The simultaneous ex vivo detection of low-frequency antigen-speciWc CD4+ and CD8+ T-cell responses using overlapping peptide pools

Cancer Immunology, Immunotherapy

Volumn 61, Issue 11, 2012, Pages 1953-1963

  Singh, Satwinder Kaur ^a   Meyering, Maaike ^a   Ramwadhdoebe, Tamara H ^a   Stynenbosch, Linda F M ^a   Redeker, Anke ^a   Kuppen, Peter J K ^a   Melief, Cornelis J M ^a   Welters, Marij J P ^a   Van Der Burg, Sjoerd H ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Flow cytometry; Immunomonitoring; Intracellular cytokine staining; Monocytes; T cells

Indexed keywords

EPITOPE; GAMMA INTERFERON; HLA ANTIGEN CLASS 1; PEPTIDE; PEPTIDE VACCINE; POLYINOSINIC POLYCYTIDYLIC ACID; PROTEIN P53 VACCINE; UNCLASSIFIED DRUG;

ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ARTICLE; BLOOD SAMPLING; CASE REPORT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CLINICAL PROTOCOL; CLINICAL TRIAL (TOPIC); COLORECTAL CANCER; CONCENTRATION RESPONSE; CONTROLLED STUDY; CRYOPRESERVATION; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSPOT ASSAY; EX VIVO STUDY; FLOW CYTOMETRY; HLA TYPING; HUMAN; HUMAN CELL; IMMUNOMONITORING; IMMUNOREACTIVITY; INTRACELLULAR CYTOKINE STAINING; MONOCYTE; PATIENT MONITORING; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; STAINING; T LYMPHOCYTE ACTIVATION;

ANTIGEN PRESENTATION; ANTIGENS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; ENZYME-LINKED IMMUNOSPOT ASSAY; EPITOPES, T-LYMPHOCYTE; FLOW CYTOMETRY; HUMANS; INTERFERON-GAMMA; LYMPHOCYTE ACTIVATION; PEPTIDES; POLY I-C;

EID: 84870976762     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-012-1251-3     Document Type: Article

References (41)

