A Novel HLA-B18 Restricted CD8+ T Cell Epitope Is Efficiently Cross-Presented by Dendritic Cells from Soluble Tumor Antigen

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Zhao, Rona Y ^a   Mifsud, Nicole A ^a   Xiao, Kun ^a   Chan, Kok Fei ^a   Oveissi, Sara ^a   Jackson, Heather M ^a   Dimopoulos, Nektaria ^a   Guillaume, Philippe ^b   Knights, Ashley J ^a   Lowen, Tamara ^a   Robson, Neil C ^a   Russell, Sarah E ^a   Scotet, Emmanuel ^c   Davis, Ian D ^a   Maraskovsky, Eugene ^d   Cebon, Jonathan ^a   Luescher, Immanuel F ^b   Chen, Weisan ^a  

^a OLIVIA NEWTON JOHN CANCER RESEARCH INSTITUTE   (Australia)

^b LUDWIG INSTITUTE FOR CANCER RESEARCH   (Switzerland)

^c INSTITUT DE BIOLOGIE   (France)

^d CSL LIMITED   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER VACCINE; EPITOPE; GAMMA INTERFERON; HLA B18 ANTIGEN; ISCOMATRIX; MELAN A; NY ESO 1 88 96; PROTEASOME; TUMOR ANTIGEN; UNCLASSIFIED DRUG;

ANTIGEN EXPRESSION; ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CLINICAL TRIAL; CONTROLLED STUDY; CROSS PRESENTATION; DENDRITIC CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; MELANOMA; TUMOR CELL; VACCINIA VIRUS; VIRUS RECOMBINANT; WESTERN BLOTTING;

BLOTTING, WESTERN; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; DENDRITIC CELLS; EPITOPES; HLA-B18 ANTIGEN; HUMANS; MELANOMA;

VACCINIA VIRUS;

EID: 84866138981     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044707     Document Type: Article

References (50)

