The human ciliopathy protein RSG1 links the CPLANE complex to transition zone architecture

Abstract Cilia are essential organelles, and variants in genes governing ciliary function result in ciliopathic diseases. The Ciliogenesis and PLANar polarity Effectors (CPLANE) protein complex is essential for ciliogenesis, and all but one subunit of the CPLANE complex have been implicated in human...

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Main Authors: Neftalí Vazquez, Chanjae Lee, Irene Valenzuela, Thao P. Phan, Camille Derderian, Marcelo Chávez, Nancie A. Mooney, Janos Demeter, Mohammad Ovais Aziz-Zanjani, Ivon Cusco, Marta Codina, Núria Martínez-Gil, Diana Valverde, Carlos Solarat, Ange-Line Buel, Cristel Thauvin-Robinet, Elisabeth Steichen, Isabel Filges, Pascal Joset, Julie De Geyter, Krishna Vaidyanathan, Tynan P. Gardner, Michinori Toriyama, Edward M. Marcotte, Kevin Drew, Elle C. Roberson, Peter K. Jackson, Jeremy F. Reiter, Eduardo F. Tizzano, John B. Wallingford
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-61005-8
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author Neftalí Vazquez
Chanjae Lee
Irene Valenzuela
Thao P. Phan
Camille Derderian
Marcelo Chávez
Nancie A. Mooney
Janos Demeter
Mohammad Ovais Aziz-Zanjani
Ivon Cusco
Marta Codina
Núria Martínez-Gil
Diana Valverde
Carlos Solarat
Ange-Line Buel
Cristel Thauvin-Robinet
Elisabeth Steichen
Isabel Filges
Pascal Joset
Julie De Geyter
Krishna Vaidyanathan
Tynan P. Gardner
Michinori Toriyama
Edward M. Marcotte
Kevin Drew
Elle C. Roberson
Peter K. Jackson
Jeremy F. Reiter
Eduardo F. Tizzano
John B. Wallingford
author_facet Neftalí Vazquez
Chanjae Lee
Irene Valenzuela
Thao P. Phan
Camille Derderian
Marcelo Chávez
Nancie A. Mooney
Janos Demeter
Mohammad Ovais Aziz-Zanjani
Ivon Cusco
Marta Codina
Núria Martínez-Gil
Diana Valverde
Carlos Solarat
Ange-Line Buel
Cristel Thauvin-Robinet
Elisabeth Steichen
Isabel Filges
Pascal Joset
Julie De Geyter
Krishna Vaidyanathan
Tynan P. Gardner
Michinori Toriyama
Edward M. Marcotte
Kevin Drew
Elle C. Roberson
Peter K. Jackson
Jeremy F. Reiter
Eduardo F. Tizzano
John B. Wallingford
author_sort Neftalí Vazquez
collection DOAJ
description Abstract Cilia are essential organelles, and variants in genes governing ciliary function result in ciliopathic diseases. The Ciliogenesis and PLANar polarity Effectors (CPLANE) protein complex is essential for ciliogenesis, and all but one subunit of the CPLANE complex have been implicated in human ciliopathy. Here, we identify three families in which variants in the remaining CPLANE subunit CPLANE2/RSG1 also cause ciliopathy. These patients display cleft palate, tongue lobulations and polydactyly, phenotypes characteristic of Oral-Facial-Digital Syndrome. We further show that these alleles disrupt two vital steps of ciliogenesis, basal body docking and recruitment of intraflagellar transport proteins. Moreover, APMS reveals that Rsg1 binds CPLANE and the transition zone protein Fam92 in a GTP-dependent manner. Finally, we show that CPLANE is generally required for normal transition zone architecture. Our work demonstrates that CPLANE2/RSG1 is a causative gene for human ciliopathy and also sheds new light on the mechanisms of ciliary transition zone assembly.
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spelling doaj-art-9a38d7d9b3174f34964d41218a0c5b5f2025-08-20T04:01:41ZengNature PortfolioNature Communications2041-17232025-07-0116111610.1038/s41467-025-61005-8The human ciliopathy protein RSG1 links the CPLANE complex to transition zone architectureNeftalí Vazquez0Chanjae Lee1Irene Valenzuela2Thao P. Phan3Camille Derderian4Marcelo Chávez5Nancie A. Mooney6Janos Demeter7Mohammad Ovais Aziz-Zanjani8Ivon Cusco9Marta Codina10Núria Martínez-Gil11Diana Valverde12Carlos Solarat13Ange-Line Buel14Cristel Thauvin-Robinet15Elisabeth Steichen16Isabel Filges17Pascal Joset18Julie De Geyter19Krishna Vaidyanathan20Tynan P. Gardner21Michinori Toriyama22Edward M. Marcotte23Kevin Drew24Elle C. Roberson25Peter K. Jackson26Jeremy F. Reiter27Eduardo F. Tizzano28John B. Wallingford29Department of Molecular Biosciences, University of Texas at AustinDepartment of Molecular Biosciences, University of Texas at AustinDepartment of Clinical and Molecular Genetics, Vall d´Hebron University Hospital. European Reference Network on Rare Congenital Malformations and Rare Intellectual Disability (ERN-ITHACA), Medicine Genetics Group, Vall d´Hebron Research InstituteDepartment of Biochemistry and Biophysics, Cardiovascular Research Institute, University of California, San FranciscoDepartment of Biochemistry and Biophysics, Cardiovascular Research Institute, University of California, San FranciscoBaxter Laboratory, Department of Microbiology & Immunology, Stanford University School of MedicineBaxter Laboratory, Department of Microbiology & Immunology, Stanford University School of MedicineBaxter Laboratory, Department of Microbiology & Immunology, Stanford University School of MedicineBaxter Laboratory, Department of Microbiology & Immunology, Stanford University School of MedicineDepartment of Clinical and