Thermodynamic and structural equivalence of two HLA-B27 subtypes complexed with a self-peptide

Journal of Molecular Biology

Volumn 346, Issue 5, 2005, Pages 1367-1379

  Hülsmeyer, Martin ^a   Welfle, Karin ^b   Pöhlmann, Thomas ^a   Misselwitz, Rolf ^b   Alexiev, Ulrike ^a   Welfle, Heinz ^b   Saenger, Wolfram ^a   Uchanska Ziegler, Barbara ^c   Ziegler, Andreas ^c  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Crystal structure; F pocket; HLA B27 subtypes; Microcalorimetry; Thermostability

Indexed keywords

AMINO ACID DERIVATIVE; ASPARTIC ACID; BUTYRATE RESPONSE FACTOR 1; EPIDERMAL GROWTH FACTOR DERIVATIVE; HISTIDINE; HLA B27 ANTIGEN; PEPTIDE DERIVATIVE; UNCLASSIFIED DRUG; WATER;

AMINO ACID SUBSTITUTION; ARTICLE; CIRCULAR DICHROISM; COMPLEX FORMATION; CONTROLLED STUDY; CORRELATION ANALYSIS; CRYSTAL STRUCTURE; CYTOTOXIC T LYMPHOCYTE; DEGRADATION KINETICS; DERIVATIZATION; DIFFERENTIAL SCANNING CALORIMETRY; DISSOCIATION; FLUORESCENCE POLARIZATION; GENE; HLA B27 GENE; HUMAN; HUMAN CELL; IMMUNOCHEMISTRY; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MECHANICS; PRIORITY JOURNAL; REACTION ANALYSIS; STRUCTURE ANALYSIS; THERMODYNAMICS; THERMOSTABILITY; X RAY CRYSTALLOGRAPHY;

EID: 13844276058     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.12.047     Document Type: Article

References (60)

