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Mechanochemical feedback control of dynamin independent endocytosis modulates membrane tension in adherent cells

Plasma membrane tension regulates many key cellular processes. It is modulated by, and can modulate, membrane trafficking. However, the cellular pathway(s) involved in this interplay is poorly understood. Here we find that, among a number of endocytic processes operating simultaneously at the cell s...

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Autores principales: Thottacherry, Joseph Jose, Kosmalska, Anita Joanna, Kumar, Amit, Vishen, Amit Singh, Elosegui-Artola, Alberto, Pradhan, Susav, Sharma, Sumit, Singh, Parvinder P., Guadamillas, Marta C., Chaudhary, Natasha, Vishwakarma, Ram, Trepat, Xavier, del Pozo, Miguel A., Parton, Robert G., Rao, Madan, Pullarkat, Pramod, Roca-Cusachs, Pere, Mayor, Satyajit
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6181995/
https://www.ncbi.nlm.nih.gov/pubmed/30310066
http://dx.doi.org/10.1038/s41467-018-06738-5
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author Thottacherry, Joseph Jose
Kosmalska, Anita Joanna
Kumar, Amit
Vishen, Amit Singh
Elosegui-Artola, Alberto
Pradhan, Susav
Sharma, Sumit
Singh, Parvinder P.
Guadamillas, Marta C.
Chaudhary, Natasha
Vishwakarma, Ram
Trepat, Xavier
del Pozo, Miguel A.
Parton, Robert G.
Rao, Madan
Pullarkat, Pramod
Roca-Cusachs, Pere
Mayor, Satyajit
author_facet Thottacherry, Joseph Jose
Kosmalska, Anita Joanna
Kumar, Amit
Vishen, Amit Singh
Elosegui-Artola, Alberto
Pradhan, Susav
Sharma, Sumit
Singh, Parvinder P.
Guadamillas, Marta C.
Chaudhary, Natasha
Vishwakarma, Ram
Trepat, Xavier
del Pozo, Miguel A.
Parton, Robert G.
Rao, Madan
Pullarkat, Pramod
Roca-Cusachs, Pere
Mayor, Satyajit
author_sort Thottacherry, Joseph Jose
collection PubMed
description Plasma membrane tension regulates many key cellular processes. It is modulated by, and can modulate, membrane trafficking. However, the cellular pathway(s) involved in this interplay is poorly understood. Here we find that, among a number of endocytic processes operating simultaneously at the cell surface, a dynamin independent pathway, the CLIC/GEEC (CG) pathway, is rapidly and specifically upregulated upon a sudden reduction of tension. Moreover, inhibition (activation) of the CG pathway results in lower (higher) membrane tension. However, alteration in membrane tension does not directly modulate CG endocytosis. This requires vinculin, a mechano-transducer recruited to focal adhesion in adherent cells. Vinculin acts by controlling the levels of a key regulator of the CG pathway, GBF1, at the plasma membrane. Thus, the CG pathway directly regulates membrane tension and is in turn controlled via a mechano-chemical feedback inhibition, potentially leading to homeostatic regulation of membrane tension in adherent cells.
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spelling pubmed-61819952018-10-15 Mechanochemical feedback control of dynamin independent endocytosis modulates membrane tension in adherent cells Thottacherry, Joseph Jose Kosmalska, Anita Joanna Kumar, Amit Vishen, Amit Singh Elosegui-Artola, Alberto Pradhan, Susav Sharma, Sumit Singh, Parvinder P. Guadamillas, Marta C. Chaudhary, Natasha Vishwakarma, Ram Trepat, Xavier del Pozo, Miguel A. Parton, Robert G. Rao, Madan Pullarkat, Pramod Roca-Cusachs, Pere Mayor, Satyajit Nat Commun Article Plasma membrane tension regulates many key cellular processes. It is modulated by, and can modulate, membrane trafficking. However, the cellular pathway(s) involved in this interplay is poorly understood. Here we find that, among a number of endocytic processes operating simultaneously at the cell surface, a dynamin independent pathway, the CLIC/GEEC (CG) pathway, is rapidly and specifically upregulated upon a sudden reduction of tension. Moreover, inhibition (activation) of the CG pathway results in lower (higher) membrane tension. However, alteration in membrane tension does not directly modulate CG endocytosis. This requires vinculin, a mechano-transducer recruited to focal adhesion in adherent cells. Vinculin acts by controlling the levels of a key regulator of the CG pathway, GBF1, at the plasma membrane. Thus, the CG pathway directly regulates membrane tension and is in turn controlled via a mechano-chemical feedback inhibition, potentially leading to homeostatic regulation of membrane tension in adherent cells. Nature Publishing Group UK 2018-10-11 /pmc/articles/PMC6181995/ /pubmed/30310066 http://dx.doi.org/10.1038/s41467-018-06738-5 Text en © The Author(s) 2018 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
Thottacherry, Joseph Jose
Kosmalska, Anita Joanna
Kumar, Amit
Vishen, Amit Singh
Elosegui-Artola, Alberto
Pradhan, Susav
Sharma, Sumit
Singh, Parvinder P.
Guadamillas, Marta C.
Chaudhary, Natasha
Vishwakarma, Ram
Trepat, Xavier
del Pozo, Miguel A.
Parton, Robert G.
Rao, Madan
Pullarkat, Pramod
Roca-Cusachs, Pere
Mayor, Satyajit
Mechanochemical feedback control of dynamin independent endocytosis modulates membrane tension in adherent cells
title Mechanochemical feedback control of dynamin independent endocytosis modulates membrane tension in adherent cells
title_full Mechanochemical feedback control of dynamin independent endocytosis modulates membrane tension in adherent cells
title_fullStr Mechanochemical feedback control of dynamin independent endocytosis modulates membrane tension in adherent cells
title_full_unstemmed Mechanochemical feedback control of dynamin independent endocytosis modulates membrane tension in adherent cells
title_short Mechanochemical feedback control of dynamin independent endocytosis modulates membrane tension in adherent cells
title_sort mechanochemical feedback control of dynamin independent endocytosis modulates membrane tension in adherent cells
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6181995/
https://www.ncbi.nlm.nih.gov/pubmed/30310066
http://dx.doi.org/10.1038/s41467-018-06738-5
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