Altered peptide ligands revisited: Vaccine design through chemically modified hla-A2-Restricted t cell epitopes

Journal of Immunology

Volumn 193, Issue 10, 2014, Pages 4803-4813

  Hoppes, Rieuwert ^a   Oostvogels, Rimke ^b   Luimstra, Jolien J ^a   Wals, Kim ^a   Toebes, Mireille ^a   Bies, Laura ^a   Ekkebus, Reggy ^a   Rijal, Pramila ^a   Celie, Patrick H N ^a   Huang, Julie H ^b   Emmelot, Maarten E ^b   Spaapen, Robbert M ^a   Lokhorst, Henk ^b   Schumacher, Ton N M ^a   Mutis, Tuna ^b   Rodenko, Boris ^a,c   Ovaa, Huib ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICALLY ENHANCED ALTERED PEPTIDE LIGAND; EPITOPE; HLA A2 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN; MELANOMA ANTIGEN; PEPTIDE DERIVATIVE; UNCLASSIFIED DRUG; CANCER VACCINE; HLA-A*02:01 ANTIGEN; MINOR HISTOCOMPATIBILITY ANTIGEN; PEPTIDE; PROTEIN BINDING; RECOMBINANT PROTEIN; TUMOR ANTIGEN;

ALLOGENEIC RESTRICTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN BINDING; ANTIGEN RECOGNITION; ARTICLE; BINDING AFFINITY; CELL EXPANSION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOTOXIC T LYMPHOCYTE; DRUG DESIGN; DRUG SYNTHESIS; HUMAN; HUMAN CELL; IMMUNIZATION; IMMUNOGENICITY; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE PROLIFERATION; MELANOMA; MOUSE; NONHUMAN; T LYMPHOCYTE ACTIVATION; AMINO ACID SEQUENCE; ANIMAL; B LYMPHOCYTE; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; GENE EXPRESSION; GENETICS; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; NEOPLASMS; TRANSGENIC MOUSE; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, NEOPLASM; B-LYMPHOCYTES; CANCER VACCINES; CRYSTALLOGRAPHY, X-RAY; EPITOPES; GENE EXPRESSION; HLA-A2 ANTIGEN; HUMANS; IMMUNIZATION; MICE; MICE, TRANSGENIC; MINOR HISTOCOMPATIBILITY ANTIGENS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEOPLASMS; PEPTIDES; PROTEIN BINDING; RECOMBINANT PROTEINS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84910135021     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400800     Document Type: Article

References (59)

1. Hodi, F. S., S. J. O'Day, D. F. McDermott, R. W. Weber, J. A. Sosman, J. B. Haanen, R. Gonzalez, C. Robert, D. Schadendorf, J. C. Hassel, et al. 2010. Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 363: 711-723.
2. Rosenberg, S. A., J. C. Yang, and N. P. Restifo. 2004. Cancer immunotherapy: moving beyond current vaccines. Nat. Med. 10: 909-915.
3. Slansky, J. E., F. M. Rattis, L. F. Boyd, T. Fahmy, E. M. Jaffee, J. P. Schneck, D. H. Margulies, and D. M. Pardoll. 2000. Enhanced antigen-specific antitumor immunity with altered peptide ligands that stabilize the MHC-peptide-TCR complex. Immunity 13: 529-538
4. Tang, Y., Z. Lin, B. Ni, J. Wei, J. Han, H. Wang, and Y. Wu. 2007. An altered peptide ligand for naïve cytotoxic T lymphocyte epitope of TRP-2(180-188) enhanced immunogenicity. Cancer Immunol. Immunother. 56: 319-329.
5. Bowerman, N. A., L. A. Colf, K. C. Garcia, and D. M. Kranz. 2009. Different strategies adopted by K(b) and L(d) to generate T cell specificity directed against their respective bound peptides. J. Biol. Chem. 284: 32551-32561.
