A novel pathway down-modulating T cell activation involves HPK-1-dependent recruitment of 14-3-3 proteins on SLP-76

Di Bartolo V, Montagne B, Salek M, Jungwirth B, Carrette F, Fourtane J, Sol-Foulon N, Michel F, Schwartz O, Lehmann WD, Acuto O (2007)
J Exp Med 204(3): 681-691.

Journal Article | Published | English

No fulltext has been uploaded

Author
; ; ; ; ; ; ; ; ; ;
Abstract
The SH2 domain-containing leukocyte protein of 76 kD (SLP-76) is a pivotal element of the signaling machinery controlling T cell receptor (TCR)-mediated activation. Here, we identify 14-3-3epsilon and zeta proteins as SLP-76 binding partners. This interaction was induced by TCR ligation and required phosphorylation of SLP-76 at serine 376. Ribonucleic acid interference and in vitro phosphorylation experiments showed that serine 376 is the target of the hematopoietic progenitor kinase 1 (HPK-1). Interestingly, either S376A mutation or HPK-1 knockdown resulted in increased TCR-induced tyrosine phosphorylation of SLP-76 and phospholipase C-gamma1. Moreover, an SLP-76-S376A mutant induced higher interleukin 2 gene transcription than wild-type SLP-76. These data reveal a novel negative feedback loop involving HPK-1-dependent serine phosphorylation of SLP-76 and 14-3-3 protein recruitment, which tunes T cell activation.
Publishing Year
ISSN
eISSN
PUB-ID

Cite this

Di Bartolo V, Montagne B, Salek M, et al. A novel pathway down-modulating T cell activation involves HPK-1-dependent recruitment of 14-3-3 proteins on SLP-76. J Exp Med. 2007;204(3):681-691.
Di Bartolo, V., Montagne, B., Salek, M., Jungwirth, B., Carrette, F., Fourtane, J., Sol-Foulon, N., et al. (2007). A novel pathway down-modulating T cell activation involves HPK-1-dependent recruitment of 14-3-3 proteins on SLP-76. J Exp Med, 204(3), 681-691.
Di Bartolo, V., Montagne, B., Salek, M., Jungwirth, B., Carrette, F., Fourtane, J., Sol-Foulon, N., Michel, F., Schwartz, O., Lehmann, W. D., et al. (2007). A novel pathway down-modulating T cell activation involves HPK-1-dependent recruitment of 14-3-3 proteins on SLP-76. J Exp Med 204, 681-691.
Di Bartolo, V., et al., 2007. A novel pathway down-modulating T cell activation involves HPK-1-dependent recruitment of 14-3-3 proteins on SLP-76. J Exp Med, 204(3), p 681-691.
V. Di Bartolo, et al., “A novel pathway down-modulating T cell activation involves HPK-1-dependent recruitment of 14-3-3 proteins on SLP-76”, J Exp Med, vol. 204, 2007, pp. 681-691.
Di Bartolo, V., Montagne, B., Salek, M., Jungwirth, B., Carrette, F., Fourtane, J., Sol-Foulon, N., Michel, F., Schwartz, O., Lehmann, W.D., Acuto, O.: A novel pathway down-modulating T cell activation involves HPK-1-dependent recruitment of 14-3-3 proteins on SLP-76. J Exp Med. 204, 681-691 (2007).
Di Bartolo, Vincenzo, Montagne, Benjamin, Salek, Mogjiborahman, Jungwirth, Britta, Carrette, Florent, Fourtane, Julien, Sol-Foulon, Nathalie, Michel, Frederique, Schwartz, Olivier, Lehmann, Wolf D, and Acuto, Oreste. “A novel pathway down-modulating T cell activation involves HPK-1-dependent recruitment of 14-3-3 proteins on SLP-76”. J Exp Med 204.3 (2007): 681-691.
This data publication is cited in the following publications:
This publication cites the following data publications:

31 Citations in Europe PMC

Data provided by Europe PubMed Central.

[Immunological synapse is a dynamic signaling platform for T cell activation].
Bouchet J, Alcover A., Med Sci (Paris) 30(6-7), 2014
PMID: 25014458
Quantitative dynamics of phosphoproteome: the devil is in the details.
Salek M, Acuto O., Anal. Chem. 84(20), 2012
PMID: 23020125
The SLP-76 Src homology 2 domain is required for T cell development and activation.
Burns JC, Corbo E, Degen J, Gohil M, Anterasian C, Schraven B, Koretzky GA, Kliche S, Jordan MS., J. Immunol. 187(9), 2011
PMID: 21949020
Antigen receptor signaling: the Tuscan connection.
Baldari CT, Koretzky GA., Nat. Immunol. 8(8), 2007
PMID: 17641655

47 References

Data provided by Europe PubMed Central.

