Antigen-specific activation and cytokine-facilitated expansion of naive, human CD8+ T cells

Nature Protocols

Volumn 9, Issue 4, 2014, Pages 950-966

  Wölfl, Matthias ^a   Greenberg, Philip D ^b,c  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b Fred Hutchinson Cancer Research Center   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 15; INTERLEUKIN 21; INTERLEUKIN 4; INTERLEUKIN 7; MELAN A; ANTIGEN; CYTOKINE;

ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; CELL ASSAY; CELL EXPANSION; CELL MATURATION; CELL PRIMING; CELL STIMULATION; CELLULAR PARAMETERS; CHEMICAL MODIFICATION; CLINICAL PROTOCOL; CONCENTRATION (PARAMETERS); DENDRITIC CELL; DRUG DEVELOPMENT; EXPERIMENTAL DESIGN; HUMAN; IMMUNOGENICITY; INTERMETHOD COMPARISON; LYMPHOCYTE COUNT; LYMPHOCYTE PROLIFERATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROCEDURES CONCERNING CELLS; RELIABILITY; REPRODUCIBILITY; T LYMPHOCYTE ACTIVATION; VACCINE PRODUCTION; VALIDITY; IMMUNOLOGICAL TECHNIQUE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; PROCEDURES;

ANTIGENS; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; HUMANS; IMMUNOLOGIC TECHNIQUES; LYMPHOCYTE ACTIVATION;

EID: 84897144168     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2014.064     Document Type: Article

References (66)

