De novo phosphorylation and conformational opening of the tyrosine kinase Lck act in concert to initiate T cell receptor signaling

Science Signaling

Volumn 10, Issue 462, 2017, Pages

  Philipsen, Lars ^a   Reddycherla, Amarendra V ^a   Hartig, Roland ^a   Gumz, Janine ^a   Kästle, Matthias ^a   Kritikos, Andreas ^a   Poltorak, Mateusz P ^a   Prokazov, Yury ^b   Turbin, Evgeny ^b   Weber, André ^b   Zuschratter, Werner ^b   Schraven, Burkhart ^a,c   Simeoni, Luca ^a   Müller, Andreas J ^a,c  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^c HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE LCK; T LYMPHOCYTE RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR; TYROSINE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOFLUORESCENCE MICROSCOPY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; WESTERN BLOTTING; CELL CULTURE; CELL MEMBRANE; CHEMISTRY; CONFOCAL MICROSCOPY; FLUORESCENCE MICROSCOPY; GENETICS; JURKAT CELL LINE; LYMPHOCYTE ACTIVATION; METABOLISM; MUTATION; PHOSPHORYLATION; T LYMPHOCYTE;

BLOTTING, WESTERN; CELL MEMBRANE; CELLS, CULTURED; HUMANS; JURKAT CELLS; LYMPHOCYTE ACTIVATION; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MUTATION; PHOSPHORYLATION; PROTEIN CONFORMATION; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TYROSINE;

EID: 85010628553     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.aaf4736     Document Type: Article

References (42)