1. Cerundolo V (1999) T cells work together to Wght cancer. Curr Biol (CB) 9(18):R695-R697
2. Melief CJ, Van Der Burg SH, Toes RE, Ossendorp F, Ovringa R (2002) EVective therapeutic anticancer vaccines based on precision guiding of cytolytic T lymphocytes. Immunol Rev 188:177-182
3. Toes RE, Ossendorp F, Ovringa R, Melief CJ (1999) CD4 T cells and their role in antitumor immune responses. J Exp Med 189(5):753-756
4. Cavallo F, Ovringa R, van der Burg SH, Forni G, Melief CJ (2006) Vaccination for treatment and prevention of cancer in animal models. Adv Immunol 90:175-213. doi:10.1016/S0065-2776(06)90005-4
5. Dudley ME, Yang JC, Sherry R, Hughes MS, Royal R, Kammula U, Robbins PF, Huang J, Citrin DE, Leitman SF, Wunderlich J, Restifo NP, Thomasian A, Downey SG, Smith FO, Klapper J, Morton K, Laurencot C, White DE, Rosenberg SA (2008) Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J Clin Oncol OV J Am Soc Clin Oncol 26(32):5233-5239. doi:10.1200/JCO.2008.16.5449
6. Verdegaal EM, Visser M, Ramwadhdoebe TH, van der Minne CE, van Steijn JA, Kapiteijn E, Haanen JB, van der Burg SH, Nortier JW, Osanto S (2011) Successful treatment of metastatic melanoma by adoptive transfer of blood-derived polyclonal tumor-speciWc CD4+ and CD8+ T cells in combination with low-dose interferonalpha. Cancer Immunol Immunother (CII) 60(7):953-963. doi:10.1007/s00262-011-1004-8
7. Daayana S, Elkord E, Winters U, Pawlita M, Roden R, Stern PL, Kitchener HC (2010) Phase II trial of imiquimod and HPV therapeutic vaccination in patients with vulval intraepithelial neoplasia. Br J Cancer 102(7):1129-1136. doi:10.1038/sj.bjc.6605611
8. Kenter GG, Welters MJ, Valentijn AR, Lowik MJ, Berends-van der Meer DM, Vloon AP, Essahsah F, Fathers LM, Ovringa R, Drijfhout JW, Wafelman AR, Oostendorp J, Fleuren GJ, van der Burg SH, Melief CJ (2009) Vaccination against HPV-16 oncoproteins for vulvar intraepithelial neoplasia. N Engl J Med 361(19):1838-1847. doi:10.1056/NEJMoa0810097
9. van Poelgeest MI, van Seters M, van Beurden M, Kwappenberg KM, Heijmans-Antonissen C, Drijfhout JW, Melief CJ, Kenter GG, Helmerhorst TJ, Ovringa R, van der Burg SH (2005) Detection of human papillomavirus (HPV) 16-speciWc CD4+ T-cell immunity in patients with persistent HPV16-induced vulvar intraepithelial neoplasia in relation to clinical impact of imiquimod treatment. Clin Cancer Res OV J Am Assoc Cancer Res 11(14):5273-5280. doi:10.1158/1078-0432.CCR-05-0616
10. Welters MJ, Kenter GG, de Vos van Steenwijk PJ, Lowik MJ, Berends-van der Meer DM, Essahsah F, Stynenbosch LF, Vloon AP, Ramwadhdoebe TH, Piersma SJ, van der Hulst JM, Valentijn AR, Fathers LM, Drijfhout JW, Franken KL, Oostendorp J, Fleuren GJ, Melief CJ, van der Burg SH (2010) Success or failure of vaccination for HPV16-positive vulvar lesions correlates with kinetics and phenotype of induced T-cell responses. Proc Natl Acad Sci USA 107(26):11895-11899. doi:10.1073/pnas.1006500107
11. Welters MJ, Kenter GG, Piersma SJ, Vloon AP, Lowik MJ, Berends-van der Meer DM, Drijfhout JW, Valentijn AR, Wafelman AR, Oostendorp J, Fleuren GJ, Ovringa R, Melief CJ, van der Burg SH (2008) Induction of tumor-speciWc CD4+ and CD8+ T-cell immunity in cervical cancer patients by a human papillomavirus type 16 E6 and E7 long peptides vaccine. Clin Cancer Res OV J Am Assoc Cancer Res 14(1):178-187. doi:10.1158/1078-0432.CCR-07-1880
12. Betts MR, Ambrozak DR, Douek DC, BonhoeVer S, Brenchley JM, Casazza JP, Koup RA, Picker LJ (2001) Analysis of total human immunodeWciency virus (HIV)-speciWc CD4(+) and CD8(+) T-cell responses: relationship to viral load in untreated HIV infection. J Virol 75(24):11983-11991. doi:10.1128/JVI.75. 24.11983-11991.2001
13. Tobery TW, Wang S, Wang XM, Neeper MP, Jansen KU, McClements WL, CaulWeld MJ (2001) A simple and eYcient method for the monitoring of antigen-speciWc T cell responses using peptide pool arrays in a modiWed ELISpot assay. J Immunol Methods 254(1-2):59-66
