Physical and functional bivalency observed among TCR/CD3 complexes isolated from primary T cells

Journal of Immunology

Volumn 187, Issue 2, 2011, Pages 870-878

  Schrum, Adam G ^a,b,c   Gil, Diana ^a,d   Turka, Laurence A ^b   Palmer, Ed ^c  

^a MAYO CLINIC   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY HOSPITAL BASEL   (Switzerland)

^d UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; HYBRID PROTEIN; IMMUNOGLOBULIN; MAJOR HISTOCOMPATIBILITY ANTIGEN; RECEPTOR ANTIBODY; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN BINDING; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; FLOW CYTOMETRY; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BINDING; RECEPTOR OCCUPANCY; T LYMPHOCYTE;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGENS, CD3; FLOW CYTOMETRY; IMMUNOPRECIPITATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PROTEIN MULTIMERIZATION; RECEPTOR-CD3 COMPLEX, ANTIGEN, T-CELL; T-LYMPHOCYTE SUBSETS;

EID: 79960484634     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100538     Document Type: Article

References (53)

1. Oltz, E. M. 2001. Regulation of antigen receptor gene assembly in lymphocytes. Immunol. Res. 23: 121-133.
2. Smith-Garvin, J. E., G. A. Koretzky, and M. S. Jordan. 2009. T cell activation. Annu. Rev. Immunol. 27: 591-619.
3. Punt, J. A., J. L. Roberts, K. P. Kearse, and A. Singer. 1994. Stoichiometry of the T cell antigen receptor (TCR) complex: each TCR/CD3 complex contains one TCR alpha, one TCR beta, and two CD3 epsilon chains. J. Exp. Med. 180: 587-593.
4. Call, M. E., J. Pyrdol, M. Wiedmann, and K. W. Wucherpfennig. 2002. The organizing principle in the formation of the T cell receptor-CD3 complex. Cell 111: 967-979.
5. Pan, Q., A. S. Gollapudi, and V. P. Dave. 2004. Biochemical evidence for the presence of a single CD3delta and CD3gamma chain in the surface T cell receptor/CD3 complex. J. Biol. Chem. 279: 51068-51074.
6. Call, M. E., J. Pyrdol, and K. W. Wucherpfennig. 2004. Stoichiometry of the Tcell receptor-CD3 complex and key intermediates assembled in the endoplasmic reticulum. EMBO J. 23: 2348-2357.
7. Call, M. E., and K. W. Wucherpfennig. 2005. The T cell receptor: critical role of the membrane environment in receptor assembly and function. Annu. Rev. Immunol. 23: 101-125.
8. Terhorst, C., M. Exley, R. Franco, C. Hall, J. Kang, B. Mueller, J. Sancho, J. She, and T. Wileman. 1993. Coupling of T-cell activation with T-cell receptor assembly. Year Immunol. 7: 1-24.
9. Jacobs, H. 1997. Pre-TCR/CD3 and TCR/CD3 complexes: decamers with differential signalling properties? Immunol. Today 18: 565-569. (Pubitemid 28010966)
10. Fernández-Miguel, G., B. Alarcón, A. Iglesias, H. Bluethmann, M. Alvarez- Mon, E. Sanz, and A. de la Hera. 1999. Multivalent structure of an alphabetaT cell receptor. Proc. Natl. Acad. Sci. USA 96: 1547-1552.
11. Schamel, W. W., I. Arechaga, R. M. Risueño, H. M. van Santen, P. Cabezas, C. Risco, J. M. Valpuesta, and B. Alarcón. 2005. Coexistence of multivalent and monovalent TCRs explains high sensitivity and wide range of response. J. Exp. Med. 202: 493-503.
12. Beyers, A. D., L. L. Spruyt, and A. F. Williams. 1992. Molecular associations between the T-lymphocyte antigen receptor complex and the surface antigens CD2, CD4, or CD8 and CD5. Proc. Natl. Acad. Sci. USA 89: 2945-2949.
13. Cerný, J., H. Stockinger, and V. Horejsí. 1996. Noncovalent associations of T lymphocyte surface proteins. Eur. J. Immunol. 26: 2335-2343.
14. Alarcón, B., M. Swamy, H. M. van Santen, and W. W. Schamel. 2006. T-cell antigen-receptor stoichiometry: pre-clustering for sensitivity. EMBO Rep. 7: 490-495.
15. Teixeiro, E., M. A. Daniels, B. Hausmann, A. G. Schrum, D. Naeher, I. Luescher, M. Thome, R. Bragado, and E. Palmer. 2004. T cell division and death are segregated by mutation of TCRbeta chain constant domains. Immunity 21: 515-526. (Pubitemid 39370507)
16. Gil, D., A. G. Schrum, B. Alarcón, and E. Palmer. 2005. T cell receptor engagement by peptide-MHC ligands induces a conformational change in the CD3 complex of thymocytes. J. Exp. Med. 201: 517-522.
