Disparate epitopes mediating protective heterologous immunity to unrelated viruses share peptide-MHC structural features recognized by cross-reactive T cells

Journal of Immunology

Volumn 191, Issue 10, 2013, Pages 5139-5152

  Shen, Zu T ^a   Nguyen, Tina T ^a   Daniels, Keith A ^a   Welsh, Raymond M ^a   Stern, Lawrence J ^a,b  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE; EPITOPE; GLYCOPROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD8+ T LYMPHOCYTE; CELL SPECIFICITY; CONTROLLED STUDY; CROSS REACTION; CRYSTAL STRUCTURE; IMMUNE RESPONSE; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; REACTION ANALYSIS; T LYMPHOCYTE; VACCINIA VIRUS; ANIMAL; C57BL MOUSE; CELL LINE; HETEROLOGOUS IMMUNITY; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; LYMPHOCYTIC CHORIOMENINGITIS; ULTRASTRUCTURE; VACCINIA; X RAY CRYSTALLOGRAPHY;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; CROSS REACTIONS; CRYSTALLOGRAPHY, X-RAY; EPITOPES, T-LYMPHOCYTE; GLYCOPROTEINS; IMMUNITY, HETEROLOGOUS; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MICE, INBRED C57BL; RECEPTORS, ANTIGEN, T-CELL; VACCINIA; VACCINIA VIRUS;

EID: 84887500887     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300852     Document Type: Article

References (45)