1. T. J. Molina, K. Kishihara, D. P. Siderovski, W. van Ewijk, A. Narendran, E. Timms, A. Wakeham, C. J. Paige, K.-U. Hartmann, A. Veillette, D. Davidson, T. W. Mak, Profound block in thymocyte development in mice lacking p56lck. Nature 357, 161-164 (1992).
2. B. Seddon, G. Legname, P. Tomlinson, R. Zamoyska, Long-term survival but impaired homeostatic proliferation of naïve T cells in the absence of p56lck. Science 290, 127-131 (2000).
3. M. A. Goldsmith, A. Weiss, Isolation and characterization of a T-lymphocyte somatic mutant with altered signal transduction by the antigen receptor. Proc. Natl. Acad. Sci. U.S.A. 84, 6879-6883 (1987).
4. J. E. Smith-Garvin, G. A. Koretzky, M. S. Jordan, T cell activation. Annu. Rev. Immunol. 27, 591-619 (2009).
5. K. Nika, C. Soldani, M. Salek, W. Paster, A. Gray, R. Etzensperger, L. Fugger, P. Polzella, V. Cerundolo, O. Dushek, T. Höfer, A. Viola, O. Acuto, Constitutively active Lck kinase in T cells drives antigen receptor signal transduction. Immunity 32, 766-777 (2010).
6. A. Stirnweiss, R. Hartig, S. Gieseler, J. A. Lindquist, P. Reichardt, L. Philipsen, L. Simeoni, M. Poltorak, C. Merten, W. Zuschratter, Y. Prokazov, W. Paster, H. Stockinger, T. Harder, M. Gunzer, B. Schraven, T cell activation results in conformational changes in the Src family kinase Lck to induce its activation. Sci. Signal. 6, ra13 (2013).
7. O. Ballek, J. Vale?ka, J. Manning, D. Filipp, The pool of preactivated Lck in the initiation of T-cell signaling: A critical re-evaluation of the Lck standby model. Immunol. Cell Biol. 93, 384-395 (2015).
8. A. L. Burkhardt, B. Stealey, R. B. Rowley, S. Mahajan, M. Prendergast, J. Fargnoli, J. B. Bolen, Temporal regulation of non-transmembrane protein tyrosine kinase enzyme activity following T cell antigen receptor engagement. J. Biol. Chem. 269, 23642-23647 (1994).
9. E. H. Palacios, A. Weiss, Function of the Src-family kinases, Lck and Fyn, in T-cell development and activation. Oncogene 23, 7990-8000 (2004).
10. M. Bergman, T. Mustelin, C. Oetken, J. Partanen, N. A. Flint, K. E. Amrein, M. Autero, P. Burn, K. Alitalo, The human p50csk tyrosine kinase phosphorylates p56lck at Tyr-505 and down regulates its catalytic activity. EMBO J. 11, 2919-2924 (1992).
11. W. Xu, A. Doshi, M. Lei, M. J. Eck, S. C. Harrison, Crystal structures of c-Src reveal features of its autoinhibitory mechanism. Mol. Cell 3, 629-638 (1999).
12. W. Xu, S. C. Harrison, M. J. Eck, Three-dimensional structure of the tyrosine kinase c-Src. Nature 385, 595-602 (1997).
13. H. L. Ostergaard, D. A. Shackelford, T. R. Hurley, P. Johnson, R. Hyman, B. M. Sefton, I. S. Trowbridge, Expression of CD45 alters phosphorylation of the lck-encoded tyrosine protein kinase in murine lymphoma T-cell lines. Proc. Natl. Acad. Sci. U.S.A. 86, 8959-8963 (1989).
14. E. Hui, R. D. Vale, In vitro membrane reconstitution of the T-cell receptor proximal signaling network. Nat. Struct. Mol. Biol. 21, 133-142 (2014).
15. U. D'Oro, K. Sakaguchi, E. Appella, J. D. Ashwell, Mutational analysis of Lck in CD45-negative T cells: Dominant role of tyrosine 394 phosphorylation in kinase activity. Mol. Cell. Biol. 16, 4996-5003 (1996).
16. J. S. Hardwick, B. M. Sefton, Activation of the Lck tyrosine protein kinase by hydrogen peroxide requires the phosphorylation of Tyr-394. Proc. Natl. Acad. Sci. U.S.A. 92, 4527-4531 (1995).
17. H. Xu, D. R. Littman, The kinase-dependent function of Lck in T-cell activation requires an intact site for tyrosine autophosphorylation. Ann. N. Y. Acad. Sci. 766, 99-116 (1995).
18. A. Alonso, N. Bottini, S. Bruckner, S. Rahmouni, S. Williams, S. P. Schoenberger, T. Mustelin, Lck dephosphorylation at Tyr-394 and inhibition of T cell antigen receptor signaling by Yersinia phosphatase YopH. J. Biol. Chem. 279, 4922-4928 (2004).
19. W. Paster, C. Paar, P. Eckerstorfer, A. Jakober, K. Drbal, G. J. Schütz, A. Sonnleitner, H. Stockinger, Genetically encoded Förster resonance energy transfer sensors for the conformation of the Src family kinase Lck. J. Immunol. 182, 2160-2167 (2009).
20. J. Goedhart, D. von Stetten, M. Noirclerc-Savoye, M. Lelimousin, L. Joosen, M. A. Hink, L. van Weeren, T. W. J. Gadella Jr., A. Royant, Structure-guided evolution of cyan fluorescent proteins towards a quantum yield of 93%. Nat. Commun. 3, 751 (2012).
21. G.-J. Kremers, J. Goedhart, E. B. van Munster, T. W. J. Gadella Jr., Cyan and yellow super fluorescent proteins with improved brightness, protein folding, and FRET Förster radius. Biochemistry 45, 6570-6580 (2006).
