CD137 stimulation and p38 MAPK inhibition improve reactivity in an in vitro model of glioblastoma immunotherapy

Cancer Immunology, Immunotherapy

Volumn 62, Issue 12, 2013, Pages 1797-1809

  Kühnöl, Caspar ^a   Herbarth, Monique ^a   Föll, Jürgen ^b   Staege, Martin S ^a   Kramm, Christof ^a,c  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^c UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

Author keywords

CD137; CD25; Dendritic cells; Glioblastoma; P38MAPK inhibitors

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CD137 ANTIGEN; CD137 LIGAND; CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; DACLIZUMAB; DENDRITIC CELL VACCINE; GAMMA INTERFERON; LACTATE DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE P38; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CANCER IMMUNIZATION; CELL MATURATION; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOLYSIS; DENDRITIC CELL; DRUG CYTOTOXICITY; ENZYME INHIBITION; GLIOBLASTOMA; GLIOMA CELL; HUMAN; HUMAN CELL; IMMUNOMODULATION; IMMUNOREACTIVITY; IMMUNOSTIMULATION; IN VITRO STUDY; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; TUMOR CELL DESTRUCTION; TUMOR IMMUNITY; TUMOR LYSATE PULSED DENDRITIC CELL;

ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIGENS, CD137; BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL PROLIFERATION; CELLS, CULTURED; CYTOTOXICITY, IMMUNOLOGIC; DENDRITIC CELLS; ENZYME INHIBITORS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GLIOBLASTOMA; HUMANS; IMIDAZOLES; IMMUNOGLOBULIN G; IMMUNOSUPPRESSIVE AGENTS; IMMUNOTHERAPY; INTERFERON-GAMMA; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LEUKOCYTES, MONONUCLEAR; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PYRIDINES;

EID: 84890355541     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-013-1484-9     Document Type: Article

References (87)

