Antigen spreading contributes to MAGE vaccination-induced regression of melanoma metastases

Cancer Research

Volumn 71, Issue 4, 2011, Pages 1253-1262

  Corbière, Véronique ^a   Chapiro, Jacques ^a,b   Stroobant, Vincent ^a,b   Ma, Wenbin ^a,b   Lurquin, Christophe ^a,b   Lethé, Bernard ^a,b   Van Baren, Nicolas ^a,b   Van Den Eynde, Benoît J ^a,b   Boon, Thierry ^a,b   Coulie, Pierre G ^a  

^a DE DUVE INSTITUTE   (Belgium)

^b LUDWIG INSTITUTE FOR CANCER RESEARCH   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; GAMMA INTERFERON; HLA A2 ANTIGEN; MELANOMA ANTIGEN; MELANOMA VACCINE; PROTEINASE; T LYMPHOCYTE RECEPTOR BETA CHAIN;

ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ARTICLE; CANARYPOX VIRUS; CANCER IMMUNIZATION; CANCER REGRESSION; CD8+ T LYMPHOCYTE; CELL CLONE; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXIC T LYMPHOCYTE; DNA LIBRARY; GENE MUTATION; GENE TARGETING; HUMAN; HUMAN TISSUE; MELANOMA; MELANOMA CELL; METASTASIS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; T LYMPHOCYTE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR REJECTION; VACCINE FAILURE;

AMINO ACID SEQUENCE; ANTIGENS, NEOPLASM; BASE SEQUENCE; CANCER VACCINES; CELLS, CULTURED; HUMANS; K562 CELLS; MELANOMA; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NEOPLASM METASTASIS; NEOPLASM PROTEINS; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; REMISSION INDUCTION; SKIN NEOPLASMS; T-LYMPHOCYTES, CYTOTOXIC; TISSUE DISTRIBUTION; TUMOR BURDEN;

EID: 79951848084     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-2693     Document Type: Article

References (45)