17. Schrum, A. G., D. Gil, E. P. Dopfer, D. L. Wiest, L. A. Turka, W. W. Schamel, and E. Palmer. 2007. High-sensitivity detection and quantitative analysis of native protein-protein interactions and multiprotein complexes by flow cytometry. Sci. STKE 2007: pl2.
18. Schrum, A. G. 2009. Visualization of multiprotein complexes by flow cytometry. Curr. Protoc. Immunol. Chapter 5: Unit 5.9.
19. Teixeiro, E., M. A. Daniels, S. E. Hamilton, A. G. Schrum, R. Bragado, S. C. Jameson, and E. Palmer. 2009. Different T cell receptor signals determine CD8+ memory versus effector development. Science 323: 502-505.
20. Murphy, K. M., A. B. Heimberger, and D. Y. Loh. 1990. Induction by antigen of intrathymic apoptosis of CD4+CD8+TCRlo thymocytes in vivo. Science 250: 1720-1723.
21. Andrew, S. M., and J. A. Titus. 2001. Fragmentation of immunoglobulin G. Curr. Protoc. Immunol. Chapter 2: Unit 2.8.
22. Karasuyama, H., and F. Melchers. 1988. Establishment of mouse cell lines which constitutively secrete large quantities of interleukin 2, 3, 4 or 5, using modified cDNA expression vectors. Eur. J. Immunol. 18: 97-104.
23. Davis, T. R., and A. G. Schrum. 2010. IP-FCM: immunoprecipitation detected by flow cytometry. J. Vis. Exp. 46: 2066 .
24. Montixi, C., C. Langlet, A. M. Bernard, J. Thimonier, C. Dubois, M. A. Wurbel, J. P. Chauvin, M. Pierres, and H. T. He. 1998. Engagement of T cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J. 17: 5334-5348.
25. Rozdzial, M. M., R. T. Kubo, S. L. Turner, and T. H. Finkel. 1994. Developmental regulation of the TCR zeta-chain. Differential expression and tyrosine phosphorylation of the TCR zeta-chain in resting immature and mature T lymphocytes. J. Immunol. 153: 1563-1580.
26. de la Hera, A., U. Müller, C. Olsson, S. Isaaz, and A. Tunnacliffe. 1991. Structure of the T cell antigen receptor (TCR): two CD3 epsilon subunits in a functional TCR/CD3 complex. J. Exp. Med. 173: 7-17.
27. Wang, J., K. Lim, A. Smolyar, M. Teng, J. Liu, A. G. Tse, J. Liu, R. E. Hussey, Y. Chishti, C. T. Thomson, et al. 1998. Atomic structure of an alphabeta T cell receptor (TCR) heterodimer in complex with an anti-TCR fab fragment derived from a mitogenic antibody. EMBO J. 17: 10-26. (Pubitemid 28041044)
28. Padovan, E., G. Casorati, P. Dellabona, S. Meyer, M. Brockhaus, and A. Lanzavecchia. 1993. Expression of two T cell receptor alpha chains: dual receptor T cells. Science 262: 422-424. (Pubitemid 23353384)
29. Schrum, A. G., and L. A. Turka. 2002. The proliferative capacity of individual naive CD4(+) T cells is amplified by prolonged T cell antigen receptor triggering. J. Exp. Med. 196: 793-803.
30. Yagüe, J., J. White, C. Coleclough, J. Kappler, E. Palmer, and P. Marrack. 1985. The T cell receptor: the alpha and beta chains define idiotype, and antigen and MHC specificity. Cell 42: 81-87. (Pubitemid 16237558)
31. Bäckström, B. T., U. Müller, B. Hausmann, and E. Palmer. 1998. Positive selection through a motif in the alphabeta T cell receptor. Science 281: 835-838. (Pubitemid 28376046)
32. Daniels, M. A., E. Teixeiro, J. Gill, B. Hausmann, D. Roubaty, K. Holmberg, G. Werlen, G. A. Holländer, N. R. Gascoigne, and E. Palmer. 2006. Thymic selection threshold defined by compartmentalization of Ras/MAPK signalling. Nature 444: 724-729. (Pubitemid 44949596)
33. Naeher, D., M. A. Daniels, B. Hausmann, P. Guillaume, I. Luescher, and E. Palmer. 2007. A constant affinity threshold for T cell tolerance. J. Exp. Med. 204: 2553-2559.
34. Gil, D., A. G. Schrum, M. A. Daniels, and E. Palmer. 2008. A role for CD8 in the developmental tuning of antigen recognition and CD3 conformational change. J. Immunol. 180: 3900-3909.
35. Daniels, M. A., S. L. Schober, K. A. Hogquist, and S. C. Jameson. 1999. Cutting edge: a test of the dominant negative signal model for TCR antagonism. J. Immunol. 162: 3761-3764.
36. Kranz, D. M., S. Tonegawa, and H. N. Eisen. 1984. Attachment of an antireceptor antibody to non-target cells renders them susceptible to lysis by a clone of cytotoxic T lymphocytes. Proc. Natl. Acad. Sci. USA 81: 7922-7926.
