Themis1 enhances T cell receptor signaling during thymocyte development by promoting Vav1 activity and Grb2 stability

Science Signaling

Volumn 9, Issue 428, 2016, Pages

  Zvezdova, Ekaterina ^a   Mikolajczak, Judith ^b,c,d,e   Garreau, Anne ^b,c,d,e   Marcellin, Marlène ^e   Rigal, Lise ^b,c,d,e   Lee, Jan ^a   Choi, Seeyoung ^a   Blaize, Gaëtan ^b,c,d,e   Argenty, Jérémy ^b,c,d,e   Familiades, Julien ^b,c,d,e   Li, Liqi ^a   De Peredo, Anne Gonzalez ^e   Burlet Schiltz, Odile ^e   Love, Paul E ^a   Lesourne, Renaud ^b,c,d,e  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b University of Toulouse III   (France)

^c INSERM   (France)

^d CNRS   (France)

^e UNIVERSITÉ PAUL SABATIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD5 ANTIGEN; CD69 ANTIGEN; CD8 ANTIGEN; GRAP2 PROTEIN; GREEN FLUORESCENT PROTEIN; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; LAT PROTEIN; LIGAND; LIS1 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; NUCLEAR RECEPTOR NUR77; PERVANADATE; PROTEIN; PROTEIN KINASE ZAP 70; SHP 2 INTERACTING TRANSMEMBRANE ADAPTOR PROTEIN; T LYMPHOCYTE RECEPTOR; THEMIS1 PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VAV1 PROTEIN; GRB2 PROTEIN, MOUSE; LYMPHOCYTE ANTIGEN RECEPTOR; NEUROPEPTIDE; PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE SHP 1; PTPN6 PROTEIN, MOUSE; RAC1 PROTEIN; RAC1 PROTEIN, MOUSE; THEMIS PROTEIN, MOUSE; VAV PROTEIN; VAV1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ISOLATION; CELL MATURATION; CELL SURFACE; CONTROLLED STUDY; CROSS LINKING; FLOW CYTOMETRY; GENE OVEREXPRESSION; HAPLOINSUFFICIENCY; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN SYNTHESIS; PROTEOMICS; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; THYMOCYTE; THYMUS; TURNOVER TIME; WESTERN BLOTTING; WILD TYPE; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PROCEDURES; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; CELL DIFFERENTIATION; GRB2 ADAPTOR PROTEIN; LYMPHOCYTE ACTIVATION; MICE; MICE, TRANSGENIC; NEUROPEPTIDES; PHOSPHORIC MONOESTER HYDROLASES; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 6; PROTEINS; PROTEOMICS; PROTO-ONCOGENE PROTEINS C-VAV; RAC1 GTP-BINDING PROTEIN; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; THYMOCYTES; TRANSGENES;

EID: 84969802775     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.aad1576     Document Type: Article

References (47)

