Mutagenesis of Beryllium-specific TCRs suggests an unusual binding topology for antigen recognition

Journal of Immunology

Volumn 187, Issue 7, 2011, Pages 3694-3703

  Bowerman, Natalie A ^a   Falta, Michael T ^a   Mack, Douglas G ^a   Kappler, John W ^b,c   Fontenot, Andrew P ^a,b  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b DEPARTMENT OF MEDICINE   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; BERYLLIUM; HLA DP ANTIGEN; HLA DP2 ANTIGEN; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; ANIMAL CELL; ANTIGEN RECOGNITION; ARTICLE; BERYLLIOSIS; BINDING SITE; CHRONIC BERYLLIUM DISEASE; GENE; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SITE DIRECTED MUTAGENESIS; T LYMPHOCYTE; TCRA GENE; TCRB GENE;

AMINO ACID SEQUENCE; ANIMALS; BERYLLIUM; EPITOPE MAPPING; EPITOPES, T-LYMPHOCYTE; FLUORESCENT ANTIBODY TECHNIQUE; HLA-DP BETA-CHAINS; HUMANS; LYMPHOCYTE ACTIVATION; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA;

EID: 80053551839     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101872     Document Type: Article

References (42)

1. Davis, M. M., and P. J. Bjorkman. 1988. T-cell antigen receptor genes and T-cell recognition. Nature 334: 395-402.
2. Lu, L., J. Vollmer, C. Moulon, H. U. Weltzien, P. Marrack, and J. Kappler. 2003. Components of the ligand for a Ni++ reactive human T cell clone. J. Exp. Med. 197: 567-574. (Pubitemid 36314652)
3. Falta, M. T., N. A. Bowerman, S. Dai, J. W. Kappler, and A. P. Fontenot. 2010. Linking genetic susceptibility and T cell activation in beryllium-induced disease. Proc. Am. Thorac. Soc. 7: 126-129.
4. Fontenot, A. P., and L. A. Maier. 2005. Genetic susceptibility and immune-mediated destruction in beryllium-induced disease. Trends Immunol. 26: 543-549. (Pubitemid 41297685)
5. + T cells in patients with chronic beryllium disease. J. Clin. Invest. 110: 1473-1482.
6. + T cells underlies disease-susceptibility HLA-DP alleles in chronic beryllium disease. Proc. Natl. Acad. Sci. USA 97: 12717-12722.
7. Maier, L. A., D. S. McGrath, H. Sato, P. Lympany, K. Welsh, R. Du Bois, L. Silveira, A. P. Fontenot, R. T. Sawyer, E. Wilcox, and L. S. Newman. 2003. Influence of MHC class II in susceptibility to beryllium sensitization and chronic beryllium disease. J. Immunol. 171: 6910-6918. (Pubitemid 37532127)
8. Richeldi, L., K. Kreiss, M. M. Mroz, B. Zhen, P. Tartoni, and C. Saltini. 1997. Interaction of genetic and exposure factors in the prevalence of berylliosis. Am. J. Ind. Med. 32: 337-340. (Pubitemid 27330274)
9. Richeldi, L., R. Sorrentino, and C. Saltini. 1993. HLA-DPB1 glutamate 69: a genetic marker of beryllium disease. Science 262: 242-244. (Pubitemid 23344468)
10. Rosenman, K. D., M. Rossman, V. Hertzberg, M. J. Reilly, C. Rice, E. Kanterakis, and D. Monos. 2011. HLA class II DPB1 and DRB1 polymorphisms associated with genetic susceptibility to beryllium toxicity. Occup. Environ. Med. 68: 487-493.
11. Rossman, M. D., J. A. Kern, J. A. Elias, M. R. Cullen, P. E. Epstein, O. P. Preuss, T. N. Markham, and R. P. Daniele. 1988. Proliferative response of bronchoalveolar lymphocytes to beryllium. A test for chronic beryllium disease. Ann. Intern. Med. 108: 687-693.
12. + T cells is dependent on a single amino acid residue of the MHC class II b-chain. J. Immunol. 175: 7029-7037.
