Architectural basis for cylindrical self-assembly governing Plk4-mediated centriole duplication in human cells
Abstract Proper organization of intracellular assemblies is fundamental for efficient promotion of biochemical processes and optimal assembly functionality. Although advances in imaging technologies have shed light on how the centrosome is organized, how its constituent proteins are coherently archi...
| Main Authors: | , , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-07-01
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| Series: | Communications Biology |
| Online Access: | https://doi.org/10.1038/s42003-023-05067-8 |
| _version_ | 1797769342852530176 |
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| author | Jong Il Ahn Liang Zhang Harsha Ravishankar Lixin Fan Klara Kirsch Yan Zeng Lingjun Meng Jung-Eun Park Hye-Yeoung Yun Rodolfo Ghirlando Buyong Ma David Ball Bonsu Ku Ruth Nussinov Jeremy D. Schmit William F. Heinz Seung Jun Kim Tatiana Karpova Yun-Xing Wang Kyung S. Lee |
| author_facet | Jong Il Ahn Liang Zhang Harsha Ravishankar Lixin Fan Klara Kirsch Yan Zeng Lingjun Meng Jung-Eun Park Hye-Yeoung Yun Rodolfo Ghirlando Buyong Ma David Ball Bonsu Ku Ruth Nussinov Jeremy D. Schmit William F. Heinz Seung Jun Kim Tatiana Karpova Yun-Xing Wang Kyung S. Lee |
| author_sort | Jong Il Ahn |
| collection | DOAJ |
| description | Abstract Proper organization of intracellular assemblies is fundamental for efficient promotion of biochemical processes and optimal assembly functionality. Although advances in imaging technologies have shed light on how the centrosome is organized, how its constituent proteins are coherently architected to elicit downstream events remains poorly understood. Using multidisciplinary approaches, we showed that two long coiled-coil proteins, Cep63 and Cep152, form a heterotetrameric building block that undergoes a stepwise formation into higher molecular weight complexes, ultimately generating a cylindrical architecture around a centriole. Mutants defective in Cep63•Cep152 heterotetramer formation displayed crippled pericentriolar Cep152 organization, polo-like kinase 4 (Plk4) relocalization to the procentriole assembly site, and Plk4-mediated centriole duplication. Given that the organization of pericentriolar materials (PCM) is evolutionarily conserved, this work could serve as a model for investigating the structure and function of PCM in other species, while offering a new direction in probing the organizational defects of PCM-related human diseases. |
| first_indexed | 2024-03-12T21:07:39Z |
| format | Article |
| id | doaj.art-06aa6e8547484fe7b186bef73965f8dc |
| institution | Directory Open Access Journal |
| issn | 2399-3642 |
| language | English |
| last_indexed | 2024-03-12T21:07:39Z |
| publishDate | 2023-07-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Communications Biology |
| spelling | doaj.art-06aa6e8547484fe7b186bef73965f8dc2023-07-30T11:22:31ZengNature PortfolioCommunications Biology2399-36422023-07-016112010.1038/s42003-023-05067-8Architectural basis for cylindrical self-assembly governing Plk4-mediated centriole duplication in human cellsJong Il Ahn0Liang Zhang1Harsha Ravishankar2Lixin Fan3Klara Kirsch4Yan Zeng5Lingjun Meng6Jung-Eun Park7Hye-Yeoung Yun8Rodolfo Ghirlando9Buyong Ma10David Ball11Bonsu Ku12Ruth Nussinov13Jeremy D. Schmit14William F. Heinz15Seung Jun Kim16Tatiana Karpova17Yun-Xing Wang18Kyung S. Lee19Cancer Innovation Laboratory, Center for Cancer Research, National Cancer Institute, National Institutes of HealthCancer Innovation Laboratory, Center for Cancer Research, National Cancer Institute, National Institutes of HealthCancer Innovation Laboratory, Center for Cancer Research, National Cancer Institute, National Institutes of HealthBasic Science Program, Frederick National Laboratory for Cancer Research, Small-Angle X-ray Scattering Core Facility, National Cancer Institute, National Institutes of HealthCancer Innovation Laboratory, Center for Cancer Research, National Cancer Institute, National Institutes of HealthCancer Innovation Laboratory, Center