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.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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Autor*in
Di Bartolo, Vincenzo; Montagne, Benjamin; Salek, Mogjiborahman; Jungwirth, BrittaUniBi; Carrette, Florent; Fourtane, Julien; Sol-Foulon, Nathalie; Michel, Frederique; Schwartz, Olivier; Lehmann, Wolf D; Acuto, Oreste
Abstract / Bemerkung
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.
Erscheinungsjahr
2007
Zeitschriftentitel
J Exp Med
Band
204
Ausgabe
3
Seite(n)
681-691
ISSN
0022-1007
eISSN
1540-9538
Page URI
https://pub.uni-bielefeld.de/record/2092153

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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. https://doi.org/10.1084/jem.20062066
Di Bartolo, Vincenzo, Montagne, Benjamin, Salek, Mogjiborahman, Jungwirth, Britta, Carrette, Florent, Fourtane, Julien, Sol-Foulon, Nathalie, 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.

40 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

ADAP is an upstream regulator that precedes SLP-76 at sites of TCR engagement and stabilizes signaling microclusters.
Lewis JB, Scangarello FA, Murphy JM, Eidell KP, Sodipo MO, Ophir MJ, Sargeant R, Seminario MC, Bunnell SC., J Cell Sci 131(21), 2018
PMID: 30305305
Germinal-center kinase-like kinase co-crystal structure reveals a swapped activation loop and C-terminal extension.
Marcotte D, Rushe M, M Arduini R, Lukacs C, Atkins K, Sun X, Little K, Cullivan M, Paramasivam M, Patterson TA, Hesson T, D McKee T, May-Dracka TL, Xin Z, Bertolotti-Ciarlet A, Bhisetti GR, Lyssikatos JP, Silvian LF., Protein Sci 26(2), 2017
PMID: 27727493
A THEMIS:SHP1 complex promotes T-cell survival.
Paster W, Bruger AM, Katsch K, Grégoire C, Roncagalli R, Fu G, Gascoigne NR, Nika K, Cohnen A, Feller SM, Simister PC, Molder KC, Cordoba SP, Dushek O, Malissen B, Acuto O., EMBO J 34(3), 2015
PMID: 25535246
Quantitative proteomics analysis of signalosome dynamics in primary T cells identifies the surface receptor CD6 as a Lat adaptor-independent TCR signaling hub.
Roncagalli R, Hauri S, Fiore F, Liang Y, Chen Z, Sansoni A, Kanduri K, Joly R, Malzac A, Lähdesmäki H, Lahesmaa R, Yamasaki S, Saito T, Malissen M, Aebersold R, Gstaiger M, Malissen B., Nat Immunol 15(4), 2014
PMID: 24584089
[Immunological synapse is a dynamic signaling platform for T cell activation].
Bouchet J, Alcover A., Med Sci (Paris) 30(6-7), 2014
PMID: 25014458
Integrative biology of T cell activation.
Malissen B, Grégoire C, Malissen M, Roncagalli R., Nat Immunol 15(9), 2014
PMID: 25137453
Hematopoietic progenitor kinase 1 (HPK1) is required for LFA-1-mediated neutrophil recruitment during the acute inflammatory response.
Jakob SM, Pick R, Brechtefeld D, Nussbaum C, Kiefer F, Sperandio M, Walzog B., Blood 121(20), 2013
PMID: 23460610
A new look at T cell receptor signaling to nuclear factor-κB.
Paul S, Schaefer BC., Trends Immunol 34(6), 2013
PMID: 23474202
SLP-76 sterile α motif (SAM) and individual H5 α helix mediate oligomer formation for microclusters and T-cell activation.
Liu H, Thaker YR, Stagg L, Schneider H, Ladbury JE, Rudd CE., J Biol Chem 288(41), 2013
PMID: 23935094
Attenuation of T cell receptor signaling by serine phosphorylation-mediated lysine 30 ubiquitination of SLP-76 protein.
Wang X, Li JP, Chiu LL, Lan JL, Chen DY, Boomer J, Tan TH., J Biol Chem 287(41), 2012
PMID: 22902619
