T-cell responses of vaccinated cancer patients

Current Opinion in Immunology

Volumn 15, Issue 2, 2003, Pages 131-137

  Coulie, Pierre G ^a   Van Der Bruggen, Pierre ^a,b  

^a DE DUVE INSTITUTE   (Belgium)

^b LUDWIG INSTITUTE FOR CANCER RESEARCH   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; GAMMA INTERFERON; HLA A1 ANTIGEN; INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 7;

CANCER PATIENT; CELL ACTIVITY; CELL FUNCTION; CORRELATION ANALYSIS; EVALUATION; HUMAN; PROTEIN EXPRESSION; REVIEW; T LYMPHOCYTE; TUMOR REGRESSION; VACCINATION;

EID: 0037375333     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0952-7915(03)00009-8     Document Type: Review

References (58)

1. Marchand M., van Baren N., Weynants P., Brichard V., Dréno B., Tessier M.-H., Rankin E., Parmiani G., Arienti F., Humblet Y.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. 80:1999;219-230.
2. Marchand M, Punt CJA, Aamdal S, Escudier B, Kruit WHJ, Keilholz U, Håkansson L, van Baren N, Humblet Y, Mulders P et al.: Immunization of metastatic cancer patients with MAGE-3 protein combined with adjuvant SBAS-2: clinical report. Eur J Cancer 2003, in press.
3. + progenitor-derived dendritic cells pulsed with Melan-A, tyrosinase, MAGE-3 and gp100 peptides, as well as influenza matrix peptide and KLH as control antigens. ELISPOT assays detected immune responses to control antigens (KLH, Flu-MP) in 16 out of 18 patients. For the same 16 patients, responses to at least one tumor antigen were detected, but only after in vitro stimulation for seven days.
4. + cells in at least one blood sample from five out of eight patients. Surprisingly these observed responses vary considerably between consecutive samples of the same vaccinated patient.
5. + cancers. Proc. Natl. Acad. Sci. USA. 97:2000;12198-12203.
6. + melanoma patients by mature monocyte-derived dendritic cells. J. Immunol. 165:2000;3492-3496.
7. + T cells for six days with peptide-pulsed cells and measuring IFN-γ production by ELISA. The results showed no increase in IFN-γ production after vaccination for two patients vaccinated without IL-12, but an increase in the four patients vaccinated with IL-12.
8. Blattman J.N., Antia R., Sourdive D.J., Wang X., Kaech S.M., Murali-Krishna K., Altman J.D., Ahmed R. Estimating the precursor frequency of naïve antigen-specific CD8 T cells. J. Exp. Med. 195:2002;657-664.
9. Chaux P., Vantomme V., Coulie P., Boon T., van der Bruggen P. Estimation of the frequencies of anti-MAGE-3 cytolytic T lymphocyte precursors in blood from individuals without cancer. Int. J. Cancer. 77:1998;538-542.
10. Coulie P.G., Karanikas V., Lurquin C., Colau D., Connerotte T., Hanagiri T., Van Pel A., Lucas S., Godelaine D., Lonchay C.et al. Cytolytic T cell responses of cancer patients vaccinated with a MAGE antigen. Immunol. Rev. 188:2002;33-42 The authors present an evaluation of the responses of melanoma patients vaccinated with peptide MAGE-3.A1 or a recombinant ALVAC coding for the peptide. In 4 out of 9 regressor patients and 1 out of 14 progressors, a low-level specific T-cell response was found, usually monoclonal.
11. Weekes M.P., Wills M.R., Mynard K., Carmichael A.J., Sissons J.G.P. The memory cytotoxic T-lymphocyte (CTL) response to human cytomegalovirus infection contains individual peptide-specific CTL clones that have undergone extensive expansion in vivo. J. Virol. 73:1999;2099-2108.
12. + T cells specific for EBV in healthy virus carriers. J. Immunol. 162:1999;1827-1835.
