Fixing an irrelevant TCRα chain reveals the importance of TCRβ diversity for optimal TCRαβ pairing and function of virus-specific CD8+ T cells

European Journal of Immunology

Volumn 40, Issue 9, 2010, Pages 2470-2481

  Valkenburg, Sophie A ^a   Day, E Bridie ^a   Swan, Natasha G ^a   Croom, Hayley A ^a   Carbone, Francis R ^a   Doherty, Peter C ^a,b   Turner, Stephen J ^a   Kedzierska, Katherine ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

CD8+ T cells; Influenza; TCR repertoire; Viral infection

Indexed keywords

T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; CORE PROTEIN; CYTOKINE; H-2KB PROTEIN, MOUSE; H2 ANTIGEN; H2D ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; NUCLEOPROTEIN (366-374), INFLUENZA VIRUS; OVALBUMIN; PEPTIDE FRAGMENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CONTROLLED STUDY; IMMUNE RESPONSE; INFLUENZA; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE; VIRUS LOAD; ANIMAL; C57BL MOUSE; CELL CULTURE; GENETIC VARIABILITY; GENETICS; IMMUNOLOGY; INFLUENZA VIRUS A; LUNG; METABOLISM; ORTHOMYXOVIRUS INFECTION; PATHOGENICITY; PATHOLOGY; PROTEIN MULTIMERIZATION; SECRETION (PROCESS); T LYMPHOCYTE RECEPTOR GENE; VIROLOGY;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CYTOKINES; GENES, T-CELL RECEPTOR BETA; GENETIC VARIATION; H-2 ANTIGENS; INFLUENZA A VIRUS; LUNG; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; ORTHOMYXOVIRIDAE INFECTIONS; OVALBUMIN; PEPTIDE FRAGMENTS; PROTEIN MULTIMERIZATION; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; VIRAL CORE PROTEINS; HISTOCOMPATIBILITY ANTIGEN H-2D;

EID: 77956471264     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201040473     Document Type: Article

References (41)