1. den Haan JMM, Bevan MJ, (2001) Antigen presentation to CD8+ T cells: cross-priming in infectious diseases. Current Opinion in Immunology 13: 437-441.
2. Melief CJ, (2003) Mini-review: Regulation of cytotoxic T lymphocyte responses by dendritic cells: peaceful coexistence of cross-priming and direct priming? Eur J Immunol 33: 2645-2654.
3. Schnurr M, Chen Q, Shin A, Chen W, Toy T, et al. (2005) Tumor antigen processing and presentation depend critically on dendritic cell type and the mode of antigen delivery. Blood 105: 2465-2472.
4. Ackerman AL, Kyritsis C, Tampe R, Cresswell P, (2005) Access of soluble antigens to the endoplasmic reticulum can explain cross-presentation by dendritic cells. Nat Immunol 6: 107-113.
5. Burgdorf S, Scholz C, Kautz A, Tampe R, Kurts C, (2008) Spatial and mechanistic separation of cross-presentation and endogenous antigen presentation. Nat Immunol 9: 558-566.
6. Davis ID, Chen W, Jackson H, Parente P, Shackleton M, et al. (2004) Recombinant NY-ESO-1 protein with ISCOMATRIX adjuvant induces broad integrated antibody and CD4(+) and CD8(+) T cell responses in humans. Proc Natl Acad Sci U S A 101: 10697-10702.
7. Chiodoni C, Paglia P, Stoppacciaro A, Rodolfo M, Parenza M, et al. (1999) Dendritic Cells Infiltrating Tumors Cotransduced with Granulocyte/Macrophage Colony-stimulating Factor (GM-CSF) and CD40 Ligand Genes Take Up and Present Endogenous Tumor-associated Antigens, and Prime Naive Mice for a Cytotoxic T Lymphocyte Response. J Exp Med 190: 125-134.
8. Macagno A, Kuehn L, de Giuli R, Groettrup M, (2001) Pronounced up-regulation of the PA28alpha/beta proteasome regulator but little increase in the steady-state content of immunoproteasome during dendritic cell maturation. Eur J Immunol 31: 3271-3280.
9. Townsend SE, Allison JP, (1993) Tumor rejection after direct costimulation of CD8+ T cells by B7-transfected melanoma cells. Science 259: 368-370.
10. Gaczynska M, Rock KL, Goldberg AL, (1993) Role of proteasomes in antigen presentation. Enzyme Protein 47: 354-369.
11. Toes RE, Nussbaum AK, Degermann S, Schirle M, Emmerich NP, et al. (2001) Discrete cleavage motifs of constitutive and immunoproteasomes revealed by quantitative analysis of cleavage products. J Exp Med 194: 1-12.
12. Van Kaer L, Ashton-Rickardt PG, Eichelberger M, Gaczynska M, Nagashima K, et al. (1994) Altered peptidase and viral-specific T cell response in LMP2 mutant mice. Immunity 1: 533-541.
13. Chen W, Norbury CC, Cho Y, Yewdell JW, Bennink JR, (2001) Immunoproteasomes Shape Immunodominance Hierarchies of Antiviral CD8+ T Cells at the Levels of T Cell Repertoire and Presentation of Viral Antigens. J Exp Med 193: 1319-1326.
14. Pang KC, Sanders MT, Monaco JJ, Doherty PC, Turner SJ, et al. (2006) Immunoproteasome subunit deficiencies impact differentially on two immunodominant influenza virus-specific CD8+ T cell responses. J Immunol 177: 7680-7688.
15. Morel S, Levy F, Burlet-Schiltz O, Brasseur F, Probst-Kepper M, et al. (2000) Processing of some antigens by the standard proteasome but not by the immunoproteasome results in poor presentation by dendritic cells. Immunity 12: 107-117.
16. Schubert U, Anton LC, Gibbs J, Norbury CC, Yewdell JW, et al. (2000) Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404: 770-774.
17. Reits EA, Vos JC, Gromme M, Neefjes J, (2000) The major substrates for TAP in vivo are derived from newly synthesized proteins. Nature 404: 774-778.
18. Norbury CC, Basta S, Donohue KB, Tscharke DC, Princiotta MF, et al. (2004) CD8+ T cell cross-priming via transfer of proteasome substrates. Science 304: 1318-1321.
19. Donohue KB, Grant JM, Tewalt EF, Palmer DC, Theoret MR, et al. (2006) Cross-priming utilizes antigen not available to the direct presentation pathway. Immunology 119: 63-73.
20. Rock KL, Shen L, (2005) Cross-presentation: underlying mechanisms and role in immune surveillance. Immunol Rev 207: 166-183.
21. Ebert LM, Liu YC, Clements CS, Robson NC, Jackson HM, et al. (2009) A long, naturally presented immunodominant epitope from NY-ESO-1 tumor antigen: implications for cancer vaccine design. Cancer Res 69: 1046-1054.
22. Schreiber H, Wu TH, Nachman J, Kast WM, (2002) Immunodominance and tumor escape. Seminars in Cancer Biology 12: 25-31.
23. Chen W, McCluskey J, (2006) Immunodominance and immunodomination: critical factors in developing effective CD8(+) T-cell-based cancer vaccines. Adv Cancer Res 95: 203-247.
24. Jungbluth AA, Chen YT, Stockert E, Busam KJ, Kolb D, et al. (2001) Immunohistochemical analysis of NY-ESO-1 antigen expression in normal and malignant human tissues. Int J Cancer 92: 856-860.
25. Odunsi K, Jungbluth AA, Stockert E, Qian F, Gnjatic S, et al. (2003) NY-ESO-1 and LAGE-1 cancer-testis antigens are potential targets for immunotherapy in epithelial ovarian cancer. Cancer Res 63: 6076-6083.
26. Sugita Y, Wada H, Fujita S, Nakata T, Sato S, et al. (2004) NY-ESO-1 expression and immunogenicity in malignant and benign breast tumors. Cancer Res 64: 2199-2204.
27. Jager E, Chen YT, Drijfhout JW, Karbach J, Ringhoffer M, et al. (1998) Simultaneous humoral and cellular immune response against cancer-testis antigen NY-ESO-1: definition of human histocompatibility leukocyte antigen (HLA)-A2-binding peptide epitopes. J Exp Med 187: 265-270.
