Constitutively oxidized CXXC motifs within the CD3 heterodimeric ectodomains of the t cell receptor complex enforce the conformation of juxtaposed segments

Journal of Biological Chemistry

Volumn 289, Issue 27, 2014, Pages 18880-18892

  Brazin, Kristine N ^a,b   Mallis, Robert J ^b   Li, Chen ^b   Keskin, Derin B ^a   Arthanari, Haribabu ^b   Gao, Yuanwei ^b   Wu, Shiaw Lin ^b   Karger, Barry L ^b   Wagner, Gerhard ^b   Reinherz, Ellis L ^a,b  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b NORTHEASTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; COVALENT BONDS; SIGNAL TRANSDUCTION;

EXTRACELLULAR; INTRACELLULAR SIGNALING; INTRAMOLECULAR DISULFIDE BONDS; MECHANOTRANSDUCTION; SIGNALING COMPONENTS; STRUCTURAL FEATURE; T CELL RECEPTOR;

T-CELLS;

1 PALMITOYL SN GLYCERO 3 PHOSPHO (1' RAC GLYCEROL) (SODIUM SALT); BIOTIN; GLYCEROPHOSPHOLIPID; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BIOTIN SWITCH ASSAY; CONTROLLED STUDY; DISULFIDE BOND; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MECHANOTRANSDUCTION; MICELLE; OXIDATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN MOTIF; PROTON NUCLEAR MAGNETIC RESONANCE; SIGNAL TRANSDUCTION; STOICHIOMETRY; T LYMPHOCYTE ACTIVATION;

CD3; DISULFIDE; MASS SPECTROMETRY (MS); MECHANOTRANSDUCTION; NUCLEAR MAGNETIC RESONANCE (NMR); SIGNALING; T-CELL RECEPTOR (TCR); TRANSMEMBRANE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD2; ANTIGENS, CD3; CELL MEMBRANE; CYTOPLASM; DISULFIDES; HUMANS; JURKAT CELLS; LYMPHOCYTE ACTIVATION; MECHANOTRANSDUCTION, CELLULAR; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES;

EID: 84903838062     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.574996     Document Type: Article

References (60)

