TCR mechanobiology: Torques and tunable structures linked to early T cell signaling

Frontiers in Immunology

Volumn 3, Issue APR, 2012, Pages

  Kim, Sun Taek ^a   Shin, Yongdae ^b   Brazin, Kristine ^a   Mallis, Robert J ^a   Sun, Zhen Yu J ^a   Wagner, Gerhard ^a   Lang, Matthew J ^c   Reinherz, Ellis L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c VANDERBILT UNIVERSITY   (United States)

Author keywords

Antigen recognition; Force transduction; Mechanosensor; quaternary change; T cell signaling

Indexed keywords

EID: 84862978540     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00076     Document Type: Review

References (67)

1. Acuto, O., Di Bartolo, V., and Michel, F. (2008). Tailoring T-cell receptor signals by proximal negative feedback mechanisms. Nat. Rev. Immunol. 8, 699-712.
2. Acuto, O., Hussey, R. E., Fitzgerald, K. A., Protentis, J. P., Meuer, S. C., Schlossman, S.F., and Reinherz, E.L. (1983). The human T cell receptor: appearance in ontogeny and biochemical relationship of the a and ß subunits on IL-2 dependent clones and T cell tumors. Cell 34, 717-726.
3. Adams, J. J., Narayanan, S., Liu, B., Birnbaum, M. E., Kruse, A., Bowerman, N. A., Chen, W., Levin, A. M., Connolly, J. M., Zhu, C., Kranz, D. M., and Garcia, K. C. (2011). T cell receptor signaling is limited by docking geometry to peptide-major histocompatibility complex. Immunity 35,681-693.
4. Aivazian, D., and Stern, L. J. (2000). Phosphorylation of T cell receptor zeta is regulated by a lipid dependent folding transition. Nat. Struct. Biol. 7, 1023-1026.
5. Arnett, K. L., Harrison, S. C., and Wiley, D. C. (2004). Crystal structure of a human CD3-epsilon/delta dimer in complex with a UCHT1 single-chain antibody fragment. Proc. Natl. Acad. Sci. U.S.A. 101, 16268-16273.
6. Backström, B. T., Muller, U., Hausmann, B., and Palmer, E. (1998). Positive selection through a motif in the alphabeta T cell receptor. Science 281,835-838.
7. Bentley, G.A., Boulot, G., Karjalainen, K.,andMariuzza,R. A. (1995). Crystal structure of the ß chain of a T cell antigen receptor. Science 267, 1984-1987.
8. Brenner, M. B. (1985). Crosslinking of human T cell receptor proteins: association between the T cell idiotype |3 subunit and the T3 glycoprotein heavy subunit. Cell 40, 183-190.
9. Call, M.E., Pyrdol, J., Wiedmann, M., and Wucherpfennig, K. W. (2002). The organizing principle in the formation of the T cell receptor-CD3 complex. Cell 111, 967-979.
10. Call, M. E., Pyrdol, J., and Wucherpfennig, K. W. (2004). Stoichiometry of the T-cell receptor-CD3 complex and key intermediates assembled in the endoplasmic reticulum. EMBO J. 23,2348-2357.
11. Chien, Y., Becker, D. M., Lindsten, T., Okamura, M., Cohen, D. I., and Davis, M. M. (1984). A third type of murine T cell receptor gene. Nature 312,31-35.
12. Chothia, C, Boswell, D. R., and Lesk, A. M. (1988). The outline structure of the T cell aß receptor. EMBO J. 7, 3745-3755.
13. Crabtree, G. R., and Clipstone, N. A. (1994). Signal transmission between the plasma membrane and nucleus of T lymphocytes. Annu. Rev. Biochem. 63,1045-1083.
14. Deford-Watts, L. M., Tassin, T. C., Becker, A. M., Medeiros, J. J., Albanesi, J. P., Love, P. E., Wülfing, C., and van Oers, N. S. (2009). The cytoplasmic tail of the T cell receptor CD3 epsilon subunit contains a phospholipid-binding motif that regulates T cell functions. J. Immunol. 183,1055-1064.
15. Demetriou, M., Granovsky, M., Quaggin, S., and Dennis, J. M. (2001). Negative regulation of T cell activation and autoimmunity by Mgat5 Nglycosylation. Nature 409, 733-739.
16. Devadas, S., Zaritskaya, L., Rhee, S. G., Oberley, L., and Williams, M. S. (2002). Discrete generation of superoxide and hydrogen peroxide by T cell receptor stimulation: selective regulation of mitogen-activated protein kinase activation and fas ligand expression. J. Exp. Med. 195, 59-70.
