Crystal structures of HLA-A*0201 complexed with melan-A/MART-1 26(27L)-35 peptidomimetics reveal conformational heterogeneity and highlight degeneracy of T cell recognition

Journal of Medicinal Chemistry

Volumn 53, Issue 19, 2010, Pages 7061-7066

  Douat Casassus, Céline ^a   Borbulevych, Oleg ^c   Tarbe, Marion ^a   Gervois, Nadine ^b   Jotereau, Francine ^b   Baker, Brian M ^c   Quideau, Stéphane ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b INSERM   (France)

^c UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; HLA A2 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MELAN A; PEPTIDOMIMETIC AGENT; HLA A ANTIGEN; HLA-A*02:01 ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; OLIGOPEPTIDE; PROTEIN BINDING; TUMOR ANTIGEN; TUMOR PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; DRUG CONFORMATION; DRUG PROTEIN BINDING; DRUG STRUCTURE; HYDROGEN BOND; T LYMPHOCYTE; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; IMMUNOLOGY; MOLECULAR MIMICRY; X RAY CRYSTALLOGRAPHY;

ANTIGENS, NEOPLASM; CRYSTALLOGRAPHY, X-RAY; HLA-A ANTIGENS; HLA-A2 ANTIGEN; MART-1 ANTIGEN; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR MIMICRY; NEOPLASM PROTEINS; OLIGOPEPTIDES; PROTEIN BINDING; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES;

EID: 77957926275     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm100683p     Document Type: Article

References (32)