Sequential phosphorylation of SLP-76 at tyrosine 173 is required for activation of T and mast cells.
Sela M, Bogin Y, Beach D, Oellerich T, Lehne J, Smith-Garvin JE, Okumura M, Starosvetsky E, Kosoff R, Libman E, Koretzky G, Kambayashi T, Urlaub H, Wienands J, Chernoff J, Yablonski D., EMBO J 30(15), 2011
PMID: 21725281
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
The kinase GLK controls autoimmunity and NF-κB signaling by activating the kinase PKC-θ in T cells.
Chuang HC, Lan JL, Chen DY, Yang CY, Chen YM, Li JP, Huang CY, Liu PE, Wang X, Tan TH., Nat Immunol 12(11), 2011
PMID: 21983831
Release of serine/threonine-phosphorylated adaptors from signaling microclusters down-regulates T cell activation.
Lasserre R, Cuche C, Blecher-Gonen R, Libman E, Biquand E, Danckaert A, Yablonski D, Alcover A, Di Bartolo V., J Cell Biol 195(5), 2011
PMID: 22105350
Coordination of receptor signaling in multiple hematopoietic cell lineages by the adaptor protein SLP-76.
Jordan MS, Koretzky GA., Cold Spring Harb Perspect Biol 2(4), 2010
PMID: 20452948
SH2 domain containing leukocyte phosphoprotein of 76-kDa (SLP-76) feedback regulation of ZAP-70 microclustering.
Liu H, Purbhoo MA, Davis DM, Rudd CE., Proc Natl Acad Sci U S A 107(22), 2010
PMID: 20534575
The LAT story: a tale of cooperativity, coordination, and choreography.
Balagopalan L, Coussens NP, Sherman E, Samelson LE, Sommers CL., Cold Spring Harb Perspect Biol 2(8), 2010
PMID: 20610546
Cytoskeletal cross-talk in the control of T cell antigen receptor signaling.
Lasserre R, Alcover A., FEBS Lett 584(24), 2010
PMID: 20828561
Understanding signal integration through targeted mutations of an adapter protein.
Zou T, May RM, Koretzky GA., FEBS Lett 584(24), 2010
PMID: 20965179
HPK1 competes with ADAP for SLP-76 binding and via Rap1 negatively affects T-cell adhesion.
Patzak IM, Königsberger S, Suzuki A, Mak TW, Kiefer F., Eur J Immunol 40(11), 2010
PMID: 20957749
T cell activation.
Smith-Garvin JE, Koretzky GA, Jordan MS., Annu Rev Immunol 27(), 2009
PMID: 19132916
SLP-65 phosphorylation dynamics reveals a functional basis for signal integration by receptor-proximal adaptor proteins.
Oellerich T, Grønborg M, Neumann K, Hsiao HH, Urlaub H, Wienands J., Mol Cell Proteomics 8(7), 2009
PMID: 19372136
Phosphorylation of CARMA1 by HPK1 is critical for NF-kappaB activation in T cells.
Brenner D, Brechmann M, Röhling S, Tapernoux M, Mock T, Winter D, Lehmann WD, Kiefer F, Thome M, Krammer PH, Arnold R., Proc Natl Acad Sci U S A 106(34), 2009
PMID: 19706536
Function, regulation and pathological roles of the Gab/DOS docking proteins.
Wöhrle FU, Daly RJ, Brummer T., Cell Commun Signal 7(), 2009
PMID: 19737390
Tailoring T-cell receptor signals by proximal negative feedback mechanisms.
Acuto O, Di Bartolo V, Michel F., Nat Rev Immunol 8(9), 2008
PMID: 18728635
Compartmentalization of ITAM and integrin signaling by adapter molecules.
Bezman N, Koretzky GA., Immunol Rev 218(), 2007
PMID: 17624941
Antigen receptor signaling: the Tuscan connection.
Baldari CT, Koretzky GA., Nat Immunol 8(8), 2007
PMID: 17641655
In vivo disruption of T cell development by expression of a dominant-negative polypeptide designed to abolish the SLP-76/Gads interaction.
Jordan MS, Maltzman JS, Kliche S, Shabason J, Smith JE, Obstfeld A, Schraven B, Koretzky GA., Eur J Immunol 37(10), 2007
PMID: 17823979

47 References

Daten bereitgestellt von Europe PubMed Central.

