CD8+ T cell responses against tap-inhibited cells are readily detected in the human population

Journal of Immunology

Volumn 185, Issue 11, 2010, Pages 6508-6517

  Lampen, Margit H ^a   Verweij, Marieke C ^b   Querido, Bianca ^a   Van Der Burg, Sjoerd H ^a   Wiertz, Emmanuel J H J ^c   Van Hall, Thorbald ^a  

^a Department of Clinical Oncology ^*  (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1;

ANTIGEN DETECTION; ARTICLE; CD8+ T LYMPHOCYTE; CELL CLONE; CELL CULTURE; CELL ISOLATION; CONTROLLED STUDY; DENDRITIC CELL; GENE TRANSFER; HUMAN; HUMAN CELL; IMMUNE EVASION; INTRACELLULAR SIGNALING; PERIPHERAL BLOOD MONONUCLEAR CELL; POPULATION; PRIORITY JOURNAL;

ANTIGEN PRESENTATION; ATP-BINDING CASSETTE TRANSPORTERS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; CELLS, CULTURED; CLONE CELLS; COCULTURE TECHNIQUES; DENDRITIC CELLS; EPITOPES, T-LYMPHOCYTE; GENE TRANSFER TECHNIQUES; HERPESVIRIDAE INFECTIONS; HERPESVIRUS 1, BOVINE; HUMANS; IMMUNE EVASION; TUMOR VIRUS INFECTIONS; VIRAL STRUCTURAL PROTEINS;

EID: 78650642313     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001774     Document Type: Article

References (53)