1. Selin, L. K., M. A. Brehm, Y. N. Naumov, M. Cornberg, S. K. Kim, S. C. Clute, and R. M. Welsh. 2006. Memory of mice and men: CD8+ T-cell cross-reactivity and heterologous immunity. Immunol. Rev. 211:164-181.
2. Selin, L. K., M. Cornberg, M. A. Brehm, S. K. Kim, C. Calcagno, D. Ghersi, R. Puzone, F. Celada, and R. M. Welsh. 2004. CD8 memory T cells: crossreactivity and heterologous immunity. Semin. Immunol. 16:335-347.
3. Welsh, R. M., J. W. Che, M. A. Brehm, and L. K. Selin. 2010. Heterologous immunity between viruses. Immunol. Rev. 235:244-266.
4. Wedemeyer, H., E. Mizukoshi, A. R. Davis, J. R. Bennink, and B. Rehermann. 2001. Cross-reactivity between hepatitis C virus and Influenza A virus determinant-specific cytotoxic T cells. J. Virol. 75:11392-11400.
5. Urbani, S., B. Amadei, P. Fisicaro, M. Pilli, G. Missale, A. Bertoletti, and C. Ferrari. 2005. Heterologous T cell immunity in severe hepatitis C virus infection. J. Exp. Med. 201:675-680.
6. Chen, A. T., M. Cornberg, S. Gras, C. Guillonneau, J. Rossjohn, A. Trees, S. Emonet, J. C. De La Torre, R. M. Welsh, and L. K. Selin. 2012. Loss of antiviral immunity by infection with a virus encoding a cross-reactive pathogenic epitope. PLoS Pathog. 8:e1002633.
7. Clute, S. C., L. B. Watkin, M. Cornberg, Y. N. Naumov, J. L. Sullivan, K. Luzuriaga, R. M. Welsh, and L. K. Selin. 2005. Cross-reactive influenza virus-specific CD8+ T cells contribute to lymphoproliferation in Epstein-Barr virus-associated infectious mononucleosis. J. Clin. Invest. 115:3602-3612.
8. Cornberg, M., S. C. Clute, L. B. Watkin, F. M. Saccoccio, S. K. Kim, Y. N. Naumov, M. A. Brehm, N. Aslan, R. M. Welsh, and L. K. Selin. 2010. CD8 T cell cross-reactivity networks mediate heterologous immunity in human EBV and murine vaccinia virus infections. J. Immunol. 184:2825-2838.
9. Mathew, A., I. Kurane, S. Green, H. A. Stephens, D. W. Vaughn, S. Kalayanarooj, S. Suntayakorn, D. Chandanayingyong, F. A. Ennis, and A. L. Rothman. 1998. Predominance of HLA-restricted cytotoxic T-lymphocyte responses to serotype-cross-reactive epitopes on nonstructural proteins following natural secondary dengue virus infection. J. Virol. 72:3999-4004.
10. Rothman, A. L. 2009. T lymphocyte responses to heterologous secondary dengue virus infections. Ann. N. Y. Acad. Sci. 1171 (Suppl. 1):E36-E41.
11. Cornberg, M., A. T. Chen, L. A. Wilkinson, M. A. Brehm, S. K. Kim, C. Calcagno, D. Ghersi, R. Puzone, F. Celada, R. M. Welsh, and L. K. Selin. 2006. Narrowed TCR repertoire and viral escape as a consequence of heterologous immunity. J. Clin. Invest. 116:1443-1456.
12. Cornberg, M., B. S. Sheridan, F. M. Saccoccio, M. A. Brehm, and L. K. Selin. 2007. Protection against vaccinia virus challenge by CD8 memory T cells resolved by molecular mimicry. J. Virol. 81:934-944.
13. Chen, H. D., A. E. Fraire, I. Joris, M. A. Brehm, R. M. Welsh, and L. K. Selin. 2001. Memory CD8+ T cells in heterologous antiviral immunity and immunopathology in the lung. Nat. Immunol. 2:1067-1076.
14. Selin, L. K., K. Vergilis, R. M. Welsh, and S. R. Nahill. 1996. Reduction of otherwise remarkably stable virus-specific cytotoxic T lymphocyte memory by heterologous viral infections. J. Exp. Med. 183:2489-2499.
15. Kim, S. K., M. Cornberg, X. Z. Wang, H. D. Chen, L. K. Selin, and R. M. Welsh. 2005. Private specificities of CD8 T cell responses control patterns of heterologous immunity. J. Exp. Med. 201:523-533.
16. Shen, Z. T., M. A. Brehm, K. A. Daniels, A. B. Sigalov, L. K. Selin, R. M. Welsh, and L. J. Stern. 2010. Bi-specific MHC heterodimers for characterization of cross-reactive T cells. J. Biol. Chem. 285:33144-33153.
17. Yin, Y., and R. A. Mariuzza. 2009. The multiple mechanisms of T cell receptor cross-reactivity. Immunity 31:849-851.
18. Hardardottir, F., J. L. Baron, and C. A. Janeway, Jr. 1995. T cells with two functional antigen-specific receptors. Proc. Natl. Acad. Sci. USA 92:354-358.
19. He, X., C. A. Janeway, Jr., M. Levine, E. Robinson, P. Preston-Hurlburt, C. Viret, and K. Bottomly. 2002. Dual receptor T cells extend the immune repertoire for foreign antigens. Nat. Immunol. 3:127-134.
20. Zal, T., S. Weiss, A. Mellor, and B. Stockinger. 1996. Expression of a second receptor rescues self-specific T cells from thymic deletion and allows activation of autoreactive effector function. Proc. Natl. Acad. Sci. USA 93:9102-9107.
21. Chaudhri, G., B. J. Quah, Y. Wang, A. H. Tan, J. Zhou, G. Karupiah, and C. R. Parish. 2009. T cell receptor sharing by cytotoxic T lymphocytes facilitates efficient virus control. Proc. Natl. Acad. Sci. USA 106:14984-14989.