Signal transduction by the TCR for antigen.
Kane LP, Lin J, Weiss A., Curr. Opin. Immunol. 12(3), 2000
PMID: 10781399
HPK1 is activated by lymphocyte antigen receptors and negatively regulates AP-1.
Liou J, Kiefer F, Dang A, Hashimoto A, Cobb MH, Kurosaki T, Weiss A., Immunity 12(4), 2000
PMID: 10795738
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
The Ste20 group kinases as regulators of MAP kinase cascades.
Dan I, Watanabe NM, Kusumi A., Trends Cell Biol. 11(5), 2001
PMID: 11316611
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
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
T cell receptor ligation induces the formation of dynamically regulated signaling assemblies.
Bunnell SC, Hong DI, Kardon JR, Yamazaki T, McGlade CJ, Barr VA, Samelson LE., J. Cell Biol. 158(7), 2002
PMID: 12356870
Progressive differentiation and selection of the fittest in the immune response.
Lanzavecchia A, Sallusto F., Nat. Rev. Immunol. 2(12), 2002
PMID: 12461571
Adaptors as central mediators of signal transduction in immune cells.
Jordan MS, Singer AL, Koretzky GA., Nat. Immunol. 4(2), 2003
PMID: 12555096
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), 2002
PMID: 12501243
Synergistic assembly of linker for activation of T cells signaling protein complexes in T cell plasma membrane domains.
Hartgroves LC, Lin J, Langen H, Zech T, Weiss A, Harder T., J. Biol. Chem. 278(22), 2003
PMID: 12646565
An epigenetic view of helper T cell differentiation.
Ansel KM, Lee DU, Rao A., Nat. Immunol. 4(7), 2003
PMID: 12830136
CD28-mediated co-stimulation: a quantitative support for TCR signalling.
Acuto O, Michel F., Nat. Rev. Immunol. 3(12), 2003
PMID: 14647476
Binding specificity of multiprotein signaling complexes is determined by both cooperative interactions and affinity preferences.
Houtman JC, Higashimoto Y, Dimasi N, Cho S, Yamaguchi H, Bowden B, Regan C, Malchiodi EL, Mariuzza R, Schuck P, Appella E, Samelson LE., Biochemistry 43(14), 2004
PMID: 15065860
Recruitment of the actin-binding protein HIP-55 to the immunological synapse regulates T cell receptor signaling and endocytosis.
Le Bras S, Foucault I, Foussat A, Brignone C, Acuto O, Deckert M., J. Biol. Chem. 279(15), 2004
PMID: 14729663
Fine-tuning lymphocyte regulation: what's new with tyrosine kinases and phosphatases?
Cannons JL, Schwartzberg PL., Curr. Opin. Immunol. 16(3), 2004
PMID: 15134778
Negative feedback loop in T-cell activation through MAPK-catalyzed threonine phosphorylation of LAT.
Matsuda S, Miwa Y, Hirata Y, Minowa A, Tanaka J, Nishida E, Koyasu S., EMBO J. 23(13), 2004
PMID: 15192708
14-3-3 proteins: a historic overview.
Aitken A., Semin. Cancer Biol. 16(3), 2006
PMID: 16678438
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), 2006
PMID: 17115060
E3 ubiquitin ligases as T cell anergy factors.
Mueller DL., Nat. Immunol. 5(9), 2004
PMID: 15334084
Molecular cloning of SLP-76, a 76-kDa tyrosine phosphoprotein associated with Grb2 in T cells.
Jackman JK, Motto DG, Sun Q, Tanemoto M, Turck CW, Peltz GA, Koretzky GA, Findell PR., J. Biol. Chem. 270(13), 1995
PMID: 7706237
Inhibition of phosphatidylinositol 3-kinase activity by association with 14-3-3 proteins in T cells.
Bonnefoy-Berard N, Liu YC, von Willebrand M, Sung A, Elly C, Mustelin T, Yoshida H, Ishizaka K, Altman A., Proc. Natl. Acad. Sci. U.S.A. 92(22), 1995
PMID: 7479742
Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels.
Shevchenko A, Wilm M, Vorm O, Mann M., Anal. Chem. 68(5), 1996
PMID: 8779443
Activation-modulated association of 14-3-3 proteins with Cbl in T cells.
Liu YC, Elly C, Yoshida H, Bonnefoy-Berard N, Altman A., J. Biol. Chem. 271(24), 1996
PMID: 8663231
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
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
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
LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation.
Zhang W, Sloan-Lancaster J, Kitchen J, Trible RP, Samelson LE., Cell 92(1), 1998
PMID: 9489702
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
Sequence tag scanning: a new explorative strategy for recognition of unexpected protein alterations by nanoelectrospray ionization-tandem mass spectrometry.
Salek M, Di Bartolo V, Cittaro D, Borsotti D, Wei J, Acuto O, Rappsilber J, Lehmann WD., Proteomics 5(3), 2005
PMID: 15714472
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
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
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
SLP76 and SLP65: complex regulation of signalling in lymphocytes and beyond.
Koretzky GA, Abtahian F, Silverman MA., Nat. Rev. Immunol. 6(1), 2006
PMID: 16493428
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