13. Lombardi, G., C. Germain, J. Uren, M. T. Fiorillo, R. M. Du Bois, W. Jones-Williams, C. Saltini, R. Sorrentino, and R. Lechler. 2001. HLA-DP allelespecific T cell responses to beryllium account for DP-associated susceptibility to chronic beryllium disease. J. Immunol. 166: 3549-3555. (Pubitemid 33117360)
14. Dai, S., G. A. Murphy, F. Crawford, D. G. Mack, M. T. Falta, P. Marrack, J. W. Kappler, and A. P. Fontenot. 2010. Crystal structure of HLA-DP2 and implications for chronic beryllium disease. Proc. Natl. Acad. Sci. USA 107: 7425-7430.
15. Rudolph, M. G., R. L. Stanfield, and I. A. Wilson. 2006. How TCRs bind MHCs, peptides, and coreceptors. Annu. Rev. Immunol. 24: 419-466.
16. Marrack, P., J. P. Scott-Browne, S. Dai, L. Gapin, and J. W. Kappler. 2008. Evolutionarily conserved amino acids that control TCR-MHC interaction. Annu. Rev. Immunol. 26: 171-203. (Pubitemid 351600374)
17. Sethi, D. K., D. A. Schubert, A. K. Anders, A. Heroux, D. A. Bonsor, C. P. Thomas, E. J. Sundberg, J. Pyrdol, and K. W. Wucherpfennig. 2011. A highly tilted binding mode by a self-reactive T cell receptor results in altered engagement of peptide and MHC. J. Exp. Med. 208: 91-102.
18. Hahn, M., M. J. Nicholson, J. Pyrdol, and K. W. Wucherpfennig. 2005. Unconventional topology of self peptide-major histocompatibility complex binding by a human autoimmune T cell receptor. Nat. Immunol. 6: 490-496. (Pubitemid 41716762)
19. Li, Y., Y. Huang, J. Lue, J. A. Quandt, R. Martin, and R. A. Mariuzza. 2005. Structure of a human autoimmune TCR bound to a myelin basic protein self-peptide and a multiple sclerosis-associated MHC class II molecule. EMBO J. 24: 2968-2979. (Pubitemid 41486334)
20. Kappler, J. W., N. Roehm, and P. Marrack. 1987. T cell tolerance by clonal elimination in the thymus. Cell 49: 273-280.
21. Newman, L. S., K. Kreiss, T. E. King, Jr., S. Seay, and P. A. Campbell. 1989. Pathologic and immunologic alterations in early stages of beryllium disease. Reexamination of disease definition and natural history. Am. Rev. Respir. Dis. 139: 1479-1486. (Pubitemid 19155510)
22. Fontenot, A. P., L. Gharavi, S. R. Bennett, S. J. Canavera, L. S. Newman, and B. L. Kotzin. 2003. CD28 costimulation independence of target organ versus circulating memory antigen-specific CD4+ T cells. J. Clin. Invest. 112: 776-784. (Pubitemid 38057718)
23. Yssel, H., D. Blanchard, A. Boylston, J. E. De Vries, and H. Spits. 1986. T cell clones which share T cell receptor epitopes differ in phenotype, function and specificity. Eur. J. Immunol. 16: 1187-1193. (Pubitemid 17171523)
24. Okamoto, Y., I. Kurane, A. M. Leporati, and F. A. Ennis. 1998. Definition of the region on NS3 which contains multiple epitopes recognized by dengue virus serotype-cross-reactive and flavivirus-cross-reactive, HLA-DPw2-restricted CD4+ T cell clones. J. Gen. Virol. 79: 697-704. (Pubitemid 28161942)
25. Scott-Browne, J. P., J. L. Matsuda, T. Mallevaey, J. White, N. A. Borg, J. McCluskey, J. Rossjohn, J. Kappler, P. Marrack, and L. Gapin. 2007. Germline-encoded recognition of diverse glycolipids by natural killer T cells. Nat. Immunol. 8: 1105-1113. (Pubitemid 47423758)
26. White, J., A. Pullen, K. Choi, P. Marrack, and J. W. Kappler. 1993. Antigen recognition properties of mutant Vβ3+ T cell receptors are consistent with an immunoglobulin-like structure for the receptor. J. Exp. Med. 177: 119-125. (Pubitemid 23008091)
