C. elegans PPEF-type phosphatase (Retinal degeneration C ortholog) functions in diverse classes of cilia to regulate nematode behaviors
Abstract Primary (non-motile) cilia represent structurally and functionally diverse organelles whose roles as specialized cellular antenna are central to animal cell signaling pathways, sensory physiology and development. An ever-growing number of ciliary proteins, including those found in vertebrat...
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Nature Portfolio
2024-11-01
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| Online Access: | https://doi.org/10.1038/s41598-024-79057-z |
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| author | Marine Barbelanne Yun Lu Keerthana Kumar Xinxing Zhang Chunmei Li Kwangjin Park Adam Warner X. Z. Shawn Xu Shai Shaham Michel R. Leroux |
| author_facet | Marine Barbelanne Yun Lu Keerthana Kumar Xinxing Zhang Chunmei Li Kwangjin Park Adam Warner X. Z. Shawn Xu Shai Shaham Michel R. Leroux |
| author_sort | Marine Barbelanne |
| collection | DOAJ |
| description | Abstract Primary (non-motile) cilia represent structurally and functionally diverse organelles whose roles as specialized cellular antenna are central to animal cell signaling pathways, sensory physiology and development. An ever-growing number of ciliary proteins, including those found in vertebrate photoreceptors, have been uncovered and linked to human disorders termed ciliopathies. Here, we demonstrate that an evolutionarily-conserved PPEF-family serine-threonine phosphatase, not functionally linked to cilia in any organism but associated with rhabdomeric (non-ciliary) photoreceptor degeneration in the Drosophila rdgC (retinal degeneration C) mutant, is a bona fide ciliary protein in C. elegans. The nematode protein, PEF-1, depends on transition zone proteins, which make up a ‘ciliary gate’ in the proximal-most region of the cilium, for its compartmentalization within cilia. Animals lacking PEF-1 protein function display structural defects to several types of cilia, including potential degeneration of microtubules. They also exhibit anomalies to cilium-dependent behaviors, including impaired responses to chemical, temperature, light, and noxious CO2 stimuli. Lastly, we demonstrate that PEF-1 function depends on conserved myristoylation and palmitoylation signals. Collectively, our findings broaden the role of PPEF proteins to include cilia, and suggest that the poorly-characterized mammalian PPEF1 and PPEF2 orthologs may also have ciliary functions and thus represent ciliopathy candidates. |
| format | Article |
| id | doaj-art-8b8b4a9133a1420bb3752bc5f2717d66 |
| institution | Kabale University |
| issn | 2045-2322 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | Nature Portfolio |
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| series | Scientific Reports |
| spelling | doaj-art-8b8b4a9133a1420bb3752bc5f2717d662024-11-17T12:26:26ZengNature PortfolioScientific Reports2045-23222024-11-0114111810.1038/s41598-024-79057-zC. elegans PPEF-type phosphatase (Retinal degeneration C ortholog) functions in diverse classes of cilia to regulate nematode behaviorsMarine Barbelanne0Yun Lu1Keerthana Kumar2Xinxing Zhang3Chunmei Li4Kwangjin Park5Adam Warner6X. Z. Shawn Xu7Shai Shaham8Michel R. Leroux9Department of Molecular Biology and Biochemistry, Simon Fraser UniversityLaboratory of Developmental Genetics, The Rockefeller UniversityDepartment of Molecular Biology and Biochemistry, Simon Fraser UniversityLife Sciences Institute, Department of Molecular and Integrative Physiology, University of MichiganDepartment of Molecular Biology and Biochemistry, Simon Fraser UniversityDepartment of Molecular Biology and Biochemistry, Simon Fraser UniversityDepartment of Molecular Biology and Biochemistry, Simon Fraser UniversityLife Sciences Institute, Department of Molecular and Integrative Physiology, University of MichiganLaboratory of Developmental Genetics, The Rockefeller UniversityDepartment of Molecular Biology and Biochemistry, Simon Fraser UniversityAbstract Primary (non-motile) cilia represent structurally and functionally diverse organelles whose roles as specialized cellular antenna are central to animal cell signaling pathways, sensory physiology and development. An ever-growing number of ciliary proteins, including those found in vertebrate photoreceptors, have been uncovered and linked to human disorders termed ciliopathies. Here, we demonstrate that an evolutionarily-conserved PPEF-family serine-threonine phosphatase, not functionally linked to cilia in any organism but associated with rhabdomeric (non-ciliary) photoreceptor degeneration in the Drosophila rdgC (retinal degeneration C) mutant, is a bona fide ciliary protein in C. elegans. The nematode protein, PEF-1, depends on transition zone proteins, which make up a ‘ciliary gate’ in the proximal-most region of the cilium, for its compartmentalization within cilia. Animals lacking PEF-1 protein function display structural defects to several types of cilia, including potential degeneration of microtubules. They also exhibit anomalies to cilium-dependent behaviors, including impaired responses to chemical, temperature, light, and noxious CO2 stimuli. Lastly, we demonstrate that PEF-1 function depends on conserved myristoylation and palmitoylation signals. Collectively, our findings broaden the role of PPEF proteins to include cilia, and suggest that the poorly-characterized mammalian PPEF1 and PPEF2 orthologs may also have ciliary functions and thus represent ciliopathy candidates.https://doi.org/10.1038/s41598-024-79057-zCiliaPPEFPhosphatasePEF-1BehaviorChemosensation |
| spellingShingle | Marine Barbelanne Yun Lu Keerthana Kumar Xinxing Zhang Chunmei Li Kwangjin Park Adam Warner X. Z. Shawn Xu Shai Shaham Michel R. Leroux C. elegans PPEF-type phosphatase (Retinal degeneration C ortholog) functions in diverse classes of cilia to regulate nematode behaviors Scientific Reports Cilia PPEF Phosphatase PEF-1 Behavior Chemosensation |
| title | C. elegans PPEF-type phosphatase (Retinal degeneration C ortholog) functions in diverse classes of cilia to regulate nematode behaviors |
| title_full | C. elegans PPEF-type phosphatase (Retinal degeneration C ortholog) functions in diverse classes of cilia to regulate nematode behaviors |
| title_fullStr | C. elegans PPEF-type phosphatase (Retinal degeneration C ortholog) functions in diverse classes of cilia to regulate nematode behaviors |
| title_full_unstemmed | C. elegans PPEF-type phosphatase (Retinal degeneration C ortholog) functions in diverse classes of cilia to regulate nematode behaviors |
| title_short | C. elegans PPEF-type phosphatase (Retinal degeneration C ortholog) functions in diverse classes of cilia to regulate nematode behaviors |
| title_sort | c elegans ppef type phosphatase retinal degeneration c ortholog functions in diverse classes of cilia to regulate nematode behaviors |
| topic | Cilia PPEF Phosphatase PEF-1 Behavior Chemosensation |
| url | https://doi.org/10.1038/s41598-024-79057-z |
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