Signaling via a CD27-TRAF2-SHP-1 axis during naive T cell activation promotes memory-associated gene regulatory networks.

Autor: Jaeger-Ruckstuhl CA; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA. Electronic address: cjaeger@fredhutch.org., Lo Y; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Fulton E; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Waltner OG; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Shabaneh TB; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Simon S; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Muthuraman PV; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Correnti CE; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Newsom OJ; Human Biology Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Engstrom IA; Human Biology Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Kanaan SB; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Bhise SS; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Peralta JMC; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Ruff R; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA; Seattle Children's Hospital, Seattle, WA 98105, USA., Price JP; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA; Seattle Children's Hospital, Seattle, WA 98105, USA., Stull SM; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Stevens AR; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Bugos G; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Kluesner MG; Human Biology Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Voillet V; Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Muhunthan V; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Morrish F; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Olson JM; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA; Seattle Children's Hospital, Seattle, WA 98105, USA., Gottardo R; Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA; Department of Statistics, University of Washington, Seattle, WA 98195, USA; Swiss Institute of Bioinformatics, University of Lausanne and Lausanne University Hospital, Lausanne 1011, Switzerland., Sarthy JF; Seattle Children's Hospital, Seattle, WA 98105, USA; Basic Science Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Henikoff S; Basic Science Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA; Howard Hughes Medical Institute, Seattle, WA 98195, USA., Sullivan LB; Human Biology Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA., Furlan SN; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA; Seattle Children's Hospital, Seattle, WA 98105, USA., Riddell SR; Translational Sciences and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA; Department of Medicine, University of Washington, Seattle, WA 98195, USA. Electronic address: sriddell@fredhutch.org.
Jazyk: angličtina
Zdroj: Immunity [Immunity] 2024 Feb 13; Vol. 57 (2), pp. 287-302.e12.
DOI: 10.1016/j.immuni.2024.01.011
Abstrakt: The interaction of the tumor necrosis factor receptor (TNFR) family member CD27 on naive CD8 + T (Tn) cells with homotrimeric CD70 on antigen-presenting cells (APCs) is necessary for T cell memory fate determination. Here, we examined CD27 signaling during Tn cell activation and differentiation. In conjunction with T cell receptor (TCR) stimulation, ligation of CD27 by a synthetic trimeric CD70 ligand triggered CD27 internalization and degradation, suggesting active regulation of this signaling axis. Internalized CD27 recruited the signaling adaptor TRAF2 and the phosphatase SHP-1, thereby modulating TCR and CD28 signals. CD27-mediated modulation of TCR signals promoted transcription factor circuits that induced memory rather than effector associated gene programs, which are induced by CD28 costimulation. CD27-costimulated chimeric antigen receptor (CAR)-engineered T cells exhibited improved tumor control compared with CD28-costimulated CAR-T cells. Thus, CD27 signaling during Tn cell activation promotes memory properties with relevance to T cell immunotherapy.
Competing Interests: Declaration of interests C.A.J.-R., C.E.C., and S.R.R. are inventors on a patent (“engineered trimeric CD70 proteins and uses thereof”; WO2021072127A3) filed by Fred Hutchinson Cancer Center and licensed by Lyell Immunopharma. S.R.R. was a founder, has served as an advisor, and has patents licensed to Juno Therapeutics; S.R.R is a founder of and holds equity in Lyell Immunopharma and has served on the advisory boards for Adaptive Biotechnologies and Nohla.
(Copyright © 2024 The Authors. Published by Elsevier Inc. All rights reserved.)
Databáze: MEDLINE