13. Gea-Banacloche J.C., Migueles S.A., Martino L., Shupert W.L., McNeil A.C., Sabbaghian M.S., Ehler L., Prussin C., Stevens R., Lambert L.et al. Maintenance of large numbers of virus-specific CD8+ T cells in HIV-infected progressors and long-term nonprogressors. J. Immunol. 165:2000;1082-1092.
14. + T cells. These T cells have been enumerated using tetramers in the thymus and periphery of newborns and adults. The replicative history of the T cells was studied by quantifying telomere length and TCR excision circles. This study demonstrates that this unusually high frequency is a result of the thymic output of a high number of naïve precursors.
15. + T cells by endogenous tumor antigen and peptide vaccines. A comparison to virus-specific T cells. Eur. J. Immunol. 32:2002;731-741.
16. Dunbar P.R., Smith C.L., Chao D., Salio M., Shepherd D., Mirza F., Lipp M., Lanzavecchia A., Sallusto F., Evans A.et al. A shift in the phenotype of melan-A-specific CTL identifies melanoma patients with an active tumor-specific immune response. J. Immunol. 165:2000;6644-6652.
17. + T lymphocytes secreting tumor necrosis factor alpha in response to HLA-A2.1-binding melanoma and viral peptide antigens. J. Immunol. Methods. 191:1996;131-142.
18. + T lymphocytes in IFN-γ ELISPOT assays. J. Immunol. Methods. 259:2002;95-110 A nice technical improvement to a method from the group that applied ELISPOT to anti-tumor T cells. A difficulty encountered when using ELISPOT assays is the lack of a permanent source of HLA-matched antigen-presenting cells, which are overcome with T2 when the peptide is presented by HLA-A2. In this paper, the authors show that the human leukemia cell line K562, which does not normally carry HLA molecules, does so after transfection with an HLA construct.
19. + T lymphocytes producing tumor necrosis factor alpha spots in response to peptide antigens. J. Immunol. Methods. 203:1997;141-152.
20. Scheibenbogen C., Romero P., Rivoltini L., Herr W., Schmittel A., Cerottini J.-C., Woelfel T., Eggermont A.M.M., Keilholz U. Quantitation of antigen-reactive T cells in peripheral blood by IFNγ-ELISPOT assay and chromium-release assay: a four-centre comparative trial. J. Immunol. Methods. 244:2000;81-89.
21. Musselli C., Ragupathi G., Gilewski T., Panageas K.S., Spinat Y., Livingston P.O. Reevaluation of the cellular immune response in breast cancer patients vaccinated with MUC1. Int. J. Cancer. 97:2002;660-667 Six breast cancer patients have been vaccinated with a long MUC1 peptide with KLH and adjuvant QS21. T-cell responses to MUC1 were minimal, with inconsistent results obtained from carefully conducted proliferation and ELISPOT assays, either directly ex vivo or following six days of in vitro re-stimulation.
22. Schultz E.S., Zhang Y., Knowles R., Tine J., Traversari C., Boon T., van der Bruggen P. A MAGE-3 peptide recognized on HLA-B35 and HLA-A1 by cytolytic T lymphocytes. Tissue Antigens. 57:2001;103-109.
23. Bilsborough J., Panichelli C., Duffour M.T., Warnier G., Lurquin C., Schultz E.S., Thielemans K., Corthals J., Boon T., van der Bruggen P. A MAGE-3 peptide presented by HLA-B44 is also recognized by cytolytic T lymphocytes on HLA-B18. Tissue Antigens. 60:2002;16-24.
24. Toungouz M., Libin M., Bulte F., Faid L., Lehmann F., Duriau D., Laporte M., Gangji D., Bruyns C., Lambermont M.et al. Transient expansion of peptide-specific lymphocytes producing IFN-γ after vaccination with dendritic cells pulsed with MAGE peptides in patients with MAGE-A1/A3-positive tumors. J. Leukoc. Biol. 69:2001;937-943.
25. Brosterhus H., Brings S., Leyendeckers H., Manz R.A., Miltenyi S., Radbruch A., Assenmacher M., Schmitz J. Enrichment and detection of live antigen-specific CD4(+) and CD8(+) T cells based on cytokine secretion. Eur. J. Immunol. 29:1999;4053-4059.