The chaperone protein 14-3-3 interacts with 3BP2/SH3BP2 and regulates its adapter function.
Foucault I, Liu YC, Bernard A, Deckert M., J. Biol. Chem. 278(9), 2003
PMID: 12501243
Uncoupling of nonreceptor tyrosine kinases from PLC-gamma1 in an SLP-76-deficient T cell.
Yablonski D, Kuhne MR, Kadlecek T, Weiss A., Science 281(5375), 1998
PMID: 9665884
Early phosphorylation kinetics of proteins involved in proximal TCR-mediated signaling pathways.
Houtman JC, Houghtling RA, Barda-Saad M, Toda Y, Samelson LE., J. Immunol. 175(4), 2005
PMID: 16081816
CD28 as a molecular amplifier extending TCR ligation and signaling capabilities.
Michel F, Attal-Bonnefoy G, Mangino G, Mise-Omata S, Acuto O., Immunity 15(6), 2001
PMID: 11754815
The Ste20 group kinases as regulators of MAP kinase cascades.
Dan I, Watanabe NM, Kusumi A., Trends Cell Biol. 11(5), 2001
PMID: 11316611
HPK1, a hematopoietic protein kinase activating the SAPK/JNK pathway.
Kiefer F, Tibbles LA, Anafi M, Janssen A, Zanke BW, Lassam N, Pawson T, Woodgett JR, Iscove NN., EMBO J. 15(24), 1996
PMID: 9003777
Hematopoietic progenitor kinase 1 negatively regulates T cell receptor signaling and T cell-mediated immune responses.
Shui JW, Boomer JS, Han J, Xu J, Dement GA, Zhou G, Tan TH., Nat. Immunol. 8(1), 2007
PMID: 17115060

AUTHOR UNKNOWN, 2005
14-3-3 protein binds to insulin receptor substrate-1, one of the binding sites of which is in the phosphotyrosine binding domain.
Ogihara T, Isobe T, Ichimura T, Taoka M, Funaki M, Sakoda H, Onishi Y, Inukai K, Anai M, Fukushima Y, Kikuchi M, Yazaki Y, Oka Y, Asano T., J. Biol. Chem. 272(40), 1997
PMID: 9312143
CD28 utilizes Vav-1 to enhance TCR-proximal signaling and NF-AT activation.
Michel F, Mangino G, Attal-Bonnefoy G, Tuosto L, Alcover A, Roumier A, Olive D, Acuto O., J. Immunol. 165(7), 2000
PMID: 11034388
CD8 T cell sensory adaptation dependent on TCR avidity for self-antigens.
Marquez ME, Ellmeier W, Sanchez-Guajardo V, Freitas AA, Acuto O, Di Bartolo V., J. Immunol. 175(11), 2005
PMID: 16301646
Implication of the GRB2-associated phosphoprotein SLP-76 in T cell receptor-mediated interleukin 2 production.
Motto DG, Ross SE, Wu J, Hendricks-Taylor LR, Koretzky GA., J. Exp. Med. 183(4), 1996
PMID: 8666952
Mutation of tyrosines 492/493 in the kinase domain of ZAP-70 affects multiple T-cell receptor signaling pathways.
Mege D, Di Bartolo V, Germain V, Tuosto L, Michel F, Acuto O., J. Biol. Chem. 271(51), 1996
PMID: 8955094
Tyrosine 315 determines optimal recruitment of ZAP-70 to the T cell antigen receptor.
Di Bartolo V, Malissen M, Dufour E, Sechet E, Malissen B, Acuto O., Eur. J. Immunol. 32(2), 2002
PMID: 11828374
CD28 costimulatory signal induces protein arginine methylation in T cells.
Blanchet F, Cardona A, Letimier FA, Hershfield MS, Acuto O., J. Exp. Med. 202(3), 2005
PMID: 16061726
Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels.
Shevchenko A, Wilm M, Vorm O, Mann M., Anal. Chem. 68(5), 1996
PMID: 8779443

Export

0 Marked Publications

Open Data PUB

Web of Science

View record in Web of Science®

Sources

PMID: 17353368
PubMed | Europe PMC

Search this title in

Google Scholar