28. Robson NC, McAlpine T, Knights AJ, Schnurr M, Shin A, et al. (2010) Processing and cross-presentation of individual HLA-A,-B, or-C epitopes from NY-ESO-1 or an HLA-A epitope for Melan-A differ according to the mode of antigen delivery. Blood 116: 218-225.
29. Dutoit V, Taub RN, Papadopoulos KP, Talbot S, Keohan ML, et al. (2002) Multiepitope CD8(+) T cell response to a NY-ESO-1 peptide vaccine results in imprecise tumor targeting. J Clin Invest 110: 1813-1822.
30. Dimopoulos N, Jackson HM, Ebert L, Guillaume P, Luescher IF, et al. (2009) Combining MHC tetramer and intracellular cytokine staining for CD8(+) T cells to reveal antigenic epitopes naturally presented on tumor cells. J Immunol Methods 340: 90-94.
31. Strehl B, Seifert U, Kruger E, Heink S, Kuckelkorn U, et al. (2005) Interferon-gamma, the functional plasticity of the ubiquitin-proteasome system, and MHC class I antigen processing. Immunol Rev 207: 19-30.
32. Fonsatti E, Nicolay HJ, Sigalotti L, Calabro L, Pezzani L, et al. (2007) Functional up-regulation of human leukocyte antigen class I antigens expression by 5-aza-2′-deoxycytidine in cutaneous melanoma: immunotherapeutic implications. Clin Cancer Res 13: 3333-3338.
33. Ochsenbein AF, Sierro S, Odermatt B, Pericin M, Karrer U, et al. (2001) Roles of tumour localization, second signals and cross priming in cytotoxic T-cell induction. Nature 411: 1058-1064.
34. Chapatte L, Ayyoub M, Morel S, Peitrequin AL, Levy N, et al. (2006) Processing of tumor-associated antigen by the proteasomes of dendritic cells controls in vivo T-cell responses. Cancer Res 66: 5461-5468.
35. Ahmad M, Rees RC, Ali SA, (2004) Escape from immunotherapy: possible mechanisms that influence tumor regression/progression. Cancer Immunol Immunother 53: 844-854.
36. Spiotto MT, Rowley DA, Schreiber H, (2004) Bystander elimination of antigen loss variants in established tumors. Nat Med 10: 294-298.
37. Kammertoens T, Schuler T, Blankenstein T, (2005) Immunotherapy: target the stroma to hit the tumor. Trends Mol Med 11: 225-231.
38. Crowe SR, Turner SJ, Miller SC, Roberts AD, Rappolo RA, et al. (2003) Differential antigen presentation regulates the changing patterns of CD8+ T cell immunodominance in primary and secondary influenza virus infections. J Exp Med 198: 399-410.
39. Chen W, Pang K, Masterman KA, Kennedy G, Basta S, et al. (2004) Reversal in the immunodominance hierarchy in secondary CD8+ T cell responses to influenza A virus: roles for cross-presentation and lysis-independent immunodomination. J Immunol 173: 5021-5027.
40. Schultz ES, Chapiro J, Lurquin C, Claverol S, Burlet-Schiltz O, et al. (2002) The production of a new MAGE-3 peptide presented to cytolytic T lymphocytes by HLA-B40 requires the immunoproteasome. J Exp Med 195: 391-399.
41. Chapiro J, Claverol S, Piette F, Ma W, Stroobant V, et al. (2006) Destructive cleavage of antigenic peptides either by the immunoproteasome or by the standard proteasome results in differential antigen presentation. J Immunol 176: 1053-1061.
42. Dannull J, Lesher DT, Holzknecht R, Qi W, Hanna G, et al. (2007) Immunoproteasome down-modulation enhances the ability of dendritic cells to stimulate antitumor immunity. Blood 110: 4341-4350.
43. Wang HY, Lee DA, Peng G, Guo Z, Li Y, et al. (2004) Tumor-specific human CD4+ regulatory T cells and their ligands: implications for immunotherapy. Immunity 20: 107-118.
44. Nicholaou T, Ebert LM, Davis ID, McArthur GA, Jackson H, et al. (2009) Regulatory T-cell-mediated attenuation of T-cell responses to the NY-ESO-1 ISCOMATRIX vaccine in patients with advanced malignant melanoma. Clin Cancer Res 15: 2166-2173.
45. Maraskovsky E, Sjolander S, Drane DP, Schnurr M, Le TT, et al. (2004) NY-ESO-1 protein formulated in ISCOMATRIX adjuvant is a potent anticancer vaccine inducing both humoral and CD8+ t-cell-mediated immunity and protection against NY-ESO-1+ tumors. Clin Cancer Res 10: 2879-2890.
46. Murphy R, Green S, Ritter G, Cohen L, Ryan D, et al. (2005) Recombinant NY-ESO-1 cancer antigen: production and purification under cGMP conditions. Prep Biochem Biotechnol 35: 119-134.
47. Carey TE, Takahashi T, Resnick LA, Oettgen HF, Old LJ, (1976) Cell surface antigens of human malignant melanoma: mixed hemadsorption assays for humoral immunity to cultured autologous melanoma cells. Proc Natl Acad Sci U S A 73: 3278-3282.
48. Dippold WG, Lloyd KO, Li LT, Ikeda H, Oettgen HF, et al. (1980) Cell surface antigens of human malignant melanoma: definition of six antigenic systems with mouse monoclonal antibodies. Proc Natl Acad Sci U S A 77: 6114-6118.
49. Jackson HM, Dimopoulos N, Chen Q, Luke T, Yee Tai T, et al. (2004) A robust human T-cell culture method suitable for monitoring CD8+ and CD4+ T-cell responses from cancer clinical trial samples. J Immunol Methods 291: 51-62.
50. Jackson H, Dimopoulos N, Mifsud NA, Tai TY, Chen Q, et al. (2006) Striking immunodominance hierarchy of naturally occurring CD8+ and CD4+ T cell responses to tumor antigen NY-ESO-1. J Immunol 176: 5908-5917.