1. Chang, C. C., M. Campoli, and S. Ferrone. 2003. HLA class I defects in malignant lesions: what have we learned? Keio J. Med. 52:220-229.
2. Hansen, T. H., and M. Bouvier. 2009. MHC class I antigen presentation: learning from viral evasion strategies. Nat. Rev. Immunol. 9:503-513.
3. Hicklin, D. J., F. M. Marincola, and S. Ferrone. 1999. HLA class I antigen downregulation in human cancers: T-cell immunotherapy revives an old story. Mol. Med. Today 5:178-186.
4. Garrido, F., and I. Algarra. 2001. MHC antigens and tumor escape from immune surveillance. Adv. Cancer Res. 83:117-158.
5. Seliger, B., M. J. Maeurer, and S. Ferrone. 2000. Antigen-processing machinery breakdown and tumor growth. Immunol. Today 21:455-464.
6. Seliger, B., D. Atkins, M. Bock, U. Ritz, S. Ferrone, C. Huber, and S. Störkel. 2003. Characterization of human lymphocyte antigen class I antigen-processing machinery defects in renal cell carcinoma lesions with special emphasis on transporter-associated with antigen-processing down-regulation. Clin. Cancer Res. 9:1721-1727.
7. Seliger, B. 2008. Molecular mechanisms of MHC class I abnormalities and APM components in human tumors. Cancer Immunol. Immunother. 57:1719-1726.
8. Koppers-Lalic, D., E. A. Reits, M. E. Ressing, A. D. Lipinska, R. Abele, J. Koch, R. M. Marcondes, P. Admiraal, D. van Leeuwen, K. Bienkowska-Szewczyk, et al. 2005. Varicelloviruses avoid T cell recognition by UL49.5-mediated inactivation of the transporter associated with antigen processing. Proc. Natl. Acad. Sci. USA 102:5144-5149.
9. Verweij, M. C., D. Koppers-Lalic, S. Loch, F. Klauschies, H. de la Salle, E. Quinten, P. J. Lehner, A. Mulder, M. R. Knittler, R. Tampé, et al. 2008. The varicellovirus UL49.5 protein blocks the transporter associated with antigen processing (TAP) by inhibiting essential conformational transitions in the 6+6 transmembrane TAP core complex. J. Immunol. 181:4894-4907.
10. Koppers-Lalic, D., M. C. Verweij, A. D. Lipińska, Y. Wang, E. Quinten, E. A. Reits, J. Koch, S. Loch, M. Marcondes Rezende, F. Daus, et al. 2008. Varicellovirus UL 49.5 proteins differentially affect the function of the transporter associated with antigen processing, TAP. PLoS Pathog. 4: e1000080.
11. Ahn, K., T. H. Meyer, S. Uebel, P. Sempé, H. Djaballah, Y. Yang, P. A. Peterson, K. Früh, and R. Tampé. 1996. Molecular mechanism and species specificity of TAP inhibition by herpes simplex virus ICP47. EMBO J. 15:3247-3255.
12. Hill, A., P. Jugovic, I. York, G. Russ, J. Bennink, J. Yewdell, H. Ploegh, and D. Johnson. 1995. Herpes simplex virus turns off the TAP to evade host immunity. Nature 375:411-415.
13. Tomazin, R., A. B. Hill, P. Jugovic, I. York, P. van Endert, H. L. Ploegh, D. W. Andrews, and D. C. Johnson. 1996. Stable binding of the herpes simplex virus ICP47 protein to the peptide binding site of TAP. EMBO J. 15:3256-3266.
14. York, I. A., C. Roop, D. W. Andrews, S. R. Riddell, F. L. Graham, and D. C. Johnson. 1994. A cytosolic herpes simplex virus protein inhibits antigen presentation to CD8+ T lymphocytes. Cell 77:525-535.
15. Dugan, G. E., and E. W. Hewitt. 2008. Structural and Functional Dissection of the Human Cytomegalovirus Immune Evasion Protein US6. J. Virol. 82:3271-3282.
16. Hewitt, E. W., S. S. Gupta, and P. J. Lehner. 2001. The human cytomegalovirus gene product US6 inhibits ATP binding by TAP. EMBO J. 20:387-396.
17. Hislop, A. D., M. E. Ressing, D. van Leeuwen, V. A. Pudney, D. Horst, D. Koppers-Lalic, N. P. Croft, J. J. Neefjes, A. B. Rickinson, and E. J. Wiertz. 2007. A CD8+ T cell immune evasion protein specific to Epstein-Barr virus and its close relatives in Old World primates. J. Exp. Med. 204:1863-1873.
18. Horst, D., D. van Leeuwen, N. P. Croft, M. A. Garstka, A. D. Hislop, E. Kremmer, A. B. Rickinson, E. J. Wiertz, and M. E. Ressing. 2009. Specific targeting of the EBV lytic phase protein BNLF2a to the transporter associated with antigen processing results in impairment of HLA class I-restricted antigen presentation. J. Immunol. 182:2313-2324.
19. Jordanova, E. S., A. Gorter, O. Ayachi, F. Prins, L. G. Durrant, G. G. Kenter, S. H. van der Burg, and G. J. Fleuren. 2008. Human leukocyte antigen class I, MHC class I chain-related molecule A, and CD8+/regulatory T-cell ratio: which variable determines survival of cervical cancer patients? Clin. Cancer Res. 14:2028-2035.