1. Dave, V. P., Cao, Z., Browne, C., Alarcon, B., Fernandez-Miguel, G., Lafaille, J., de la Hera, A., Tonegawa, S., and Kappes, D. J. (1997) CD3- deficiency arrests development of the - but not the - T cell lineage. EMBO J. 16, 1360-1370
2. Haks, M. C., Krimpenfort, P., Borst, J., and Kruisbeek, A. M. (1998) The CD3- chain is essential for development of both the TCR- and TCR- lineages. EMBO J. 17, 1871-1882
3. Kim, S. T., Shin, Y., Brazin, K., Mallis, R. J., Sun, Z. Y., Wagner, G., Lang, M. J., and Reinherz, E. L. (2012) TCR mechanobiology: torques and tunable structures linked to early T cell signaling. Front. Immunol. 3, 76
4. Malissen, M., Gillet, A., Ardouin, L., Bouvier, G., Trucy, J., Ferrier, P., Vivier, E., and Malissen, B. (1995) Altered T cell development in mice with a targeted mutation of the CD3- gene. EMBO J. 14, 4641-4653
5. Smith-Garvin, J. E., Koretzky, G. A., and Jordan, M. S. (2009) T cell activation. Annu. Rev. Immunol. 27, 591-619
6. Arnaiz-Villena, A., Timon, M., Rodriguez-Gallego, C., Iglesias-Casarrubios, P., Pacheco, A., and Regueiro, J. R. (1993) T lymphocyte signalling defects and immunodeficiency due to the lack of CD3-. Immunodeficiency 4, 121-129
7. de Saint Basile, G., Geissmann, F., Flori, E., Uring-Lambert, B., Soudais, C., Cavazzana-Calvo, M., Durandy, A., Jabado, N., Fischer, A., and Le Deist, F. (2004) Severe combined immunodeficiency caused by deficiency in either the - or the - subunit of CD3. J. Clin. Invest. 114, 1512-1517
8. Gil, J., Busto, E. M., Garcillán, B., Chean, C., García-Rodríguez, M. C., Díaz-Alderete, A., Navarro, J., Reiné, J., Mencía, A., Gurbindo, D., Beléndez, C., Gordillo, I., Duchniewicz, M., Höhne, K., García-Sánchez, F., Fernández-Cruz, E., López-Granados, E., Schamel, W. W., Moreno-Pelayo, M. A., Recio, M. J., and Regueiro, J. R. (2011) A leaky mutation in CD3D differentially affects - and - T cells and leads to a T- T-BNK human SCID. J. Clin. Invest. 121, 3872-3876
9. Tokgoz, H., Caliskan, U., Keles, S., Reisli, I., Guiu, I. S., and Morgan, N. V. (2013) Variable presentation of primary immune deficiency: two cases with CD3 - deficiency presenting with only autoimmunity. Pediatr. Allergy Immunol. 24, 257-262
10. Blumberg, R. S., Alarcon, B., Sancho, J., McDermott, F. V., Lopez, P., Breitmeyer, J., and Terhorst, C. (1990) Assembly and function of the T cell antigen receptor. Requirement of either the lysine or arginine residues in the transmembrane region of the - chain. J. Biol. Chem. 265, 14036-14043
11. Letourneur, F., and Klausner, R. D. (1992) Activation of T cells by a tyrosine kinase activation domain in the cytoplasmic tail of CD3-. Science 255, 79-82
12. Manolios, N., Letourneur, F., Bonifacino, J. S., and Klausner, R. D. (1991) Pairwise, cooperative, and inhibitory interactions describe the assembly and probable structure of the T-cell antigen receptor. EMBO J. 10, 1643-1651
13. Kuhns, M. S., and Davis, M. M. (2012) TCR signaling emerges from the sum of many parts. Front. Immunol. 3, 159
14. Reth, M. (1989) Antigen receptor tail clue. Nature 338, 383-384
15. van der Merwe, P. A., and Dushek, O. (2011) Mechanisms for T cell receptor triggering. Nat. Rev. Immunol. 11, 47-55
16. Call, M. E., and Wucherpfennig, K. W. (2005) The T cell receptor: critical role of the membrane environment in receptor assembly and function. Annu Rev. Immunol. 23, 101-125
17. Borroto, A., Mallabiabarrena, A., Albar, J. P., Martínez-A, C., and Alarcón, B. (1998) Characterization of the region involved in CD3 pairwise interactions within the T cell receptor complex. J. Biol. Chem. 273, 12807-12816
18. Sun, Z.-Y. 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- heterodimer. Cell 105, 913-923