1. J. N. Mandl, J. P. Monteiro, N. Vrisekoop, R. N. Germain, T cell-positive selection uses self-ligand binding strength to optimize repertoire recognition of foreign antigens. Immunity 38, 263-274 (2013).
2. G. Fu, S. Vallée, V. Rybakin, M. V. McGuire, J. Ampudia, C. Brockmeyer, M. Salek, P. R. Fallen, J. A. H. Hoerter, A. Munshi, Y. H. Huang, J. Hu, H. S. Fox, K. Sauer, O. Acuto, N. R. J. Gascoigne, Themis controls thymocyte selection through regulation of T cell antigen receptor-mediated signaling. Nat. Immunol. 10, 848-856 (2009).
3. A. L. Johnson, L. Aravind, N. Shulzhenko, A. Morgun, S.-Y. Choi, T. L. Crockford, T. Lambe, H. Domaschenz, E. M. Kucharska, L. Zheng, C. G. Vinuesa, M. J. Lenardo, C. C. Goodnow, R. J. Cornall, R. H. Schwartz, Themis is a member of a new metazoan gene family and is required for the completion of thymocyte positive selection. Nat. Immunol. 10, 831-839 (2009).
4. K. Kakugawa, T. Yasuda, I. Miura, A. Kobayashi, H. Fukiage, R. Satoh, M. Matsuda, H. Koseki, S. Wakana, H. Kawamoto, H. Yoshida, A novel gene essential for the development of single positive thymocytes. Mol. Cell. Biol. 29, 5128-5135 (2009).
5. R. Lesourne, S. Uehara, J. Lee, K.-D. Song, L. Li, J. Pinkhasov, Y. Zhang, N.-P. Weng, K. F. Wildt, L. Wang, R. Bosselut, P. E. Love, Themis, a T cell-specific protein important for late thymocyte development. Nat. Immunol. 10, 840-847 (2009).
6. M. S. Patrick, H. Oda, K. Hayakawa, Y. Sato, K. Eshima, T. Kirikae, S.-i. Iemura, M. Shirai, T. Abe, T. Natsume, T. Sasazuki, H. Suzuki, Gasp, a Grb2-associating protein, is critical for positive selection of thymocytes. Proc. Natl. Acad. Sci. U.S.A. 106, 16345-16350 (2009).
7. W. Paster, C. Brockmeyer, G. Fu, P. C. Simister, B. de Wet, A. Martinez-Riaño, J. A. H. Hoerter, S. M. Feller, C. Wülfing, N. R. J. Gascoigne, O. Acuto, GRB2-mediated recruitment of THEMIS to LAT is essential for thymocyte development. J. Immunol. 190, 3749-3756 (2013).
8. C. Brockmeyer, W. Paster, D. Pepper, C. P. Tan, D. C. Trudgian, S. McGowan, G. Fu, N. R. J. Gascoigne, O. Acuto, M. Salek, T cell receptor (TCR)-induced tyrosine phosphorylation dynamics identifies THEMIS as a new TCR signalosome component. J. Biol. Chem. 286, 7535-7547 (2011).
9. R. Lesourne, E. Zvezdova, K.-D. Song, D. El-Khoury, S. Uehara, V. A. Barr, L. E. Samelson, P. E. Love, Interchangeability of Themis1 and Themis2 in thymocyte development reveals two related proteins with conserved molecular function. J. Immunol. 189, 1154-1161 (2012).
10. G. Fu, J. Casas, S. Rigaud, V. Rybakin, F. Lambolez, J. Brzostek, J. A. H. Hoerter, W. Paster, O. Acuto, H. Cheroutre, K. Sauer, N. R. J. Gascoigne, Themis sets the signal threshold for positive and negative selection in T-cell development. Nature 504, 441-445 (2013).
11. W. Paster, A. M. Bruger, K. Katsch, C. Grégoire, R. Roncagalli, G. Fu, N. R. J. Gascoigne, K. Nika, A. Cohnen, S. M. Feller, P. C. Simister, K. C. Molder, S.-P. Cordoba, O. Dushek, B. Malissen, O. Acuto, A THEMIS:SHP1 complex promotes T-cell survival. EMBO J. 34, 393-409 (2015).
12. K. G. Johnson, F. G. LeRoy, L. K. Borysiewicz, R. J. Matthews, TCR signaling thresholds regulating T cell development and activation are dependent upon SHP-1. J. Immunol. 162, 3802-3813 (1999).
13. D. R. Plas, C. B. Williams, G. J. Kersh, L. S. White, J. M. White, S. Paust, T. Ulyanova, P. M. Allen, M. L. Thomas, Cutting edge: The tyrosine phosphatase SHP-1 regulates thymocyte positive selection. J. Immunol. 162, 5680-5684 (1999).
14. J. Zhang, A.-K. Somani, D. Yuen, Y. Yang, P. E. Love, K. A. Siminovitch, Involvement of the SHP-1 tyrosine phosphatase in regulation of T cell selection. J. Immunol. 163, 3012-3021 (1999).
