Single-celled tubules represent a complicated structure that forms during development, requiring extension of a narrow cytoplasm surrounding a lumen exerting osmotic pressure that can burst the luminal membrane. Genetic studies on the excretory canal cell of Caenorhabditis elegans have revealed many proteins that regulate the cytoskeleton, vesicular transport, and physiology of the narrow canals. Here, we show that βH-spectrin regulates the placement of intermediate filament proteins forming a terminal web around the lumen, and that the terminal web in turn retains a highly conserved protein (EXC-9/CRIP1) that regulates apical endosomal trafficking. EXC-1/IRG, the binding partner of EXC-9, is also localized to the apical membrane and affects apical actin placement and RAB-8–mediated vesicular transport. The results suggest that an intermediate filament protein acts in a novel pathway to direct the traffic of vesicles to locations of lengthening apical surface during single-celled tubule development.
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2 November 2020
Article|
August 28 2020
Terminal web and vesicle trafficking proteins mediate nematode single-cell tubulogenesis
Zhe Yang
,
Zhe Yang
1
Department of Molecular Biosciences, University of Kansas, Lawrence, KS
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Brendan C. Mattingly
,
Brendan C. Mattingly
2
Department of Undergraduate Biology, University of Kansas, Overland Park, KS
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David H. Hall
,
David H. Hall
3
Center for C. elegans Anatomy, Albert Einstein College of Medicine, Bronx, NY
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Brian D. Ackley
,
Brian D. Ackley
1
Department of Molecular Biosciences, University of Kansas, Lawrence, KS
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Matthew Buechner
1
Department of Molecular Biosciences, University of Kansas, Lawrence, KS
Correspondence to Matthew Buechner: buechner@ku.edu
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1
Department of Molecular Biosciences, University of Kansas, Lawrence, KS
Brendan C. Mattingly
2
Department of Undergraduate Biology, University of Kansas, Overland Park, KS
David H. Hall
3
Center for C. elegans Anatomy, Albert Einstein College of Medicine, Bronx, NY
Brian D. Ackley
1
Department of Molecular Biosciences, University of Kansas, Lawrence, KS
Matthew Buechner
1
Department of Molecular Biosciences, University of Kansas, Lawrence, KS
Correspondence to Matthew Buechner: buechner@ku.edu
Received:
March 25 2020
Revision Received:
June 15 2020
Accepted:
August 03 2020
Online Issn: 1540-8140
Print Issn: 0021-9525
Funding:
Kansas State University Research Foundation
(2144091)
National Institutes of Health
(OD 010943, P40 OD-010440)
© 2020 Yang et al.
2020
This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
J Cell Biol (2020) 219 (11): e202003152.
Article history
Received:
March 25 2020
Revision Received:
June 15 2020
Accepted:
August 03 2020
Citation
Zhe Yang, Brendan C. Mattingly, David H. Hall, Brian D. Ackley, Matthew Buechner; Terminal web and vesicle trafficking proteins mediate nematode single-cell tubulogenesis. J Cell Biol 2 November 2020; 219 (11): e202003152. doi: https://doi.org/10.1083/jcb.202003152
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