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In vivo cell biological screening identifies an endocytic capture mechanism for T-tubule formation

The skeletal muscle T-tubule is a specialized membrane domain essential for coordinated muscle contraction. However, in the absence of genetically tractable systems the mechanisms involved in T-tubule formation are unknown. Here, we use the optically transparent and genetically tractable zebrafish s...

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Autores principales: Hall, Thomas E., Martel, Nick, Ariotti, Nicholas, Xiong, Zherui, Lo, Harriet P., Ferguson, Charles, Rae, James, Lim, Ye-Wheen, Parton, Robert G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7381618/
https://www.ncbi.nlm.nih.gov/pubmed/32709891
http://dx.doi.org/10.1038/s41467-020-17486-w
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author Hall, Thomas E.
Martel, Nick
Ariotti, Nicholas
Xiong, Zherui
Lo, Harriet P.
Ferguson, Charles
Rae, James
Lim, Ye-Wheen
Parton, Robert G.
author_facet Hall, Thomas E.
Martel, Nick
Ariotti, Nicholas
Xiong, Zherui
Lo, Harriet P.
Ferguson, Charles
Rae, James
Lim, Ye-Wheen
Parton, Robert G.
author_sort Hall, Thomas E.
collection PubMed
description The skeletal muscle T-tubule is a specialized membrane domain essential for coordinated muscle contraction. However, in the absence of genetically tractable systems the mechanisms involved in T-tubule formation are unknown. Here, we use the optically transparent and genetically tractable zebrafish system to probe T-tubule development in vivo. By combining live imaging of transgenic markers with three-dimensional electron microscopy, we derive a four-dimensional quantitative model for T-tubule formation. To elucidate the mechanisms involved in T-tubule formation in vivo, we develop a quantitative screen for proteins that associate with and modulate early T-tubule formation, including an overexpression screen of the entire zebrafish Rab protein family. We propose an endocytic capture model involving firstly, formation of dynamic endocytic tubules at transient nucleation sites on the sarcolemma, secondly, stabilization by myofibrils/sarcoplasmic reticulum and finally, delivery of membrane from the recycling endosome and Golgi complex.
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spelling pubmed-73816182020-07-28 In vivo cell biological screening identifies an endocytic capture mechanism for T-tubule formation Hall, Thomas E. Martel, Nick Ariotti, Nicholas Xiong, Zherui Lo, Harriet P. Ferguson, Charles Rae, James Lim, Ye-Wheen Parton, Robert G. Nat Commun Article The skeletal muscle T-tubule is a specialized membrane domain essential for coordinated muscle contraction. However, in the absence of genetically tractable systems the mechanisms involved in T-tubule formation are unknown. Here, we use the optically transparent and genetically tractable zebrafish system to probe T-tubule development in vivo. By combining live imaging of transgenic markers with three-dimensional electron microscopy, we derive a four-dimensional quantitative model for T-tubule formation. To elucidate the mechanisms involved in T-tubule formation in vivo, we develop a quantitative screen for proteins that associate with and modulate early T-tubule formation, including an overexpression screen of the entire zebrafish Rab protein family. We propose an endocytic capture model involving firstly, formation of dynamic endocytic tubules at transient nucleation sites on the sarcolemma, secondly, stabilization by myofibrils/sarcoplasmic reticulum and finally, delivery of membrane from the recycling endosome and Golgi complex. Nature Publishing Group UK 2020-07-24 /pmc/articles/PMC7381618/ /pubmed/32709891 http://dx.doi.org/10.1038/s41467-020-17486-w Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Hall, Thomas E.
Martel, Nick
Ariotti, Nicholas
Xiong, Zherui
Lo, Harriet P.
Ferguson, Charles
Rae, James
Lim, Ye-Wheen
Parton, Robert G.
In vivo cell biological screening identifies an endocytic capture mechanism for T-tubule formation
title In vivo cell biological screening identifies an endocytic capture mechanism for T-tubule formation
title_full In vivo cell biological screening identifies an endocytic capture mechanism for T-tubule formation
title_fullStr In vivo cell biological screening identifies an endocytic capture mechanism for T-tubule formation
title_full_unstemmed In vivo cell biological screening identifies an endocytic capture mechanism for T-tubule formation
title_short In vivo cell biological screening identifies an endocytic capture mechanism for T-tubule formation
title_sort in vivo cell biological screening identifies an endocytic capture mechanism for t-tubule formation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7381618/
https://www.ncbi.nlm.nih.gov/pubmed/32709891
http://dx.doi.org/10.1038/s41467-020-17486-w
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