22. Macdonald, W. A., Z. Chen, S. Gras, J. K. Archbold, F. E. Tynan, C. S. Clements, M. Bharadwaj, L. Kjer-Nielsen, P. M. Saunders, M. C. Wilce, et al. 2009. T cell allorecognition via molecular mimicry. Immunity 31:897-908.
23. Borbulevych, O. Y., K. H. Piepenbrink, B. E. Gloor, D. R. Scott, R. F. Sommese, D. K. Cole, A. K. Sewell, and B. M. Baker. 2009. T cell receptor cross-reactivity directed by antigen-dependent tuning of peptide-MHC molecular flexibility. Immunity 31:885-896.
24. Borbulevych, O. Y., S. M. Santhanagopolan, M. Hossain, and B. M. Baker. 2011. TCRs used in cancer gene therapy cross-react with MART-1/Melan-A tumor antigens via distinct mechanisms. J. Immunol. 187:2453-2463.
25. Borbulevych, O. Y., K. H. Piepenbrink, and B. M. Baker. 2011. Conformational melding permits a conserved binding geometry in TCR recognition of foreign and self molecular mimics. J. Immunol. 186:2950-2958.
26. Mazza, C., N. Auphan-Anezin, C. Gregoire, A. Guimezanes, C. Kellenberger, A. Roussel, A. Kearney, P. A. Van Der Merwe, A. M. Schmitt-Verhulst, and B. Malissen. 2007. How much can a T-cell antigen receptor adapt to structurally distinct antigenic peptides? EMBO J. 26:1972-1983.
27. 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.
28. Garboczi, D. N., D. T. Hung, and D. C. Wiley. 1992. HLA-A2-peptide complexes: refolding and crystallization of molecules expressed in Escherichia coli and complexed with single antigenic peptides. Proc. Natl. Acad. Sci. USA 89:3429-3433.
29. Schumacher, T. N., M. T. Heemels, J. J. Neefjes, W. M. Kast, C. J. Melief, and H. L. Ploegh. 1990. Direct binding of peptide to empty MHC class I molecules on intact cells and in vitro. Cell 62:563-567.
30. Niesen, F. H., H. Berglund, and M. Vedadi. 2007. The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nat. Protoc. 2:2212-2221.
31. Selin, L. K., S. R. Nahill, and R. M. Welsh. 1994. Cross-reactivities in memory cytotoxic T lymphocyte recognition of heterologous viruses. J. Exp. Med. 179:1933-1943.
32. Yang, H. Y., P. L. Dundon, S. R. Nahill, and R. M. Welsh. 1989. Virus-induced polyclonal cytotoxic T lymphocyte stimulation. J. Immunol. 142:1710-1718.
33. Minor, W., M. Cymborowski, Z. Otwinowski, and M. Chruszcz. 2006. HKL-3000: the integration of data reduction and structure solution-from diffraction images to an initial model in minutes. Acta Crystallogr. D Biol. Crystallogr. 62:859-866.
34. McCoy, A. J., R. W. Grosse-Kunstleve, P. D. Adams, M. D. Winn, L. C. Storoni, and R. J. Read. 2007. Phaser crystallographic software. J. Appl. Cryst. 40:658-674.
35. Brunger, A. T. 2007. Version 1.2 of the crystallography and NMR system. Nat. Protoc. 2:2728-2733.
36. Emsley, P., and K. Cowtan. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132.
37. Adams, P. D., P. V. Afonine, G. Bunkóczi, V. B. Chen, I. W. Davis, N. Echols, J. J. Headd, L. W. Hung, G. J. Kapral, R. W. Grosse-Kunstleve, et al. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66:213-221.
38. Moskophidis, D., F. Lechner, H. Pircher, and R. M. Zinkernagel. 1993. Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature 362:758-761.
39. Santori, F. R., I. Arsov, and S. Vukmanović. 2001. Modulation of CD8+ T cell response to antigen by the levels of self MHC class I. J. Immunol. 166:5416-5421.
40. Fremont, D. H., M. Matsumura, E. A. Stura, P. A. Peterson, and I. A. Wilson. 1992. Crystal structures of two viral peptides in complex with murine MHC class I H-2Kb. Science 257:919-927.
41. Matsumura, M., D. H. Fremont, P. A. Peterson, and I. A. Wilson. 1992. Emerging principles for the recognition of peptide antigens by MHC class I molecules. Science 257:927-934.
42. Kim, S. K., M. A. Brehm, R. M. Welsh, and L. K. Selin. 2002. Dynamics of memory T cell proliferation under conditions of heterologous immunity and bystander stimulation. J. Immunol. 169:90-98.
43. Riberdy, J. M., A. Zirkel, S. Surman, J. L. Hurwitz, and P. C. Doherty. 2001. Cutting edge: culture with high doses of viral peptide induces previously unprimed CD8 (+) T cells to produce cytokine. J. Immunol. 167:2437-2440.
44. Achour, A., J. Michaëlsson, R. A. Harris, J. Odeberg, P. Grufman, J. K. Sandberg, V. Levitsky, K. Kärre, T. Sandalova, and G. Schneider. 2002. A structural basis for LCMV immune evasion: subversion of H-2D (b) and H-2K (b) presentation of gp33 revealed by comparative crystal structure. Analyses. Immunity 17:757-768.
45. Khanolkar, A., M. J. Fuller, and A. J. Zajac. 2004. CD4 T cell-dependent CD8 T cell maturation. J. Immunol. 172:2834-2844.