17. Doggett, T. A., Girdhar, G., Lawshé, A., Schmidtke, D. W., Laurenzi, I. J., Diamond, S. L., and Diacovo, T. G. (2002). Selectin-like kinetics and biomechanics promote rapid platelet adhesion in flow: the GPIb(alpha)-vWF tether bond. Biophys. J. 83,194-205.
18. Fields, B. A., Ober, B., Malchiodi, E. L., Lebedeva, M. I., Braden, B. C., Ysern, X., Kim, J. K., Shao, X., Ward, E. S., and Mariuzza, R. A. (1995). Crystal structure of the Va domain of a T cell antigen receptor. Science 270, 1821-1824.
19. Garboczi, D. N., Ghosh, P., Utz, U., Fan, Q. R., Biddison, W E., and Wiley, D. C. (1996). Structure of the complex between human T cell receptor, viral peptide and HLA-A2. Nature 384, 134-141.
20. Garcia, K. C., Degano, M., Stanfield, R. L., Brunmark, A., Jackson, M. R., Peterson, P. A., Tayton, L., and Wilson, I. A. (1996). An aßT cell receptor structure at 2.5Å and its orientation in the TCR-MHC complex. Science 274, 209-219.
21. Ghendler,Y., Smolyar, A., Chang, H. C., and Reinherz, E. L. (1998). One of the CD3epsilon subunits within a T cell receptor complex lies in close proximity to the Cbeta FG loop. J. Exp. Med. 187,1529-1536.
22. Hsu, H. J., Chang, H. J., Peng, H. P., Huang, S. S., Lin, M. Y., and Yang, A. S. (2006). Assessing computational amino acid beta turn propensities with a phage-displayed combinatorial library and directed evolution. Structure 14,1499-1510.
23. Husson, J., Chemin, K., Bohineust, A., Hivroz, C., and Henry, N. (2011). Force generation upon T cell receptor engagement. PLoS ONE 6, e19680. doi:10.1371/journal.pone.0019680
24. Iqbalsyah, T. M., Moutevelis, E., Warwicker, J., Errington, N., and Doig, A. J. (2006). The CXXC motif at the N terminus of an alpha-helical peptide. Protein Sci. 15, 1945-1950.
25. Judokusumo, E., Tabdanov, E., Kumari, S., Dustin, M. L., and Kam, L. C. (2012). Mechanosensing in T lymphocyte activation. Biophys. J. 102, L05-L07.
26. Kabat, E. A., Wu, T. T., Perry, H. M., Gottesman, K. S., and Faeller, C. (1991). Sequences of Proteins of Immunological Interest. Bethesda: U.S. Dept. of Health and Human Services, DHS, NIH.
27. Kim, S. T., Takeuchi, K., Sun, Z. Y., Touma, M., Castro, C. E., Fahmy, A., Lang, M. J., Wagner, G., and Reinherz, E. L. (2009). The alphabeta T cell receptor is an anisotropic mechanosensor. J. Biol. Chem. 284, 31028-31037.
28. Kim, S. T., Touma, M., Takeuchi, K., Sun, Z. Y., Dave, V. P., Kappes, D. J., Wagner, G., and Reinherz, E. L. (2010). Distinctive CD3 heterodimeric ectodomain topologies maximize antigentriggered activation of alpha beta T cell receptors. J. Immunol. 185, 2951-2959.
29. Kjer-Nielsen, L., Clements, C. S., Purcell, A. W., Brooks, A. G., Whisstock, J. C., Burrows, S. R., McCluskey, J., and Rossjohn, J. (2003). A structural basis for the selection of dominant alphabeta T cell receptors in antiviral immunity. Immunity 18, 53-64.
30. Kjer-Nielsen, L., Dunstone, M. A., Kostenko, L., Ely, L. K., Beddoe, T., Mifsud, N. A., Purcell, A. W., Brooks, A. G., McCluskey, J., and Rossjohn, J. (2004). Crystal structure of the human T cell receptor CD3 epsilon gamma heterodimer complexed to the therapeutic mAb OKT3. Proc. Natl. Acad. Sci. U.S.A. 101,7675-7680.
31. Koning, F., Maloy, W. L., and Coligan, J. E. (1990). The implications of subunit interactions for the structure of the T cell receptor-CD3 complex. Eur. J. Immunol. 20, 299-305.
32. Kuball, J., Hauptrock, B., Malina, V., Antunes, E., Voss, R. H., Wolfl, M., Strong, R., Theobald, M., and Greenberg, P. D. (2009). Increasing functional avidity of TCR-redirected T cells by removing defined Nglycosylation sites in the TCR constant domain. J. Exp. Med. 206, 463-475.