1. De Vleeschouwer S, Rapp M, Sorg RV, Steiger HJ, Stummer W, van Gool S et al (2006) Dendritic cell vaccination in patients with malignant gliomas: current status and future directions. Neurosurgery 59:988-1000
2. De Vleeschouwer S, Fieuws S, Rutkowski S, Van Calenbergh F, Van Loon J, Goffin J et al (2008) Postoperative adjuvant dendritic cell-based immunotherapy in patients with relapsed glioblastoma multiforme. Clin Cancer Res 14:3098-3104
3. Locksley RM, Killeen N, Lenardo MJ (2001) The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104:487-501
4. Kwon BS, Weissman SM (1989) cDNA sequences of two inducible T-cell genes. Proc Natl Acad Sci USA 86:1963-1967
5. Vinay DS, Kwon BS (1999) Relative abilities of 4-1BB (CD137) and CD28 to co-stimulate the response of cytokine deflected Th1 and Th2 cells. Immunobiology 200:246-263
6. Wilcox RA, Chapoval AI, Gorski KS, Otsuji M, Shin T, Flies DB et al (2002) Cutting edge: expression of functional CD137 receptor by dendritic cells. J Immunol 168:4262-4267
7. Futagawa T, Akiba H, Kodama T, Takeda K, Hosoda Y, Yagita H et al (2002) Expression and function of 4-1BB and 4-1BB ligand on murine dendritic cells. Int Immunol 14:275-286
8. Nishimoto H, Lee SW, Hong H, Potter KG, Maeda-Yamamoto M, Kinoshita T et al (2005) Costimulation of mast cells by 4-1BB, a member of the tumour necrosis factor receptor superfamily, with the high-affinity IgE receptor. Blood 106:4241-4248
9. Alderson MR, Smith CA, Tough TW, Davis-Smith T, Armitage RJ, Falk B et al (1994) Molecular and biological characterization of human 4-1BB and its ligand. Eur J Immunol 24:2219-2227
10. Goodwin RG, Din WS, Davis-Smith T, Anderson DM, Gimpel SD, Sato TA et al (1993) Molecular cloning of a ligand for the inducible T cell gene 4-1BB: a member of an emerging family of cytokines with homology to tumour necrosis factor. Eur J Immunol 10:2631-2641
11. DeBenedette MA, Shahinian A, Mak TW, Watts TH (1997) Costimulation of CD28- T lymphocytes by 4-1BB ligand. J Immunol 158:551-559
12. Pollok KE, Kim YJ, Hurtado J, Zhou Z, Kim KK, Kwon BS (1994) 4-1BB T cell antigen binds to mature B cells and macrophages, and costimulates anti-mu-primed splenic B cells. Eur J Immunol 24:367-374
13. Cannons JL, Choi Y, Watts TH (2000) Role of TNF receptor-associated factor 2 and p38 mitogen-activated protein kinase activation during 4-1BB-dependent immune response. J Immunol 165:6193-6204
14. Saoulli K, Lee SY, Cannons JL, Yeh WC, Santana A, Goldstein MD et al (1998) CD28-independent, TRAF2-dependent costimulation of resting T cells by 4-1BB ligand. J Exp Med 187:1849-1862
15. Cannons JL, Hoeflich KP, Woodgett JR, Watts TH (1999) Role of the stress kinase pathway in signaling via the T cell costimulatory receptor 4-1BB. J Immunol 163:2990-2998
16. Cannons JL, Lau P, Ghumman B, DeBenedette MA, Yagita H, Okumura K et al (2001) 4-1BB ligand induces cell division, sustains survival, and enhances effector function of CD4 and CD8 T cells with similar efficacy. J Immunol 167:1313-1324
17. Cooper D, Bansal-Pakala P, Croft M (2002) 4-1BB (CD137) controls the clonal expansion and survival of CD8 T cells in vivo but does not contribute to the development of cytotoxicity. Eur J Immunol 32:521-529
18. Shuford WW, Klussman K, Tritchler DD, Loo DT, Chalupny J, Siadak AW et al (1997) 4-1BB costimulatory signals preferentially induce CD8+ T cell proliferation and lead to the amplification in vivo of cytotoxic T cell responses. J Exp Med 186:47-55
19. Hurtado JC, Kim YJ, Kwon BS (1997) Signals through 4-1BB are costimulatory to previously activated splenic T cells and inhibit activation-induced cell death. J Immunol 158:2600-2609
20. Han J, Lee JD, Jiang Y, Li Z, Feng L, Ulevitch RJ (1994) A MAP kinase targeted by endotoxin in mammalian cells. Science 265:808-811
21. Lee JC, Laydon JT, McDonnell PC, Gallagher TF, Kumar S, Green D et al (1994) A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature 372:739-746
22. Nebreda AR, Porras A (2000) p38 MAP kinases: beyond the stress response. Trends Biochem Sci 25:257-260
23. Dodeller F, Schulze-Koops H (2006) The p38 mitogen-activated protein kinase signalling cascade in CD4 T cells. Arthritis Res Ther 8:205
24. Rincón M, Enslen H, Raingeaud J, Recht M, Zapton T, Su MS et al (1998) Interferon-gamma expression by Th1 effector T cells mediated by the p38 MAP kinase signaling pathway. EMBO J 17:2817-2829