15. C. C. Fowler, L. I. Pao, J. N. Blattman, P. D. Greenberg, SHP-1 in T cells limits the production of CD8 effector cells without impacting the formation of long-lived central memory cells. J. Immunol. 185, 3256-3267 (2010).
16. reg and iNKT cell development demonstrated by a novel fluorescent reporter mouse. J. Exp. Med. 208, 1279-1289 (2011).
17. R. M. Siegel, M. Katsumata, T. Miyashita, D. C. Louie, M. I. Greene, J. C. Reed, Inhibition of thymocyte apoptosis and negative antigenic selection in bcl-2 transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 89, 7003-7007 (1992).
18. O. Williams, T. Norton, M. Halligey, D. Kioussis, H. J. M. Brady, The action of Bax and bcl-2 on T cell selection. J. Exp. Med. 188, 1125-1133 (1998).
19. L. F. Reynolds, L. A. Smyth, T. Norton, N. Freshney, J. Downward, D. Kioussis, V. L. J. Tybulewicz, Vav1 transduces T cell receptor signals to the activation of phospholipase C-γ1 via phosphoinositide 3-kinase-dependent and -independent pathways. J. Exp. Med. 195, 1103-1114 (2002).
20. A. Saveliev, L. Vanes, O. Ksionda, J. Rapley, S. J. Smerdon, K. Rittinger, V. L. J. Tybulewicz, Function of the nucleotide exchange activity of vav1 in T cell development and activation. Sci. Signal. 2, ra83 (2009).
21. J. Wu, D. G. Motto, G. A. Koretzky, A. Weiss, Vav and SLP-76 interact and functionally cooperate in IL-2 gene activation. Immunity 4, 593-602 (1996).
22. B. Aghazadeh, W. E. Lowry, X.-Y. Huang, M. K. Rosen, Structural basis for relief of autoinhibition of the Dbl homology domain of proto-oncogene Vav by tyrosine phosphorylation. Cell 102, 625-633 (2000).
23. S. P. Hehner, T. G. Hofmann, O. Dienz, W. Dröge, M. L. Schmitz, Tyrosine-phosphorylated Vav1 as a point of integration for T-cell receptor- and CD28-mediated activation of JNK, p38, and interleukin-2 transcription. J. Biol. Chem. 275, 18160-18171 (2000).
24. K. V. Salojin, J. Zhang, T. L. Delovitch, TCR and CD28 are coupled via ZAP-70 to the activation of the Vav/Rac-1-/PAK-1/p38 MAPK signaling pathway. J. Immunol. 163, 844-853 (1999).
25. M. Deckert, S. Tartare-Deckert, C. Couture, T. Mustelin, A. Altman, Functional and physical interactions of Syk family kinases with the Vav proto-oncogene product. Immunity 5, 591-604 (1996).
26. M. Nishida, K. Nagata, Y. Hachimori, M. Horiuchi, K. Ogura, V. Mandiyan, J. Schlessinger, F. Inagaki, Novel recognition mode between Vav and Grb2 SH3 domains. EMBO J. 20, 2995-3007 (2001).
27. Z.-S. Ye, D. Baltimore, Binding of Vav to Grb2 through dimerization of Src homology 3 domains. Proc. Natl. Acad. Sci. U.S.A. 91, 12629-12633 (1994).
28. W. Zhang, R. P. Trible, M. Zhu, S. K. Liu, C. J. McGlade, L. E. Samelson, Association of Grb2, Gads, and phospholipase C-γ1 with phosphorylated LAT tyrosine residues. Effect of LAT tyrosine mutations on T cell antigen receptor-mediated signaling. J. Biol. Chem. 275, 23355-23361 (2000).
29. N. Fang, G. A. Koretzky, SLP-76 and Vav function in separate, but overlapping pathways to augment interleukin-2 promoter activity. J. Biol. Chem. 274, 16206-16212 (1999).
30. H. Asada, N. Ishii, Y. Sasaki, K. Endo, H. Kasai, N. Tanaka, T. Takeshita, S. Tsuchiya, T. Konno, K. Sugamura, Grf40, A novel Grb2 family member, is involved in T cell signaling through interaction with SLP-76 and LAT. J. Exp. Med. 189, 1383-1390 (1999).
31. S. K. Liu, N. Fang, G. A. Koretzky, C. J. McGlade, The hematopoietic-specific adaptor protein gads functions in T-cell signaling via interactions with the SLP-76 and LAT adaptors. Curr. Biol. 9, 67-75 (1999).
