Quantitative proteomics analysis of signalosome dynamics in primary T cells identifies the surface receptor CD6 as a Lat adaptor-independent TCR signaling hub

Nature Immunology

Volumn 15, Issue 4, 2014, Pages 384-392

  Roncagalli, Romain ^a   Hauri, Simon ^b   Fiore, Fréderic ^c   Liang, Yinming ^a   Chen, Zhi ^d   Sansoni, Amandine ^c   Kanduri, Kartiek ^d   Joly, Rachel ^a   Malzac, Aurélie ^a   Lähdesmäki, Harri ^d,e   Lahesmaa, Riitta ^d   Yamasaki, Sho ^f   Saito, Takashi ^g   Malissen, Marie ^a   Aebersold, Ruedi ^b,h   Gstaiger, Matthias ^b   Malissen, Bernard ^a,c  

^a CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^b ETH ZURICH   (Switzerland)

^c Aix Marseille University UMS3367   (France)

^d TURKU CENTRE FOR BIOTECHNOLOGY   (Finland)

^e AALTO UNIVERSITY   (Finland)

^f KYUSHU UNIVERSITY   (Japan)

^g RIKEN Center for Integrative Medical Sciences   (Japan)

^h UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CD6 ANTIGEN; CELL SURFACE RECEPTOR; LAT PROTEIN; PROTEIN KINASE ZAP 70; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; COMPLEX FORMATION; CONTROLLED STUDY; GENE TARGETING; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEOMICS; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; CALCIUM SIGNALING; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MULTIPROTEIN COMPLEXES; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEOMICS; PROTO-ONCOGENE PROTEINS C-VAV; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTE SUBSETS; ZAP-70 PROTEIN-TYROSINE KINASE;

EID: 84897046940     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2843     Document Type: Article

References (53)

