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

Jaeger-Ruckstuhl, C.A.; Lo, Y.; Fulton, E.; Waltner, O.G.; Shabaneh, T.B.; Simon, S.; Muthuraman, P.V.; Correnti, C.E.; Newsom, O.J.; Engstrom, I.A.; Kanaan, S.B.; Bhise, S.S.; Peralta, JMC; Ruff, R.; Price, J.P.; Stull, S.M.; Stevens, A.R.; Bugos, G.; Kluesner, M.G.; Voillet, V.; Muhunthan, V.; Morrish, F.; Olson, J.M.; Gottardo, R.; Sarthy, J.F.; Henikoff, S.; Sullivan, L.B.; Furlan, S.N.; Riddell, S.R.

doi:10.1016/j.immuni.2024.01.011

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

Details

Download: 38354704.pdf (6794.20 [Ko])
State: Public
Version: Final published version
License: CC BY-NC-ND 4.0

Serval ID

serval:BIB_A730B5E1D986

Type

Article: article from journal or magazin.

Collection

Publications

Institution

UNIL/CHUV

Title

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

Journal

Immunity

Author(s)

Jaeger-Ruckstuhl C.A., Lo Y., Fulton E., Waltner O.G., Shabaneh T.B., Simon S., Muthuraman P.V., Correnti C.E., Newsom O.J., Engstrom I.A., Kanaan S.B., Bhise S.S., Peralta JMC, Ruff R., Price J.P., Stull S.M., Stevens A.R., Bugos G., Kluesner M.G., Voillet V., Muhunthan V., Morrish F., Olson J.M., Gottardo R., Sarthy J.F., Henikoff S., Sullivan L.B., Furlan S.N., Riddell S.R.

ISSN

1097-4180 (Electronic)

ISSN-L

1074-7613

Publication state

Published

Issued date

13/02/2024

Peer-reviewed

Oui

Volume

Number

Pages

287-302.e12

Language

english

Notes

Publication types: Journal Article
Publication Status: ppublish

Abstract

The interaction of the tumor necrosis factor receptor (TNFR) family member CD27 on naive CD8 <sup>+</sup> 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.

Keywords

TNF Receptor-Associated Factor 2/genetics, TNF Receptor-Associated Factor 2/metabolism, CD28 Antigens/metabolism, Gene Regulatory Networks, Signal Transduction, Lymphocyte Activation, Receptors, Antigen, T-Cell/metabolism, Tumor Necrosis Factor Receptor Superfamily, Member 7/genetics, Tumor Necrosis Factor Receptor Superfamily, Member 7/metabolism, CD27 Ligand/genetics, CD27 Ligand/metabolism, CD8-Positive T-Lymphocytes, CAR-T cell therapy, CD27, CD8(+) T cell, SHP-1 phosphatase, chimeric antigen receptor, costimulation, memory and effector fate determination, naive T cell activation

URN

urn:nbn:ch:serval-BIB_A730B5E1D9864

OAI-PMH

oai:serval.unil.ch:BIB_A730B5E1D986

DOI

10.1016/j.immuni.2024.01.011

Pubmed

38354704

Web of science

001184533900001

Open Access

Yes