» Articles » PMID: 31105694

Protein Kinase C δ Regulates the Depletion of Actin at the Immunological Synapse Required for Polarized Exosome Secretion by T Cells

Abstract

Multivesicular bodies (MVB) are endocytic compartments that enclose intraluminal vesicles (ILVs) formed by inward budding from the limiting membrane of endosomes. In T lymphocytes, ILVs are secreted as Fas ligand-bearing, pro-apoptotic exosomes following T cell receptor (TCR)-induced fusion of MVB with the plasma membrane at the immune synapse (IS). In this study we show that protein kinase C δ (PKCδ), a novel PKC isotype activated by diacylglycerol (DAG), regulates TCR-controlled MVB polarization toward the IS and exosome secretion. Concomitantly, we demonstrate that PKCδ-interfered T lymphocytes are defective in activation-induced cell death. Using a DAG sensor based on the C1 DAG-binding domain of PKCδ and a GFP-PKCδ chimera, we reveal that T lymphocyte activation enhances DAG levels at the MVB endomembranes which mediates the association of PKCδ to MVB. Spatiotemporal reorganization of F-actin at the IS is inhibited in PKCδ-interfered T lymphocytes. Therefore, we propose PKCδ as a DAG effector that regulates the actin reorganization necessary for MVB traffic and exosome secretion.

Citing Articles

Formin-like 1β phosphorylation at S1086 is necessary for secretory polarized traffic of exosomes at the immune synapse in Jurkat T lymphocytes.

Ruiz-Navarro J, Fernandez-Hermira S, Sanz-Fernandez I, Barbeito P, Navarro-Zapata A, Perez-Martinez A Elife. 2024; 13.

PMID: 39479958 PMC: 11527432. DOI: 10.7554/eLife.96942.


Is the tumor cell side of the immunological synapse a polarized secretory domain?.

Biolato A, Filali L, Pereira Fernandes D, Moreau F, Mgrditchian T, Hoffmann C Front Immunol. 2024; 15:1452810.

PMID: 39380986 PMC: 11458426. DOI: 10.3389/fimmu.2024.1452810.


Two roads diverged in a cell: insights from differential exosome regulation in polarized cells.

Komori T, Fukuda M Front Cell Dev Biol. 2024; 12:1451988.

PMID: 39286483 PMC: 11402822. DOI: 10.3389/fcell.2024.1451988.


CRABP1-complexes in exosome secretion.

Nhieu J, Wei C, Ludwig M, Drake J, Wei L Cell Commun Signal. 2024; 22(1):381.

PMID: 39075476 PMC: 11285139. DOI: 10.1186/s12964-024-01749-w.


The potential roles of exosomes in pathological cardiomyocyte hypertrophy mechanisms and therapy: A review.

Zhang L, Xie F, Zhang F, Lu B Medicine (Baltimore). 2024; 103(17):e37994.

PMID: 38669371 PMC: 11049793. DOI: 10.1097/MD.0000000000037994.


References
1.
Topham M, Prescott S . Mammalian diacylglycerol kinases, a family of lipid kinases with signaling functions. J Biol Chem. 1999; 274(17):11447-50. DOI: 10.1074/jbc.274.17.11447. View

2.
Martinez-Lorenzo M, Anel A, Gamen S, Monle n I, Lasierra P, Larrad L . Activated human T cells release bioactive Fas ligand and APO2 ligand in microvesicles. J Immunol. 1999; 163(3):1274-81. View

3.
Sanjuan M, Jones D, Izquierdo M, Merida I . Role of diacylglycerol kinase alpha in the attenuation of receptor signaling. J Cell Biol. 2001; 153(1):207-20. PMC: 2185527. DOI: 10.1083/jcb.153.1.207. View

4.
Monleon I, Martinez-Lorenzo M, Monteagudo L, Lasierra P, Taules M, Iturralde M . Differential secretion of Fas ligand- or APO2 ligand/TNF-related apoptosis-inducing ligand-carrying microvesicles during activation-induced death of human T cells. J Immunol. 2001; 167(12):6736-44. DOI: 10.4049/jimmunol.167.12.6736. View

5.
Blanchard N, Lankar D, Faure F, Regnault A, Dumont C, Raposo G . TCR activation of human T cells induces the production of exosomes bearing the TCR/CD3/zeta complex. J Immunol. 2002; 168(7):3235-41. DOI: 10.4049/jimmunol.168.7.3235. View