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PMID: 18453591 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The chemokine receptor CXCR3 is degraded following internalization and is replenished at the cell surface by de novo synthesis of receptor.

Journal of immunology (Baltimore, Md. : 1950) ·Vol. 180 ·No. 10 ·2008-05-15 ·Pages 6713-24

Meiser A, Mueller A, Wise EL, McDonagh EM, Petit SJ, Saran N, Clark PC, Williams TJ, Pease JE

Abstract

The chemokine receptor CXCR3 is expressed on the surface of both resting and activated T lymphocytes. We describe in this study the endocytosis of CXCR3 using T lymphocytes and CXCR3 transfectants. Chemokine-induced CXCR3 down-regulation occurred in a rapid, dose-dependent manner, with CXCL11 the most potent and efficacious ligand. Endocytosis was mediated in part by arrestins, but appeared to occur independently of clathrin and caveolae. In contrast to other chemokine receptors, which are largely recycled to the cell surface within an hour, cell surface replenishment of CXCR3 occurred over several hours and was dependent upon mRNA transcription, de novo protein synthesis, and transport through the endoplasmic reticulum and Golgi. Confocal microscopy and Western blotting confirmed the fate of endocytosed CXCR3 to be degradation, mediated in part by lysosomes and proteosomes. Site-directed mutagenesis of the CXCR3 C terminus revealed that internalization and degradation were independent of phosphorylation, ubiquitination, or a conserved LL motif. CXCR3 was found to be efficiently internalized in the absence of ligand, a process involving a YXXL motif at the extreme of the C terminus. Although freshly isolated T lymphocytes expressed moderate cell surface levels of CXCR3, they were only responsive to CXCL11 with CXCL9 and CXCL10 only having significant activity on activated T lymphocytes. Thus, the activities of CXCR3 are tightly controlled following mRNA translation. Because CXCR3(+) cells are themselves a source of IFN-gamma, which potently induces the expression of CXCR3 ligands, such tight regulation of CXCR3 may serve as a control to avoid the unnecessary amplification of activated T lymphocyte recruitment.

MeSH Terms
Amino Acid Motifs Amino Acid Sequence Animals Blotting, Western Cell Line Cell Membrane/metabolism Electrophoresis, Polyacrylamide Gel Endocytosis/physiology Flow Cytometry Gene Expression Humans Mice Microscopy, Confocal Molecular Sequence Data Mutagenesis, Site-Directed Protein Biosynthesis Protein Structure, Tertiary Protein Transport/physiology Receptors, CXCR3/chemistry,genetics,metabolism T-Lymphocytes/metabolism Transfection
Chemicals
CXCR3 protein, human Receptors, CXCR3
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Meiser Andrea
Leukocyte Biology Section, National Heart and Lung Institute, Faculty of Medicine, Imperial College London, South Kensington Campus, London, UK.
Mueller Anja
Wise Emma L
McDonagh Ellen M
Petit Sarah J
Saran Namita
Clark Peter C
Williams Timothy J
Pease James E
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Article Info
Journal
Journal of immunology (Baltimore, Md. : 1950)
Abbr.
J Immunol
ISSN
0022-1767
Published
2008-05-15
Pages
6713-24
Language
English
Region
United States
NLM ID
2985117R
PMCID
PMC2556381
Subset
IM
Grants
British Heart Foundation · PG/03/134/16204 · United Kingdom
Arthritis Research UK · 17424 · United Kingdom
Arthritis Research UK · 174240 · United Kingdom
British Heart Foundation · FS/05/021 · United Kingdom
Wellcome Trust · United Kingdom
British Heart Foundation · PG/2000055 · United Kingdom
Wellcome Trust · 076036 · United Kingdom
Wellcome Trust · 076036/Z/04/Z · United Kingdom
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