19. 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 -strand and membrane proximal stalk in thymic development and receptor assembly. J. Immunol. 178, 3668-3679
20. Xu, C., Call, M. E., and Wucherpfennig, K. W. (2006) A membrane-proximal tetracysteine motif contributes to assembly of CD3- and CD3- dimers with the T cell receptor. J. Biol. Chem. 281, 36977-36984
21. Wang, Y., Becker, D., Vass, T., White, J., Marrack, P., and Kappler, J. W. (2009) A conserved C XX C motif in CD3- is critical for T cell development and TCR signaling. PLoS Biol. 7, e1000253
22. Iqbalsyah, T. M., Moutevelis, E., Warwicker, J., Errington, N., and Doig, A. J. (2006) The C XX C motif at the N terminus of an -helical peptide. Protein Sci. 15, 1945-1950
23. Husson, J., Chemin, K., Bohineust, A., Hivroz, C., and Henry, N. (2011) Force generation upon T cell receptor engagement. PLoS ONE 6, e19680
24. Judokusumo, E., Tabdanov, E., Kumari, S., Dustin, M. L., and Kam, L. C. (2012) Mechanosensing in T lymphocyte activation. Biophys. J. 102, L5-L7
25. 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 - T cell receptor is an anisotropic mechanosensor. J. Biol. Chem. 284, 31028-31037
26. 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
27. Ma, Z., and Finkel, T. H. (2010) T cell receptor triggering by force. Trends Immunol. 31, 1-6
28. 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 - and - subunits on IL-2-dependent clones and T cell tumors. Cell 34, 717-726
29. Reinherz, E. L., Meuer, S., Fitzgerald, K. A., Hussey, R. E., Levine, H., and Schlossman, S. F. (1982) Antigen recognition by human T lymphocytes is linked to surface expression of the T3 molecular complex. Cell 30, 735-743
30. Meuer, S. C., Hussey, R. E., Fabbi, M., Fox, D., Acuto, O., Fitzgerald, K. A., Hodgdon, J. C., Protentis, J. P., Schlossman, S. F., and Reinherz, E. L. (1984) An alternative pathway of T-cell activation: a functional role for the 50 kD T11 sheep erythrocyte receptor protein. Cell 36, 897-906
31. Meuer, S. C., Cooper, D. A., Hodgdon, J. C., Hussey, R. E., Fitzgerald, K. A., Schlossman, S. F., and Reinherz, E. L. (1983) Identification of the receptor for antigen and major histocompatibility complex on human inducer T lymphocytes. Science 222, 1239-1242
32. 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
33. Hyberts, S. G., Milbradt, A. G., Wagner, A. B., Arthanari, H., and Wagner, G. (2012) Application of iterative soft thresholding for fast reconstruction ofNMRdata non-uniformly sampled with multidimensional Poisson Gap scheduling. J. Biomol. NMR 52, 315-327
34. Hyberts, S. G., Takeuchi, K., and Wagner, G. (2010) Poisson-gap sampling and forward maximum entropy reconstruction for enhancing the resolution and sensitivity of protein NMR data. J. Am. Chem. Soc. 132, 2145-2147
35. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based onUNIX pipes. J. Biomol. NMR 6, 277-293
36. Johnson, B. A., and Blevins, R. A. (1994) NMRView: a computer program for the visualization and analysis ofNMRdata. J. Biomol. NMR 4, 603-614
37. Keller, R. (2004) Computer aided resonance assignment tutorial. Cantina, Zurich, Switzerland
38. Piotukh, K., Kosslick, D., Zimmermann, J., Krause, E., and Freund, C. (2007) Reversible disulfide bond formation of intracellular proteins probed by NMR spectroscopy. Free Radic. Biol. Med. 43, 1263-1270
39. Hwang, C., Sinskey, A. J., and Lodish, H. F. (1992) Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257, 1496-1502
40. Jones, D. P., Carlson, J. L., Mody, V. C., Cai, J., Lynn, M. J., and Sternberg, P. (2000) Redox state of glutathione in human plasma. Free Radic. Biol. Med. 28, 625-635
41. Varki, A. (2009) Essentials of Glycobiology, 2nd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
42. Forrester, M. T., Foster, M. W., Benhar, M., and Stamler, J. S. (2009) Detection of protein S-nitrosylation with the biotin-switch technique. Free Radic. Biol. Med. 46, 119-126