33. Letourneur, F., and Klausner, R. D. (1992). Activation of T cells by a tyrosine kinase activation domain in the cytoplasmic tail of CD3 epsilon. Science 255, 79-82.
34. Li, Y. C., Chen, B. M., Wu, P. C., Cheng, T. L., Kao, L. S., Tao, M. H., Lieber, A., and Roffler, S. R. (2010). Cutting Edge: mechanical forces acting on T cells immobilized via the TCR complex can trigger TCR signaling. J. Immunol. 184, 5959-5963.
35. Ma, Z., and Finkel, T. H. (2010). T cell receptor triggering by force. Trends Immunol. 31, 1-6.
36. Manolios, N., Kemp, O., and Li, Z. G. (1994). The T cell antigen receptor a and ß chains interact via distinct regions with CD3 chains. Eur. I Immunol. 24, 84-92.
37. Manolios, N., Letourneur, F., Bonifacino, J.S.,andKlausner,R.D. (1991). Pairwise, cooperative and inhibitory interactions describe the assembly and probable structure of the Tcell antigen receptor. EMBO J. 10, 1643-1651.
38. Marshall, B. T., Long, M., Piper, J. W., Yago, T., McEver, R. P., and Zhu, C. (2003). Direct observation of catch bonds involving cell-adhesion molecules. Nature 423, 190-193.
39. Martínez-Martín, N., Risueño, R. M., Morreale, A.,Zaldívar, I., Fernández-Arenas, E., Herranz, F., Ortiz, A. R., and Alarcón, B. (2009). Cooperativity between T cell receptor complexes revealed by conformational mutants of CD3epsilon. Sci. Signal. 2,ra43.
40. Meuer, S. C., Acuto, O., Hussey, R. E., Hodgdon, J. C., Fitzgerald, K. A., Schlossman, S. F., and Reinherz, E. L. (1983a). Evidence for the T3-associated 90KD heterodimer as the T cell antigen receptor. Nature 303, 808-810.
41. Meuer, S. C., Fitzgerald, K. A., Hussey, R. E., Hodgdon, J. C., Schlossman, S. F., and Reinherz, E. L. (1983b). Clonotypic structures involved in antigen specific human T cell function: relationship to the T3 molecular complex. J. Exp. Med 157, 705-719.
42. Nika, K., Soldani, C., Salek, M., Paster, W., Gray, A., Etzensperger, R., Fugger, L., Polzella, P., Cerundolo, V., Dushek, O., Höfer, T., Viola, A., and Acuto, O. (2010). Constitutively active Lck kinase in T cells drives antigen receptor signal transduction. Immunity 32, 766-777.
43. Novotny, J., Tonegawa, S., Saito, H., Kranz, D. M., and Eisen, H. N. (1986). Secondary, tertiary, and quaternary structure of T-cell-specific immunoglobulin-like polypeptide chains. Proc. Natl. Acad. Sci. U.S.A. 83, 742-746.
44. Otsuji, M., Kimura, Y., Aoe, T., Okamoto, Y., and Saito, T. (1996). Oxidative stress by tumor-derived macrophages suppresses the expression of CD3 ? chain of T-cell receptor complex and antigen-specific T cell responses. Proc. Natl. Acad. Sci. U.S.A. 93, 13119-13124.
45. Pani, G., Colavitti, R., Borrello, S., and Galeotti,T. (2000). Endogenous oxygen radicals modulate protein tyrosine phosphorylation and JNK-1 activation in lectin-stimulated thymocytes. Biochem. J. 347,173-181.
46. Reinherz, E. L., Tan, K., Tang, L., Kern, P., Liu, J.-H., Xiong, Y., Hussey, R. E., Smolyar, A., Hare, B., Zhang, R., Joachimiak, A., Chang, H. C., Wagner, G., and Wang, J. (1999). The crystal structure of a T cell receptor in complex with peptide and MHC class II. Science 286, 1913-1921.
47. Reth, M. (1989). Antigen receptor tail clue. Nature 338, 383-384.
48. Rudolph, M G., Stanfield, R. L., and Wilson, I. A. (2006). How TCRs bind MHCs, peptides, and coreceptors. Annu. Rev. Immunol, 24, 419-466.
49. Ruggeri, Z. M. (2007). Von Willebrand factor: looking back and looking forward. Thromb. Haemost. 98, 55-62.
50. Sasada, T, Touma, M., Chang, H.-C., Clayton, L. K., Wang, J., and Reinherz, E. L. (2002). Involvement of the TCR Cß FG loop in thymic selection and T cell function. J. Exp. Med, 195, 1419-1431.
51. Smith-Garvin, J. E., Koretzky, G. A., and Jordan, M. S. (2009). T cell activation. Annu. Rev. Immunol. 27, 591-619.