6. Engels, B., V. H. Engelhard, J. Sidney, A. Sette, D. C. Binder, R. B. Liu, D. M. Kranz, S. C. Meredith, D. A. Rowley, and H. Schreiber. 2013. Relapse or eradication of cancer is predicted by peptide-major histocompatibility complex affinity. Cancer Cell 23: 516-526.
7. Moutaftsi, M., S. Salek-Ardakani, M. Croft, B. Peters, J. Sidney, H. Grey, and A. Sette. 2009. Correlates of protection efficacy induced by vaccinia virusspecific CD8+ T-cell epitopes in the murine intranasal challenge model. Eur. J. Immunol. 39: 717-722.
8. van der Burg, S. H., M. J. Visseren, R. M. Brandt, W. M. Kast, and C. J. Melief. 1996. Immunogenicity of peptides bound to MHC class I molecules depends on the MHC-peptide complex stability. J. Immunol. 156: 3308-3314.
9. Yu, Z., M. R. Theoret, C. E. Touloukian, D. R. Surman, S. C. Garman, L. Feigenbaum, T. K. Baxter, B. M. Baker, and N. P. Restifo. 2004. Poor immunogenicity of a self/tumor antigen derives from peptide-MHC-I instability and is independent of tolerance. J. Clin. Invest. 114: 551-559.
10. Rudolph, M. G., R. L. Stanfield, and I. A. Wilson. 2006. How TCRs bind MHCs, peptides, and coreceptors. Annu. Rev. Immunol. 24: 419-466.
11. Evavold, B. D., J. Sloan-Lancaster, and P. M. Allen. 1993. Tickling the TCR: selective T-cell functions stimulated by altered peptide ligands. Immunol. Today 14: 602-609.
12. Valmori, D., J. F. Fonteneau, C. M. Lizana, N. Gervois, D. Liénard, D. Rimoldi, V. Jongeneel, F. Jotereau, J. C. Cerottini, and P. Romero. 1998. Enhanced generation of specific tumor-reactive CTL in vitro by selected Melan-A/MART-1 immunodominant peptide analogues. J. Immunol. 160: 1750-1758.
13. Rammensee, H. G., T. Friede, and S. Stevanoviíc. 1995. MHC ligands and peptide motifs: first listing. Immunogenetics 41: 178-228.
14. 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.
15. Silver, M. L., H. C. Guo, J. L. Strominger, and D. C. Wiley. 1992. Atomic structure of a human MHC molecule presenting an influenza virus peptide. Nature 360: 367-369.
16. Falk, K., O. Rötzschke, S. Stevanović, G. Jung, and H. G. Rammensee. 1991. Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature 351: 290-296.
17. Lee, J. K., G. Stewart-Jones, T. Dong, K. Harlos, K. Di Gleria, L. Dorrell, D. C. Douek, P. A. van der Merwe, E. Y. Jones, and A. J. McMichael. 2004. T cell cross-reactivity and conformational changes during TCR engagement. J. Exp. Med. 200: 1455-1466.
18. Chen, J.-L., G. Stewart-Jones, G. Bossi, N. M. Lissin, L. Wooldridge, E. M. L. Choi, G. Held, P. R. Dunbar, R. M. Esnouf, M. Sami, et al. 2005. Structural and kinetic basis for heightened immunogenicity of T cell vaccines. J. Exp. Med. 201: 1243-1255.
19. Ekeruche-Makinde, J., M. Clement, D. K. Cole, E. S. J. Edwards, K. Ladell, J. J. Miles, K. K. Matthews, A. Fuller, K. A. Lloyd, F. Madura, et al. 2012. T-cell receptor-optimized peptide skewing of the T-cell repertoire can enhance antigen targeting. J. Biol. Chem. 287: 37269-37281.
20. Tangri, S., G. Y. Ishioka, X. Huang, J. Sidney, S. Southwood, J. Fikes, and A. Sette. 2001. Structural features of peptide analogs of human histocompatibility leukocyte antigen class I epitopes that are more potent and immunogenic than wild-Type peptide. J. Exp. Med. 194: 833-846.