20. Kamarashev, J., S. Ferrone, B. Seifert, R. Böni, F. O. Nestle, G. Burg, and R. Dummer. 2001. TAP1 down-regulation in primary melanoma lesions: an independent marker of poor prognosis. Int. J. Cancer 95:23-28.
21. Alimonti, J., Q. J. Zhang, R. Gabathuler, G. Reid, S. S. Chen, and W. A. Jefferies. 2000. TAP expression provides a general method for improving the recognition of malignant cells in vivo. Nat. Biotechnol. 18:515-520.
22. Chen, H. L., D. Gabrilovich, R. Tampé, K. R. Girgis, S. Nadaf, and D. P. Carbone. 1996. A functionally defective allele of TAP1 results in loss of MHC class I antigen presentation in a human lung cancer. Nat. Genet. 13:210-213.
23. Evans, M., L. K. Borysiewicz, A. S. Evans, M. Rowe, M. Jones, U. Gileadi, V. Cerundolo, and S. Man. 2001. Antigen processing defects in cervical carcinomas limit the presentation of a CTL epitope from human papillomavirus 16 E6. J. Immunol. 167:5420-5428.
24. Lou, Y., T. Z. Vitalis, G. Basha, B. Cai, S. S. Chen, K. B. Choi, A. P. Jeffries, W. M. Elliott, D. Atkins, B. Seliger, and W. A. Jefferies. 2005. Restoration of the expression of transporters associated with antigen processing in lung carcinoma increases tumor-specific immune responses and survival. Cancer Res. 65:7926-7933.
25. Henderson, R. A., H. Michel, K. Sakaguchi, J. Shabanowitz, E. Appella, D. F. Hunt, and V. H. Engelhard. 1992. HLA-A2.1-associated peptides from a mutant cell line: a second pathway of antigen presentation. Science 255:1264-1266.
26. Wei, M. L., and P. Cresswell. 1992. HLA-A2 molecules in an antigen-processing mutant cell contain signal sequence-derived peptides. Nature 356:443-446.
27. Weinzierl, A. O., D. Rudolf, N. Hillen, S. Tenzer, P. van Endert, H. Schild, H. G. Rammensee, and S. Stevanović. 2008. Features of TAP-independent MHC class I ligands revealed by quantitative mass spectrometry. Eur. J. Immunol. 38:1503-1510.
28. Oliveira, C. C., P. A. van Veelen, B. Querido, A. de Ru, M. Sluijter, S. Laban, J. W. Drijfhout, S. H. van der Burg, R. Offringa, and T. van Hall. 2010. The nonpolymorphic MHC Qa-1b mediates CD8+ T cell surveillance of antigenprocessing defects. J. Exp. Med. 207:207-221.
29. van Hall, T., E. Z. Wolpert, P. van Veelen, S. Laban, M. van der Veer, M. Roseboom, S. Bres, P. Grufman, A. de Ru, H. Meiring, et al. 2006. Selective cytotoxic T-lymphocyte targeting of tumor immune escape variants. Nat. Med. 12:417-424.
30. Chambers, B., P. Grufman, V. Fredriksson, K. Andersson, M. Roseboom, S. Laban, M. Camps, E. Z. Wolpert, E. J. Wiertz, R. Offringa, et al. 2007. Induction of protective CTL immunity against peptide transporter TAP-deficient tumors through dendritic cell vaccination. Cancer Res. 67:8450-8455.
31. van Hall, T., S. Laban, D. Koppers-Lalic, J. Koch, C. Precup, P. Asmawidjaja, R. Offringa, and E. J. Wiertz. 2007. The varicellovirus-encoded TAP inhibitor UL49.5 regulates the presentation of CTL epitopes by Qa-1b1. J. Immunol. 178:657-662.
32. Oosten, L. E., D. Koppers-Lalic, E. Blokland, A. Mulder, M. E. Ressing, T. Mutis, A. G. van Halteren, E. J. Wiertz, and E. Goulmy. 2007. TAP-inhibiting proteins US6, ICP47 and UL49.5 differentially affect minor and major histocompatibility antigen-specific recognition by cytotoxic T lymphocytes. Int. Immunol. 19:1115-1122.
33. Schuurhuis, D. H., P. Verdijk, G. Schreibelt, E. H. Aarntzen, N. Scharenborg, A. de Boer, M. W. van de Rakt, M. Kerkhoff, M. J. Gerritsen, F. Eijckeler, et al. 2009. In situ expression of tumor antigens by messenger RNA-electroporated dendritic cells in lymph nodes of melanoma patients. Cancer Res. 69:2927-2934.
34. Lipińska, A. D., D. Koppers-Lalic, M. Rychlowski, P. Admiraal, F. A. Rijsewijk, K. Bieńkowska-Szewczyk, and E. J. Wiertz. 2006. Bovine herpesvirus 1 UL49.5 protein inhibits the transporter associated with antigen processing despite complex formation with glycoprotein M. J. Virol. 80:5822-5832.
35. Meyer, T. H., P. M. van Endert, S. Uebel, B. Ehring, and R. Tampé. 1994. Functional expression and purification of the ABC transporter complex associated with antigen processing (TAP) in insect cells. FEBS Lett. 351:443-447.