1. Arstila, T. P., Casrouge, A., Baron, V., Even, J., Kanellopoulos, J. and Kourilsky, P., A direct estimate of the human alphabeta T cell receptor diversity. Science 1999. 286: 958-961.
2. Casrouge, A., Beaudoing, E., Dalle, S., Pannetier, C., Kanellopoulos, J. and Kourilsky, P., Size estimate of the alpha beta TCR repertoire of naive mouse splenocytes. J. Immunol. 2000. 164: 5782-5787.
3. Turner, S. J., Doherty, P. C., McCluskey, J. and Rossjohn, J., Structural determinants of T-cell receptor bias in immunity. Nat. Rev. Immunol. 2006. 6: 883-894.
4. Davis, M. M., McHeyzer-Williams, M. and Chien, Y. H., T-cell receptor V-region usage and antigen specificity. The cytochrome c model system. Ann. NY Acad. Sci. 1995. 756: 1-11.
5. Kjer-Nielsen, L., Clements, C. S., Purcell, A. W., Brooks, A. G., Whisstock, J. C., Burrows, S. R., McCluskey, J. and Rossjohn, J., A structural basis for the selection of dominant alphabeta T cell receptors in antiviral immunity. Immunity 2003. 18: 53-64.
6. Messaoudi, I., Guevara Patino, J. A., Dyall, R., LeMaoult, J. and Nikolich-Zugich, J., Direct link between mhc polymorphism, T cell avidity, and diversity in immune defense. Science 2002. 298: 1797-1800.
7. Price, D. A., West, S. M., Betts, M. R., Ruff, L. E., Brenchley, J. M., Ambrozak, D. R., Edghill-Smith, Y. et al., T cell receptor recognition motifs govern immune escape patterns in acute SIV infection. Immunity 2004. 21: 793-803.
8. Chothia, C., Boswell, D. R. and Lesk, A. M., The outline structure of the T-cell alpha beta receptor. EMBO J. 1988. 7: 3745-3755.
9. Garboczi, D. N. and Biddison, W. E., Shapes of MHC restriction. Immunity 1999. 10: 1-7.
10. Garboczi, D. N., Ghosh, P., Utz, U., Fan, Q. R., Biddison, W. E. and Wiley, D. C., Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature 1996. 384: 134-141.
11. Garcia, K. C., Degano, M., Stanfield, R. L., Brunmark, A., Jackson, M. R., Peterson, P. A., Teyton, L. and Wilson, I. A., An alphabeta T cell receptor structure at 2.5 A and its orientation in the TCR-MHC complex. Science 1996. 274: 209-219.
12. Stewart-Jones, G. B., McMichael, A. J., Bell, J. I., Stuart, D. I. and Jones, E. Y., A structural basis for immunodominant human T cell receptor recognition. Nat. Immunol. 2003. 4: 657-663.
13. Turner, S. J., Diaz, G., Cross, R. and Doherty, P. C., Analysis of clonotype distribution and persistence for an influenza virus-specific CD8+T cell response. Immunity 2003. 18: 549-559.
14. Kedzierska, K., Turner, S. J. and Doherty, P. C., Conserved T cell receptor usage in primary and recall responses to an immunodominant influenza virus nucleoprotein epitope. Proc. Natl. Acad. Sci. USA 2004. 101: 4942-4947.
15. Zhong, W. and Reinherz, E. L., In vivo selection of a TCR Vbeta repertoire directed against an immunodominant influenza virus CTL epitope. Int. Immunol. 2004. 16: 1549-1559.
16. Zhong, W., Dixit, S. B., Mallis, R. J., Arthanari, H., Lugovskoy, A. A., Beveridge, D. L., Wagner, G. and Reinherz, E. L., CTL recognition of a protective immunodominant influenza A virus nucleoprotein epitope utilizes a highly restricted Vbeta but diverse Valpha repertoire: functional and structural implications. J. Mol. Biol. 2007. 372: 535-548.
17. Turner, S. J., Kedzierska, K., Komodromou, H., La Gruta, N. L., Dunstone, M. A., Webb, A. I., Webby, R. et al., Lack of prominent peptide-major histocompatibility complex features limits repertoire diversity in virus-specific CD8(+) T cell populations. Nat. Immunol. 2005. 6: 382-389.
18. Turner, S. J., Cose, S. C. and Carbone, F. R., TCR alpha-chain usage can determine antigen-selected TCR beta-chain repertoire diversity. J. Immunol. 1996. 157: 4979-4985.
19. Feng, D., Bond, C. J., Ely, L. K., Maynard, J. and Garcia, K. C., Structural evidence for a germline-encoded T cell receptor-major histocompatibility complex interaction 'codon'. Nat. Immunol. 2007. 8: 975-983.
20. Scott-Browne, J. P., White, J., Kappler, J. W., Gapin, L. and Marrack, P., Germline-encoded amino acids in the alphabeta T-cell receptor control thymic selection. Nature 2009. 458: 1043-1046.
21. Kedzierska, K., Venturi, V., Valkenburg, S. A., Davenport, M. P., Turner, S. J. and Doherty, P. C., Homogenization of TCR repertoires within secondary CD62Lhigh and CD62Llow virus-specific CD8+T cell populations. J. Immunol. 2008. 180: 7938-7947.
22. Kedzierska, K., Guillonneau, C., Gras, S., Hatton, L. A., Webby, R., Purcell, A. W., Rossjohn, J. et al., Complete modification of TCR specificity and repertoire selection does not perturb a CD8+T cell immunodominance hierarchy. Proc. Natl. Acad. Sci. USA 2008. 105: 19408-19413.