21. Gladney, K. H., J. Pohling, N. A. Hollett, K. Zipperlen, M. E. Gallant, and M. D. Grant. 2012. Heteroclitic peptides enhance human immunodeficiency virus-specific CD8(+) T cell responses. Vaccine 30: 6997-7004.
22. Douat-Casassus, C., N. Marchand-Geneste, E. Diez, N. Gervois, F. Jotereau, and S. Quideau. 2007. Synthetic anticancer vaccine candidates: rational design of antigenic peptide mimetics that activate tumor-specific T-cells. J. Med. Chem. 50: 1598-1609.
23. Jones, M. A., J. K. Notta, M. Cobbold, M. Palendira, A. D. Hislop, J. Wilkie, and J. S. Snaith. 2008. Synthesis and ex vivo profiling of chemically modified cytomegalovirus CMVpp65 epitopes. J. Pept. Sci. 14: 313-320.
24. Weber, J. S., N. J. Vogelzang, M. S. Ernstoff, O. B. Goodman, L. D. Cranmer, J. L. Marshall, S. Miles, D. Rosario, D. C. Diamond, Z. Qiu, et al. 2011. A phase 1 study of a vaccine targeting preferentially expressed antigen in melanoma and prostate-specific membrane antigen in patients with advanced solid tumors. J. Immunother. 34: 556-567.
25. Liu, L., A. I. Bot, and D. C. Diamond, inventors; Mannkind Corporation, assignee. Peptide analogues. United States patent application 13/481,741, Publication No. US 2013/0017213 A1. 2013 Jan 17.
26. Gómez-Nuñez, M., K. J. Haro, T. Dao, D. Chau, A. Won, S. Escobar-Alvarez, V. Zakhaleva, T. Korontsvit, D. Y. Gin, and D. A. Scheinberg. 2008. Non-natural and photo-reactive amino acids as biochemical probes of immune function. PLoS ONE 3: e3938.
27. Blanchet, J. S., D. Valmori, I. Dufau, M. Ayyoub, C. Nguyen, P. Guillaume, B. Monsarrat, J. C. Cerottini, P. Romero, and J. E. Gairin. 2001. 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. 167: 5852-5861.
28. Webb, A. I., M. A. Dunstone, N. A. Williamson, J. D. Price, A. de Kauwe, W. Chen, A. Oakley, P. Perlmutter, J. McCluskey, M. I. Aguilar, et al. 2005. T cell determinants incorporating beta-amino acid residues are protease resistant and remain immunogenic in vivo. J. Immunol. 175: 3810-3818.
29. Guichard, G., A. Zerbib, F. A. Le Gal, J. Hoebeke, F. Connan, J. Choppin, J. P. Briand, and J. G. Guillet. 2000. Melanoma peptide MART-1(27-35) analogues with enhanced binding capacity to the human class I histocompatibility molecule HLA-A2 by introduction of a beta-amino acid residue: implications for recognition by tumor-infiltrating lymphocytes. J. Med. Chem. 43: 3803-3808.
30. Reinelt, S., M. Marti, S. Dédier, T. Reitinger, G. Folkers, J. A. de Castro, and D. Rognan. 2001. Beta-amino acid scan of a class I major histocompatibility complex-restricted alloreactive T-cell epitope. J. Biol. Chem. 276: 24525-24530.
31. Purcell, A. W., J. McCluskey, and J. Rossjohn. 2007. More than one reason to rethink the use of peptides in vaccine design. Nat. Rev. Drug Discov. 6: 404-414.
32. Guichard, G., F. Connan, R. Graff, M. Ostankovitch, S. Muller, J. G. Guillet, J. Choppin, and J. P. Briand. 1996. Partially modified retro-inverso pseudopeptides as non-natural ligands for the human class I histocompatibility molecule HLA-A2. J. Med. Chem. 39: 2030-2039.
