Chaperone-mediated autophagy regulates T cell responses through targeted degradation of negative regulators of T cell activation

Nat Immunol. 2014 Nov;15(11):1046-54. doi: 10.1038/ni.3003. Epub 2014 Sep 28.

Abstract

Chaperone-mediated autophagy (CMA) targets soluble proteins for lysosomal degradation. Here we found that CMA was activated in T cells in response to engagement of the T cell antigen receptor (TCR), which induced expression of the CMA-related lysosomal receptor LAMP-2A. In activated T cells, CMA targeted the ubiquitin ligase Itch and the calcineurin inhibitor RCAN1 for degradation to maintain activation-induced responses. Consequently, deletion of the gene encoding LAMP-2A in T cells caused deficient in vivo responses to immunization or infection with Listeria monocytogenes. Impaired CMA activity also occurred in T cells with age, which negatively affected their function. Restoration of LAMP-2A in T cells from old mice resulted in enhancement of activation-induced responses. Our findings define a role for CMA in regulating T cell activation through the targeted degradation of negative regulators of T cell activation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aging / immunology
  • Animals
  • Autophagy / immunology*
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / biosynthesis
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / genetics
  • Calcineurin Inhibitors / metabolism
  • Calcium-Binding Proteins
  • Cells, Cultured
  • Dual Oxidases
  • Female
  • Humans
  • Immunization
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Listeria monocytogenes / immunology
  • Listeriosis / immunology
  • Lymphocyte Activation / immunology*
  • Lysosomal-Associated Membrane Protein 2 / biosynthesis
  • Lysosomal-Associated Membrane Protein 2 / genetics
  • Lysosomal-Associated Membrane Protein 2 / immunology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Molecular Chaperones / immunology*
  • Muscle Proteins / metabolism
  • NADPH Oxidases / genetics
  • Oxidative Stress / immunology
  • RNA Interference
  • RNA, Messenger / biosynthesis
  • RNA, Small Interfering
  • Reactive Oxygen Species / metabolism
  • Receptors, Antigen, T-Cell / immunology
  • Th1 Cells / immunology*
  • Ubiquitin-Protein Ligases / metabolism

Substances

  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
  • Calcineurin Inhibitors
  • Calcium-Binding Proteins
  • DSCR1 protein, mouse
  • Intracellular Signaling Peptides and Proteins
  • Lysosomal-Associated Membrane Protein 2
  • Molecular Chaperones
  • Muscle Proteins
  • RNA, Messenger
  • RNA, Small Interfering
  • Reactive Oxygen Species
  • Receptors, Antigen, T-Cell
  • Tcfeb protein, mouse
  • Dual Oxidases
  • NADPH Oxidases
  • Duox1 protein, mouse
  • Itch protein, mouse
  • Ubiquitin-Protein Ligases