23. Kedzierska, K., La Gruta, N. L., Stambas, J., Turner, S. J. and Doherty, P. C., Tracking phenotypically and functionally distinct T cell subsets via T cell repertoire diversity. Mol. Immunol. 2008. 45: 607-618.
24. Kedzierska, K., Day, E. B., Pi, J., Heard, S. B., Doherty, P. C., Turner, S. J. and Perlman, S., Quantification of repertoire diversity of influenza-specific epitopes with predominant public or private TCR usage. J. Immunol. 2006. 177: 6705-6712.
25. Kedzierska, K., Thomas, P. G., Venturi, V., Davenport, M. P., Doherty, P. C., Turner, S. J. and La Gruta, N. L., Terminal deoxynucleotidyltransferase is required for the establishment of private virus-specific CD8+TCR repertoires and facilitates optimal CTL responses. J. Immunol. 2008. 181: 2556-2562.
26. Heath, W. R. and Miller, J. F., Expression of two alpha chains on the surface of T cells in T cell receptor transgenic mice. J. Exp. Med. 1993. 178: 1807-1811.
27. La Gruta, N. L., Turner, S. J. and Doherty, P. C., Hierarchies in cytokine expression profiles for acute and resolving influenza virus-specific CD8+ T cell responses: correlation of cytokine profile and TCR avidity. J. Immunol. 2004. 172: 5553-5560.
28. Darrah, P. A., Patel, D. T., De Luca, P. M., Lindsay, R. W., Davey, D. F., Flynn, B. J., Hoff, S. T. et al., Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat. Med. 2007. 13: 843-850.
29. Betts, M. R., Nason, M. C., West, S. M., De Rosa, S. C., Migueles, S. A., Abraham, J., Lederman, M. M. et al., HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+T cells. Blood 2006. 107: 4781-4789.
30. Daucher, M., Price, D. A., Brenchley, J. M., Lamoreaux, L., Metcalf, J. A., Rehm, C., Nies-Kraske, E. et al., Virological outcome after structured interruption of antiretroviral therapy for human immunodeficiency virus infection is associated with the functional profile of virus-specific CD8+ T cells. J. Virol. 2008. 82: 4102-4114.
31. Kim, S. K., Cornberg, M., Wang, X. Z., Chen, H. D., Selin, L. K. and Welsh, R. M., Private specificities of CD8 T cell responses control patterns of heterologous immunity. J. Exp. Med. 2005. 201: 523-533.
32. Kedzierska, K., La Gruta, N. L., Turner, S. J. and Doherty, P. C., Establishment and recall of CD8+T cell memory in a model of localized transient infection. Immunol. Rev. 2006. 211: 133-145.
33. Crowe, S. R., Turner, S. J., Miller, S. C., Roberts, A. D., Rappolo, R. A., Doherty, P. C., Ely, K. H. and Woodland, D. L., Differential antigen presentation regulates the changing patterns of CD8+T cell immunodominance in primary and secondary influenza virus infections. J. Exp. Med. 2003. 198: 399-410.
34. La Gruta, N. L., Kedzierska, K., Pang, K., Webby, R., Davenport, M. P., Chen, W., Turner, S. J. and Doherty, P. C., A virus specific CD8+T cell immunodominance hierarchy determined by antigen dose and percursor frequencies. Proc. Natl. Acad. Sci. USA 2006. 103: 994-999.
35. Malherbe, L., Hausl, C., Teyton, L. and McHeyzer-Williams, M. G., Clonal selection of helper T cells is determined by an affinity threshold with no further skewing of TCR binding properties. Immunity 2004. 21: 669-679.
36. Yokosuka, T., Takase, K., Suzuki, M., Nakagawa, Y., Taki, S., Takahashi, H., Fujisawa, T. et al., Predominant role of T cell receptor (TCR)-alpha chain in forming preimmune TCR repertoire revealed by clonal TCR reconstitution system. J. Exp. Med. 2002. 195: 991-1001.
37. Kelly, J. M., Sterry, S. J., Cose, S., Turner, S. J., Fecondo, J., Rodda, S., Fink, P. J. and Carbone, F. R., Identification of conserved T cell receptor CDR3 residues contacting known exposed peptide side chains from a major histocompatibility complex class I-bound determinant. Eur. J. Immunol. 1993. 23: 3318-3326.
38. Carbone, F. R., Sterry, S. J., Butler, J., Rodda, S. and Moore, M. W., T cell receptor alpha-chain pairing determines the specificity of residue 262 within the Kb-restricted, ovalbumin257-264 determinant. Int. Immunol. 1992. 4: 861-867.
39. Nikolic-Zugic, J. and Carbone, F. R., The effect of mutations in the MHC class I peptide binding groove on the cytotoxic T lymphocyte recognition of the Kb-restricted ovalbumin determinant. Eur. J. Immunol. 1990. 20: 2431-2437.
40. Allan, W., Tabi, Z., Cleary, A. and Doherty, P. C., Cellular events in the lymph node and lung of mice with influenza. Consequences of depleting CD4+T cells. J. Immunol. 1990. 144: 3980-3986.
41. Arden, B., Clark, S. P., Kabelitz, D. and Mak, T. W., Mouse T-cell receptor variable gene segment families. Immunogenetics 1995. 42: 501-530.