14. Karlsson AC, Martin JN, Younger SR, Bredt BM, Epling L, Ronquillo R, Varma A, Deeks SG, McCune JM, Nixon DF, Sinclair E (2003) Comparison of the ELISPOT and cytokine Xow cytometry assays for the enumeration of antigen-speciWc T cells. J Immunol Methods 283(1-2):141-153
15. Kiecker F, Streitz M, Ay B, Cherepnev G, Volk HD, Volkmer-Engert R, Kern F (2004) Analysis of antigen-speciWc T-cell responses with synthetic peptides-what kind of peptide for which purpose? Hum Immunol 65(5):523-536. doi:10.1016/j.humimm. 2004.02.017
16. de Jong A, van der Hulst JM, Kenter GG, Drijfhout JW, Franken KL, Vermeij P, Ovringa R, van der Burg SH, Melief CJ (2005) Rapid enrichment of human papillomavirus (HPV)-speciWc polyclonal T cell populations for adoptive immunotherapy of cervical cancer. Int J Cancer (Journal international du cancer) 114(2):274-282. doi:10.1002/ijc.20721
17. Janetzki S, Panageas KS, Ben-Porat L, Boyer J, Britten CM, Clay TM, Kalos M, Maecker HT, Romero P, Yuan J, Kast WM, Hoos A, Elispot ProWciency Panel of the CVCIAWG (2008) Results and harmonization guidelines from two large-scale international Elispot proWciency panels conducted by the Cancer Vaccine Consortium (CVC/SVI). Cancer Immunol Immunother (CII) 57(3): 303-315. doi:10.1007/s00262-007-0380-6
18. Moodie Z, Price L, Gouttefangeas C, Mander A, Janetzki S, Lower M, Welters MJ, Ottensmeier C, van der Burg SH, Britten CM (2010) Response deWnition criteria for ELISPOT assays revisited. Cancer Immunol Immunother (CII) 59(10):1489-1501. doi:10.1007/s00262-010-0875-4
19. van der Burg SH, Ressing ME, Kwappenberg KM, de Jong A, Straathof K, de Jong J, Geluk A, van Meijgaarden KE, Franken KL, OttenhoV TH, Fleuren GJ, Kenter G, Melief CJ, Ovringa R (2001) Natural T-helper immunity against human papillomavirus type 16 (HPV16) E7-derived peptide epitopes in patients with HPV16-positive cervical lesions: identiWcation of 3 human leukocyte antigen class II-restricted epitopes. Int J Cancer (Journal international du cancer) 91(5):612-618
20. Welters MJ, de Jong A, van den Eeden SJ, van der Hulst JM, Kwappenberg KM, Hassane S, Franken KL, Drijfhout JW, Fleuren GJ, Kenter G, Melief CJ, Ovringa R, van der Burg SH (2003) Frequent display of human papillomavirus type 16 E6-speciWc memory t-Helper cells in the healthy population as witness of previous viral encounter. Cancer Res 63(3):636-641
21. Britten CM, Janetzki S, van der Burg SH, Huber C, Kalos M, Levitsky HI, Maecker HT, Melief CJ, O'Donnell-Tormey J, Odunsi K, Old LJ, Pawelec G, Roep BO, Romero P, Hoos A, Davis MM (2011) Minimal information about T cell assays: the process of reaching the community of T cell immunologists in cancer and beyond. Cancer Immunol Immunother (CII) 60(1):15-22. doi:10.1007/s00262-010-0940-z
22. Janetzki S, Britten CM, Kalos M, Levitsky HI, Maecker HT, Melief CJ, Old LJ, Romero P, Hoos A, Davis MM (2009) "MIATA"-minimal information about T cell assays. Immunity 31(4):527-528. doi:10.1016/j.immuni.2009.09.007
23. van der Burg SH, Kwappenberg KM, Geluk A, van der Kruk M, Pontesilli O, Hovenkamp E, Franken KL, van Meijgaarden KE, Drijfhout JW, OttenhoV TH, Melief CJ, Ovringa R (1999) Identi-Wcation of a conserved universal Th epitope in HIV-1 reverse transcriptase that is processed and presented to HIV-speciWc CD4+ T cells by at least four unrelated HLA-DR molecules. J Immunol 162(1):152-160
24. Britten CM, Gouttefangeas C, Welters MJ, Pawelec G, Koch S, Ottensmeier C, Mander A, Walter S, Paschen A, Muller-Berghaus J, Haas I, Mackensen A, Kollgaard T, Thor Straten P, Schmitt M, Giannopoulos K, Maier R, Veelken H, Bertinetti C, Konur A, Huber C, Stevanovic S, Wolfel T, van der Burg SH (2008) The CIMT-monitoring panel: a two-step approach to harmonize the enumeration of antigen-speciWc CD8+ T lymphocytes by structural and functional assays. Cancer Immunol Immunother (CII) 57(3):289-302. doi:10.1007/s00262-007-0378-0