27. Xu, H., and D. R. Littman. 1993. A kinase-independent function of Lck in potentiating antigen-specific T cell activation. Cell 74: 633-643. (Pubitemid 23259744)
28. Watson, A. J., R. DeMars, I. S. Trowbridge, and F. H. Bach. 1983. Detection of a novel human class II HLA antigen. Nature 304: 358-361. (Pubitemid 13072758)
29. Huseby, E. S., F. Crawford, J. White, P. Marrack, and J. W. Kappler. 2006. Interface-disrupting amino acids establish specificity between T cell receptors and complexes of major histocompatibility complex and peptide. Nat. Immunol. 7: 1191-1199. (Pubitemid 44594315)
30. Kreiss, K., L. S. Newman, M. M. Mroz, and P. A. Campbell. 1989. Screening blood test identifies subclinical beryllium disease. J. Occup. Med. 31: 603-608. (Pubitemid 19179743)
31. Mroz, M. M., K. Kreiss, D. C. Lezotte, P. A. Campbell, and L. S. Newman. 1991. Reexamination of the blood lymphocyte transformation test in the diagnosis of chronic beryllium disease. J. Allergy Clin. Immunol. 88: 54-60.
32. Fontenot, A. P., M. T. Falta, B. M. Freed, L. S. Newman, and B. L. Kotzin. 1999. Identification of pathogenic T cells in patients with beryllium-induced lung disease. J. Immunol. 163: 1019-1026. (Pubitemid 29328115)
33. Fontenot, A. P., B. L. Kotzin, C. E. Comment, and L. S. Newman. 1998. Expansions of T-cell subsets expressing particular T-cell receptor variable regions in chronic beryllium disease. Am. J. Respir. Cell Mol. Biol. 18: 581-589. (Pubitemid 128353633)
34. Manning, T. C., C. J. Schlueter, T. C. Brodnicki, E. A. Parke, J. A. Speir, K. C. Garcia, L. Teyton, I. A. Wilson, and D. M. Kranz. 1998. Alanine scanning mutagenesis of an alphabeta T cell receptor: mapping the energy of antigen recognition. Immunity 8: 413-425. (Pubitemid 28196796)
35. Lee, P. U., H. R. Churchill, M. Daniels, S. C. Jameson, and D. M. Kranz. 2000. Role of 2CT cell receptor residues in the binding of self- and allo-major histocompatibility complexes. J. Exp. Med. 191: 1355-1364. (Pubitemid 30227123)
36. Colf, L. A., A. J. Bankovich, N. A. Hanick, N. A. Bowerman, L. L. Jones, D. M. Kranz, and K. C. Garcia. 2007. How a single T cell receptor recognizes both self and foreign MHC. Cell 129: 135-146. (Pubitemid 46507586)
37. Wu, L. C., D. S. Tuot, D. S. Lyons, K. C. Garcia, and M. M. Davis. 2002. Two-step binding mechanism for T-cell receptor recognition of peptide MHC. Nature 418: 552-556. (Pubitemid 34851403)
38. Gras, S., S. R. Burrows, L. Kjer-Nielsen, C. S. Clements, Y. C. Liu, L. C. Sullivan, M. J. Bell, A. G. Brooks, A. W. Purcell, J. McCluskey, and J. Rossjohn. 2009. The shaping of T cell receptor recognition by self-tolerance. Immunity 30: 193-203.
39. Jerne, N. K. 1971. The somatic generation of immune recognition. Eur. J. Immunol. 1: 1-9.
40. Sim, B. C., L. Zerva, M. I. Greene, and N. R. Gascoigne. 1996. Control of MHC restriction by TCR Valpha CDR1 and CDR2. Science 273: 963-966. (Pubitemid 26275174)
41. Feng, D., C. J. Bond, L. K. Ely, J. Maynard, and K. C. Garcia. 2007. Structural evidence for a germline-encoded T cell receptor-major histocompatibility complex interaction 'codon'. Nat. Immunol. 8: 975-983. (Pubitemid 47300012)
42. Painter, C. A., A. Cruz, G. E. López, L. J. Stern, and Z. Zavala-Ruiz. 2008. Model for the peptide-free conformation of class II MHC proteins. PLoS ONE 3: e2403.