1. Peaper, D. R.; Cresswell, P. Regulation of MHC class I assembly and peptide binding Annu. Rev. Cell Dev. Biol. 2008, 24, 343-368
2. Rammensee, H. G.; Falk, K.; Rotzschke, O. Peptides naturally presented by MHC class I molecules Annu. Rev. Immunol. 1993, 11, 213-244
3. Garcia, K. C.; Teyton, L.; Wilson, I. A. Structural basis of T cell recognition Annu. Rev. Immunol. 1999, 17, 369-397
4. Rudolph, M. G.; Wilson, I. A. The specificity of TCR/pMHC interaction Curr. Opin. Immunol. 2002, 14, 52-65
5. Murer, K.; Urosevic, M.; Willers, J.; Selvam, P.; Laine, E.; Burg, G.; Dummer, R. Expression of Melan-A/MART-1 in primary melanoma cell cultures has prognostic implication in metastatic melanoma patients Melanoma Res. 2004, 14, 257-262
6. Pittet, M. J.; Valmori, D.; Dunbar, P. R.; Speiser, D. E.; Liénard, D.; Lejeune, F.; Fleischhauer, K.; Cerundolo, V.; Cerottini, J. C.; Romero, P. High frequencies of naive Melan-A/MART-1-specific CD8+ T cells in a large proportion of human histocompatibility leukocyte antigen (HLA)-A2 individuals J. Exp. Med. 1999, 190, 705-715
7. Valmori, D.; Fonteneau, J. F.; Maranon Lizana, C.; Gervois, N.; Liénard, D.; Rimoldi, D.; Jongeneel, C. V.; Jotereau, F.; Cerottini, J. C.; Romero, P. Enhanced generation of specific tumor-reactive CTL in vitro by selected Melan-A/MART-1 immunodominant peptide analogs J. Immunol. 1998, 160, 1750-1758
8. Nisticò, P.; Capone, I.; Palermo, B.; Del Bello, D.; Ferraresi, V.; Moschella, F.; Aricò, E.; Valentini, M.; Bracci, L.; Cognetti, F.; Ciccarese, M.; Vercillo, G.; Roselli, M.; Fossile, E.; Tosti, M. E.; Wang, E.; Marincola, F.; Imberti, L.; Catricalà, C.; Natali, P. G.; Belardelli, F.; Proietti, E. Chemotherapy enhanced vaccine-induced immunity in melanoma patients Int. J. Cancer 2009, 124, 130-139
9. Blanchet, J. S.; Valmori, D.; Dufau, I.; Ayyoub, M.; Nguyen, C.; Guillaume, P.; Monsarrat, B.; Cerottini, J. C.; Romero, P.; Gairin, J. E. A new generation of Melan-A/MART-1 peptides that fulfill both increased immunogenicity and high resistance to biodegradation: implication for molecular anti-melanoma immunotherapy J. Immunol. 2001, 167, 5852-5861
10. Quesnel, A.; Zerbib, A.; Connan, F.; Guillet, J. G.; Briand, J. P.; Choppin, J. Synthesis and antigenic properties of reduced peptide bond analogues of an immunodominant epitope of the melanoma MART-1 protein J. Pept. Sci. 2001, 7, 157-165
11. Douat-Casassus, C.; Marchand-Geneste, N.; Diez, E.; Gervois, N.; Jotereau, F.; Quideau, S. Synthetic anticancer vaccine candidates: rational design of antigenic peptide mimetics that activate tumor-specific T-cells J. Med. Chem. 2007, 50, 1598-1609
12. Sliz, P.; Michielin, O.; Cerottini, J. C.; Luescher, I.; Romero, P.; Karplus, M.; Wiley, D. C. Structures of two closely related but antigenically distinct HLA-A2/melanocyte-melanoma tumor-antigen peptide complexes J. Immunol. 2001, 167, 3276-3284
13. 26/27-35 peptide/HLA-A2 complexes reveal a remarkable disconnect between antigen structural homology and T cell recognition J. Mol. Biol. 2007, 372, 1123-1136
14. Baxter, T. K.; Gagnon, S. J.; Davis-Harrison, R. L.; Beck, J. C.; Binz, A. K.; Turner, R. V.; Biddison, W. E.; Baker, B. M. Strategic mutations in the class I major histocompatibility complex HLA-A2 independently affect both peptide binding and T cell receptor recognition J. Biol. Chem. 2004, 279, 29175-29184 and references cited therein
15. Gagnon, S. J.; Borbulevych, O. Y.; Davis-Harrison, R. L.; Baxter, T. K.; Clemens, J. R.; Armstrong, K. M.; Turner, R. V.; Damirjian, M.; Biddison, W. E.; Baker, B. M. Unrevealing a hotspot for TCR recognition on HLA-A2: evidence against the existence of peptide-independent TCR binding determinants J. Mol. Biol. 2005, 353, 556-573 and references cited therein
16. Bouvier, M.; Wiley, D. C. Importance of peptide amino and carboxyl termini to the stability of MHC class I molecules Science 1994, 265, 398-402
17. Madden, D. R. The three-dimensional structure of peptide-MHC complexes Annu. Rev. Immunol. 1995, 13, 587-622
18. Purcell, A. W.; McCluskey, J.; Rossjohn, J. More than one reason to rethink the use of peptides in vaccine design Nat. Drug Discovery 2007, 6, 404-414
19. Macdonald, W. A.; Chen, Z.; Gras, S.; Archbold, J. K.; Tynan, F. E.; Clements, C. S.; Bharadwaj, M.; Kjer-Nielsen, L.; Saunders, P. M.; Wilce, M. C. J.; Crawford, F.; Stadinsky, B.; Jackson, D.; Brooks, A. G.; Purcell, A. W.; Kappler, J. W.; Burrows, S. R.; Rossjohn, J.; McCluskey, J. T cell allorecognition via molecular mimicry Immunity 2009, 31, 897-908
20. Armstrong, K. M.; Piepenbrink, K. H.; Baker, B. M. Conformational changes and flexibility in T-cell receptor recognition of peptide-MHC complexes Biochem. J. 2008, 415, 183-196
21. Borbulevych, O. Y.; Insaidoo, F. K.; Baxter, T. K.; Powell, D. J., Jr.; Johnson, L. A.; Restifo, N. P.; Baker, B. M. Structures of MART-1(26/27-35) peptide/HLA-A2 complexes reveal a remarkable disconnect between antigen structural homology and T cell recognition J. Mol. Biol. 2007, 372, 1123-1136
22. Gagnon, S. J.; Borbulevych, O. Y.; Davis-Harrison, R. L.; Turner, R. V.; Damirjian, M.; Wojnarowicz, A.; Biddison, W. E.; Baker, B. M. T cell receptor recognition via cooperative conformational plasticity J. Mol. Biol. 2006, 363, 228-243
23. Borbulevych, O. Y.; Piepenbrink, K. H.; Gloor, B. E.; Scott, D. R.; Sommese, R. F.; Cole, D. K.; Sewell, A. K.; Baker, B. M. T cell receptor cross-reactivity directed by antigen-dependent tuning of peptide-MHC molecular flexibility Immunity 2009, 31, 885-896
24. Cole, D. K.; Yuan, F.; Rizkallah, P. J.; Miles, J. J.; Gostick, E.; Price, D. A.; Gao, G. F.; Jakobsen, B. K.; Sewell, A. K. Germ line-governed recognition of a cancer epitope by an immunodominant human T-cell receptor J. Biol. Chem. 2009, 284, 27281-27289
25. Davis-Harrison, R. L.; Armstrong, K. M.; Baker, B. M. Two different T cell receptors use different thermodynamic strategies to recognize the same peptide/MHC ligand J. Mol. Biol. 2005, 346, 533-550
26. Otwinowski, Z.; Minor, W. Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 1997, 276, 307-326
27. Vagin, A.; Teplyakov, A. Molecular replacement with MOLREP Acta Crystallogr., Sect. D: Biol. Crystallogr. 2010, 66, 22-25
28. Murshudov, G. N.; Vagin, A. A.; Dodson, E. J. Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr., Sect. D: Biol. Crystallogr. 1997, 53, 240-255
29. Perrakis, A.; Sixma, T. K.; Wilson, K. S.; Lamzin, V. S. wARP: improvement and extension of crystallographic phases by weighted averaging of multiple-refined dummy atomic models Acta Crystallogr., Sect. D: Biol. Crystallogr. 1997, 53, 448-455
30. Emsley, P.; Cowtan, K. Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, 60, 2126-2132
31. McRee, D. E. XtalView/Xfit-a versatile program for manipulating atomic coordinates and electron density J. Struct. Biol. 1999, 125, 156-165
32. Laskowski, R. A.; MacArthur, M. W.; Moss, D. S.; Thornton, J. M. PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 1993, 26, 283-291