25. Merritt C, Enslen H, Diehl N, Conze D, Davis RJ, Rincón M (2000) Activation of p38 mitogen-activated protein kinase in vivo selectively induces apoptosis of CD8(+) but not CD4(+) T cells. Mol Cell Biol 20:936-946
26. Nakagawa S, Ohtani T, Mizuashi M, Mollah ZU, Ito Y, Tagami H et al (2004) p38 mitogen-activated protein kinase mediates dual role of ultraviolet B radiation in induction of maturation and apoptosis of monocyte-derived dendritic cells. J Invest Dermatol 123:361-370
27. Puig-Kröger A, Relloso M, Fernández-Capetillo O, Zubiaga A, Silva A, Bernabéu C et al (2001) Extracellular signal-regulated protein kinase signaling pathway negatively regulates the phenotypic and functional maturation of monocyte-derived human dendritic cells. Blood 98:2175-2182
28. Arrighi JF, Rebsamen M, Rousset F, Kindler B, Hauser C (2001) A critical role for p38 mitogen-activated protein kinase in the maturation of human blood-derived dendritic cells induced by lipopolysaccharide, TNF-alpha, and contact sensitizers. J Immunol 166:3837-3845
29. Xie J, Qian J, Wang S, Freeman ME III, Epstein J, Yi Q (2003) Novel and detrimental effects of lipopolysaccharide on in vitro generation of immature dendritic cells: involvement of mitogen-activated protein kinase p38. J Immunol 171:4792-4800
30. Yao Y, Xu Q, Kwon MJ, Matta R, Liu Y, Hong SC et al (2006) ERK and p38 MAPK signalling pathways negatively regulate CIITA gene expression in dendritic cells and macrophages. J Immunol 177:70-76
31. Jarnicki AG, Conroy H, Brereton C, Donnelly G, Toomey D, Walsh K et al (2008) Attenuating regulatory T cell induction by TLR agonists through inhibition of p38 MAPK signaling in dendritic cells enhances their efficacy as vaccine adjuvants and cancer immunotherapeutics. J Immunol 180:3797-3806
32. Wang S, Yang J, Qian J, Wezeman M, Kwak LW, Yi Q (2006) Tumor evasion of the immune system: inhibiting p38 MAPK signaling restores the function of dendritic cells in multiple myeloma. Blood 107:2432-2439
33. Franks HA, Wang Q, Lax SJ, Collins MK, Escors D, Patel PM et al (2013) Novel function for the p38-MK2 signalling pathway in circulating CD1c+ (BDCA-1+) myeloid dendritic cells from healthy donors and advanced cancer patients; inhibition of p38 enhances IL-12 whilst suppressing IL-10. Int J Cancer. doi: 10.1002/ijc.28398
34. Boyman O, Surh CD, Sprent J (2006) Potential use of IL-2/anti-IL-2 antibody immune complexes for the treatment of cancer and autoimmune disease. Expert Opin Biol Ther 6:1323-1331
35. Malek TR (2008) The biology of interleukin-2. Annu Rev Immunol 26:453-479
36. Létourneau S, Krieg C, Pantaleo G, Boyman O (2009) IL-2- and CD25-dependent immunoregulatory mechanisms in the homeostasis of T-cell subsets. J Allergy Clin Immunol 123:758-762
37. Fontenot JD, Rudensky AY (2005) A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat Immunol 6:331-337
38. Maes W, Rosas GG, Verbinnen B, Boon L, De Vleeschouwer S, Ceuppens JL et al (2009) DC vaccination with anti-CD25 treatment leads to long-term immunity against experimental glioma. Neuro-oncology 11:529-542
39. Beckman G, Beckman L, Pontén J, Westermark B (1971) G-6-PD and PGM phenotypes of 16 continuous human tumor cell lines. Evidence against cross-contamination and contamination by HeLa cells. Hum Hered 21:238-241
40. Stein GH (1979) T98G: an anchorage-independent human tumor cell line that exhibits stationary phase G1 arrest in vitro. J Cell Physiol 99:43-54
41. Chen TR, Hay RJ, Macy ML (1983) Intercellular karyotypic similarity in near-diploid cell lines of human tumor origins. Cancer Genet Cytogenet 10:351-362
42. Foell JL, Volkmer I, Giersberg C, Kornhuber M, Horneff G, Staege MS (2008) Loss of detectability of Charcot-Leyden crystal protein transcripts in blood cells after treatment with dimethyl sulfoxide. J Immunol Methods 339:99-103
43. Hoennscheidt C, Max D, Richter N, Staege MS (2009) Expression of CD4 on Epstein-Barr virus-immortalized B cells. Scand J Immunol 70:216-225
44. Staege MS, Schneider J, Eulitz M, Scholz S, Bornkamm GW, Wölfel T et al (2000) Consequences of antigen self-presentation by tumor-specific cytotoxic T cells. Immunobiology 201:332-346
45. De Vleeschouwer S, Arredouani M, Adé M, Cadot P, Vermassen E, Ceuppens JL et al (2005) Uptake and presentation of malignant glioma tumour cell lysates by monocyte derived dendritic cells. Cancer Immunol Immunother 54:372-382