Molecular Genetics, Vall d´Hebron University Hospital. European Reference Network on Rare Congenital Malformations and Rare Intellectual Disability (ERN-ITHACA), Medicine Genetics Group, Vall d´Hebron Research InstituteDepartment of Clinical and Molecular Genetics, Vall d´Hebron University Hospital. European Reference Network on Rare Congenital Malformations and Rare Intellectual Disability (ERN-ITHACA), Medicine Genetics Group, Vall d´Hebron Research InstituteDepartment of Clinical and Molecular Genetics, Vall d´Hebron University Hospital. European Reference Network on Rare Congenital Malformations and Rare Intellectual Disability (ERN-ITHACA), Medicine Genetics Group, Vall d´Hebron Research InstituteCINBIO, University of Vigo and Research Group on Rare Diseases and Pediatric Medicine, Health Research Institute Galicia Sur (IIS Galicia Sur), SERGASUVIGOCINBIO, University of Vigo and Research Group on Rare Diseases and Pediatric Medicine, Health Research Institute Galicia Sur (IIS Galicia Sur), SERGASUVIGOFunctional Unity of Innovative Diagnosis for Rare Diseases and Inserm UMR1231 team GAD, University of BurgundyFunctional Unity of Innovative Diagnosis for Rare Diseases and Inserm UMR1231 team GAD, University of BurgundyDepartment of Pediatrics, Medical School, University of InnsbruckMedical Genetics, Institute of Medical Genetics and Pathology and Department of Clinical Research, University Hospital BaselMedical Genetics, Institute of Medical Genetics and Pathology and Department of Clinical Research, University Hospital BaselMedical Genetics, Institute of Medical Genetics and Pathology and Department of Clinical Research, University Hospital BaselDepartment of Molecular Biosciences, University of Texas at AustinDepartment of Molecular Biosciences, University of Texas at AustinDepartment of Biomedical Sciences, School of Biological and Environmental Sciences, Kwansei Gakuin University, SandaDepartment of Molecular Biosciences, University of Texas at AustinDepartment of Biological Sciences, University of Illinois at ChicagoDevelopmental Biology and Pediatrics, CU Anschutz Medical CampusBaxter Laboratory, Department of Microbiology & Immunology, Stanford University School of MedicineDepartment of Biochemistry and Biophysics, Cardiovascular Research Institute, University of California, San FranciscoDepartment of Clinical and Molecular Genetics, Vall d´Hebron University Hospital. European Reference Network on Rare Congenital Malformations and Rare Intellectual Disability (ERN-ITHACA), Medicine Genetics Group, Vall d´Hebron Research InstituteDepartment of Molecular Biosciences, University of Texas at AustinAbstract Cilia are essential organelles, and variants in genes governing ciliary function result in ciliopathic diseases. The Ciliogenesis and PLANar polarity Effectors (CPLANE) protein complex is essential for ciliogenesis, and all but one subunit of the CPLANE complex have been implicated in human ciliopathy. Here, we identify three families in which variants in the remaining CPLANE subunit CPLANE2/RSG1 also cause ciliopathy. These patients display cleft palate, tongue lobulations and polydactyly, phenotypes characteristic of Oral-Facial-Digital Syndrome. We further show that these alleles disrupt two vital steps of ciliogenesis, basal body docking and recruitment of intraflagellar transport proteins. Moreover, APMS reveals that Rsg1 binds CPLANE and the transition zone protein Fam92 in a GTP-dependent manner. Finally, we show that CPLANE is generally required for normal transition zone architecture. Our work demonstrates that CPLANE2/RSG1 is a causative gene for human ciliopathy and also sheds new light on the mechanisms of ciliary transition zone assembly.https://doi.org/10.1038/s41467-025-61005-8
spellingShingle Neftalí Vazquez
Chanjae Lee
Irene Valenzuela
Thao P. Phan
Camille Derderian
Marcelo Chávez
Nancie A. Mooney
Janos Demeter
Mohammad Ovais Aziz-Zanjani
Ivon Cusco
Marta Codina
Núria Martínez-Gil
Diana Valverde
Carlos Solarat
Ange-Line Buel
Cristel Thauvin-Robinet
Elisabeth Steichen
Isabel Filges
Pascal Joset
Julie De Geyter
Krishna Vaidyanathan
Tynan P. Gardner
Michinori Toriyama
Edward M. Marcotte
Kevin Drew
Elle C. Roberson
Peter K. Jackson
Jeremy F. Reiter
Eduardo F. Tizzano
John B. Wallingford
The human ciliopathy protein RSG1 links the CPLANE complex to transition zone architecture
Nature Communications
title The human ciliopathy protein RSG1 links the CPLANE complex to transition zone architecture
title_full The human ciliopathy protein RSG1 links the CPLANE complex to transition zone architecture
title_fullStr The human ciliopathy protein RSG1 links the CPLANE complex to transition zone architecture
title_full_unstemmed The human ciliopathy protein RSG1 links the CPLANE complex to transition zone architecture
title_short The human ciliopathy protein RSG1 links the CPLANE complex to transition zone architecture
title_sort human ciliopathy protein rsg1 links the cplane complex to transition zone architecture
url https://doi.org/10.1038/s41467-025-61005-8
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