.9 Å, 2.8 Å, and 3.0 Å, respectively. The structure of the procapsid allowed us to build an accurate model of the coat protein gp5 and the C-terminal region of the scaffolding protein gp8. In addition, interactions among the gp5 subunits responsible for procapsid assembly and stabilization were identified. Two C-terminal α-helices of gp8 were observed to interact with the coat protein in the procapsid. The amino acid interactions between gp5 and gp8 in the procapsid were consistent with the results of previous biochemical studies involving mutant proteins. Our structures reveal hydrogen bonds and salt bridges between the gp5 subunits in the procapsid and the conformational changes of the gp5 domains involved in the closure of the local sixfold opening and a thinner capsid shell during capsid maturation.https://www.mdpi.com/1999-4915/15/2/355bacteriophage P22virus assemblyscaffolding proteincapsid expansioncryo-EM |
| spellingShingle | Hao Xiao Junquan Zhou Fan Yang Zheng Liu Jingdong Song Wenyuan Chen Hongrong Liu Lingpeng Cheng Assembly and Capsid Expansion Mechanism of Bacteriophage P22 Revealed by High-Resolution Cryo-EM Structures Viruses bacteriophage P22 virus assembly scaffolding protein capsid expansion cryo-EM |
| title | Assembly and Capsid Expansion Mechanism of Bacteriophage P22 Revealed by High-Resolution Cryo-EM Structures |
| title_full | Assembly and Capsid Expansion Mechanism of Bacteriophage P22 Revealed by High-Resolution Cryo-EM Structures |
| title_fullStr | Assembly and Capsid Expansion Mechanism of Bacteriophage P22 Revealed by High-Resolution Cryo-EM Structures |
| title_full_unstemmed | Assembly and Capsid Expansion Mechanism of Bacteriophage P22 Revealed by High-Resolution Cryo-EM Structures |
| title_short | Assembly and Capsid Expansion Mechanism of Bacteriophage P22 Revealed by High-Resolution Cryo-EM Structures |
| title_sort | assembly and capsid expansion mechanism of bacteriophage p22 revealed by high resolution cryo em structures |
| topic | bacteriophage P22 virus assembly scaffolding protein capsid expansion cryo-EM |
| url | https://www.mdpi.com/1999-4915/15/2/355 |
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