46. Yoshida S, Morii K, Watanabe M, Saito T, Yamamoto K, Tanaka R (2001) The generation of anti-tumoral cells using dendritic cells from the peripheral blood of patients with malignant brain tumors. Cancer Immunol Immunother 50:321-327
47. Okada H, Tahara H, Shurin MR, Attanucci J, Giezeman-Smits KM, Fellows WK et al (1998) Bone marrow-derived dendritic cells pulsed with a tumor-specific peptide elicit effective anti-tumor immunity against intracranial neoplasms. Int J Cancer 78:196-201
48. Siesjo P, Visse E, Sjogren HO (1996) Cure of established, intracerebral rat gliomas induced by therapeutic immunizations with tumor cells and purified APC or adjuvant IFN-gamma treatment. J Immunother Emphas Tumor Immunol 19:334-345
49. De Vleeschouwer S, Van Calenbergh F, Demaerel P, Flamen P, Rutkowski S, Kaempgen E et al (2004) Transient local response and persistent tumor control of recurrent malignant glioma treated with combination therapy including dendritic cell therapy. J Neurosurg 100:492-497
50. Rutkowski S, De Vleeschouwer S, Kaempgen E, Wolff JE, Kühl J, Demaerel P et al (2004) Surgery and adjuvant dendritic cell-based tumour vaccination for patients with relapsed malignant glioma, a feasibility study. Br J Cancer 91:1656-1662
51. Kikuchi T, Akasaki Y, Irie M, Homma S, Abe T, Ohno T (2001) Results of a phase I clinical trial of vaccination of glioma patients with fusions of dendritic and glioma cells. Cancer Immunol Immunother 50:337-344
52. Kikuchi T, Akasaki Y, Abe T, Fukuda T, Saotome H, Ryan JL et al (2004) Vaccination of glioma patients with fusions of dendritic and glioma cells and recombinant human interleukin 12. J Immunother 27:452-459
53. Liau LM, Black KL, Martin NA, Sykes SN, Bronstein JM, Jouben-Steele L et al (2000) Treatment of a patient by vaccination with autologous dendritic cells pulsed with allogeneic major histocompatibility complex class I-matched tumor peptides. Case report. Neurosurg Focus 9:e8
54. Liau LM, Prins RM, Kiertscher SM, Odesa SK, Kremen TJ, Giovannone AJ et al (2005) Dendritic cell vaccination in glioblastoma patients induces systemic and intracranial T-cell responses modulated by the local central nervous system tumor microenvironment. Clin Cancer Res 11:5515-5525
55. Wheeler CJ, Black KL, Liu G, Ying H, Yu JS, Zhang W et al (2003) Thymic CD8+ T cell production strongly influences tumor antigen recognition and age dependent glioma mortality. J Immunol 171:4927-4933
56. Yamanaka R, Abe T, Yajima N, Tsuchiya N, Homma J, Kobayashi T et al (2003) Vaccination of recurrent glioma patients with tumour lysate-pulsed dendritic cells elicits immune responses: results of a clinical phase I/II trial. Br J Cancer 89:1172-1179
57. Yamanaka R, Homma J, Yajima N, Tsuchiya N, Sano M, Kobayashi T et al (2005) Clinical evaluation of dendritic cell vaccination for patients with recurrent glioma: results of a clinical phase I/II trial. Clin Cancer Res 11:4160-4167
58. Yu JS, Wheeler CJ, Zeltzer PM, Ying H, Finger DN, Lee PK et al (2001) Vaccination of malignant glioma patients with peptide-pulsed dendritic cells elicits systemic cytotoxicity and intracranial T-cell infiltration. Cancer Res 61:842-847
59. Yu JS, Liu G, Ying H, Yong WH, Black KL, Wheeler CJ (2004) Vaccination with tumor lysate-pulsed dendritic cells elicits antigen-specific, cytotoxic T-cells in patients with malignant glioma. Cancer Res 64:4973-4979
60. Ardon H, De Vleeschouwer S, Van Calenbergh F, Claes L, Kramm CM, Rutkowski S et al (2010) Adjuvant dendritic cell-based tumour vaccination for children with malignant brain tumours. Pediatr Blood Cancer 54:519-525
61. Mellman I, Steinman R (2001) Dendritic cells: specialized and regulated antigen processing machines. Cell 106:255-258
62. Rock KL, Goldberg AL (1999) Degradation of cell proteins and the generation of MHC class I-presented peptides. Annu Rev Immunol 17:739-779
63. Natsume A, Wakabayashi T, Tsujimura K, Shimato S, Ito M, Kuzushima K et al (2008) The DNA demethylating agent 5-aza-2′-deoxycytidine activates NY-ESO-1 antigenicity in orthotopic human glioma. Int J Cancer 122:2542-2553
64. Pollok KE, Kim YJ, Zhou Z, Hurtado J, Kim KK, Pickard RT et al (1993) Inducible T cell antigen 4-1BB. Analysis of expression and function. J Immunol 150:771-781
65. Hurtado JC, Kim SH, Pollok KE, Lee ZH, Kwon BS (1995) Potential role of 4-1BB in T cell activation. Comparison with the costimulatory molecule CD28. J Immunol 155:3360-3367