1. Coulie PG, Karanikas V, Colau D, Lurquin C, Landry C, Marchand M, et al. A monoclonal cytolytic T-lymphocyte response observed in a melanoma patient vaccinated with a tumor-specific antigenic peptide encoded by gene MAGE-3. Proc Natl Acad Sci U S A 2001;98:10290-5. (Pubitemid 32803013)
2. Karanikas V, Lurquin C, Colau D, van Baren N, De Smet C, Lethé B, et al. Monoclonal anti-MAGE-3 CTL responses in melanoma patients displaying tumor regression after vaccination with a recombinant canarypox virus. J Immunol 2003;171:4898-904. (Pubitemid 37310613)
3. Godelaine D, Carrasco J, Lucas S, Karanikas V, Schuler-Thurner B, Coulie PG, et al. Polyclonal CTL responses observed in melanoma patients vaccinated with dendritic cells pulsed with a MAGE-3 A1 peptide. J Immunol 2003;171:4893-7. (Pubitemid 37310612)
4. Lonchay C, Van Der Bruggen P, Connerotte T, Hanagiri T, Coulie P, Colau D, et al. Correlation between tumor regression and T cell responses in melanoma patients vaccinated with a MAGE antigen. Proc Natl Acad Sci U S A 2004;101:14631-8. (Pubitemid 39346735)
5. Germeau C, Ma W, Schiavetti F, Lurquin C, Henry E, Vigneron N, et al. High frequency of anti-tumor T cells in the blood of melanoma patients before and after vaccination with tumor antigens. J Exp Med 2005;201:241-8. (Pubitemid 40189433)
6. van Baren N, Bonnet M-C, Dréno B, Khammari A, Dorval T, Piperno-Neumann S, et al. Tumoral and immunologic response after vaccination of melanoma patients with an ALVAC virus encoding MAGE antigens recognized by T cells. J Clin Oncol 2005;23:9008-21. (Pubitemid 46211485)
7. Lurquin C, Lethé B, Corbière V, Théate I, van Baren N, Coulie PG, et al. Contrasting frequencies of anti-tumor and anti-vaccine T cells in metastases of a melanoma patient vaccinated with a MAGE tumor antigen. J Exp Med 2005;201:249-57. (Pubitemid 40189434)
8. Ma W, Germeau C, Vigneron N, Maernoudt A-S, Morel S, Boon T, et al. Two new tumor-specific antigenic peptides encoded by gene MAGEC2 and presented to cytolytic T lymphocytes by HLA-A2. Int J Cancer 2004;109:698-702. (Pubitemid 38405616)
9. Espevik T, Nissen-Meyer J. A highly sensitive cell line, WEHI 164 clone 13, for measuring cytotoxic factor/tumor necrosis factor from human monocytes. J Immunol Methods 1986;95:99-105. (Pubitemid 17196641)
10. Hansen MB, Nielsen SE, Berg K. Re-examination and further development of a precise and rapid dye method for measuring cell growth/ cell kill. J Immunol Methods 1989;119:203-10. (Pubitemid 19132276)
11. Chapiro J, Claverol S, Piette F, Ma W, Stroobant V, Guillaume B, et al. Destructive cleavage of antigenic peptides either by the immunoproteasome or by the standard proteasome results in differential antigen presentation. J Immunol 2006; 176:1053-61. (Pubitemid 43099706)
12. Parker KC, Bednarek MA, Hull LK, Utz U, Cunningham B, Zweerink HJ, et al. Sequence motifs important for peptide binding to the human MHC class I molecule, HLA-A2. J Immunol 1992;149:3580-7.
13. Pleasance ED, Cheetham RK, Stephens PJ, McBride DJ, Humphray SJ, Greenman CD, et al. A comprehensive catalogue of somatic mutations from a human cancer genome. Nature 2010;463: 191-6.
14. Parker KC, Bednarek MA, Coligan JE. Scheme for ranking potential HLA-A2 binding peptides based on independent binding of individual peptide side-chains. J Immunol 1994;152:163-75.
15. Yewdell JW, Anton LC, Bennink JR. Defective ribosomal products (DRiPs): a major source of antigenic peptides for MHC class I molecules?J Immunol 1996;157:1823-6.
16. Princiotta MF, Finzi D, Qian SB, Gibbs J, Schuchmann S, Buttgereit F, et al. Quantitating protein synthesis, degradation, and endogenous antigen processing. Immunity 2003; 18:343-54.
17. Schultz ES, Chapiro J, Lurquin C, Claverol S, Burlet-Schiltz O, Warnier G, et al. The production of a new MAGE-3 peptide presented to cytolytic T lymphocytes by HLA-B40 requires the immunoproteasome. J Exp Med 2002;195:391-9. (Pubitemid 34461293)
18. Basler M, Youhnovski N, Van Den Broek M, Przybylski M, Groettrup M. Immunoproteasomes down-regulate presentation of a subdominant T cell epitope from lymphocytic choriomeningitis virus. J Immunol 2004;173:3925-34. (Pubitemid 39280756)
19. Morel S, Lévy F, Burlet-Schiltz O, Brasseur F, Probst-Kepper M, Peitrequin A-L, et al. Processing of some antigens by the standard proteasome but not by the immunoproteasome results in poor presentation by dendritic cells. Immunity 2000;12:107-17. (Pubitemid 30069219)
20. Carrasco J, Van Pel A, Neyns B, Lethé B, Brasseur F, Renkvist N, et al. Vaccination of a melanoma patient with mature dendritic cells pulsed with MAGE-3 peptides triggers the activity of nonvaccine anti-tumor cells. J Immunol 2008;180:3585-93.
21. Lally KM, Mocellin S, Ohnmacht GA, Nielsen MB, Bettinotti M, Panelli MC, et al. Unmasking cryptic epitopes after loss of immunodominant tumor antigen expression through epitope spreading. Int J Cancer 2001;93:841-7. (Pubitemid 32756754)
22. Brossart P, Wirths S, Stuhler G, Reichardt VL, Kanz L, Brugger W. Induction of cytotoxic T-lymphocyte responses in vivo after vaccinations with peptide-pulsed dendritic cells. Blood 2000;96:3102-8.