22. S. C. Ley, M. Marsh, C. R. Bebbington, K. Proudfoot, P. Jordan, Distinct intracellular localization of Lck and Fyn protein tyrosine kinases in human T lymphocytes. J. Cell Biol. 125, 639-649 (1994).
23. O. Anton, A. Batista, J. Millán, L. Andrés-Delgado, R. Puertollano, I. Correas, M. A. Alonso, An essential role for the MAL protein in targeting Lck to the plasma membrane of human T lymphocytes. J. Exp. Med. 205, 3201-3213 (2008).
24. J. H. Hanke, J. P. Gardner, R. L. Dow, P. S. Changelian, W. H. Brissette, E. J. Weringer, B. A. Pollok, P. A. Connelly, Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck-and FynT-dependent T cell activation. J. Biol. Chem. 271, 695-701 (1996).
25. V. Imbert, J. F. Peyron, D. Farahi Far, B. Mari, P. Auberger, B. Rossi, Induction of tyrosine phosphorylation and T-cell activation by vanadate peroxide, an inhibitor of protein tyrosine phosphatases. Biochem. J. 297 (Pt. 1), 163-173 (1994).
26. A. M. Nyakeriga, H. Garg, A. Joshi, TCR-induced T cell activation leads to simultaneous phosphorylation at Y505 and Y394 of p56lck residues. Cytometry 81A, 797-805 (2012).
27. S. Dornan, Z. Sebestyen, J. Gamble, P. Nagy, A. Bodnar, L. Alldridge, S. Doe, N. Holmes, L. K. Goff, P. Beverley, J. Szollosi, D. R. Alexander, Differential association of CD45 isoforms with CD4 and CD8 regulates the actions of specific pools of p56lck tyrosine kinase in T cell antigen receptor signal transduction. J. Biol. Chem. 277, 1912-1918 (2002).
28. H. D. Moreau, F. Lemaître, E. Terriac, G. Azar, M. Piel, A.-M. Lennon-Dumenil, P. Bousso, Dynamic in situ cytometry uncovers T cell receptor signaling during immunological synapses and kinapses in vivo. Immunity 37, 351-363 (2012).
29. M. Jose, D. K. Nair, C. Reissner, R. Hartig, W. Zuschratter, Photophysics of Clomeleon by FLIM: Discriminating excited state reactions along neuronal development. Biophys. J. 92, 2237-2254 (2007).
30. S. P. Laptenok, J. W. Borst, K. M. Mullen, I. H. M. van Stokkum, A. J. W. G. Visser, H. van Amerongen, Global analysis of Förster resonance energy transfer in live cells measured by fluorescence lifetime imaging microscopy exploiting the rise time of acceptor fluorescence. Phys. Chem. Chem. Phys. 12, 7593-7602 (2010).
31. M. Millington, G. J. Grindlay, K. Altenbach, R. K. Neely, W. Kolch, M. Ben?ina, N. D. Read, A. C. Jones, D. T. F. Dryden, S. W. Magennis, High-precision FLIM-FRET in fixed and living cells reveals heterogeneity in a simple CFP-YFP fusion protein. Biophys. Chem. 127, 155-164 (2007).
32. D. K. Nair, M. Jose, T. Kuner, W. Zuschratter, R. Hartig, FRET-FLIM at nanometer spectral resolution from living cells. Opt. Express 14, 12217-12229 (2006).
33. A. J. W. G. Visser, S. P. Laptenok, N. V. Visser, A. van Hoek, D. J. S. Birch, J.-C. Brochon, J. W. Borst, Time-resolved FRET fluorescence spectroscopy of visible fluorescent protein pairs. Eur. Biophys. J. 39, 241-253 (2010).
34. J. Rossy, D. M. Owen, D. J. Williamson, Z. Yang, K. Gaus, Conformational states of the kinase Lck regulate clustering in early T cell signaling. Nat. Immunol. 14, 82-89 (2013).
35. A. Weiss, J. Imboden, D. Shoback, J. Stobo, Role of T3 surface molecules in human T-cell activation: T3-dependent activation results in an increase in cytoplasmic free calcium. Proc. Natl. Acad. Sci. U.S.A. 81, 4169-4173 (1984).
36. S. Swift, J. Lorens, P. Achacoso, G. P. Nolan, Rapid production of retroviruses for efficient gene delivery to mammalian cells using 293T cell-based systems. Curr. Protoc. Immunol. Chapter 10, Unit 10.17C (2001).
37. S. Mizushima, S. Nagata, pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res. 18, 5322 (1990).
38. R. Hartig, Y. Prokazov, E. Turbin, W. Zuschratter, Wide-field fluorescence lifetime imaging with multi-anode detectors. Methods Mol. Biol. 1076, 457-480 (2014).
39. M. Vitali, F. Picazo, Y. Prokazov, A. Duci, E. Turbin, C. Götze, J. Llopis, R. Hartig, A. J. W. G. Visser, W. Zuschratter, Wide-Field Multi-Parameter FLIM: Long-term minimal invasive observation of proteins in living cells. PLOS ONE 6, e15820 (2011).
40. J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, A. Cardona, Fiji: An open-source platform for biological-image analysis. Nat. Methods 9, 676-682 (2012).
41. M. A. Young, S. Gonfloni, G. Superti-Furga, B. Roux, J. Kuriyan, Dynamic coupling between the SH2 and SH3 domains of c-Src and Hck underlies their inactivation by C-terminal tyrosine phosphorylation. Cell 105, 115-126 (2001).
42. J. A. Moroco, J. K. Craigo, R. E. Iacob, T. E. Wales, J. R. Engen, T. E. Smithgall, Differential sensitivity of Src-family kinases to activation by SH3 domain displacement. PLOS ONE 9, e105629 (2014).