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A composition-dependent molecular clutch between T cell signaling condensates and actin

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Ditlev, Jonathon A., Vega, Anthony R., Köster, Darius Vasco, Su, Xiaolei, Tani, Tomomi, Lakoduk, Ashley M., Vale, Ronald D., Mayor, Satyajit, Jaqaman, Khuloud and Rosen, Michael K. (2019) A composition-dependent molecular clutch between T cell signaling condensates and actin. eLife, 8 . e42695 . doi:10.7554/eLife.42695 ISSN 2050-084X.

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Official URL: http://dx.doi.org/10.7554/eLife.42695

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Abstract

During T cell activation, biomolecular condensates form at the immunological synapse (IS) through multivalency-driven phase separation of LAT, Grb2, Sos1, SLP-76, Nck, and WASP. These condensates move radially at the IS, traversing successive radially-oriented and concentric actin networks. To understand this movement, we biochemically reconstituted LAT condensates with actomyosin filaments. We found that basic regions of Nck and N-WASP/WASP promote association and co-movement of LAT condensates with actin, indicating conversion of weak individual affinities to high collective affinity upon phase separation. Condensates lacking these components were propelled differently, without strong actin adhesion. In cells, LAT condensates lost Nck as radial actin transitioned to the concentric network, and engineered condensates constitutively binding actin moved aberrantly. Our data show that Nck and WASP form a clutch between LAT condensates and actin in vitro and suggest that compositional changes may enable condensate movement by distinct actin networks in different regions of the IS.

Item Type: Journal Article
Subjects: Q Science > QP Physiology
Q Science > QR Microbiology
Divisions: Faculty of Science, Engineering and Medicine > Medicine > Warwick Medical School > Biomedical Sciences > Cell & Developmental Biology
Faculty of Science, Engineering and Medicine > Medicine > Warwick Medical School > Biomedical Sciences
Faculty of Science, Engineering and Medicine > Medicine > Warwick Medical School
Library of Congress Subject Headings (LCSH): T cells, T cells -- Receptors, Immune response -- Molecular aspects, Synapses, Antigen presenting cells
Journal or Publication Title: eLife
Publisher: eLife Sciences Publications Ltd.
ISSN: 2050-084X
Official Date: 3 July 2019
Dates:
DateEvent
3 July 2019Published
14 June 2019Accepted
Volume: 8
Article Number: e42695
DOI: 10.7554/eLife.42695
Status: Peer Reviewed
Publication Status: Published
Access rights to Published version: Open Access (Creative Commons)
Date of first compliant deposit: 5 July 2019
Date of first compliant Open Access: 8 July 2019
RIOXX Funder/Project Grant:
Project/Grant IDRIOXX Funder NameFunder ID
Collaborative Innovation AwardHoward Hughes Medical Institutehttp://dx.doi.org/10.13039/100000011
I-1544Welch Foundationhttp://dx.doi.org/10.13039/100000928
J. C. Bose FellowshipIndia. Department of Science and Technologyhttp://viaf.org/viaf/159510027
Margadarshi FellowshipWellcome Trusthttp://dx.doi.org/10.13039/100010269
UNSPECIFIEDDepartment of Biotechnology , Ministry of Science and Technologyhttp://dx.doi.org/10.13039/501100001407
IA/M/15/1/502018DBT India Alliancehttp://dx.doi.org/10.13039/501100009053
R01 GM100160National Institutes of Healthhttp://dx.doi.org/10.13039/100000002
R35 GM119619 National Institutes of Healthhttp://dx.doi.org/10.13039/100000002
R1216Cancer Prevention and Research Institute of Texashttp://dx.doi.org/10.13039/100004917
UNSPECIFIEDGraduate School of Biomedical Sciences, University of Texas Southwestern Medical Centerhttp://dx.doi.org/10.13039/100008260
National Research Service Award F32National Cancer Institutehttp://dx.doi.org/10.13039/100000054
RP140110, PICancer Prevention and Research Institute of Texashttp://dx.doi.org/10.13039/100004917
UNSPECIFIEDAXA Research Fundhttp://dx.doi.org/10.13039/501100001961
UNSPECIFIEDTata Institute of Fundamental Researchhttp://dx.doi.org/10.13039/501100001405
Irvington postdoctoral fellowshipCancer Research Institutehttp://dx.doi.org/10.13039/100000884
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