33. Nair, D. T., K. J. Kaur, K. Singh, P. Mukherjee, D. Rajagopal, A. George, V. Bal, S. Rath, K. V. S. Rao, and D. M. Salunke. 2003. Mimicry of native peptide antigens by the corresponding retro-inverso analogs is dependent on their intrinsic structure and interaction propensities. J. Immunol. 170: 1362-1373.
34. Marschütz, M. K., W. Zauner, F. Mattner, A. Otava, M. Buschle, and A. Bernkop-Schnürch. 2002. Improvement of the enzymatic stability of a cytotoxic T-lymphocyte-epitope model peptide for its oral administration. Peptides 23: 1727-1733.
35. McGregor, D. P. 2008. Discovering and improving novel peptide therapeutics. Curr. Opin. Pharmacol. 8: 616-619.
36. Oostvogels, R., M. C. Minnema, M. van Elk, R. M. Spaapen, G. D. Te Raa, B. Giovannone, A. Buijs, D. van Baarle, A. P. Kater, M. Griffioen, et al. 2013. Towards effective and safe immunotherapy after allogeneic stem cell transplantation: identification of hematopoietic-specific minor histocompatibility antigen UTA2-1. Leukemia 27: 642-649.
37. van Buuren, M. M., F. E. Dijkgraaf, C. Linnemann, M. Toebes, C. X. L. Chang, J. Y. Mok, M. Nguyen, W. J. E. van Esch, P. Kvistborg, G. M. Grotenbreg, and T. N. M. Schumacher. 2014. HLA micropolymorphisms strongly affect peptide-MHC multimer-based monitoring of antigen-specific CD8+ T cell responses. J. Immunol. 192: 641-648.
38. Rodenko, B., M. Toebes, P. H. N. Celie, A. Perrakis, T. N. M. Schumacher, and H. Ovaa. 2009. Class I major histocompatibility complexes loaded by a periodate trigger. J. Am. Chem. Soc. 131: 12305-12313.
39. Toebes, M., M. Coccoris, A. Bins, B. Rodenko, R. Gomez, N. J. Nieuwkoop, W. van de Kasteele, G. F. Rimmelzwaan, J. B. A. G. Haanen, H. Ovaa, and T. N. M. Schumacher. 2006. Design and use of conditional MHC class I ligands. Nat. Med. 12: 246-251.
40. Toebes, M., B. Rodenko, H. Ovaa, and T. N. M. Schumacher. 2009. Generation of peptide MHC class I monomers and multimers through ligand exchange. Curr. Protoc. Immunol. 18: 18.16.
41. Celie, P. H. N., M. Toebes, B. Rodenko, H. Ovaa, A. Perrakis, and T. N. M. Schumacher. 2009. UV-induced ligand exchange in MHC class I protein crystals. J. Am. Chem. Soc. 131: 12298-12304.
42. Kabsch, W. 2010. XDS. Acta Crystallogr. D Biol. Crystallogr. 66: 125-132
43. Evans, P. 2006. Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 62: 72-82.
44. Winn, M. D., C. C. Ballard, K. D. Cowtan, E. J. Dodson, P. Emsley, P. R. Evans, R. M. Keegan, E. B. Krissinel, A. G. W. Leslie, A. McCoy, et al. 2011. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67: 235-242.
45. Navaza, J. 1994. AMoRe: an automated package for molecular replacement. Acta Crystollagr. A. 50: 157-163.
46. Sliz, P., O. Michielin, J. C. Cerottini, I. Luescher, P. Romero, M. Karplus, and D. C. Wiley. 2001. Crystal structures of two closely related but antigenically distinct HLA-A2/melanocyte-melanoma tumor-antigen peptide complexes. J. Immunol. 167: 3276-3284.