36. Plewnia, G., K. Schulze, C. Hunte, R. Tampé, and J. Koch. 2007. Modulation of the antigenic peptide transporter TAP by recombinant antibodies binding to the last five residues of TAP1. J. Mol. Biol. 369:95-107.
37. Verdegaal, E. M., C. Hoogstraten, M. H. Sandel, P. J. Kuppen, A. A. Brink, F. H. Claas, M. C. Gorsira, J. F. Graadt van Roggen, and S. Osanto. 2007. Functional CD8+ T cells infiltrate into nonsmall cell lung carcinoma. Cancer Immunol. Immunother. 56:587-600.
38. den Haan, J. M., L. M. Meadows, W. Wang, J. Pool, E. Blokland, T. L. Bishop, C. Reinhardus, J. Shabanowitz, R. Offringa, D. F. Hunt, et al. 1998. The minor histocompatibility antigen HA-1: a diallelic gene with a single amino acidpolymorphism. Science 279:1054-1057.
39. Bui, H. H., J. Sidney, K. Dinh, S. Southwood, M. J. Newman, and A. Sette. 2006. Predicting population coverage of T-cell epitope-based diagnostics and vaccines. BMC Bioinformatics 7:153.
40. Hillen, N., G. Mester, C. Lemmel, A. O. Weinzierl, M. Müller, D. Wernet, J. Hennenlotter, A. Stenzl, H. G. Rammensee, and S. Stevanović. 2008. Essential differences in ligand presentation and T cell epitope recognition among HLA molecules of the HLA-B44 supertype. Eur. J. Immunol. 38:2993-3003.
41. Thammavongsa, V., G. Raghuraman, T. M. Filzen, K. L. Collins, and M. Raghavan. 2006. HLA-B44 polymorphisms at position 116 of the heavy chain influence TAP complex binding via an effect on peptide occupancy. J. Immunol. 177:3150-3161.
42. Zernich, D., A. W. Purcell, W. A. Macdonald, L. Kjer-Nielsen, L. K. Ely, N. Laham, T. Crockford, N. A. Mifsud, M. Bharadwaj, L. Chang, et al. 2004. Natural HLA class I polymorphism controls the pathway of antigen presentation and susceptibility to viral evasion. J. Exp. Med. 200:13-24.
43. de la Salle, H., E. Houssaint, M. A. Peyrat, D. Arnold, J. Salamero, D. Pinczon, S. Stevanovic, H. Bausinger, D. Fricker, E. Gomard, et al. 1997. Human peptide transporter deficiency: importance of HLA-B in the presentation of TAP-independent EBV antigens. J. Immunol. 158:4555-4563.
44. Doytchinova, I., S. Hemsley, and D. R. Flower. 2004. Transporter associated with antigen processing preselection of peptides binding to the MHC: a bioinformatic evaluation. J. Immunol. 173:6813-6819.
45. Grandea, A. G., III, M. J. Androlewicz, R. S. Athwal, D. E. Geraghty, and T. Spies. 1995. Dependence of peptide binding by MHC class I molecules on their interaction with TAP. Science 270:105-108.
46. Luckey, C. J., J. A. Marto, M. Partridge, E. Hall, F. M. White, J. D. Lippolis, J. Shabanowitz, D. F. Hunt, and V. H. Engelhard. 2001. Differences in the expression of human class I MHC alleles and their associated peptides in the presence of proteasome inhibitors. J. Immunol. 167:1212-1221.
47. Neisig, A., R. Wubbolts, X. Zang, C. Melief, and J. Neefjes. 1996. Allelespecific differences in the interaction of MHC class I molecules with transporters associated with antigen processing. J. Immunol. 156:3196-3206.
48. Sarantopoulos, S., L. Lu, and H. Cantor. 2004. Qa-1 restriction of CD8+ suppressor T cells. J. Clin. Invest. 114:1218-1221.
49. Bontkes, H. J., D. Kramer, J. J. Ruizendaal, C. J. Meijer, and E. Hooijberg. 2008. Tumor associated antigen and interleukin-12 mRNA transfected dendritic cells enhance effector function of natural killer cells and antigen specific T-cells. Clin. Immunol. 127:375-384.
50. Kyte, J. A., and G. Gaudernack. 2006. Immuno-gene therapy of cancer with tumour-mRNA transfected dendritic cells. Cancer Immunol. Immunother. 55:1432-1442.
51. Milano, F., J. W. van Baal, A. M. Rygiel, J. J. Bergman, S. J. Van Deventer, M. L. Kapsenberg, M. P. Peppelenbosch, and K. K. Krishnadath. 2007. An improved protocol for generation of immuno-potent dendritic cells through direct electroporation of CD14+ monocytes. J. Immunol. Methods 321:94-106.
52. Saebøe-Larssen, S., E. Fossberg, and G. Gaudernack. 2002. mRNA-based electrotransfection of human dendritic cells and induction of cytotoxic T lymphocyte responses against the telomerase catalytic subunit (hTERT). J. Immunol. Methods 259:191-203.
53. Sousa-Canavez, J. M., F. C. Canavez, K. R. Leite, and L. H. Camara-Lopes. 2008. Therapeutic dendritic cell vaccine preparation using tumor RNA transfection: a promising approach for the treatment of prostate cancer. Genet. Vaccines Ther. 6:2.