Systematic studies of all PIH proteins in zebrafish reveal their distinct roles in axonemal dynein assembly
Construction of motile cilia/flagella requires cytoplasmic preassembly of axonemal dyneins before transport into cilia. Axonemal dyneins have various subtypes, but the roles of each dynein subtype and their assembly processes remain elusive in vertebrates. The PIH protein family, consisting of four...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2018-05-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/36979 |
| _version_ | 1811181116269264896 |
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| author | Hiroshi Yamaguchi Toshiyuki Oda Masahide Kikkawa Hiroyuki Takeda |
| author_facet | Hiroshi Yamaguchi Toshiyuki Oda Masahide Kikkawa Hiroyuki Takeda |
| author_sort | Hiroshi Yamaguchi |
| collection | DOAJ |
| description | Construction of motile cilia/flagella requires cytoplasmic preassembly of axonemal dyneins before transport into cilia. Axonemal dyneins have various subtypes, but the roles of each dynein subtype and their assembly processes remain elusive in vertebrates. The PIH protein family, consisting of four members, has been implicated in the assembly of different dynein subtypes, although evidence for this idea is sparse. Here, we established zebrafish mutants of all four PIH-protein genes: pih1d1, pih1d2, ktu, and twister, and analyzed the structures of axonemal dyneins in mutant spermatozoa by cryo-electron tomography. Mutations caused the loss of specific dynein subtypes, which was correlated with abnormal sperm motility. We also found organ-specific compositions of dynein subtypes, which could explain the severe motility defects of mutant Kupffer’s vesicle cilia. Our data demonstrate that all vertebrate PIH proteins are differently required for cilia/flagella motions and the assembly of axonemal dyneins, assigning specific dynein subtypes to each PIH protein. |
| first_indexed | 2024-04-11T09:14:12Z |
| format | Article |
| id | doaj.art-b3dd1158a1b2473aa5e78120f4a21481 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:14:12Z |
| publishDate | 2018-05-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-b3dd1158a1b2473aa5e78120f4a214812022-12-22T04:32:25ZengeLife Sciences Publications LtdeLife2050-084X2018-05-01710.7554/eLife.36979Systematic studies of all PIH proteins in zebrafish reveal their distinct roles in axonemal dynein assemblyHiroshi Yamaguchi0https://orcid.org/0000-0002-8722-129XToshiyuki Oda1https://orcid.org/0000-0001-8090-2159Masahide Kikkawa2https://orcid.org/0000-0001-7656-8194Hiroyuki Takeda3https://orcid.org/0000-0002-7932-6358Department of Cell Biology and Anatomy, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan; Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, JapanDepartment of Anatomy and Structural Biology, Graduate School of Medicine, University of Yamanashi, Yamanashi, JapanDepartment of Cell Biology and Anatomy, Graduate School of Medicine, The University of Tokyo, Tokyo, JapanDepartment of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, JapanConstruction of motile cilia/flagella requires cytoplasmic preassembly of axonemal dyneins before transport into cilia. Axonemal dyneins have various subtypes, but the roles of each dynein subtype and their assembly processes remain elusive in vertebrates. The PIH protein family, consisting of four members, has been implicated in the assembly of different dynein subtypes, although evidence for this idea is sparse. Here, we established zebrafish mutants of all four PIH-protein genes: pih1d1, pih1d2, ktu, and twister, and analyzed the structures of axonemal dyneins in mutant spermatozoa by cryo-electron tomography. Mutations caused the loss of specific dynein subtypes, which was correlated with abnormal sperm motility. We also found organ-specific compositions of dynein subtypes, which could explain the severe motility defects of mutant Kupffer’s vesicle cilia. Our data demonstrate that all vertebrate PIH proteins are differently required for cilia/flagella motions and the assembly of axonemal dyneins, assigning specific dynein subtypes to each PIH protein.https://elifesciences.org/articles/36979ciliaaxonemal dyneincryo-electron tomographyspermzebrafishPIH protein |
| spellingShingle | Hiroshi Yamaguchi Toshiyuki Oda Masahide Kikkawa Hiroyuki Takeda Systematic studies of all PIH proteins in zebrafish reveal their distinct roles in axonemal dynein assembly eLife cilia axonemal dynein cryo-electron tomography sperm zebrafish PIH protein |
| title | Systematic studies of all PIH proteins in zebrafish reveal their distinct roles in axonemal dynein assembly |
| title_full | Systematic studies of all PIH proteins in zebrafish reveal their distinct roles in axonemal dynein assembly |
| title_fullStr | Systematic studies of all PIH proteins in zebrafish reveal their distinct roles in axonemal dynein assembly |
| title_full_unstemmed | Systematic studies of all PIH proteins in zebrafish reveal their distinct roles in axonemal dynein assembly |
| title_short | Systematic studies of all PIH proteins in zebrafish reveal their distinct roles in axonemal dynein assembly |
| title_sort | systematic studies of all pih proteins in zebrafish reveal their distinct roles in axonemal dynein assembly |
| topic | cilia axonemal dynein cryo-electron tomography sperm zebrafish PIH protein |
| url | https://elifesciences.org/articles/36979 |
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