47. Murshudov, G. N., A. A. Vagin, and E. J. Dodson. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53: 240-255.
48. Joosten, R. P., K. Joosten, S. X. Cohen, G. Vriend, and A. Perrakis. 2011. Automatic rebuilding and optimization of crystallographic structures in the Protein Data Bank. Bioinformatics 27: 3392-3398.
49. Li, L.-P., J. C. Lampert, X. Chen, C. Leitao, J. Popović, W. Müller, and T. Blankenstein. 2010. Transgenic mice with a diverse human T cell antigen receptor repertoire. Nat. Med. 16: 1029-1034.
50. Morrison, J., J. Elvin, F. Latron, F. Gotch, R. Moots, J. L. Strominger, and A. McMichael. 1992. Identification of the nonamer peptide from influenza A matrix protein and the role of pockets of HLA-A2 in its recognition by cytotoxic T lymphocytes. Eur. J. Immunol. 22: 903-907.
51. Diamond, D. J., J. York, J. Y. Sun, C. L. Wright, and S. J. Forman. 1997. Development of a candidate HLA A∗0201 restricted peptide-based vaccine against human cytomegalovirus infection. Blood 90: 1751-1767.
52. Buchli, R., R. S. VanGundy, H. D. Hickman-Miller, C. F. Giberson, W. Bardet, and W. H. Hildebrand. 2005. Development and validation of a fluorescence polarization-based competitive peptide-binding assay for HLA-A∗0201-A new tool for epitope discovery. Biochemistry 44: 12491-12507.
53. Kawakami, Y., S. Eliyahu, K. Sakaguchi, P. F. Robbins, L. Rivoltini, J. R. Yannelli, E. Appella, and S. A. Rosenberg. 1994. Identification of the immunodominant peptides of the MART-1 human melanoma antigen recognized by the majority of HLA-A2-restricted tumor infiltrating lymphocytes. J. Exp. Med. 180: 347-352.
54. Parkhurst, M. R., E. B. Fitzgerald, S. Southwood, A. Sette, S. A. Rosenberg, and Y. Kawakami. 1998. Identification of a shared HLA-A∗0201-restricted T-cell epitope from the melanoma antigen tyrosinase-related protein 2 (TRP2). Cancer Res. 58: 4895-4901.
55. Mitchell, M. S., J. Kan-Mitchell, B. Minev, C. Edman, and R. J. Deans. 2000. A novel melanoma gene (MG50) encoding the interleukin 1 receptor antagonist and six epitopes recognized by human cytolytic T lymphocytes. Cancer Res. 60: 6448-6456.
56. Ma, W., C. Germeau, N. Vigneron, A.-S. Maernoudt, S. Morel, T. Boon, P. G. Coulie, and B. J. Van den Eynde. 2004. Two new tumor-specific antigenic peptides encoded by gene MAGE-C2 and presented to cytolytic T lymphocytes by HLA-A2. Int. J. Cancer 109: 698-702.
57. van Stipdonk, M. J. B., D. Badia-Martinez, M. Sluijter, R. Offringa, T. van Hall, and A. Achour. 2009. Design of agonistic altered peptides for the robust induction of CTL directed towards H-2Db in complex with the melanomaassociated epitope gp100. Cancer Res. 69: 7784-7792.
58. Uchtenhagen, H., E. T. Abualrous, E. Stahl, E. B. Allerbring, M. Sluijter, M. Zacharias, T. Sandalova, T. van Hall, S. Springer, P.-Å . Nygren, and A. Achour. 2013. Proline substitution independently enhances H-2D(b) complex stabilization and TCR recognition of melanoma-associated peptides. Eur. J. Immunol. 43: 3051-3060.
59. Martinez-Hackert, E., N. Anikeeva, S. A. Kalams, B. D.Walker,W. A. Hendrickson, and Y. Sykulev. 2006. Structural basis for degenerate recognition of natural HIV peptide variants by cytotoxic lymphocytes. J. Biol. Chem. 281: 20205-20212.