66. Melero I, Johnston JV, Shufford WW, Mittler RS, Chen L (1998) NK1.1 cells express 4-1BB (CDw137) costimulatory molecule and are required for tumour immunity elicited by anti-4-1BB monoclonal antibodies. Cell Immunol 190:167-172
67. Gramaglia I, Cooper D, Miner KT, Kwon BS, Croft M (2000) Co-stimulation of antigen-specific CD4 T cells by 4-1BB ligand. Eur J Immunol 30:392-402
68. Schwarz H, Blanco FJ, von Kempis J, Valbracht J, Lotz M (1996) ILA, a member of the human nerve growth factor/tumour necrosis factor receptor family, regulates T-lymphocyte proliferation and survival. Blood 87:2839-2845
69. Takahashi C, Mittler RS, Vella AT (1999) Cutting edge: 4-1BB is a bona fide CD8 T cell survival signal. J Immunol 162:5037-5040
70. Laderach D, Movassagh M, Johnson A, Mittler RS, Galy A (2002) 4-1BB co-stimulation enhances human CD8(1) T cell priming by augmenting the proliferation and survival of effector CD8(1) T cells. Int Immunol 14:1155-1167
71. Chen L, McGowan P, Ashe S, Johnston J, Li Y, Hellström I et al (1994) Tumour immunogenicity determines the effect of B7 costimulation on T cell-mediated tumour immunity. J Exp Med 179:523-532
72. Strome SE, Martin B, Flies D, Tamada K, Chapoval AI, Sargent DJ et al (2000) Enhanced therapeutic potential of adoptive immunotherapy by in vitro CD28/4-1BB costimulation of tumour-reactive T cells against a poorly immunogenic, major histocompatibility complex class I-negative A9P melanoma. J Immunother 23:430-437
73. Lenschow DJ, Walunas TL, Bluestone JA (1996) CD28/B7 system of T cell costimulation. Annu Rev Immunol 14:233-258
74. Ito F, Li Q, Shreiner AB, Okuyama R, Jure-Kunkel MN, Teitz-Tennenbaum S et al (2004) Anti-CD137 monoclonal antibody administration augments the antitumour efficacy of dendritic cell-based vaccines. Cancer Res 64:8411-8419
75. Xu DP, Sauter BV, Huang TG, Meseck M, Woo SL, Chen SH (2005) The systemic administration of Ig-4-1BB ligand in combination with IL-12 gene transfer eradicates hepatic colon carcinoma. Gene Ther 12:1526-1533
76. Zhang L, Wang Q, Wang X, Ding P, Song J, Ma C et al (2004) Anti-CD137 monoclonal antibody promotes the direct anti-tumour effect mediated by peripheral blood-derived human dendritic cells in vitro. Cell Mol Immunol 1:71-76
77. Adler HS, Kubsch S, Graulich E, Ludwig S, Knop J, Steinbrink K (2007) Activation of MAP kinase p38 is critical for the cell-cycle-controlled suppressor function of regulatory T cells. Blood 109:4351-4359
78. Dodeller F, Skapenko A, Kalden JR, Lipsky PE, Schulze-Koops H (2005) The p38 mitogen-activated protein kinase regulates effector functions of primary human CD4 T cells. Eur J Immunol 35:3631-3642
79. Lu HT, Yang DD, Wysk M, Gatti E, Mellman I, Davis RJ et al (1999) Defective IL-12 production in mitogen-activated protein (MAP) kinase kinase 3 (Mkk3)-deficient mice. EMBO J 18:1845-1857
80. Yong HY, Koh MS, Moon A (2009) The p38 MAPK inhibitors for the treatment of inflammatory diseases and cancer. Expert Opin Investig Drugs 18:1893-1905
81. Ascierto PA, Simeone E, Sznol M, Fu YX, Melero I (2010) Clinical experiences with anti-CD137 and anti-PD1 therapeutic antibodies. Semin Oncol 37:508-516
82. Vinay DS, Kwon BS (2012) Immunotherapy of cancer with 4-1BB. Mol Cancer Ther 11:1062-1070
83. Moore AC, Gallimore A, Draper SJ, Watkins KR, Gilbert SC, Hill AV (2005) Anti-CD25 antibody enhancement of vaccine-induced immunogenicity: increased durable cellular immunity with reduced immunodominance. J Immunol 175:7264-7273
84. Shah AH, Bregy A, Heros DO, Komotar RJ, Goldberg J (2013) Dendritic cell vaccine for recurrent high grade gliomas in pediatric and adult subjects: clinical trial protocol. Neurosurgery. doi: 10.1227/NEU.0000000000000107
85. Krause P, Singer E, Darley PI, Klebensberger J, Groettrup M, Legler DF (2007) Prostaglandin E2 is a key factor for monocyte-derived dendritic cell maturation: enhanced T cell stimulatory capacity despite IDO. J Leukoc Biol 82:1106-1114
86. Nava S, Dossena M, Pogliani S, Pellegatta S, Antozzi C, Baggi F et al (2012) An optimized method for manufacturing a clinical scale dendritic cell-based vaccine for the treatment of glioblastoma. PLoS One 7:e52301
87. Shimabukuro-Vornhagen A, Liebig TM, Koslowsky T, Theurich S, von Bergwelt-Baildon MS (2013) The ratio between dendritic cells and T cells determines whether prostaglandin E2 has a stimulatory or inhibitory effect. Cell Immunol 281:62-67