Structural basis for the restoration of TCR recognition of an MHC allelic variant by peptide secondary anchor substitution

Journal of Experimental Medicine

Volumn 200, Issue 11, 2004, Pages 1445-1454

  Miley, Michael J ^a   Messaoudi, Ilhem ^b,c   Metzner, Beatrix M ^b,c   Wu, Yudong ^a   Nikolich Žugich, Janko ^b,c   Fremont, Daved H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Antigen presentation; Crystallography; Herpes simplex virus 1; Major histocompatibility complex; T cells

Indexed keywords

GLUTAMIC ACID; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PEPTIDE; SERINE; T LYMPHOCYTE RECEPTOR;

ALLELE; AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CONFORMATION; CORRELATION ANALYSIS; CRYSTAL STRUCTURE; GENETIC VARIABILITY; MOLECULAR BIOLOGY; MOLECULE; PRIORITY JOURNAL; PROTEIN STRUCTURE;

EID: 10644220257     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20040217     Document Type: Article

References (46)

1. 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.
2. Madden, D.R. 1995. The three-dimensional structure of peptide-MHC complexes. Annu. Rev. Immunol. 13:587-622.
3. Bjorkman, P.J., M.A. Saper, B. Samraoui, W.S. Bennett, J.L. Strominger, and D.C. Wiley. 1987. The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature. 329:512-518.
4. Rammensee, H.G., K. Falk, and O. Rotzschke. 1993. Peptides naturally presented by MHC class I molecules. Annu. Rev. Immunol. 11:213-244.
5. van der Merwe, P.A., and S.J. Davis. 2003. Molecular interactions mediating T cell antigen recognition. Annu. Rev. Immunol. 21:659-684.
6. Hennecke, J., and D.C. Wiley. 2001. T cell receptor-MHC interactions up close. Cell. 104:1-4.
7. Garcia, K.C., L. Teyton, and I.A. Wilson. 1999. Structural basis of T cell recognition. Annu. Rev. Immunol. 17:369-397.
8. Housset, D., and B. Malissen. 2003. What do TCR-pMHC crystal structures teach us about MHC restriction and alloreactivity? Trends Immunol. 24:429-437.
9. Sloan-Lancaster, J., and P.M. Allen. 1996. Altered peptide ligand-induced partial T cell activation: molecular mechanisms and role in T cell biology. Annu. Rev. Immunol. 14:1-27.
10. Thomson, C.T., A.M. Kalergis, J.C. Sacchettini, and S.G. Nathenson. 2001. A structural difference limited to one residue of the antigenic peptide can profoundly alter the biological outcome of the TCR-peptide/MHC class I interaction. J. Immunol. 166:3994-3997.
11. Huard, R., R. Dyall, and J. Nikolic-Zugic. 1997. The critical role of a solvent-exposed residue of an MHC class I-restricted peptide in MHC-peptide binding. Int. Immunol. 9:1701-1707.
12. Wang, B., A. Sharma, R. Maile, M. Saad, E.J. Collins, and J.A. Frelinger. 2002. Peptidic termini play a significant role in TCR recognition. J. Immunol. 169:3137-3145.
13. Kersh, G.J., M.J. Miley, C.A. Nelson, A. Grakoui, S. Horvath, D.L. Donermeyer, J. Kappler, P.M. Allen, and D.H. Fremont. 2001. Structural and functional consequences of altering a peptide MHC anchor residue. J. Immunol. 166:3345-3354.
14. Dyall, R., D.H. Fremont, S.C. Jameson, and J. Nikolic-Zugic. 1996. T cell receptor (TCR) recognition of MHC class I variants: intermolecular second-site reversion provides evidence for peptide/MHC confbrmational variation. J. Exp. Med. 184:253-258.
15. Saito, N.G., H.C. Chang, and Y. Paterson. 1999. Recognition of an MHC class I-restricted antigenic peptide can be modulated by para-substitution of its buried tyrosine residues in a TCR-specific manner. J. Immunol. 162:5998-6008.
16. Nathenson, S.G., J. Geliebter, G.M. Pfaffenbach, and R.A. Zeff. 1986. Murine major histocompatibility complex class-I mutants: molecular analysis and structure-function implications. Annu. Rev. Immunol. 4:471-502.
17. Rudolph, M.G., J.A. Speir, A. Brunmark, N. Mattsson, M.R. Jackson, P.A. Peterson, L. Teyton, and I.A. Wilson. 2001. The crystal structures of K(bm1) and K(bm8) reveal that subtle changes in the peptide environment impact thermostability and alloreactivity. Immunity. 14:231-242.
18. Pullen, J.K., H.D. Hunt, and L.R. Pease. 1991. Peptide interactions with the Kb antigen recognition site. J. Immunol. 146:2145-2151.
19. 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.
20. Saito, Y., P.A. Peterson, and M. Matsumura. 1993. Quantitation of peptide anchor residue contributions to class I major histocompatibility complex molecule binding. J. Biol. Chem. 268:21309-21317.
21. Fremont, D.H., E.A. Stura, M. Matsumura, P.A. Peterson, and I.A. Wilson. 1995. Crystal structure of an H-2Kb-ovalbumin peptide complex reveals the interplay of primary and secondary anchor positions in the major histocompatibility complex binding groove. Proc. Natl. Acad. Sci. USA. 92:2479-2483.