43. Miyamoto, S., Sakamoto, T., Soejima, H., Shimomura, H., Kajiwara, I., Kojima, S., Hokamaki, J., Sugiyama, S., Yoshimura, M., Ozaki, Y., Nakamura, H., Yodoi, J., and Ogawa, H. (2003) Plasma thioredoxin levels and platelet aggregability in patients with acute myocardial infarction. Am. Heart. J. 146, 465-471
44. Son, A., Kato, N., Horibe, T., Matsuo, Y., Mochizuki, M., Mitsui, A., Kawakami, K., Nakamura, H., and Yodoi, J. (2009)) Direct association of thioredoxin-1 (Trx) with macrophage migration inhibitory factor (MIF): regulatory role of Trx on MIF internalization and signaling. Antioxid. Redox Signal. 11, 2595-2605
45. Xu, S.-Z., Sukumar, P., Zeng, F., Li, J., Jairaman, A., English, A., Naylor, J., Ciurtin, C., Majeed, Y., Milligan, C. J., Bahnasi, Y. M., Al-Shawaf, E., Porter, K. E., Jiang, L.-H., Emery, P., Sivaprasadarao, A., and Beech, D. J. (2008) TRPC channel activation by extracellular thioredoxin. Nature 451, 69-72
46. Lillig, C. H., and Holmgren, A. (2007) Thioredoxin and related molecules: from biology to health and disease. Antioxid. Redox Signal. 9, 25-47
47. Ohmori Hnt, Yamauchi, T., and Yamamoto, I. (1986) Augmentation of the antibody response by lipoic acid in mice. I. Analysis of the mode of action in an in vitro cultures system. Jpn. J. Pharmacol. 42, 135-140
48. Jin, Y. J., Koyasu, S., Moingeon, P., Steinbrich, R., Tarr, G. E., and Reinherz, E. L. (1990) A fraction of CD3 - subunits exists as disulfide-linked dimers in both human and murine T lymphocytes. J. Biol. Chem. 265, 15850-15853
49. Metcalfe, C., Cresswell, P., Ciaccia, L., Thomas, B., and Barclay, A. N. (2011) Labile disulfide bonds are common at the leucocyte cell surface. Open Biol. 1, 110010
50. Sun, Z.-Y. J., Kim, S. T., Kim, I. C., Fahmy, A., Reinherz, E. L., and Wagner, G. (2004) Solution structure of the CD3- ectodomain and comparison with CD3- as a basis for modeling T cell receptor topology and signaling. Proc. Natl. Acad. Sci. U. S. A. 101, 16867-16872
51. Manolios, N., Bonifacino, J. S., and Klausner, R. D. (1990) Transmembrane helical interactions and the assembly of the T cell receptor complex. Science 249, 274-277
52. Cosson, P., Lankford, S. P., Bonifacino, J. S., and Klausner, R. D. (1991) Membrane protein association by potential intramembrane charge pairs. Nature 351, 414-416
53. Aslund, F., Berndt, K. D., and Holmgren, A. (1997) Redox potentials of glutaredoxins and other thiol-disulfide oxidoreductases of the thioredoxin superfamily determined by direct protein-protein redox equilibria. J. Biol. Chem. 272, 30780-30786
54. Indu, S., Kumar, S. T., Thakurela, S., Gupta, M., Bhaskara, R. M., Ramakrishnan, C., and Varadarajan, R. (2010) Disulfide conformation and design at helix N termini. Proteins 78, 1228-1242
55. Liu, B., Chen, W., Evavold, B. D., and Zhu, C. (2014) Accumulation of dynamic catch bonds between TCR and agonist peptide-MHC triggers T cell signaling. Cell 157, 357-368
56. Chen, W., and Zhu, C. (2013) Mechanical regulation of T-cell functions. Immunol. Rev. 256, 160-176
57. Choi, Y. I., Duke-Cohan, J. S., Chen, W., Liu, B., Rossy, J., Tabarin, T., Ju, L., Gui, J., Gaus, K., Zhu, C., and Reinherz, E. L. (2014) Dynamic control of-1 integrin adhesion by the plexinD1-sema3E axis. Proc. Natl. Acad. Sci. U. S. A. 111, 379-384
58. Zhou, Y. F., Eng, E. T., Zhu, J., Lu, C., Walz, T., and Springer, T. A. (2012) Sequence and structure relationships within von Willebrand factor. Blood 120, 449-458
59. Zhou, Y. F., and Springer, T. A. (2014) Highly reinforced structure of a C-terminal dimerization domain in von Willebrand factor. Blood 123, 1785-1793
60. DeLano, W. L. (2010) The PyMOL Molecular Graphics System, Version 1. 3r1, Schrodinger, LLC, New York