52. Sun, Z. J., Kim, K. S., Wagner, G., and Reinherz, E. L. (2001). Mechanisms contributing to T cell receptor signaling and assembly revealed by the solution structure of an ectodomain fragment of the CD3 epsilon gamma heterodimer. Cell 105, 913-923.
53. Sun, Z.-Y J., Kim, S. T., Kim, I. L., Fahmy, A., Reinherz, E. L., and Wagner, G. (2004). Solution structure of the CD3eS ectodomain and comparison with CD3ey as a basis for modeling T cell receptor topology and signaling. Proc. Natl. Acad. Sci. U.S.A. 101, 16867-16872.
54. Sundberg, E. J., Li, Y C, and Mariuzza, R. A. (2002). So many ways of getting in the way: diversity in the molecular architecture of superantigendependent T cell signaling complexes. Curr. Opin. Immunol. 14, 36-44.
55. Tarsa, P. B., Brau, R. R., Barch, M., Ferrer, J. M., Freyzon, Y., Matsudaira, P., and Lang, M. J. (2007). Detecting forceinduced molecular transitions with fluorescence resonant energy transfer. Angew. Chem. Int. Ed. Engl. 46, 1999-2001.
56. Thomassen, E. A. J., Dekking, E. H. A., Thompson, A., Franken, K. L., O'Sanal, O., Abrahams, J. P., van Tol, M. J. D., and Koning, F. (2006). The impact of single amino acid substitutions in CD3? on the CD3ey interaction and T-cell receptor-CD3 complex formation. Hum. Immunol. 67, 579-588.
57. Touma, M., Sun, Z. Y., Clayton, L. K., Marissen, W. E., Kruisbeek, A. M., Wagner, G., and Reinherz, E. L. (2007). Importance of the CD3? ectodomain terminal ß-strand and membrane proximal stalk in thymic development and receptor assembly. J. Immunol. 178, 3668-3679.
58. van der Merwe, P. A., and Dushek, O. (2011). Mechanisms for T cell receptor triggering. Nat. Rev. Immunol. 11,47-55.
59. Wang, J.,Lim, K., Smolyar, A., Teng, M.-K., Liu, J.-H., Tse, A. G. T., Liu, J., Hussey, R. E., Chishti, Y., Thomson, C. T., Sweet, R. M., Nathenson, S. G., Chang, H. C., Sacchettini, J. C., and Reinherz, E. L.. (1998). Atomic structure of an aß T cell receptor (TCR) heterodimer in complex with an anti-TCR Fab fragment derived from a mitogenic antibody. EMBOJ. 17, 10-26.
60. Wang, Y., Becker, D., Vass, T., White, J., Marrack, P., and Kappler, J. W. (2009). A conserved CXXC motif in CD3epsilon is critical for T cell development and TCR signaling. PLoS Biol. 7, e1000253. doi:10.1371/journal.pone.0018079
61. Werlen, G., Hausmann, B., and Palmer, E. (2000). A motif in the alphabeta T-cell receptor controls positive selection by modulating ERK activity. Nature 406, 422-426.
62. White, J., Haskins, K. M., Marrack, P., and Kappler, J. (1983). Use of I region-restricted, antigen-specific T cell hybridomas to produce idiotypically specific anti-receptor antibodies. J. Immunol. 130, 1033-1037.
63. Xu, C., Call, M. E., and Wucherpfennig, K. W (2006).Amembrane-proximal tetracysteine motif contributes to assembly of CD3k and CD3ye dimers with the T cell receptor. J. Biol. Chem. 281, 36977-36984.
64. Xu, C., Gagnon, E., Call, M. E., Schnell, J. R., Schwieters, C. D., Carman, C. V., Chou, J. J., and Wucherpfennig, K. W (2008). Regulation of T cell receptor activation by dynamic membrane binding of the CD3 epsilon cytoplasmic tyrosine-based motif. Cell 135, 702-713.
65. Yanagi, Y., Yoshikai, Y., Leggett, K., Clark, S. P., Aleksander, I., and Mak, T. W. (1984). A human T cell-specific cDNA clone encodes a protein having extensive homology to immunoglobulin chains. Nature 308, 145-149.
66. Yokosuka, T., Kobayashi, W., Sakata-Sogawa, K., Takamatsu, M., Hashimoto-Tane, A., Dustin, M. L., Tokunaga, M., and Saito, T. (2008). Spatiotemporal regulation of T cell costimulation by TCR-CD28 microclusters and protein kinase C theta translocation. Immunity 29, 589-601.
67. Zech, T., Ejsing, C. S., Gaus, K., de Wet, B., Shevchenko, A., Simons, K., and Harder, T. (2009). Accumulation of raft lipids in T-cell plasma membrane domains engaged in TCR signalling. EMBO J. 28, 466-476.