26. + cells, respectively.
27. Kammula U.S., Lee K.H., Riker A.I., Wang E., Ohnmacht G.A., Rosenberg S.A., Marincola F.M. Functional analysis of antigen-specific T lymphocytes by serial measurement of gene expression in peripheral blood mononuclear cells and tumor specimens. J. Immunol. 163:1999;6867-6875.
28. Altman J.D., Moss P.A.H., Goulder P.J.R., Barouch D.H., McHeyzer-Williams M.G., Bell J.I., McMichael A.J., Davis M.M. Phenotypic analysis of antigen-specific T lymphocytes. Science. 274:1996;94-96.
29. + T cells through the combination of MHC class I tetramer and intracellular staining. J. Immunol. Methods. 268:2002;9-19.
30. + T cells. J. Immunol. Methods. 268:2002;71-81.
31. Bodinier M., Peyrat M.A., Tournay C., Davodeau F., Romagne F., Bonneville M., Lang F. Efficient detection and immunomagnetic sorting of specific T cells using multimers of MHC class I and peptide with reduced CD8 binding. Nat. Med. 6:2000;707-710.
32. + T cells with a Melan-A.A2 tetramer. One-third of the tetramer-positive cells failed to recognize the Melan-A.A2 peptide in a functional assay, but efficiently recognized other peptides.
33. -13 M). The streptavidin-peptide bonds of the tetramers can be competitively disrupted by adding free biotin.
34. + cells produce IFN-γ in response to contact with an envelope peptide. However, these cells cannot be detected with the relevant tetramer, unless they are re-stimulated repeatedly in vitro.
35. Welsh R.M. Assessing CD8 T cell number and dysfunction in the presence of antigen. J. Exp. Med. 193:2001;F19-F22.
36. + T lymphocytes involving loss of tetramer labeling. Eur. J. Immunol. 32:2002;1688-1697.
37. Coulie P.G., Karanikas V., Colau D., Lurquin C., Landry C., Marchand M., Dorval T., Brichard V., Boon T. 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. USA. 98:2001;10290-10295 This paper documents that MAGE-3.A1 peptide administered without adjuvant elicited a monoclonal CTL response in a patient who showed regression of his melanoma metastases after vaccination. The CTLs were detected by tetramer after in vitro stimulation in limiting dilution conditions, and frequencies were confirmed by clonotypic PCR. This work suggests that low-level CTL responses can initiate tumor rejection.
38. + T cells.
39. Steller M.A., Gurski K.J., Murakami M., Daniel R.W., Shah K.V., Celis E., Sette A., Trimble E.L., Park R.C., Marincola F.M. Cell-mediated immunological responses in cervical and vaginal cancer patients immunized with a lipidated epitope of human papillomavirus type 16 E7. Clin. Cancer Res. 4:1998;2103-2109.
40. + T cells after vaccination with antigenic peptide. Clin. Cancer Res. 7:2001;S796-S803.
41. Wang F., Bade E., Kuniyoshi C., Spears L., Jeffery G., Marty V., Groshen S., Weber J. Phase I trial of a MART-1 peptide vaccine with incomplete Freund's adjuvant for resected high-risk melanoma. Clin. Cancer Res. 5:1999;2756-2765.
42. + T-cell evolution in vivo: response to peptide vaccination with Melan-A/MART-1. Int. J. Cancer. 98:2002;376-388.
43. Valmori D., Dutoit V., Schnuriger V., Quiquerez A.-L., Pittet M.J., Guillaume P., Rubio-Godoy V., Walker P.R., Rimoldi D., Liénard D.et al. Vaccination with a Melan-A peptide selects an oligoclonal T cell population with increased functional avidity and tumor reactivity. J. Immunol. 168:2002;4231-4240.
44. + T cells in melanoma patients receiving interleukin 12. Cancer Res. 60:2000;3559-3568.