1. Kaech, S.M. & Ahmed, R. Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat. Immunol. 2, 415-422 (2001).
2. Kaech, S.M., Wherry, E.J. & Ahmed, R. Effector and memory T-cell differentiation: implications for vaccine development. Nat. Rev. Immunol. 2, 251-262 (2002).
3. Arens, R. & Schoenberger, S.P. Plasticity in programming of effector and memory CD8 T-cell formation. Immunol. Rev. 235, 190-205 (2010).
4. Ahmed, R. & Oldstone, M.B. Organ-specific selection of viral variants during chronic infection. J. Exp. Med. 167, 1719-1724 (1988).
5. Dissanayake, D., Gronski, M.A., Lin, A., Elford, A.R. & Ohashi, P.S. Immunological perspective of self versus tumor antigens: insights from the RIP-gp model. Immunol. Rev. 241, 164-179 (2011).
6. Jensen, E.R., Shen, H., Wettstein, F.O., Ahmed, R. & Miller, J.F. Recombinant Listeria monocytogenes as a live vaccine vehicle and a probe for studying cell-mediated immunity. Immunol. Rev. 158, 147-157 (1997).
7. Ohlen, C. et al. CD8+ T cell tolerance to a tumor-associated antigen is maintained at the level of expansion rather than effector function. J. Exp. Med. 195, 1407-1418 (2002).
8. Seok, J. et al. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc. Natl. Acad. Sci. USA 110, 3507-3512 (2013).
9. Davis, M.M. A prescription for human immunology. Immunity 29, 835-838 (2008).
10. Donahue, R.E. & Dunbar, C.E. Update on the use of nonhuman primate models for preclinical testing of gene therapy approaches targeting hematopoietic cells. Hum. Gene Therapy 12, 607-617 (2001).
11. Haigwood, N.L. Predictive value of primate models for AIDS. AIDS Rev. 6, 187-198 (2004).
12. Coulie, P.G. et al. A new gene coding for a differentiation antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas. J. Exp. Med. 180, 35-42 (1994).
13. Kawakami, Y. et al. Cloning of the gene coding for a shared human melanoma antigen recognized by autologous T cells infiltrating into tumor. Proc. Natl. Acad. Sci. USA 91, 3515-3519 (1994).
14. Kawakami, Y. et al. Identification of the immunodominant peptides of the MART-1 human melanoma antigen recognized by the majority of HLA-A2-restricted tumor infiltrating lymphocytes. J Exp. Med. 180, 347-352 (1994).
15. Romero, P. et al. Antigenicity and immunogenicity of Melan-A/MART-1 derived peptides as targets for tumor reactive CTL in human melanoma. Immunol. Rev. 188, 81-96 (2002).
16. Alanio, C., Lemaitre, F., Law, H.K., Hasan, M. & Albert, M.L. Enumeration of human antigen-specific naive CD8+ T cells reveals conserved precursor frequencies. Blood 115, 3718-3725 (2010).
17. Pittet, M.J. et al. High frequencies of naive Melan-A/MART-1-specific CD8+ T cells in a large proportion of human histocompatibility leukocyte antigen (HLA)-A2 individuals. J. Exp. Med. 190, 705-715 (1999).
18. Zippelius, A. et al. Thymic selection generates a large T cell pool recognizing a self-peptide in humans. J. Exp. Med. 195, 485-494 (2002).
19. Dutoit, V. et al. Degeneracy of antigen recognition as the molecular basis for the high frequency of naive A2/Melan-A peptide multimer+ CD8+ T cells in humans. J. Exp. Med. 196, 207-216 (2002).
20. Wolfl, M. et al. Primed tumor-reactive multifunctional CD62L+ human CD8+ T cells for immunotherapy. Cancer Immunol. Immunotherapy 60, 173-186 (2011).
21. Wolfl, M. et al. Hepatitis C virus immune escape via exploitation of a hole in the T cell repertoire. J. Immunol. 181, 6435-6446 (2008).
22. Pufnock, J.S. et al. Priming CD8+ T cells with dendritic cells matured using TLR4 and TLR7/8 ligands together enhances generation of CD8+ T cells retaining CD28. Blood 117, 6542-6551 (2011).
23. Wolfl, M. et al. Activation-induced expression of CD137 permits detection, isolation, and expansion of the full repertoire of CD8+ T cells responding to antigen without requiring knowledge of epitope specificities. Blood 110, 201-210 (2007).
24. Wolfl, M. et al. Src-kinase inhibitors sensitize human cells of myeloid origin to Toll-like-receptor-induced IL12 synthesis. Blood 122, 1203-1213 (2013).
25. Schade, A.E. et al. Dasatinib, a small-molecule protein tyrosine kinase inhibitor, inhibits T-cell activation and proliferation. Blood 111, 1366-1377 (2008).
26. von Bergwelt-Baildon, M.S. et al. Human primary and memory cytotoxic T lymphocyte responses are efficiently induced by means of CD40-activated B cells as antigen-presenting cells: potential for clinical application. Blood 99, 3319-3325 (2002).
27. Suhoski, M.M. et al. Engineering artificial antigen-presenting cells to express a diverse array of co-stimulatory molecules. Mol. Therapy 15, 981-988 (2007).
28. van Stipdonk, M.J., Lemmens, E.E. & Schoenberger, S.P. Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat. Immunol. 2, 423-429 (2001).
29. Oelke, M. & Schneck, J.P. Overview of a HLA-Ig based 'Lego-like system' for T cell monitoring, modulation and expansion. Immunolog. Res. 47, 248-256 (2010).
30. Oelke, M. et al. Ex vivo induction and expansion of antigen-specific cytotoxic T cells by HLA-Ig-coated artificial antigen-presenting cells. Nat. Med. 9, 619-624 (2003).
31. Geginat, J., Lanzavecchia, A. & Sallusto, F. Proliferation and differentiation potential of human CD8+ memory T-cell subsets in response to antigen or homeostatic cytokines. Blood 101, 4260-4266 (2003).
32. Altman, J.D. et al. Phenotypic analysis of antigen-specific T lymphocytes. Science 274, 94-96 (1996).
33. Ma, X. et al. The interleukin 12 p40 gene promoter is primed by interferon-? in monocytic cells. J. Exp. Med. 183, 147-157 (1996).
34. Langenkamp, A., Messi, M., Lanzavecchia, A. & Sallusto, F. Kinetics of dendritic cell activation: impact on priming of TH1, TH2 and nonpolarized T cells. Nat. Immunol. 1, 311-316 (2000).
35. Jonuleit, H. et al. Pro-inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serum-free conditions. European Journal of Immunology 27, 3135-3142 (1997).