1. Balagopalan, L., Coussens, N.P., Sherman, E., Samelson, L.E. & Sommers, C.L. The LAT story: A tale of cooperativity, coordination, and choreography. Cold Spring Harb. Perspect. Biol. 2, a005512 (2010.
2. Roncagalli, R., Mingueneau, M., Gregoire, C., Malissen, M. & Malissen, B. LAT signaling pathology: An autoimmune' condition without T cell self-reactivity. Trends Immunol. 31, 253-259 (2010.
3. Sommers, C.L. et al. A LAT mutation that inhibits T cell development yet induces lymphoproliferation. Science 296, 2040-2043 (2002.
4. Mingueneau, M. et al. Loss of the LAT adaptor converts antigen-responsive T cells into pathogenic effectors that function independently of the T cell receptor. Immunity 31, 197-208 (2009.
5. Chuck, M.I., Zhu, M., Shen, S. & Zhang, W. The role of the LAT-PLC-γ1 interaction in T regulatory cell function. J. Immunol. 184, 2476-2486 (2010.
6. Ou-Yang, C.W. et al. Role of LAT in the granule-mediated cytotoxicity of CD8 T cells. Mol. Cell. Biol. 32, 2674-2684 (2012.
7. Zheng, Y. et al. Temporal regulation of EGF signalling networks by the scaffold protein Shc1. Nature 499, 166-171 (2013.
8. Glatter, T., Wepf, A., Aebersold, R. & Gstaiger, M. An integrated workflow for charting the human interaction proteome: Insights into the PP2A system. Mol. Syst. Biol. 5, 237 (2009.
9. Varjosalo, M. et al. Interlaboratory reproducibility of large-scale human protein-complex analysis by standardized AP-MS. Nat. Methods 10, 307-314 (2013.
10. Mayya, V. et al. Quantitative phosphoproteomic analysis of T cell receptor signaling reveals system-wide modulation of protein-protein interactions. Sci. Signal. 2, ra46 (2009.
11. Mbonye, U.R. et al. Phosphorylation of CDK9 at Ser175 enhances HIV transcription and is a marker of activated P-TEFb in CD4+ T lymphocytes. PLoS Pathog. 9, e1003338 (2013.
12. Astoul, E., Edmunds, C., Cantrell, D.A. & Ward, S.G. PI 3-K and T-cell activation: Limitations of T-leukemic cell lines as signaling models. Trends Immunol. 22, 490-496 (2001.
13. Junttila, M.R., Saarinen, S., Schmidt, T., Kast, J. & Westermarck, J. Single-step Strep-Tag purification for the isolation and identification of protein complexes from mammalian cells. Proteomics 5, 1199-1203 (2005.
14. Secrist, J.P., Burns, L.A., Karnitz, L., Koretzky, G.A. & Abraham, R.T. Stimulatory effects of the protein tyrosine phosphatase inhibitor, pervanadate, on T-cell activation events. J. Biol. Chem. 268, 5886-5893 (1993.
15. Carvalho, P.C., Hewel, J., Barbosa, V.C. & Yates, J.R. III. Identifying differences in protein expression levels by spectral counting and feature selection. Genet. Mol. Res. 7, 342-356 (2008.
16. Harkiolaki, M. et al. Structural basis for SH3 domain-mediated high-Affinity binding between Mona/Gads and SLP-76. EMBO J. 22, 2571-2582 (2003.
17. Di Bartolo, V. 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. 204, 681-691 (2007.
18. Lasserre, R. et al. Release of serine/threonine-phosphorylated adaptors from signaling microclusters down-regulates T cell activation. J. Cell Biol. 195, 839-853 (2011.
19. Evans, R., Lellouch, A.C., Svensson, L., McDowall, A. & Hogg, N. The integrin LFA-1 signals through ZAP-70 to regulate expression of high-Affinity LFA-1 on T lymphocytes. Blood 117, 3331-3342 (2011.
20. Salmerón, A. et al. Transferrin receptor induces tyrosine phosphorylation in T cells and is physically associated with the TCR ζ-chain. J. Immunol. 154, 1675-1683 (1995.
21. Kobarg, J., Whitney, G.S., Palmer, D., Aruffo, A. & Bowen, M.A. Analysis of the tyrosine phosphorylation and calcium fluxing of human CD6 isoforms with different cytoplasmatic domains. Eur. J. Immunol. 27, 2971-2980 (1997.
22. Wee, S. et al. Tyrosine phosphorylation of CD6 by stimulation of CD3: Augmentation by the CD4 and CD2 coreceptors. J. Exp. Med. 177, 219-223 (1993.
23. Hassan, N.J. et al. CD6 regulates T-cell responses through activation-dependent recruitment of the positive regulator SLP-76. Mol. Cell. Biol. 26, 6727-6738 (2006.
24. Williams, B.L. et al. Genetic evidence for differential coupling of Syk family kinases to the T-cell receptor: Reconstitution studies in a ZAP-70-deficient Jurkat T-cell line. Mol. Cell. Biol. 18, 1388-1399 (1998.
25. Finco, T.S., Kadlecek, T., Zhang, W., Samelson, L.E. & Weiss, A. LAT is required for TCR-mediated activation of PLCγ1 and the Ras pathway. Immunity 9, 617-626 (1998.
