Real time detection of peptide-MHC dissociation reveals that improvement of primary MHC-binding residues can have a minimal, or no, effect on stability

Molecular Immunology

Volumn 48, Issue 4, 2011, Pages 728-732

  Miles, Kim M ^a   Miles, John J ^a,b   Madura, Florian ^a   Sewell, Andrew K ^a   Cole, David K ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

Cancer vaccines; Heteroclitic anchor residue modified peptide; Peptide major histocompatibility complex (pMHC); PMHC stability; Surface plasmon resonance (SPR); T cells

Indexed keywords

GOLD; HETEROCLITIC PEPTIDE; HLA A ANTIGEN; PEPTIDE; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ANTIGEN BINDING; ANTIGEN SPECIFICITY; ARTICLE; BINDING ASSAY; CELL SURFACE; CONTROLLED STUDY; DENSITY; DISSOCIATION; HALF LIFE TIME; IMMUNE RESPONSE; IN VIVO STUDY; MAJOR HISTOCOMPATIBILITY COMPLEX; PRIORITY JOURNAL; PROTEIN STABILITY; PROTEIN VARIANT; RECEPTOR BINDING; SENSOR; SURFACE PLASMON RESONANCE; WILD TYPE;

ALGORITHMS; AMINO ACID SEQUENCE; AMINO ACIDS; ATP-BINDING CASSETTE TRANSPORTERS; BINDING SITES; BIOLOGICAL ASSAY; CELL LINE; FLOW CYTOMETRY; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN BINDING; PROTEIN STABILITY; SURFACE PLASMON RESONANCE; TIME FACTORS;

EID: 78650612655     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2010.11.004     Document Type: Article

References (28)