32. H. S. Azzam, A. Grinberg, K. Lui, H. Shen, E. W. Shores, P. E. Love, CD5 expression is developmentally regulated by T cell receptor (TCR) signals and TCR avidity. J. Exp. Med. 188, 2301-2311 (1998).
33. Q. Gong, A. M. Cheng, A. M. Akk, J. Alberola-Ila, G. Gong, T. Pawson, A. C. Chan, Disruption of T cell signaling networks and development by Grb2 haploid insufficiency. Nat. Immunol. 2, 29-36 (2001).
34. I. K. Jang, J. Zhang, Y. J. Chiang, H. K. Kole, D. G. Cronshaw, Y. Zou, H. Gu, Grb2 functions at the top of the T-cell antigen receptor-induced tyrosine kinase cascade to control thymic selection. Proc. Natl. Acad. Sci. U.S.A. 107, 10620-10625 (2010).
35. K.-I. Pfrepper, A. Marie-Cardine, L. Simeoni, Y. Kuramitsu, A. Leo, J. Spicka, I. Hilgert, J. Scherer, B. Schraven, Structural and functional dissection of the cytoplasmic domain of the transmembrane adaptor protein SIT (SHP2-interacting transmembrane adaptor protein). Eur. J. Immunol. 31, 1825-1836 (2001).
36. L. Simeoni, V. Posevitz, U. Kölsch, I. Meinert, E. Bruyns, K. Pfeffer, D. Reinhold, B. Schraven, The transmembrane adapter protein SIT regulates thymic development and peripheral T-cell functions. Mol. Cell. Biol. 25, 7557-7568 (2005).
37. A. K. Chakraborty, J. Das, J. Zikherman, M. Yang, C. C. Govern, M. Ho, A. Weiss, J. Roose, Molecular origin and functional consequences of digital signaling and hysteresis during Ras activation in lymphocytes. Sci. Signal. 2, pt2 (2009).
38. J. Das, M. Ho, J. Zikherman, C. Govern, M. Yang, A. Weiss, A. K. Chakraborty, J. P. Roose, Digital signaling and hysteresis characterize ras activation in lymphoid cells. Cell 136, 337-351 (2009).
39. O. Ksionda, A. Saveliev, R. Köchl, J. Rapley, M. Faroudi, J. E. Smith-Garvin, C. Wülfing, K. Rittinger, T. Carter, V. L. J. Tybulewicz, Mechanism and function of Vav1 localisation in TCR signalling. J. Cell Sci. 125, 5302-5314 (2012).
40. N. Bisson, D. A. James, G. Ivosev, S. A. Tate, R. Bonner, L. Taylor, T. Pawson, Selected reaction monitoring mass spectrometry reveals the dynamics of signaling through the GRB2 adaptor. Nat. Biotechnol. 29, 653-658 (2011).
41. K. Neumann, T. Oellerich, H. Urlaub, J. Wienands, The B-lymphoid Grb2 interaction code. Immunol. Rev. 232, 135-149 (2009).
42. M. Naramura, H. K. Kole, R.-J. Hu, H. Gu, Altered thymic positive selection and intracellular signals in Cbl-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 95, 15547-15552 (1998).
43. E. Naik, J. D. Webster, J. DeVoss, J. Liu, R. Suriben, V. M. Dixit, Regulation of proximal T cell receptor signaling and tolerance induction by deubiquitinase Usp9X. J. Exp. Med. 211, 1947-1955 (2014).
44. S. S. Kholmanskikh, H. B. Koeller, A. Wynshaw-Boris, T. Gomez, P. C. Letourneau, M. E. Ross, Calcium-dependent interaction of Lis1 with IQGAP1 and Cdc42 promotes neuronal motility. Nat. Neurosci. 9, 50-57 (2005).
45. C. Pedros, G. Gaud, I. Bernard, S. Kassem, M. Chabod, D. Lagrange, O. Andréoletti, A. S. Dejean, R. Lesourne, G. J. Fournié, A. Saoudi, An epistatic interaction between Themis1 and Vav1 modulates regulatory T cell function and inflammatory bowel disease development. J. Immunol. 195, 1608-1616 (2015).
46. S. Hwang, K.-D. Song, R. Lesourne, J. Lee, J. Pinkhasov, L. Li, D. El-Khoury, P. E. Love, Reduced TCR signaling potential impairs negative selection but does not result in autoimmune disease. J. Exp. Med., 209, 1781-1795 (2012).
47. B. Schwanhäusser, D. Busse, N. Li, G. Dittmar, J. Schuchhardt, J. Wolf, W. Chen, M. Selbach, Global quantification of mammalian gene expression control. Nature 473, 337-342 (2011).