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Article

Rab6-dependent retrograde traffic of LAT controls immune synapse formation and T cell activation

Jean-Marie Carpier, Andres E. Zucchetti, Laurence Bataille, Stéphanie Dogniaux, Massiullah Shafaq-Zadah, Sabine Bardin, Marco Lucchino, View ORCID ProfileMathieu Maurin, Leonel D. Joannas, View ORCID ProfileJoao Gamelas Magalhaes, View ORCID ProfileLudger Johannes, View ORCID ProfileThierry Galli, Bruno Goud, View ORCID ProfileClaire Hivroz  Correspondence email
Jean-Marie Carpier
Crosstalk between T Cells and Dendritic Cells Group, Institut Curie, Paris Sciences and Lettres Research University, INSERM U932, Paris, France
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Andres E. Zucchetti
Crosstalk between T Cells and Dendritic Cells Group, Institut Curie, Paris Sciences and Lettres Research University, INSERM U932, Paris, France
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Laurence Bataille
Crosstalk between T Cells and Dendritic Cells Group, Institut Curie, Paris Sciences and Lettres Research University, INSERM U932, Paris, France
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Stéphanie Dogniaux
Crosstalk between T Cells and Dendritic Cells Group, Institut Curie, Paris Sciences and Lettres Research University, INSERM U932, Paris, France
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Massiullah Shafaq-Zadah
Cellular and Chemical Biology of Membranes and Therapeutic Delivery Unit, Institut Curie, Paris Sciences and Lettres Research University, INSERM U1143, CNRS UMR 3666, Paris, France
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Sabine Bardin
Molecular Mechanisms of Intracellular Transport Group, Institut Curie, Paris Sciences and Lettres Research University, CNRS UMR 144, Paris, France
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Marco Lucchino
Cellular and Chemical Biology of Membranes and Therapeutic Delivery Unit, Institut Curie, Paris Sciences and Lettres Research University, INSERM U1143, CNRS UMR 3666, Paris, France
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Mathieu Maurin
Crosstalk between T Cells and Dendritic Cells Group, Institut Curie, Paris Sciences and Lettres Research University, INSERM U932, Paris, France
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  • ORCID record for Mathieu Maurin
Leonel D. Joannas
Crosstalk between T Cells and Dendritic Cells Group, Institut Curie, Paris Sciences and Lettres Research University, INSERM U932, Paris, France
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Joao Gamelas Magalhaes
Crosstalk between T Cells and Dendritic Cells Group, Institut Curie, Paris Sciences and Lettres Research University, INSERM U932, Paris, France
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  • ORCID record for Joao Gamelas Magalhaes
Ludger Johannes
Cellular and Chemical Biology of Membranes and Therapeutic Delivery Unit, Institut Curie, Paris Sciences and Lettres Research University, INSERM U1143, CNRS UMR 3666, Paris, France
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  • ORCID record for Ludger Johannes
Thierry Galli
Center of Psychiatry and Neurosciences, Membrane Traffic in Health and Diseased Brain, Université Paris Descartes, Sorbonne Paris Cité, INSERM ERL U950, Paris, France
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Bruno Goud
Molecular Mechanisms of Intracellular Transport Group, Institut Curie, Paris Sciences and Lettres Research University, CNRS UMR 144, Paris, France
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Claire Hivroz
Crosstalk between T Cells and Dendritic Cells Group, Institut Curie, Paris Sciences and Lettres Research University, INSERM U932, Paris, France
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  • ORCID record for Claire Hivroz
  • For correspondence: claire.hivroz@curie.fr
DOI: 10.1084/jem.20162042 | Published February 12, 2018
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Abstract

The adapter molecule linker for activation of T cells (LAT) orchestrates the formation of signalosomes upon T cell receptor (TCR) stimulation. LAT is present in different intracellular pools and is dynamically recruited to the immune synapse upon stimulation. However, the intracellular traffic of LAT and its function in T lymphocyte activation are ill defined. We show herein that LAT, once internalized, transits through the Golgi–trans-Golgi network (TGN), where it is repolarized to the immune synapse. This retrograde transport of LAT depends on the small GTPase Rab6 and the target soluble N-ethylmaleimide-sensitive factor attachment protein receptor (t-SNARE) Syntaxin-16, two regulators of the endosome-to-Golgi/TGN retrograde transport. We also show in vitro in Syntaxin-16– or Rab6-silenced human cells and in vivo in CD4+ T lymphocytes of the Rab6 knockout mouse that this retrograde traffic controls TCR stimulation. These results establish that the retrograde traffic of LAT from the plasma membrane to the Golgi-TGN controls the polarized delivery of LAT at the immune synapse and T lymphocyte activation.

  • Submitted: 20 December 2016
  • Revision received 30 November 2017
  • Accepted: 11 January 2018
Creative Commons logoCreative Commons logohttp://www.rupress.org/terms/https://creativecommons.org/licenses/by-nc-sa/4.0/

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/).

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© 2018 Carpier et al. http://www.rupress.org/terms/https://creativecommons.org/licenses/by-nc-sa/4.0/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/).

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Rab6-dependent retrograde traffic of LAT controls immune synapse formation and T cell activation
Jean-Marie Carpier, Andres E. Zucchetti, Laurence Bataille, Stéphanie Dogniaux, Massiullah Shafaq-Zadah, Sabine Bardin, Marco Lucchino, Mathieu Maurin, Leonel D. Joannas, Joao Gamelas Magalhaes, Ludger Johannes, Thierry Galli, Bruno Goud, Claire Hivroz
Journal of Experimental Medicine Feb 2018, jem.20162042; DOI: 10.1084/jem.20162042

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The Journal of Experimental Medicine: 215 (4)

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April 2, 2018
Volume 215, No. 4

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