for Cancer Research, National Cancer Institute, National Institutes of HealthCancer Innovation Laboratory, Center for Cancer Research, National Cancer Institute, National Institutes of HealthCancer Innovation Laboratory, Center for Cancer Research, National Cancer Institute, National Institutes of HealthDisease Target Structure Research Center, Korea Research Institute of Bioscience and BiotechnologyLaboratory of Molecular Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of HealthBasic Science Program, Leidos Biomedical Research, Inc., Cancer and Inflammation Program, National Cancer InstituteLaboratory of Receptor Biology and Gene Expression, Optical Microscopy Core, National Cancer Institute, National Institutes of HealthDisease Target Structure Research Center, Korea Research Institute of Bioscience and BiotechnologyBasic Science Program, Leidos Biomedical Research, Inc., Cancer and Inflammation Program, National Cancer InstituteDepartment of Physics, Kansas State UniversityOptical Microscopy and Analysis Laboratory, Cancer Research Technology Program, Frederick National Laboratory for Cancer ResearchDisease Target Structure Research Center, Korea Research Institute of Bioscience and BiotechnologyLaboratory of Receptor Biology and Gene Expression, Optical Microscopy Core, National Cancer Institute, National Institutes of HealthProtein-Nucleic Acid Interaction Section, Center for Structural Biology, National Cancer Institute, National Institutes of HealthCancer Innovation Laboratory, Center for Cancer Research, National Cancer Institute, National Institutes of HealthAbstract Proper organization of intracellular assemblies is fundamental for efficient promotion of biochemical processes and optimal assembly functionality. Although advances in imaging technologies have shed light on how the centrosome is organized, how its constituent proteins are coherently architected to elicit downstream events remains poorly understood. Using multidisciplinary approaches, we showed that two long coiled-coil proteins, Cep63 and Cep152, form a heterotetrameric building block that undergoes a stepwise formation into higher molecular weight complexes, ultimately generating a cylindrical architecture around a centriole. Mutants defective in Cep63•Cep152 heterotetramer formation displayed crippled pericentriolar Cep152 organization, polo-like kinase 4 (Plk4) relocalization to the procentriole assembly site, and Plk4-mediated centriole duplication. Given that the organization of pericentriolar materials (PCM) is evolutionarily conserved, this work could serve as a model for investigating the structure and function of PCM in other species, while offering a new direction in probing the organizational defects of PCM-related human diseases.https://doi.org/10.1038/s42003-023-05067-8 |
| spellingShingle | Jong Il Ahn Liang Zhang Harsha Ravishankar Lixin Fan Klara Kirsch Yan Zeng Lingjun Meng Jung-Eun Park Hye-Yeoung Yun Rodolfo Ghirlando Buyong Ma David Ball Bonsu Ku Ruth Nussinov Jeremy D. Schmit William F. Heinz Seung Jun Kim Tatiana Karpova Yun-Xing Wang Kyung S. Lee Architectural basis for cylindrical self-assembly governing Plk4-mediated centriole duplication in human cells Communications Biology |
| title | Architectural basis for cylindrical self-assembly governing Plk4-mediated centriole duplication in human cells |
| title_full | Architectural basis for cylindrical self-assembly governing Plk4-mediated centriole duplication in human cells |
| title_fullStr | Architectural basis for cylindrical self-assembly governing Plk4-mediated centriole duplication in human cells |
| title_full_unstemmed | Architectural basis for cylindrical self-assembly governing Plk4-mediated centriole duplication in human cells |
| title_short | Architectural basis for cylindrical self-assembly governing Plk4-mediated centriole duplication in human cells |
| title_sort | architectural basis for cylindrical self assembly governing plk4 mediated centriole duplication in human cells |
| url | https://doi.org/10.1038/s42003-023-05067-8 |
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