Tuft cells are a rare epithelial cell type that play important roles in sensing and responding to luminal antigens. A defining morphological feature of this lineage is the actin-rich apical “tuft,” which contains large fingerlike protrusions. However, details of the cytoskeletal ultrastructure underpinning the tuft, the molecules involved in building this structure, or how it supports tuft cell biology remain unclear. In the context of the small intestine, we found that tuft cell protrusions are supported by long-core bundles that consist of F-actin crosslinked in a parallel and polarized configuration; they also contain a tuft cell–specific complement of actin-binding proteins that exhibit regionalized localization along the bundle axis. Remarkably, in the sub-apical cytoplasm, the array of core actin bundles interdigitates and co-aligns with a highly ordered network of microtubules. The resulting cytoskeletal superstructure is well positioned to support subcellular transport and, in turn, the dynamic sensing functions of the tuft cell that are critical for intestinal homeostasis.
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October 01 2024
Organization of a cytoskeletal superstructure in the apical domain of intestinal tuft cells
Jennifer B. Silverman
,
Jennifer B. Silverman
(Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Validation, Visualization, Writing - original draft, Writing - review & editing)
1Department of Cell and Developmental Biology,
Vanderbilt University School of Medicine
, Nashville, TN, USA
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Evan E. Krystofiak
,
Evan E. Krystofiak
(Data curation, Formal analysis, Investigation, Methodology, Visualization, Writing - review & editing)
1Department of Cell and Developmental Biology,
Vanderbilt University School of Medicine
, Nashville, TN, USA
2
Vanderbilt Cell Imaging Shared Resource, Vanderbilt University
, Nashville, TN, USA
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Leah R. Caplan
,
Leah R. Caplan
(Data curation, Formal analysis, Methodology, Software, Writing - review & editing)
1Department of Cell and Developmental Biology,
Vanderbilt University School of Medicine
, Nashville, TN, USA
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Ken S. Lau
,
Ken S. Lau
(Data curation, Formal analysis, Resources, Software, Visualization, Writing - original draft, Writing - review & editing)
1Department of Cell and Developmental Biology,
Vanderbilt University School of Medicine
, Nashville, TN, USA
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Matthew J. Tyska
(Conceptualization, Funding acquisition, Methodology, Project administration, Supervision, Writing - original draft, Writing - review & editing)
1Department of Cell and Developmental Biology,
Vanderbilt University School of Medicine
, Nashville, TN, USA
Correspondence to Matthew J. Tyska: [email protected]
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Jennifer B. Silverman
Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Validation, Visualization, Writing - original draft, Writing - review & editing
1Department of Cell and Developmental Biology,
Vanderbilt University School of Medicine
, Nashville, TN, USA
Evan E. Krystofiak
Data curation, Formal analysis, Investigation, Methodology, Visualization, Writing - review & editing
1Department of Cell and Developmental Biology,
Vanderbilt University School of Medicine
, Nashville, TN, USA
2
Vanderbilt Cell Imaging Shared Resource, Vanderbilt University
, Nashville, TN, USA
Leah R. Caplan
Data curation, Formal analysis, Methodology, Software, Writing - review & editing
1Department of Cell and Developmental Biology,
Vanderbilt University School of Medicine
, Nashville, TN, USA
Ken S. Lau
Data curation, Formal analysis, Resources, Software, Visualization, Writing - original draft, Writing - review & editing
1Department of Cell and Developmental Biology,
Vanderbilt University School of Medicine
, Nashville, TN, USA
Correspondence to Matthew J. Tyska: [email protected]
Disclosures: The authors declare no competing interests exist.
Received:
April 13 2024
Revision Received:
August 26 2024
Accepted:
September 16 2024
Online ISSN: 1540-8140
Print ISSN: 0021-9525
Funding
Funder(s):
National Cancer Institute
- Award Id(s): P30 CA068485
Funder(s):
National Institutes of Health
- Award Id(s): R01 DK103831,R01 DK095811,R01 DK125546,R01 DK111949
Funder(s):
National Institute of Diabetes and Digestive and Kidney Diseases
- Award Id(s): F31 DK141157
© 2024 Silverman et al.
2024
Silverman et al.
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 (2024) 223 (12): e202404070.
Article history
Received:
April 13 2024
Revision Received:
August 26 2024
Accepted:
September 16 2024
Citation
Jennifer B. Silverman, Evan E. Krystofiak, Leah R. Caplan, Ken S. Lau, Matthew J. Tyska; Organization of a cytoskeletal superstructure in the apical domain of intestinal tuft cells. J Cell Biol 2 December 2024; 223 (12): e202404070. doi: https://doi.org/10.1083/jcb.202404070
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