45. Lee P., Wang F., Kuniyoshi J., Rubio V., Stuges T., Groshen S., Gee C., Lau R., Jeffery G., Margolin K.et al. Effects of interleukin-12 on the immune response to a multipeptide vaccine for resected metastatic melanoma. J. Clin. Oncol. 19:2001;3836-3847.
46. Lee K.-H., Wang E., Nielsen M.-B., Wunderlich J., Migueles S., Connors M., Steinberg S.M., Rosenberg S.A., Marincola F.M. Increased vaccine-specific T cell frequency after peptide-based vaccination correlates with increased susceptibility to in vitro stimulation but does not lead to tumor regression. J. Immunol. 163:1999;6292-6300.
47. 280-288 peptide and tetanus helper peptide in adjuvant: immunologic and clinical outcomes. Clin. Cancer Res. 7:2001;3012-3024.
48. Monsurro V., Nielsen M.-B., Perez-Diez A., Dudley M.E., Wang E., Rosenberg S.A., Marincola F.M. Kinetics of TCR use in response to repeated epitope-specific immunization. J. Immunol. 166:2001;5817-5825.
49. Yamshchikov G.V., Barnd D.L., Eastham S., Galavotti H., Patterson J.W., Deacon D.H., Teates D., Neese P., Grosh W.W., Petroni G.et al. Evaluation of peptide vaccine immunogenicity in draining lymph nodes and peripheral blood of melanoma patients. Int. J. Cancer. 92:2001;703-711 The authors present an indication that monitoring clinical trials using PBMC alone may underestimate immunogenicity. An evaluation of T cells in the lymph node draining the vaccine site was more sensitive.
50. Knutson K.L., Disis M.L. Clonal diversity of the T-cell population responding to a dominant HLA-A2 epitope of HER-2/neu after active immunization in an ovarian cancer patient. Hum. Immunol. 63:2002;547-557.
51. Disis M.L., Gooley T.A., Rinn K., Davis D., Piepkorn M., Cheever M.A., Knutson K.L., Schiffman K. Generation of T-cell immunity to the HER-2/neu protein after active immunization with HER-2/neu peptide-based vaccines. J. Clin. Oncol. 20:2002;2624-2632.
52. Scholl S.M., Balloul J.-M., Le Goc G., Bizouarne N., Schatz C., Kieny M.P., von Mensdorff-Pouilly S., Vincent-Salomon A., Deneux L., Tartour E.et al. Recombinant vaccinia virus encoding human MUC1 and IL2 as immunotherapy in patients with breast cancer. J. Immunother. 23:2000;570-580.
53. van der Burg S.H., Menon A.G., Redeker A., Bonnet M.-C., Drijfhout J.W., Tollenaar R.A.E.M., van de Velde C.J.H., Moingeon P., Kuppen P.J.K., Offringa R.et al. Induction of p53-specific immune responses in colorectal cancer patients receiving a recombinant ALVAC-p53 candidate vaccine. Clin. Cancer Res. 8:2002;1019-1027.
54. + hematopoietic progenitor cells. Int. J. Cancer. 86:2000;385-392.
55. Brossart P., Wirths S., Stuhler G., Reichardt V.L., Kanz L., Brugger W. Induction of cytotoxic T-lymphocyte responses in vivo after vaccinations with peptide-pulsed dendritic cells. Blood. 96:2000;3102-3108.
56. Lim S.H., Bailey-Wood R. Idiotypic protein-pulsed dendritic cell vaccination in multiple myeloma. Int. J. Cancer. 83:1999;215-222.
57. Lally K.M., Mocellin S., Ohnmacht G.A., Nielsen M.B., Bettinotti M., Panelli M.C., Monsurro V., Marincola F.M. Unmasking cryptic epitopes after loss of immunodominant tumor antigen expression through epitope spreading. Int. J. Cancer. 93:2001;841-847.
58. Ohnmacht G.A., Wang E., Mocellin S., Abati A., Filie A., Fetsch P., Riker A.I., Kammula U.S., Rosenberg S.A., Marincola F.M. Short-term kinetics of tumor antigen expression in response to vaccination. J. Immunol. 167:2001;1809-1820 An interesting insight into regressing metastases. The expression of gp100 was tested in fine needle aspirate biopsies obtained from melanoma patients before and after vaccination with gp100 peptides. The results suggest that metastases may lose gp100 expression before they regress.