22. Rohren, E.M., L.R. Pease, H.L. Ploegh, and T.N. Schumacher. 1993. Polymorphisms in pockets of major histocompatibility complex class I molecules influence peptide preference. J. Exp. Med. 177:1713-1721.
23. Messaoudi, I., J. LeMaoult, and J. Nikolic-Zugic. 1999. The mode of ligand recognition by two peptide:MHC class I-specific monoclonal antibodies. J. Immunol. 163:3286-3294.
24. Chattopadhyay, S., M. Theobald, J. Biggs, and L.A. Sherman. 1994. Conformational differences in major histocompatibility complex-peptide complexes can result in alloreactivity. J. Exp. Med. 179:213-219.
25. Yun, T.J., M.D. Tallquist, E.M. Rohren, J.M. Shell, and L.R. Pease. 1994. Minor pocket B influences peptide binding, peptide presentation and alloantigenicity of H-2Kb. Int. Immunol. 6:1037-1047.
26. Nikolic-Zugic, J., and F.R. Carbone. 1990. 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. 20:2431-2437.
27. Nikolic-Zugic, J., and M.J. Bevan. 1990. Role of self-peptides in positively selecting the T-cell repertoire. Nature. 344:65-67.
28. Dyall, R., I. Messaoudi, S. Janetzki, and J. Nikolic-Zugic. 2000. MHC polymorphism can enrich the T cell repertoire of the species by shifts in intrathymic selection. J. Immunol. 164:1695-1698.
29. Messaoudi, I., J.A. Guevara Patino, R. Dyall, J. LeMaoult, and J. Nikolich-Žugich. 2002. Direct link between mhc polymorphism, T cell avidity, and diversity in immune defense. Science. 298:1797-1800.
30. Busch, D.H., I.M. Pilip, S. Vijh, and E.G. Pamer. 1998. Coordinate regulation of complex T cell populations responding to bacterial infection. Immunity. 8:353-362.
31. Batalia, M.A., T.J. Kirksey, A. Sharma, L. Jiang, J.P. Abastado, S. Yan, R. Zhao, and E.J. Collins. 2000. Class I MHC is stabilized against thermal denaturation by physiological concentrations of NaCl. Biochemistry. 39:9030-9038.
32. Fahnestock, M.L., I. Tamir, L. Narhi, and P.J. Bjorkman. 1992. Thermal stability comparison of purified empty and peptide-filled forms of a class I MHC molecule. Science. 258: 1658-1662.
33. Otwinowski, Z., and W. Minor. 1997. Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307-344.
34. Jones, T.A., J.Y. Zou, S.W. Cowan, and Kjeldgaard. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta. Crystallogr. A. 47:110-119.
35. Brunger, A.T., P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, R.W. Grosse-Kunstleve, J.S. Jiang, J. Kuszewski, M. Nilges, N.S. Pannu, et al. 1998. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta. Crystallogr. D. Biol. Crystallogr. 54:905-921.
36. Carson, M. 1987. Ribbon models of macromolecules. J. Mol. Graph. 5:103-106.
37. Lawrence, M.C., and P.M. Colman. 1993. Shape complemetarity at protein/protein interfaces. J. Mol. Biol. 234:946-950.
38. Nicholls, A., K.A. Sharp, and B. Honig. 1991. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins. 11:281-296.
39. Sayle, R., M. Saqi, M. Weir, and A. Lyall. 1995. PdbAlign, PdbDist and DistAlign: tools to aid in relating sequence variability to structure. Comput. Appl. Biosci. 11:571-573.
40. McDonald, I.K., and J.M. Thornton. 1994. Satisfying hydrogen bonding potential in proteins. J. Mol. Biol. 238:777-793.
41. Messaoudi, I., J. LeMaoult, B.M. Metzner, M.J. Miley, D.H. Fremont, and J. Nikolich-Žugich. 2001. Functional evidence that conserved TCR CDR alpha 3 loop docking governs the cross-recognition of closely related peptide:class I complexes. J. Immunol. 167:836-843.
42. Sharma, A.K., J.J. Kuhns, S. Yan, R.H. Friedline, B. Long, R. Tisch, and E.J. Collins. 2001. Class I major histocompatibility complex anchor substitutions alter the conformation of T cell receptor contacts. J. Biol. Chem. 276:21443-21449.
43. Peterson, D.A., R.J. DiPaolo, O. Kanagawa, and E.R. Unanue. 2001. Cutting edge: a single MHC anchor residue alters the conformation of a peptide-MHC complex inducing T cells that survive negative selection. J. Immunol. 166:5874-5877.
44. Denkberg, G., E. Klechevsky, and Y. Reiter. 2002. Modification of a tumor-derived peptide at an HLA-A2 anchor residue can alter the conformation of the MHC-peptide complex: probing with TCR-like recombinant antibodies. J. Immunol. 169:4399-4407.
45. Luz, J.G., M. Huang, K.C. Garcia, M.G. Rudolph, V. Apostolopoulos, L. Teyton, and I.A. Wilson. 2002. Structural comparison of allogeneic and syngeneic T cell receptor-peptide-major histocompatibility complex complexes: a buried alloreactive mutation subtly alters peptide presentation substantially increasing Vβ interactions. J. Exp. Med. 195:1175-1186.
46. 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.