1. Bell M.J., Burrows J.M., Brennan R., Miles J.J., Tellam J., McCluskey J., Rossjohn J., Khanna R., Burrows S.R. The peptide length specificity of some HLA class I alleles is very broad and includes peptides of up to 25 amino acids in length. Mol. Immunol. 2009, 46:1911-1917.
2. Bjorkman P.J., Saper M.A., Samraoui B., Bennett W.S., Strominger J.L., Wiley D.C. The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature 1987, 329:512-518.
3. Chen J.L., Dunbar P.R., Gileadi U., Jager E., Gnjatic S., Nagata Y., Stockert E., Panicali D.L., Chen Y.T., Knuth A., Old L.J., Cerundolo V. Identification of NY-ESO-1 peptide analogues capable of improved stimulation of tumor-reactive CTL. J. Immunol. 2000, 165:948-955.
4. Chen J.L., Stewart-Jones G., Bossi G., Lissin N.M., Wooldridge L., Choi E.M., Held G., Dunbar P.R., Esnouf R.M., Sami M., Boulter J.M., Rizkallah P., Renner C., Sewell A., van der Merwe P.A., Jakobsen B.K., Griffiths G., Jones E.Y., Cerundolo V. Structural and kinetic basis for heightened immunogenicity of T cell vaccines. J. Exp. Med. 2005, 201:1243-1255.
5. Cole D.K., Dunn S.M., Sami M., Boulter J.M., Jakobsen B.K., Sewell A.K. T cell receptor engagement of peptide-major histocompatibility complex class I does not modify CD8 binding. Mol. Immunol. 2008, 45:2700-2709.
6. Cole D.K., Edwards E.S., Wynn K.K., Clement M., Miles J.J., Ladell K., Ekeruche J., Gostick E., Adams K.J., Skowera A., Peakman M., Wooldridge L., Price D.A., Sewell A.K. Modification of MHC anchor residues generates heteroclitic peptides that alter TCR binding and T cell recognition. J. Immunol. 2010, 185:2600-2610.
7. Cole D.K., Rizkallah P.J., Boulter J.M., Sami M., Vuidepot A.L., Glick M., Gao F., Bell J.I., Jakobsen B.K., Gao G.F. Computational design and crystal structure of an enhanced affinity mutant human CD8 alphaalpha coreceptor. Proteins 2007, 67:65-74.
8. 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. Germline-governed recognition of a cancer epitope by an immunodominant human T-cell receptor. J. Biol. Chem. 2009, 284(40):27281-27289.
9. Falk K., Rotzschke O., Stevanovic S., Jung G., Rammensee H.G. Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature 1991, 351:290-296.
10. Guo H.C., Madden D.R., Silver M.L., Jardetzky T.S., Gorga J.C., Strominger J.L., Wiley D.C. Comparison of the P2 specificity pocket in three human histocompatibility antigens: HLA*6801, HLA A*0201, and HLA-B*2705. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:8053-8057.
11. Henderson R.A., Michel H., Sakaguchi K., Shabanowitz J., Appella E., Hunt D.F., Engelhard V.H. HLA-A2.1-associated peptides from a mutant cell line: a second pathway of antigen presentation. Science 1992, 255:1264-1266.
12. Keogh E., Fikes J., Southwood S., Celis E., Chesnut R., Sette A. Identification of new epitopes from four different tumor-associated antigens: recognition of naturally processed epitopes correlates with HLA A*0201-binding affinity. J. Immunol. 2001, 167:787-796.
13. Lienard D., Rimoldi D., Marchand M., Dietrich P.Y., van Baren N., Geldhof C., Batard P., Guillaume P., Ayyoub M., Pittet M.J., Zippelius A., Fleischhauer K., Lejeune F., Cerottini J.C., Romero P., Speiser D.E. Ex vivo detectable activation of Melan-A-specific T cells correlating with inflammatory skin reactions in melanoma patients vaccinated with peptides in IFA. Cancer Immun. 2004, 4:4.
14. Parker K.C., Bednarek M.A., Coligan J.E. Scheme for ranking potential HLA-A2 binding peptides based on independent binding of individual peptide side-chains. J. Immunol. 1994, 152:163-175.
15. Parkhurst M.R., Salgaller M.L., Southwood S., Robbins P.F., Sette A., Rosenberg S.A., Kawakami Y. Improved induction of melanoma-reactive CTL with peptides from the melanoma antigen gp100 modified at HLA A*0201-binding residues. J. Immunol. 1996, 157:2539-2548.
16. Rammensee H., Bachmann J., Emmerich N.P., Bachor O.A., Stevanovic S. SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 1999, 50:213-219.
17. Reche P.A., Glutting J.P., Zhang H., Reinherz E.L. Enhancement to the RANKPEP resource for the prediction of peptide binding to MHC molecules using profiles. Immunogenetics 2004, 56:405-419.
18. Reid S.W., McAdam S., Smith K.J., Klenerman P., O'Callaghan C.A., Harlos K., Jakobsen B.K., McMichael A.J., Bell J.I., Stuart D.I., Jones E.Y. Antagonist HIV-1 Gag peptides induce structural changes in HLA B8. J. Exp. Med. 1996, 184:2279-2286.
19. Rosenberg S.A., Yang J.C., Restifo N.P. Cancer immunotherapy: moving beyond current vaccines. Nat. Med. 2004, 10:909-915.
20. Rosenberg S.A., Yang J.C., Schwartzentruber D.J., Hwu P., Marincola F.M., Topalian S.L., Restifo N.P., Dudley M.E., Schwarz S.L., Spiess P.J., Wunderlich J.R., Parkhurst M.R., Kawakami Y., Seipp C.A., Einhorn J.H., White D.E. Immunologic and therapeutic evaluation of a synthetic peptide vaccine for the treatment of patients with metastatic melanoma. Nat. Med. 1998, 4:321-327.
21. Speiser D.E., Lienard D., Pittet M.J., Batard P., Rimoldi D., Guillaume P., Cerottini J.C., Romero P. In vivo activation of melanoma-specific CD8(+) T cells by endogenous tumor antigen and peptide vaccines A comparison to virus-specific T cells. Eur. J. Immunol. 2002, 32:731-741.
22. Terasawa H., Tsang K.Y., Gulley J., Arlen P., Schlom J. Identification and characterization of a human agonist cytotoxic T-lymphocyte epitope of human prostate-specific antigen. Clin. Cancer Res. 2002, 8:41-53.
23. Theodossis A., Guillonneau C., Welland A., Ely L.K., Clements C.S., Williamson N.A., Webb A.I., Wilce J.A., Mulder R.J., Dunstone M.A., Doherty P.C., McCluskey J., Purcell A.W., Turner S.J., Rossjohn J. Constraints within major histocompatibility complex class I restricted peptides: presentation and consequences for T-cell recognition. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:5534-5539.
24. Turner S.J., Kedzierska K., Komodromou H., La Gruta N.L., Dunstone M.A., Webb A.I., Webby R., Walden H., Xie W., McCluskey J., Purcell A.W., Rossjohn J., Doherty P.C. Lack of prominent peptide-major histocompatibility complex features limits repertoire diversity in virus-specific CD8+ T cell populations. Nat. Immunol. 2005, 6:382-389.
25. Valkenburg S.A., Gras S., Guillonneau C., La Gruta N.L., Thomas P.G., Purcell A.W., Rossjohn J., Doherty P.C., Turner S.J., Kedzierska K. Protective efficacy of cross-reactive CD8+ T cells recognising mutant viral epitopes depends on peptide-MHC-I structural interactions and T cell activation threshold. PLoS Pathog. 2010, 6:e1001039.
26. Valmori D., Fonteneau J.F., Lizana C.M., Gervois N., Lienard D., Rimoldi D., Jongeneel 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 analogues. J. Immunol. 1998, 160:1750-1758.
27. Wieckowski S., Baumgaertner P., Corthesy P., Voelter V., Romero P., Speiser D.E., Rufer N. Fine structural variations of alphabetaTCRs selected by vaccination with natural versus altered self-antigen in melanoma patients. J. Immunol. 2009, 183:5397-5406.
28. Yu Z., Theoret M.R., Touloukian C.E., Surman D.R., Garman S.C., Feigenbaum L., Baxter T.K., Baker B.M., Restifo N.P. Poor immunogenicity of a self/tumor antigen derives from peptide-MHC-I instability and is independent of tolerance. J. Clin. Invest. 2004, 114:551-559.