25. Lattanzi L, Rozera C, Marescotti D, D'Agostino G, Santodonato L, Cellini S, Belardelli F, Gavioli R, Ferrantini M (2011) IFNalpha boosts epitope cross-presentation by dendritic cells via modulation of proteasome activity. Immunobiology 216(5):537-547. doi:10.1016/j.imbio.2010.10.003
26. Le Bon A, Tough DF (2008) Type I interferon as a stimulus for cross-priming. Cytokine Growth Factor Rev 19(1):33-40. doi:10.1016/j.cytogfr. 2007.10.007
27. Sikora AG, JaVarzad N, Hailemichael Y, Gelbard A, Stonier SW, Schluns KS, Frasca L, Lou Y, Liu C, Andersson HA, Hwu P, Overwijk WW (2009) IFN-Alpha enhances peptide vaccineinduced CD8+ T cell numbers, eVector function, and antitumor activity. J Immunol 182(12):7398-7407. doi:10.4049/jimmunol. 0802982
28. de Vos van Steenwijk PJ, Heusinkveld M, Ramwadhdoebe TH, Lowik MJ, van der Hulst JM, Goedemans R, Piersma SJ, Kenter GG, van der Burg SH (2010) An unexpectedly large polyclonal repertoire of HPV-speciWc T cells is poised for action in patients with cervical cancer. Cancer Res 70(7):2707-2717. doi:10.1158/ 0008-5472.CAN-09-4299
29. Harcourt GC, Scriba TJ, Semmo N, Bounds S, Taylor E, Klenerman P (2006) IdentiWcation of key peptide-speciWc CD4+ T cell responses to human cytomegalovirus: implications for tracking antiviral populations. Clin Exp Immunol 146(2):203-210. doi:10.1111/j.1365-2249.2006.03193.x
30. Reiser M, Wieland A, Plachter B, Mertens T, Greiner J, Schirmbeck R (2011) The immunodominant CD8 T cell response to the human cytomegalovirus tegument phosphoprotein pp 65(495-503) epitope critically depends on CD4 T cell help in vaccinated HLA-A.*0201 transgenic mice. J Immunol 187(5):2172-2180. doi:10.4049/jimmunol.1002512
31. Speetjens FM, Kuppen PJ, Welters MJ, Essahsah F, Voet van den Brink AM, Lantrua MG, Valentijn AR, Oostendorp J, Fathers LM, Nijman HW, Drijfhout JW, van de Velde CJ, Melief CJ, van der Burg SH (2009) Induction of p53-speciWc immunity by a p53 synthetic long peptide vaccine in patients treated for metastatic colorectal cancer. Clin Cancer Res OV J Am Assoc Cancer Res 15(3):1086-1095. doi:10.1158/1078-0432.CCR-08-2227
32. 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(5):558-566. doi:10.1038/ ni.1601
33. Singh SK, Stephani J, Schaefer M, Kalay H, Garcia-Vallejo JJ, den Haan J, Saeland E, Sparwasser T, van Kooyk Y (2009) Targeting glycan modiWed OVA to murine DC-SIGN transgenic dendritic cells enhances MHC class I and II presentation. Mol Immunol 47(2-3):164-174. doi:10.1016/j.molimm.2009.09.026
34. Bauvois B (2009) Types I and II interferons upregulate the costimulatory CD80 molecule in monocytes via interferon regulatory factor-1. Biochem Pharmacol 78(5):514-522. doi:10.1016/ j.bcp.2009.05.005
35. Linsley PS, Brady W, Urnes M, Grosmaire LS, Damle NK, Ledbetter JA (1991) CTLA-4 is a second receptor for the B cell activation antigen B7. J Exp Med 174(3):561-569
36. Duthie MS, Windish HP, Fox CB, Reed SG (2011) Use of deWned TLR ligands as adjuvants within human vaccines. Immunol Rev 239(1):178-196. doi:10.1111/j.1600-065X.2010.00978.x
37. Pulendran B, Ahmed R (2006) Translating innate immunity into immunological memory: implications for vaccine development. Cell 124(4):849-863. doi:10.1016/j.cell.2006.02.019
38. Gauduin MC (2006) Intracellular cytokine staining for the characterization and quantitation of antigen-speciWc T lymphocyte responses. Methods 38(4):263-273. doi:10.1016/j.ymeth.2005. 12.004
39. Horton H, Thomas EP, Stucky JA, Frank I, Moodie Z, Huang Y, Chiu YL, McElrath MJ, De Rosa SC (2007) Optimization and validation of an 8-color intracellular cytokine staining (ICS) assay to quantify antigen-speciWc T cells induced by vaccination. J Immunol Methods 323(1):39-54. doi:10.1016/j.jim.2007. 03.002
40. van der Burg SH, Kalos M, Gouttefangeas C, Janetzki S, Ottensmeier C, Welters MJ, Romero P, Britten CM, Hoos A (2011) Harmonization of immune biomarker assays for clinical studies. Science Trans Med 3(108):108ps44. doi:10.1126/scitranslmed. 3002785
41. Marrack P, Kappler J, Mitchell T (1999) Type I interferons keep activated T cells alive. J Exp Med 189(3):521-530