36. Kalinski, P., Vieira, P.L., Schuitemaker, J.H., de Jong, E.C. & Kapsenberg, M.L. Prostaglandin E2 is a selective inducer of interleukin-12 p40 (IL-12p40) production and an inhibitor of bioactive IL-12p70 heterodimer. Blood 97, 3466-3469 (2001).
37. Huang, J. et al. Irradiation enhances human T-cell function by upregulating CD70 expression on antigen-presenting cells in vitro. J. Immunotherapy 34, 327-335 (2011).
38. Merrick, A. et al. Immunosuppressive effects of radiation on human dendritic cells: reduced IL-12 production on activation and impairment of naive T-cell priming. Br. J. Cancer 92, 1450-1458 (2005).
39. Geginat, J., Sallusto, F. & Lanzavecchia, A. Cytokine-driven proliferation and differentiation of human naive, central memory, and effector memory CD4+ T cells. J. Exp. Med. 194, 1711-1719 (2001).
40. Li, Y. & Yee, C. IL-21 mediated Foxp3 suppression leads to enhanced generation of antigen-specific CD8+ cytotoxic T lymphocytes. Blood 111, 229-235 (2008).
41. Coulie, P.G. et al. Precursor frequency analysis of human cytolytic T lymphocytes directed against autologous melanoma cells. Int. J. Cancer 50, 289-297 (1992).
42. Li, Y., Bleakley, M. & Yee, C. IL-21 influences the frequency, phenotype, and affinity of the antigen-specific CD8 T cell response. J. Immunol. 175, 2261-2269 (2005).
43. Alves, N.L., Arosa, F.A. & van Lier, R.A. IL-21 sustains CD28 expression on IL-15-activated human naive CD8+ T cells. J. Immunol. 175, 755-762 (2005).
44. Ho, W.Y., Nguyen, H.N., Wolfl, M., Kuball, J. & Greenberg, P.D. In vitro methods for generating CD8+ T-cell clones for immunotherapy from the naive repertoire. J. Immunolog. Methods 310, 40-52 (2006).
45. Surh, C.D., Boyman, O., Purton, J.F. & Sprent, J. Homeostasis of memory T cells. Immunolog. Rev. 211, 154-163 (2006).
46. Kamimura, D. & Bevan, M.J. Naive CD8+ T cells differentiate into protective memory-like cells after IL-2 anti IL-2 complex treatment in vivo. J. Exp. Med. 204, 1803-1812 (2007).
47. Wolfl, M., Langhammer, F., Wiegering, V., Eyrich, M. & Schlegel, P.G. Dasatinib medication causing profound immunosuppression in a patient after haploidentical SCT: functional assays from whole blood as diagnostic clues. Bone Marrow Transplant. 48, 875-877 (2013).
48. Rodeberg, D.A., Nuss, R.A., Elsawa, S.F. & Celis, E. Recognition of six-transmembrane epithelial antigen of the prostate-expressing tumor cells by peptide antigen-induced cytotoxic T lymphocytes. Clin. Cancer Res. 11, 4545-4552 (2005).
49. Quintarelli, C. et al. High-avidity cytotoxic T lymphocytes specific for a new PRAME-derived peptide can target leukemic and leukemic-precursor cells. Blood 117, 3353-3362 (2011).
50. Godet, Y. et al. MELOE-1 is a new antigen overexpressed in melanomas and involved in adoptive T cell transfer efficiency. J. Exp. Med. 205, 2673-2682 (2008).
51. Sharrock, C.E., Kaminski, E. & Man, S. Limiting dilution analysis of human T cells: a useful clinical tool. Immunol. Today 11, 281-286 (1990).
52. Bonnefoix, T., Bonnefoix, P., Callanan, M., Verdiel, P. & Sotto, J.J. Graphical representation of a generalized linear model-based statistical test estimating the fit of the single-hit Poisson model to limiting dilution assays. J. Immunol. 167, 5725-5730 (2001).
53. Bonnefoix, T. & Callanan, M. Accurate hematopoietic stem cell frequency estimates by fitting multicell Poisson models substituting to the single-hit Poisson model in limiting dilution transplantation assays. Blood 116, 2472-2475 (2010).
54. Klebanoff, C.A. et al. Central memory self/tumor-reactive CD8+ T cells confer superior antitumor immunity compared with effector memory T cells. Proc. Natl. Acad. Sci. USA 102, 9571-9576 (2005).
55. Berger, C. et al. Adoptive transfer of effector CD8+ T cells derived from central memory cells establishes persistent T cell memory in primates. J. Clin. Invest. 118, 294-305 (2008).
56. Chapuis, A.G. et al. Transferred WT1-reactive CD8+ T cells can mediate antileukemic activity and persist in post-transplant patients. Sci. Transl. Med. 5, 174ra127 (2013).
57. Oelke, M. et al. Generation and purification of CD8+ melan-A-specific cytotoxic T lymphocytes for adoptive transfer in tumor immunotherapy. Clin. Cancer Res. 6, 1997-2005 (2000).
58. Blanchet, J.S. et al. A new generation of Melan-A/MART-1 peptides that fulfill both increased immunogenicity and high resistance to biodegradation: implication for molecular anti-melanoma immunotherapy. J. Immunol. 167, 5852-5861 (2001).
59. Xu, S. et al. Rapid high efficiency sensitization of CD8+ T cells to tumor antigens by dendritic cells leads to enhanced functional avidity and direct tumor recognition through an IL-12-dependent mechanism. J. Immunol. 171, 2251-2261 (2003).
60. Hirano, N. et al. Efficient presentation of naturally processed HLA class I peptides by artificial antigen-presenting cells for the generation of effective antitumor responses. Clin. Cancer Res. 12, 2967-2975 (2006).
61. Rudolf, D. et al. Potent costimulation of human CD8 T cells by anti-4-1BB and anti-CD28 on synthetic artificial antigen presenting cells. Cancer Immunol. Immunotherapy 57, 175-183 (2008).
62. Dubsky, P. et al. IL-15-induced human DC efficiently prime melanoma-specific naive CD8+ T cells to differentiate into CTL. Eur. J. Immunol. 37, 1678-1690 (2007).
63. Dauer, M. et al. FastDC derived from human monocytes within 48 h effectively prime tumor antigen-specific cytotoxic T cells. J. Immunolog. Methods 302, 145-155 (2005).
64. Chauvin, J.M. et al. HLA anchor optimization of the melan-A-HLA-A2 epitope within a long peptide is required for efficient cross-priming of human tumor-reactive T cells. J. Immunol. 188, 2102-2110 (2012).
65. Hervas-Stubbs, S. et al. CD8 T cell priming in the presence of IFN-α renders CTLs with improved responsiveness to homeostatic cytokines and recall antigens: important traits for adoptive T cell therapy. J. Immunol. 189, 3299-3310 (2012).
66. Lissina, A. et al. Protein kinase inhibitors substantially improve the physical detection of T-cells with peptide-MHC tetramers. J. Immunolog. Methods 340, 11-24 (2009).