37. Speir, J. A., K. C. Garcia, A. Brunmark, M. Degano, P. A. Peterson, L. Teyton, and I. A. Wilson. 1998. Structural basis of 2C TCR allorecognition of H-2Ld peptide complexes. Immunity 8: 553-562.
38. Cochran, J. R., T. O. Cameron, and L. J. Stern. 2000. The relationship of MHC-peptide binding and T cell activation probed using chemically defined MHC class II oligomers. Immunity 12: 241-250.
39. Sun, Z. Y., S. T. Kim, I. C. Kim, A. Fahmy, E. L. Reinherz, and G. Wagner. 2004. Solution structure of the CD3epsilondelta ectodomain and comparison with CD3epsilongamma as a basis for modeling T cell receptor topology and signaling. Proc. Natl. Acad. Sci. USA 101: 16867-16872.
40. Kuhns, M. S., A. T. Girvin, L. O. Klein, R. Chen, K. D. Jensen, E. W. Newell, J. B. Huppa, B. F. Lillemeier, M. Huse, Y. H. Chien, et al. 2010. Evidence for a functional sidedness to the alphabetaTCR. Proc. Natl. Acad. Sci. USA 107: 5094-5099.
41. Lillemeier, B. F., M. A. Mörtelmaier, M. B. Forstner, J. B. Huppa, J. T. Groves, and M. M. Davis. 2010. TCR and Lat are expressed on separate protein islands on T cell membranes and concatenate during activation. Nat. Immunol. 11: 90-96.
42. Reich, Z., J. J. Boniface, D. S. Lyons, N. Borochov, E. J. Wachtel, and M. M. Davis. 1997. Ligand-specific oligomerization of T-cell receptor molecules. Nature 387: 617-620.
43. Alam, S. M., G. M. Davies, C. M. Lin, T. Zal, W. Nasholds, S. C. Jameson, K. A. Hogquist, N. R. Gascoigne, and P. J. Travers. 1999. Qualitative and quantitative differences in T cell receptor binding of agonist and antagonist ligands. Immunity 10: 227-237.
44. Deng, L., R. J. Langley, P. H. Brown, G. Xu, L. Teng, Q. Wang, M. I. Gonzales, G. G. Callender, M. I. Nishimura, S. L. Topalian, and R. A. Mariuzza. 2007. Structural basis for the recognition of mutant self by a tumor-specific, MHC class II-restricted T cell receptor. Nat. Immunol. 8: 398-408.
45. Brown, J. H., T. S. Jardetzky, J. C. Gorga, L. J. Stern, R. G. Urban, J. L. Strominger, and D. C. Wiley. 1993. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364: 33-39. (Pubitemid 23233452)
46. Schafer, P. H., S. K. Pierce, and T. S. Jardetzky. 1995. The structure of MHC class II: a role for dimer of dimers. Semin. Immunol. 7: 389-398.
47. Cherry, R. J., K. M. Wilson, K. Triantafilou, P. O'Toole, I. E. Morrison, P. R. Smith, and N. Fernández. 1998. Detection of dimers of dimers of human leukocyte antigen (HLA)-DR on the surface of living cells by single-particle fluorescence imaging. J. Cell Biol. 140: 71-79. (Pubitemid 28070895)
48. Unternaehrer, J. J., A. Chow, M. Pypaert, K. Inaba, and I. Mellman. 2007. The tetraspanin CD9 mediates lateral association of MHC class II molecules on the dendritic cell surface. Proc. Natl. Acad. Sci. USA 104: 234-239.
49. Krogsgaard, M., Q. J. Li, C. Sumen, J. B. Huppa, M. Huse, and M. M. Davis. 2005. Agonist/endogenous peptide-MHC heterodimers drive T cell activation and sensitivity. Nature 434: 238-243.
50. Yachi, P. P., J. Ampudia, N. R. Gascoigne, and T. Zal. 2005. Nonstimulatory peptides contribute to antigen-induced CD8-T cell receptor interaction at the immunological synapse. Nat. Immunol. 6: 785-792.
51. Cebecauer, M., P. Guillaume, S. Mark, O. Michielin, N. Boucheron, M. Bezard, B. H. Meyer, J. M. Segura, H. Vogel, and I. F. Luescher. 2005. CD8+ cytotoxic T lymphocyte activation by soluble major histocompatibility complex-peptide dimers. J. Biol. Chem. 280: 23820-23828.
52. Bjorkman, P. J., M. A. Saper, B. Samraoui, W. S. Bennett, J. L. Strominger, and D. C. Wiley. 1987. Structure of the human class I histocompatibility antigen, HLA-A2. Nature 329: 506-512. (Pubitemid 17131093)
53. Fooksman, D. R., S. Vardhana, G. Vasiliver-Shamis, J. Liese, D. A. Blair, J. Waite, C. Sacristán, G. D. Victora, A. Zanin-Zhorov, and M. L. Dustin. 2010. Functional anatomy of T cell activation and synapse formation. Annu. Rev. Immunol. 28: 79-105.