Cleavage of the Meckel-Gruber syndrome protein TMEM67 by ADAMTS9 uncouples Wnt signaling and ciliogenesis

Abstract TMEM67 mutations cause Meckel-Gruber syndrome and other related ciliopathies. TMEM67 is involved in both ciliary transition zone assembly, and non-canonical Wnt signaling mediated by its extracellular domain. How TMEM67 performs these two separate functions is not known. We identify a cleav...

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Main Authors: Manu Ahmed, Sydney Fischer, Karyn L. Robert, Karen I. Lange, Michael W. Stuck, Sunayna Best, Colin A. Johnson, Gregory J. Pazour, Oliver E. Blacque, Sumeda Nandadasa
Format: Article
Language:English
Published: Nature Portfolio 2025-05-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-60294-3
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author Manu Ahmed
Sydney Fischer
Karyn L. Robert
Karen I. Lange
Michael W. Stuck
Sunayna Best
Colin A. Johnson
Gregory J. Pazour
Oliver E. Blacque
Sumeda Nandadasa
author_facet Manu Ahmed
Sydney Fischer
Karyn L. Robert
Karen I. Lange
Michael W. Stuck
Sunayna Best
Colin A. Johnson
Gregory J. Pazour
Oliver E. Blacque
Sumeda Nandadasa
author_sort Manu Ahmed
collection DOAJ
description Abstract TMEM67 mutations cause Meckel-Gruber syndrome and other related ciliopathies. TMEM67 is involved in both ciliary transition zone assembly, and non-canonical Wnt signaling mediated by its extracellular domain. How TMEM67 performs these two separate functions is not known. We identify a cleavage motif in the extracellular domain of TMEM67 cleaved by the extracellular matrix metalloproteinase ADAMTS9. This cleavage regulates the abundance of two functional forms: a C-terminal portion which localizes to the ciliary transition zone regulating ciliogenesis, and a non-cleaved form which regulates Wnt signaling. By characterizing three TMEM67 ciliopathy patient variants within the cleavage motif utilizing mammalian cell culture and C. elegans, we show the cleavage motif is essential for cilia structure and function, highlighting its clinical significance. We generated a non-cleavable TMEM67 mouse model which develop severe ciliopathies phenocopying Tmem67 -/- mice, but in contrast, transduces normal Wnt signaling, substantiating the existence of two functional forms of TMEM67.
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series Nature Communications
spelling doaj-art-259cf775655d408ca4ad1a788ea75c2c2025-08-20T03:16:47ZengNature PortfolioNature Communications2041-17232025-05-0116112010.1038/s41467-025-60294-3Cleavage of the Meckel-Gruber syndrome protein TMEM67 by ADAMTS9 uncouples Wnt signaling and ciliogenesisManu Ahmed0Sydney Fischer1Karyn L. Robert2Karen I. Lange3Michael W. Stuck4Sunayna Best5Colin A. Johnson6Gregory J. Pazour7Oliver E. Blacque8Sumeda Nandadasa9Department of Pediatrics, University of Massachusetts Chan Medical SchoolDepartment of Pediatrics, University of Massachusetts Chan Medical SchoolDepartment of Pediatrics, University of Massachusetts Chan Medical SchoolSchool of Biomolecular & Biomedical Science, University College DublinProgram in Molecular Medicine, University of Massachusetts Chan Medical SchoolDivision of Molecular Medicine, Leeds Institute of Medical Research, The University of LeedsDivision of Molecular Medicine, Leeds Institute of Medical Research, The University of LeedsProgram in Molecular Medicine, University of Massachusetts Chan Medical SchoolSchool of Biomolecular & Biomedical Science, University College DublinDepartment of Pediatrics, University of Massachusetts Chan Medical SchoolAbstract TMEM67 mutations cause Meckel-Gruber syndrome and other related ciliopathies. TMEM67 is involved in both ciliary transition zone assembly, and non-canonical Wnt signaling mediated by its extracellular domain. How TMEM67 performs these two separate functions is not known. We identify a cleavage motif in the extracellular domain of TMEM67 cleaved by the extracellular matrix metalloproteinase ADAMTS9. This cleavage regulates the abundance of two functional forms: a C-terminal portion which localizes to the ciliary transition zone regulating ciliogenesis, and a non-cleaved form which regulates Wnt signaling. By characterizing three TMEM67 ciliopathy patient variants within the cleavage motif utilizing mammalian cell culture and C. elegans, we show the cleavage motif is essential for cilia structure and function, highlighting its clinical significance. We generated a non-cleavable TMEM67 mouse model which develop severe ciliopathies phenocopying Tmem67 -/- mice, but in contrast, transduces normal Wnt signaling, substantiating the existence of two functional forms of TMEM67.https://doi.org/10.1038/s41467-025-60294-3
spellingShingle Manu Ahmed
Sydney Fischer
Karyn L. Robert
Karen I. Lange
Michael W. Stuck
Sunayna Best
Colin A. Johnson
Gregory J. Pazour
Oliver E. Blacque
Sumeda Nandadasa
Cleavage of the Meckel-Gruber syndrome protein TMEM67 by ADAMTS9 uncouples Wnt signaling and ciliogenesis
Nature Communications
title Cleavage of the Meckel-Gruber syndrome protein TMEM67 by ADAMTS9 uncouples Wnt signaling and ciliogenesis
title_full Cleavage of the Meckel-Gruber syndrome protein TMEM67 by ADAMTS9 uncouples Wnt signaling and ciliogenesis
title_fullStr Cleavage of the Meckel-Gruber syndrome protein TMEM67 by ADAMTS9 uncouples Wnt signaling and ciliogenesis
title_full_unstemmed Cleavage of the Meckel-Gruber syndrome protein TMEM67 by ADAMTS9 uncouples Wnt signaling and ciliogenesis
title_short Cleavage of the Meckel-Gruber syndrome protein TMEM67 by ADAMTS9 uncouples Wnt signaling and ciliogenesis
title_sort cleavage of the meckel gruber syndrome protein tmem67 by adamts9 uncouples wnt signaling and ciliogenesis
url https://doi.org/10.1038/s41467-025-60294-3
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