23. Butterfield LH, Ribas A, Dissette VB, Amarnani SN, Vu HT, Oseguera D, et al. Determinant spreading associated with clinical response in dendritic cell-based immunotherapy for malignant melanoma. Clin Cancer Res 2003;9:998-1008. (Pubitemid 36323703)
24. Disis ML, Gooley TA, Rinn K, Davis D, Piepkorn M, Cheever MA, et al. Generation of T-cell immunity to the HER-2/neu protein after active immunization with HER-2/neu peptide-based vaccines. J Clin Oncol 2002;20:2624-32. (Pubitemid 34575634)
25. Disis ML, Wallace DR, Gooley TA, Dang Y, Slota M, Lu H, et al. Concurrent trastuzumab and HER2/neu-specific vaccination in patients with metastatic breast cancer. J Clin Oncol 2009;27: 4685-92.
26. Carmichael MG, Benavides LC, Holmes JP, Gates JD, Mittendorf EA, Ponniah S, et al. Results of the first phase 1 clinical trial of the HER-2/ neu peptide (GP2) vaccine in disease-free breast cancer patients: United States Military Cancer Institute Clinical Trials Group Study I-04. Cancer 2010;116:292-301.
27. Gulley JL, Arlen PM, Bastian A, Morin S, Marte J, Beetham P, et al. Combining a recombinant cancer vaccine with standard definitive radiotherapy in patients with localized prostate cancer. Clin Cancer Res 2005;11:3353-62. (Pubitemid 40627887)
28. Vignard V, Lemercier B, Lim A, Pandolfino MC, Guilloux Y, Khammari A, et al. Adoptive transfer of tumor-reactive Melan-A-specific CTL clones in melanoma patients is followed by increased frequencies of additional Melan-A-specific T cells. J Immunol 2005; 175:4797-805. (Pubitemid 41362023)
29. Khammari A, Labarriere N, Vignard V, Nguyen JM, Pandolfino MC, Knol AC, et al. Treatment of metastatic melanoma with autologous Melan-A/MART-1-specific cytotoxic T lymphocyte clones. J Invest Dermatol 2009;129:2835-42.
30. Hunder NN, Wallen H, Cao J, Hendricks DW, Reilly JZ, Rodmyre R, et al. Treatment of metastatic melanoma with autologous CD4+ T cells against NY-ESO-1. N Engl J Med 2008;358:2698-703. (Pubitemid 351860862)
31. Riener MO, Wild PJ, Soll C, Knuth A, Jin B, Jungbluth A, et al. Frequent expression of the novel cancer testis antigen MAGE-C2/CT-10 in hepatocellular carcinoma. Int J Cancer 2009;124:352-7.
32. Marchand M, van Baren N, Weynants P, Brichard V, Dréno B, Tessier M-H, et al. Tumor regressions observed in patients with metastatic melanoma treated with an antigenic peptide encoded by gene MAGE- 3 and presented by HLA-A1. Int J Cancer 1999;80:219-30. (Pubitemid 29001725)
33. Maurizi MR, Xia D. Protein binding and disruption by Clp/Hsp100 chaperones. Structure 2004;12:175-83. (Pubitemid 38224541)
34. Kang SG, Dimitrova MN, Ortega J, Ginsburg A, Maurizi MR. Human mitochondrial ClpP is a stable heptamer that assembles into a tetradecamer in the presence of ClpX. J Biol Chem 2005; 280:35424-32. (Pubitemid 41532732)
35. Kessel M, Maurizi MR, Kim B, Kocsis E, Trus BL, Singh SK, et al. Homology in structural organization between E coli ClpAP protease and the eukaryotic 26 S proteasome. J Mol Biol 1995;250: 587-94.
36. Yu AY, Houry WA. ClpP: a distinctive family of cylindrical energy-dependent serine proteases. FEBS Lett 2007;581:3749-57. (Pubitemid 47082517)
37. Bross P, Andresen BS, Knudsen I, Kruse TA, Gregersen N. Human ClpP protease: cDNA sequence, tissue-specific expression and chromosomal assignment of the gene. FEBS Lett 1995;377:249-52. (Pubitemid 26018529)
38. de Sagarra MR, Mayo I, Marco S, Rodriguez-Vilarino S, Oliva J, Carrascosa JL, et al. Mitochondrial localization and oligomeric structure of HClpP, the human homologue of E. coli ClpP. J Mol Biol 1999;292:819-25. (Pubitemid 29465476)
39. Dabhi VM, Hovik R, Van Kaer L, Fischer Lindahl K. The alloreactive T cell response against the class Ib molecule H2-M3 is specific for high affinity peptides. J Immunol 1998;161:5171-8. (Pubitemid 28519074)
40. Sasada T, Ghendler Y, Neveu JM, Lane WS, Reinherz EL. A naturally processed mitochondrial self-peptide in complex with thymic MHC molecules functions as a selecting ligand for a viral-specific T cell receptor. J Exp Med 2001;194:883-92.
41. Kita H, Lian ZX, Van de Water J, He XS, Matsumura S, Kaplan M, et al. Identification of HLA-A2-restricted CD8(+) cytotoxic T cell responses in primary biliary cirrhosis: T cell activation is augmented by immune complexes cross-presented by dendritic cells. J Exp Med 2002;195:113-23. (Pubitemid 34074501)
42. Major T, von Janowsky B, Ruppert T, Mogk A, Voos W. Proteomic analysis of mitochondrial protein turnover: identification of novel substrate proteins of the matrix protease pim1. Mol Cell Biol 2006;26:762-76. (Pubitemid 43146474)
43. Langer T. AAA proteases: cellular machines for degrading membrane proteins. Trends Biochem Sci 2000;25:247-51. (Pubitemid 30236223)
44. Young L, Leonhard K, Tatsuta T, Trowsdale J, Langer T. Role of the ABC transporter Mdl1 in peptide export from mitochondria. Science 2001;291:2135-8. (Pubitemid 32224441)
45. Ma W, Vigneron N, Chapiro J, Stroobant V, Germeau C, Boon T, et al. A MAGE-C2 antigenic peptide processed by the immunoproteasome is recognized by cytolytic T cells isolated from a melanoma patient after successful immunotherapy. Int J Cancer 2011 Jan 4. [Epub ahead of print].