1. D.R. Madden The three-dimensional structure of peptide-MHC complexes Annu. Rev. Immunol. 13 1995 587 622
2. E. Pamer, and P. Cresswell Mechanisms of MHC class I-restricted antigen processing Annu. Rev. Immunol. 16 1998 323 358
3. H.G. Rammensee, T. Friede, and S. Stevanovic MHC ligands and peptide motifs: first listing Immunogenetics 41 1995 178 228
4. M. Bouvier, and D.C. Wiley Importance of peptide amino and carboxyl termini to the stability of MHC class I molecules Science 265 1994 398 402
5. D.R. Madden, J.C. Gorga, J.L. Strominger, and D.C. Wiley The three-dimensional structure of HLA-B27 at 2.1 A resolution suggests a general mechanism for tight peptide binding to MHC Cell 70 1992 1035 1048
6. M.A. Saper, P.J. Bjorkman, and D.C. Wiley Refined structure of 6 the human histocompatibility antigen HLA-A2 at 2.6 A resolution J. Mol. Biol. 219 1991 277 319
7. M. Matsumura, D.H. Fremont, P.A. Peterson, and I.A. Wilson Emerging principles for the recognition of peptide antigens by MHC class I molecules Science 257 1992 927 934
8. M.A. Khan Update on spondyloarthropathies Ann. Int. Med. 136 2002 896 907
9. M. Ramos, and J.A. López de Castro HLA-B27 and the pathogenesis of spondyloarthritis Tissue Antigens 60 2002 191 205
10. R. Benjamin, and P. Parham Guilt by association: HLA-B27 and ankylosing spondylitis Immunol. Today 11 1990 137 142
11. R.L. Allen, C.A. O'Callaghan, A.J. McMichael, and P. Bowness Cutting edge: HLA-B27 can form a novel beta 2-microglobulin-free heavy chain homodimer structure J. Immunol. 162 1999 5045 5048
12. R.A. Colbert HLA-B27 misfolding: a solution to the spondyloarthropathy conundrum? Mol. Med. Today 6 2000 224 230
13. 2m-deposition disease? Trends Immunol. 24 2003 73 76
14. L.H. Boyle, J.C. Goodall, and J.S. Gaston The recognition of abnormal forms of HLA-B27 by CD4+ T cells Curr. Mol. Med. 4 2004 51 58
15. M. D'Amato, M.T. Fiorillo, C. Carcassi, A. Mathieu, A. Zuccarelli, and P.P. Bitti Relevance of residue 116 of HLA-B27 in determining susceptibility to ankylosing spondylitis Eur. J. Immunol. 25 1995 3199 3201
16. M. Ramos, A. Paradela, M. Vazquez, A. Marina, J. Vazquez, and J.A. López de Castro Differential association of HLA-B*2705 and B*2709 to ankylosing spondylitis correlates with limited peptide subsets but not with altered cell surface stability J. Biol. Chem. 277 2002 28749 28756
17. J.A. López de Castro, I. Alvarez, M. Marcilla, A. Paradela, M. Ramos, L. Sesma, and M. Vazquez HLA-B27: a registry of constitutive peptide ligands Tissue Antigens 63 2004 424 445
18. M. Hülsmeyer, R.C. Hillig, A. Volz, M. Rühl, W. Schröder, and W. Saenger HLA-B27 subtypes differentially associated with disease exhibit subtle structural alterations J. Biol. Chem. 277 2002 47844 47853
19. M. Hülsmeyer, M.T. Fiorillo, F. Bettosini, R. Sorrentino, W. Saenger, A. Ziegler, and B. Uchanska-Ziegler Dual, HLA-B27 subtype-dependent conformation of a self-peptide J. Expt. Med. 199 2004 271 281
20. M.T. Fiorillo, C. Rückert, M. Hülsmeyer, R. Sorrentino, W. Saenger, A. Ziegler, and B. Uchanska-Ziegler Allele-dependent similarity between viral and self-peptide presentation by HLA-B27 subtypes J. Biol. Chem. 280 2005 2962 2971
21. M.T. Fiorillo, M. Maragno, R. Butler, M.L. Dupuis, and R. Sorrentino CD8(+) T-cell autoreactivity to an HLA-B27-restricted self-epitope correlates with ankylosing spondylitis J. Clin. Invest. 106 2000 47 53
22. D.M. Gakamsky, P.J. Bjorkman, and I. Pecht Peptide interaction with a class I major histocompatibility complex-encoded molecule: allosteric control of the ternary complex stability Biochemistry 35 1996 14841 14848
23. D.M. Gakamsky, D.M. Davis, E. Haas, J.L. Strominger, and I. Pecht Photophysical analysis of class I major histocompatibility complex protein assembly using a xanthene-derivatized beta2-microglobulin Biophys. J. 76 1999 1552 1560
24. D.M. Gakamsky, D.M. Davis, J.L. Strominger, and I. Pecht Assembly and dissociation of human leukocyte antigen (HLA)-A2 studied by real-time fluorescence resonance energy transfer Biochemistry 39 2000 11163 11169
25. S. Dédier, S. Reinelt, T. Reitinger, G. Folkers, and D. Rognan Thermodynamic stability of HLA-B*2705 peptide complexes. Effect of peptide and major histocompatibility complex protein mutations J. Biol. Chem. 275 2000 27055 27061
26. S. Reinelt, S. Dédier, G. Asuni, G. Folkers, and D. Rognan Mutation of Cys-67 alters the thermodynamic stability of the human leukocyte antigen HLA0-B*2705 J. Biol. Chem. 276 2001 18472 18477
27. A.K. Binz, R.C. Rodriguez, W.E. Biddison, and B.M. Baker Thermodynamic and kinetic analysis of a peptide-class I MHC interaction highlights the noncovalent nature and conformational dynamics of the class I heterotrimer Biochemistry. 42 2003 4954 4961
28. R.K. Strong, M.A. Holmes, P. Li, L. Braun, N. Lee, and D.E. Geraghty HLA-E allelic variants. Correlating differential expression, peptide affinities, crystal structures, and thermal stabilities J. Biol. Chem. 278 2003 5082 5090
29. B. Uchanska-Ziegler, U. Alexiev, R.C. Hillig, M. Hülsmeyer, T. Pöhlmann, and W. Saenger J.A. Hansen B. Dupont HLA 2004. Immunobiology of the Human MHC Proceedings of the 13th International Histocompatibility Workshop and Congress 2004 IHWG Press Seattle In the press