26. Letourneur, F. & Klausner, R.D. Activation of T cells by a tyrosine kinase activation domain in the cytoplasmic tail of CD3ε. Science 255, 79-82 (1992.
27. Wegener, A.M. et al. The T cell receptor/CD3 complex is composed of at least two autonomous transduction modules. Cell 68, 83-95 (1992.
28. Irving, B.A., Chan, A.C. & Weiss, A. Functional characterization of a signal transducing motif present in the T cell antigen receptor ζ chain. J. Exp. Med. 177, 1093-1103 (1993.
29. Gimferrer, I. et al. Relevance of CD6-mediated interactions in T cell activation and proliferation. J. Immunol. 173, 2262-2270 (2004.
30. Zimmerman, A.W. et al. Long-Term engagement of CD6 and ALCAM is essential for T-cell proliferation induced by dendritic cells. Blood 107, 3212-3220 (2006.
31. Oliveira, M.I. et al. CD6 attenuates early and late signaling events, setting thresholds for T-cell activation. Eur. J. Immunol. 42, 195-205 (2012.
32. Wakamatsu, E., Mathis, D. & Benoist, C. Convergent and divergent effects of costimulatory molecules in conventional and regulatory CD4+ T cells. Proc. Natl. Acad. Sci. USA 110, 1023-1028 (2013.
33. Diehn, M. et al. Genomic expression programs and the integration of the CD28 costimulatory signal in T cell activation. Proc. Natl. Acad. Sci. USA 99, 11796-11801 (2002.
34. Ibáñez, A. et al. Mitogen-Activated protein kinase pathway activation by the CD6 lymphocyte surface receptor. J. Immunol. 177, 1152-1159 (2006.
35. Ménasché, G. et al. RIAM links the ADAP/SKAP-55 signaling module to Rap1, facilitating T-cell-receptor-mediated integrin activation. Mol. Cell. Biol. 27, 4070-4081 (2007.
36. Burdette, D.L. & Vance, R.E. STING and the innate immune response to nucleic acids in the cytosol. Nat. Immunol. 14, 19-26 (2013.
37. Hassan, N.J., Barclay, A.N. & Brown, M.H. Frontline: Optimal T cell activation requires the engagement of CD6 and CD166. Eur. J. Immunol. 34, 930-940 (2004.
38. De Jager, P.L. et al. Meta-Analysis of genome scans and replication identify CD6, IRF8 and TNFRSF1A as new multiple sclerosis susceptibility loci. Nat. Genet. 41, 776-782 (2009.
39. Kofler, D.M., Severson, C.A., Mousissian, N., De Jager, P.L. & Hafler, D.A. The CD6 multiple sclerosis susceptibility allele is associated with alterations in CD4+ T cell proliferation. J. Immunol. 187, 3286-3291 (2011.
40. Grégoire, C. et al. Deletion of the LIME adaptor protein minimally affects T and B cell development and function. Eur. J. Immunol. 37, 3259-3269 (2007.
41. May, R.M. et al. Murine natural killer immunoreceptors use distinct proximal signaling complexes to direct cell function. Blood 121, 3135-3146 (2013.
42. Mingueneau, M. et al. The proline-rich sequence of CD3ε controls T cell antigen receptor expression on and signaling potency in preselection CD4+CD8+ thymocytes. Nat. Immunol. 9, 522-532 (2008.
43. Zhang, Y., Muyrers, J.P., Testa, G. & Stewart, A.F. DNA cloning by homologous recombination in Escherichia coli. Nat. Biotechnol. 18, 1314-1317 (2000.
44. Köntgen, F., Suss, G., Stewart, C., Steinmetz, M. & Bluethmann, H. Targeted disruption of the MHC class II Aa gene in C57BL/6 mice. Int. Immunol. 5, 957-964 (1993.
45. Pettitt, S.J. et al. Agouti C57BL/6N embryonic stem cells for mouse genetic resources. Nat. Methods 6, 493-495 (2009.
46. Malissen, M. et al. Altered T cell development in mice with a targeted mutation of the CD3-ε gene. EMBO J. 14, 4641-4653 (1995.
47. Craig, R. & Beavis, R.C. TANDEM: Matching proteins with tandem mass spectra. Bioinformatics 20, 1466-1467 (2004.
48. Deutsch, E.W. et al. A guided tour of the Trans-Proteomic Pipeline. Proteomics 10, 1150-1159 (2010.
49. Fermin, D., Basrur, V., Yocum, A.K. & Nesvizhskii, A.I. Abacus: A computational tool for extracting and pre-processing spectral count data for label-free quantitative proteomic analysis. Proteomics 11, 1340-1345 (2011.
50. Donnadieu, E. et al. Reconstitution of CD3ζ coupling to calcium mobilization via genetic complementation. J. Biol. Chem. 269, 32828-32834 (1994.
51. Irizarry, R.A. et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264 (2003.
52. Lee, H.J. et al. Direct transfer of a-synuclein from neuron to astroglia causes inflammatory responses in synucleinopathies. J. Biol. Chem. 285, 9262-9272 (2010.
53. Smyth, G.K. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, 1-29 (2004.