Heme-binding protein CYB5D1 is a radial spoke component required for coordinated ciliary beating
Coordinated beating is crucial for the function of multiple cilia. However, the molecular mechanism is poorly understood. Here, we characterize a conserved ciliary protein CYB5D1 with a heme-binding domain and a cordon-bleu ubiquitin-like domain. Mutation or knockdown of Cyb5d1 in zebrafish impaired...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2021-04, Vol.118 (17), p.1-12 |
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| creator | Zhao, Lijuan Xie, Haibo Kang, Yunsi Lin, Yiwen Liu, Gai Sakato-Antoku, Miho Patel-King, Ramila S. Wang, Bing Wan, Cuihong King, Stephen M. Zhao, Chengtian Huang, Kaiyao |
| description | Coordinated beating is crucial for the function of multiple cilia. However, the molecular mechanism is poorly understood. Here, we characterize a conserved ciliary protein CYB5D1 with a heme-binding domain and a cordon-bleu ubiquitin-like domain. Mutation or knockdown of Cyb5d1 in zebrafish impaired coordinated ciliary beating in the otic vesicle and olfactory epithelium. Similarly, the two flagella of an insertional mutant of the CYB5D1 ortholog in Chlamydomonas (Crcyb5d1) showed an uncoordinated pattern due to a defect in the cis-flagellum. Biochemical analyses revealed that CrCYB5D1 is a radial spoke stalk protein that binds heme only under oxidizing conditions. Lack of CrCYB5D1 resulted in a reductive shift in flagellar redox state and slowing down of the phototactic response. Treatment of Crcyb5d1 with oxidants restored coordinated flagellar beating. Taken together, these data suggest that CrCYB5D1 may integrate environmental and intraciliary signals and regulate the redox state of cilia, which is crucial for the coordinated beating of multiple cilia. |
| doi_str_mv | 10.1073/pnas.2015689118 |
| format | Article |
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However, the molecular mechanism is poorly understood. Here, we characterize a conserved ciliary protein CYB5D1 with a heme-binding domain and a cordon-bleu ubiquitin-like domain. Mutation or knockdown of Cyb5d1 in zebrafish impaired coordinated ciliary beating in the otic vesicle and olfactory epithelium. Similarly, the two flagella of an insertional mutant of the CYB5D1 ortholog in Chlamydomonas (Crcyb5d1) showed an uncoordinated pattern due to a defect in the cis-flagellum. Biochemical analyses revealed that CrCYB5D1 is a radial spoke stalk protein that binds heme only under oxidizing conditions. Lack of CrCYB5D1 resulted in a reductive shift in flagellar redox state and slowing down of the phototactic response. Treatment of Crcyb5d1 with oxidants restored coordinated flagellar beating. Taken together, these data suggest that CrCYB5D1 may integrate environmental and intraciliary signals and regulate the redox state of cilia, which is crucial for the coordinated beating of multiple cilia.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.2015689118</identifier><identifier>PMID: 33875586</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Biological Sciences ; Cilia ; Cobl protein ; Domains ; Environmental regulations ; Flagella ; Heme ; Mutation ; Olfactory epithelium ; Oxidants ; Oxidation ; Oxidizing agents ; Proteins ; Redox properties ; Ubiquitin ; Zebrafish</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2021-04, Vol.118 (17), p.1-12</ispartof><rights>Copyright National Academy of Sciences Apr 27, 2021</rights><rights>2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c509t-1fd5b4f4203fe729e5481fa16a8d602547e3e0561922fc8979cd99ab6a19eac33</citedby><cites>FETCH-LOGICAL-c509t-1fd5b4f4203fe729e5481fa16a8d602547e3e0561922fc8979cd99ab6a19eac33</cites><orcidid>0000-0001-8669-1065 ; 0000-0003-1236-914X ; 0000-0002-5884-5140 ; 0000-0002-6802-133X ; 0000-0002-8303-194X ; 0000-0002-6028-3239 ; 0000-0002-5484-5530 ; 0000-0003-3050-4712</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/27040203$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/27040203$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33875586$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhao, Lijuan</creatorcontrib><creatorcontrib>Xie, Haibo</creatorcontrib><creatorcontrib>Kang, Yunsi</creatorcontrib><creatorcontrib>Lin, Yiwen</creatorcontrib><creatorcontrib>Liu, Gai</creatorcontrib><creatorcontrib>Sakato-Antoku, Miho</creatorcontrib><creatorcontrib>Patel-King, Ramila S.</creatorcontrib><creatorcontrib>Wang, Bing</creatorcontrib><creatorcontrib>Wan, Cuihong</creatorcontrib><creatorcontrib>King, Stephen M.</creatorcontrib><creatorcontrib>Zhao, Chengtian</creatorcontrib><creatorcontrib>Huang, Kaiyao</creatorcontrib><title>Heme-binding protein CYB5D1 is a radial spoke component required for coordinated ciliary beating</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Coordinated beating is crucial for the function of multiple cilia. However, the molecular mechanism is poorly understood. Here, we characterize a conserved ciliary protein CYB5D1 with a heme-binding domain and a cordon-bleu ubiquitin-like domain. Mutation or knockdown of Cyb5d1 in zebrafish impaired coordinated ciliary beating in the otic vesicle and olfactory epithelium. Similarly, the two flagella of an insertional mutant of the CYB5D1 ortholog in Chlamydomonas (Crcyb5d1) showed an uncoordinated pattern due to a defect in the cis-flagellum. Biochemical analyses revealed that CrCYB5D1 is a radial spoke stalk protein that binds heme only under oxidizing conditions. Lack of CrCYB5D1 resulted in a reductive shift in flagellar redox state and slowing down of the phototactic response. Treatment of Crcyb5d1 with oxidants restored coordinated flagellar beating. 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However, the molecular mechanism is poorly understood. Here, we characterize a conserved ciliary protein CYB5D1 with a heme-binding domain and a cordon-bleu ubiquitin-like domain. Mutation or knockdown of Cyb5d1 in zebrafish impaired coordinated ciliary beating in the otic vesicle and olfactory epithelium. Similarly, the two flagella of an insertional mutant of the CYB5D1 ortholog in Chlamydomonas (Crcyb5d1) showed an uncoordinated pattern due to a defect in the cis-flagellum. Biochemical analyses revealed that CrCYB5D1 is a radial spoke stalk protein that binds heme only under oxidizing conditions. Lack of CrCYB5D1 resulted in a reductive shift in flagellar redox state and slowing down of the phototactic response. Treatment of Crcyb5d1 with oxidants restored coordinated flagellar beating. 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| subjects | Biological Sciences Cilia Cobl protein Domains Environmental regulations Flagella Heme Mutation Olfactory epithelium Oxidants Oxidation Oxidizing agents Proteins Redox properties Ubiquitin Zebrafish |
| title | Heme-binding protein CYB5D1 is a radial spoke component required for coordinated ciliary beating |
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