30. R.C. Hillig, M. Hülsmeyer, W. Saenger, K. Welfle, R. Misselwitz, and H. Welfle Thermodynamic and structural analysis of peptide- and allele-dependent properties of two HLA-B27 subtypes exhibiting differential disease association J. Biol. Chem. 279 2004 652 663
31. T. Pöhlmann, R.A. Böckmann, H. Grubmüller, B. Uchanska-Ziegler, A. Ziegler, and U. Alexiev Differential peptide dynamics is linked to major histocompatibility complex polymorphism J. Biol. Chem. 279 2004 28197 28201
32. O. Rötzschke, K. Falk, S. Stevanovic, V. Gnau, G. Jung, and H.G. Rammensee Dominant aromatic/aliphatic C-terminal anchor in HLA-B*2702 and B*2705 peptide motifs Immunogenetics 39 1994 74 77
33. M.T. Fiorillo, G. Greco, M. Maragno, I. Potolicchio, A. Monizio, M.L. Dupuis, and R. Sorrentino The naturally occurring polymorphism Asp116→His116, differentiating the ankylosing spondylitis-associated HLA-B*2705 from the non-associated HLA-B*2709 subtype, influences peptide-specific CD8 T cell recognition Eur. J. Immunol. 28 1998 2508 2516
34. M.G. Rudolph, J.A. Speir, A. Brunmark, N. Mattsson, M.R. Jackson, and P.A. Peterson The crystal structures of K(bm1) and K(bm8) reveal that subtle changes in the peptide environment impact thermostability and alloreactivity Immunity 14 2001 231 242
35. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallog. 26 1993 283 291
36. M. García-Peydro, M. Marti, and J.A. López de Castro High T cell epitope sharing between two HLA-B27 subtypes (B*2705 and B*2709) differentially associated to ankylosing spondylitis J. Immunol. 163 1999 2299 2305
37. L. Sesma, V. Montserrat, J.R. Lamas, A. Marina, J. Vazquez, and J.A. López de Castro The peptide repertoires of HLA-B27 subtypes differentially associated to spondyloarthropathy (B*2704 and B*2706) differ by specific changes at three anchor positions J. Biol. Chem. 277 2002 16744 16749
38. C. López-Larrea, K. Sujirachato, N.K. Mehra, P. Chiewsilp, D. Isarangkura, and U. Kanga HLA-B27 subtypes in Asian patients with ankylosing spondylitis. Evidence for new associations Tissue Antigens 45 1995 169 176
39. A.R. Nasution, A. Mardjuadi, S. Kunmartini, N.G. Suryadhana, B. Setyohadi, and D. Sudarsono HLA-B27 subtypes positively and negatively associated with spondyloarthropathy J. Rheumatol. 24 1997 1111 1114
40. E.C. Ren, W.H. Koh, D. Sim, M.L. Boey, G.B. Wee, and S.H. Chan Possible protective role of HLA-B*2706 for ankylosing spondylitis Tissue Antigens 49 1997 67 69
41. D.N. Garboczi, D.T. Hung, and D.C. Wiley 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 1992 3429 3433
42. R. Menssen, P. Orth, A. Ziegler, and W. Saenger Decamer-like conformation of a nona-peptide bound to HLA-B*3501 due to non-standard positioning of the C terminus J. Mol. Biol. 285 1999 645 653
43. C.N. Pace, and J.M. Scholtz Measuring the Conformational Stability of a Protein T.E. Creighton Protein Structure, A Practical Approach 2nd edit. 1997 IRL Press Oxford 299 321
44. A. Horovitz, J.M. Mathews, and A.R. Fersht Alpha-helix stability in proteins. II. Factors that influence stability at an internal position J. Mol. Biol. 227 1992 560 568
45. L.M. Mayr, O. Landt, U. Hahn, and F.X. Schmid Stability and folding kinetics of ribonuclease T1 are strongly altered by the replacement of cis-proline 39 with alanine J. Mol. Biol. 231 1993 897 912
46. P.L. Privalov, and S.A. Potekhin Scanning microcalorimetry in studying temperature-induced changes in proteins Methods Enzymol. 131 1986 4 51
47. U. Alexiev, I. Rimke, and T. Pöhlmann Elucidation of the nature of the conformational changes of the EF-interhelical loop in bacteriorhodopsin and of the helix VIII on the cytoplasmic surface of bovine rhodopsin: a time-resolved fluorescence depolarization study J. Mol. Biol. 328 2003 705 719
48. M.R. Eftink The use of fluorescence methods to monitor unfolding transitions in proteins Biophys. J. 66 1994 482 501
49. T. Bergfors Seeds to crystals J. Struct. Biol. 142 2003 66 76
50. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
51. Collaborative Computational Project Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallog. sect. D 50 1994 760 763
52. G.N. Murshudov, A.A. Vagin, A. Lebedev, K.S. Wilson, and E.J. Dodson Efficient anisotropic refinement of macromolecular structures using FFT Acta Crystallog. sect. D 55 1999 247 255
53. A.T. Brünger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, and R.W. Grosse-Kunstleve Crystallography, NMR system: a new software suite for macromolecular structure determination Acta Crystallog. sect. D 54 1998 905 921
54. T.A. Jones, and M. Kjeldgaard Electron-density map interpretation Methods Enzymol. 277 1997 173 208
55. A. Perrakis, R. Morris, and V.S. Lamzin Automated protein model building combined with iterative structure refinement Nature Struct. Biol. 6 1999 458 463
56. M.D. Winn, M.N. Isupov, and G.N. Murshudov Use of TLS parameters to model anisotropic displacements in macromolecular refinement Acta Crystallog. sect. D 57 2001 122 133
57. R.W. Hooft, G. Vriend, C. Sander, and E.E. Abola Errors in protein structures Nature 381 1996 272
58. A.D. McLachlan Rapid comparison of protein structures Acta Crystallog. sect. A 38 1982 871 873
59. P.J. Kraulis MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures J. Appl. Crystallog. 24 1991 946 950
60. E.A. Merritt, and D.J. Bacon Raster3D photorealistic molecular graphics Methods Enzymol. 277 1997 505 524