Antitumor efficacy of radiation plus immunotherapy depends upon dendritic cell activation of effector cd8 T cells

Cancer Immunology Research

Volumn 4, Issue 7, 2016, Pages 621-630

  Dovedi, Simon J ^a   Lipowska Bhalla, Grazyna ^a   Beers, Stephen A ^b   Cheadle, Eleanor J ^a   Mu, Lijun ^c   Glennie, Martin J ^b   Illidge, Timothy M ^a   Honeychurch, Jamie ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^c DALIAN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 LIGAND MONOCLONAL ANTIBODY; RESIQUIMOD; TOLL LIKE RECEPTOR 7; CD40 ANTIGEN; CYTOKINE; MONOCLONAL ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B CELL LYMPHOMA; B LYMPHOCYTE; CANCER IMMUNOTHERAPY; CANCER RADIOTHERAPY; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CROSS PRESENTATION; DENDRITIC CELL; DRUG EFFICACY; EFFECTOR CELL; EXTERNAL BEAM RADIOTHERAPY; IMMUNOPROPHYLAXIS; IONIZING RADIATION; LYMPH NODE METASTASIS; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PHAGOCYTOSIS; RADIATION RESPONSE; T CELL LYMPHOMA; THERAPY EFFECT; TUMOR IMMUNITY; WHOLE BODY RADIATION; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; DRUG EFFECTS; IMMUNOLOGY; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; MACROPHAGE; METABOLISM; MULTIMODALITY CANCER THERAPY; NEOPLASM; PATHOLOGY; RADIOTHERAPY;

ANIMALS; ANTIBODIES, MONOCLONAL; B-LYMPHOCYTES; CD40 ANTIGENS; CD8-POSITIVE T-LYMPHOCYTES; COMBINED MODALITY THERAPY; CYTOKINES; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; MACROPHAGES; MICE; NEOPLASMS; PHAGOCYTOSIS; RADIOTHERAPY;

EID: 84979787901     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-15-0253     Document Type: Article

References (50)

1. Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012;366:2455-65.
2. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survivalwith ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363:711-23.
3. Dovedi SJ, Melis MH, Wilkinson RW, Adlard AL, Stratford IJ, Honeychurch J, et al. Systemic delivery of a TLR7 agonist in combination with radiation primes durable antitumor immune responses in mouse models of lymphoma. Blood 2013;121:251-9.
4. French RR, Chan HT, Tutt AL, Glennie MJ. CD40 antibody evokes a cytotoxic T-cell response that eradicates lymphoma and bypasses T-cell help. Nat Med 1999;5:548-53.
5. Koga-Yamakawa E, Dovedi SJ, Murata M, Matsui H, Leishman AJ, Bell J, et al. Intratracheal and oral administration of SM-276001: A selective TLR7 agonist, leads to antitumor efficacy in primary and metastatic models of cancer. Int J Cancer 2013;132:580-90.
6. Vonderheide RH, Glennie MJ. Agonistic CD40 antibodies and cancer therapy. Clin Cancer Res 2013;19:1035-43.
7. Honeychurch J, Glennie MJ, Johnson PW, Illidge TM. Anti-CD40 monoclonal antibody therapy in combination with irradiation results in a CD8 T-cell-dependent immunity to B-cell lymphoma. Blood 2003;102:1449-57.
8. Adlard AL, Dovedi SJ, Telfer BA, Koga-Yamakawa E, Pollard C, Honeychurch J, et al. A novel systemically administered Toll-like receptor 7 agonist potentiates the effect of ionizing radiation in murine solid tumor models. Int J Cancer 2014;135:820-9.
9. Honeychurch J, Glennie MJ, Illidge TM. Cyclophosphamide inhibition of anti-CD40 monoclonal antibody-based therapy of B cell lymphoma is dependent on CD11b cells. Cancer Res 2005;65: 7493-501.
10. Kroemer G, Galluzzi L, Kepp O, Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol 2013;31:51-72.
11. Reits EA, Hodge JW, Herberts CA, Groothuis TA, Chakraborty M, Wansley EK, et al. Radiationmodulates the peptide repertoire, enhancesMHCclass I expression, and induces successful antitumor immunotherapy. J Exp Med 2006;203:1259-71.
12. Sistigu A, Yamazaki T, Vacchelli E, Chaba K, Enot DP, Adam J, et al. Cancer cell- Autonomous contribution of type I interferon signaling to the efficacy of chemotherapy. Nat Med 2014;20:1301-9.
13. Surace L, Lysenko V, Fontana AO, Cecconi V, Janssen H, Bicvic A, et al. Complement is a central mediator of radiotherapy-induced tumor-specific immunity and clinical response. Immunity 2015;42:767-77.
14. Heath WR, Carbone FR. Cross-presentation, dendritic cells, tolerance and immunity. Annu Rev Immunol 2001;19:47-64.
15. den Haan JM, Lehar SM, Bevan MJ. CD8() but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J Exp Med 2000;192:1685-96.
16. Pozzi LA, Maciaszek JW, Rock KL. Both dendritic cells and macrophages can stimulate naive CD8 T cells in vivo to proliferate, develop effector function, and differentiate into memory cells. J Immunol 2005;175: 2071-81.
17. Norian LA, Rodriguez PC, O'Mara LA, Zabaleta J, Ochoa AC, Cella M, et al. Tumor-infiltrating regulatory dendritic cells inhibit CD8 T cell function via L- Arginine metabolism. Cancer Res 2009;69:3086-94.
18. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: Tumor- Associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 2002;23:549-55.
19. Schultze JL, Cardoso AA, Freeman GJ, Seamon MJ, Daley J, Pinkus GS, et al. Follicular lymphomas can be induced to present alloantigen efficiently: A conceptual model to improve their tumor immunogenicity. Proc Natl Acad Sci U S A 1995;92:8200-4.
20. Van Rooijen N, Sanders A. Liposome mediated depletion of macrophages: mechanismof action, preparation of liposomes and applications. J Immunol Methods 1994;174:83-93.
21. Schulz O, Reise Sousa C. Cross-presentation of cell- Associated antigens by CD8alpha dendritic cells is attributable to their ability to internalize dead cells. Immunology 2002;107:183-9.
22. Jung S, Unutmaz D, Wong P, Sano G, De los Santos K, Sparwasser T, et al. In vivo depletion of CD11c() dendritic cells abrogates priming of CD8() T cells by exogenous cell- Associated antigens. Immunity 2002;17:211-20.
23. Miyake Y, Asano K, Kaise H, Uemura M, Nakayama M, Tanaka M. Critical role of macrophages in the marginal zone in the suppression of immune responses to apoptotic cell- Associated antigens. J Clin Invest 2007; 117:2268-78.
24. Lum HD, Buhtoiarov IN, Schmidt BE, Berke G, Paulnock DM, Sondel PM, et al. Tumoristatic effects of anti-CD40 mAb- Activated macrophages involve nitric oxide and tumour necrosis factor- Alpha. Immunology 2006;118:261-70.
25. Makela SM, Strengell M, Pietila TE, Osterlund P, Julkunen I. Multiple signaling pathways contribute to synergistic TLR ligand-dependent cytokine gene expression in human monocyte-derived macrophages and dendritic cells. J Leukoc Biol 2009;85:664-72.
26. Delamarre L, Pack M, Chang H, Mellman I, Trombetta ES. Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 2005;307:1630-4.
27. Huynh ML, Fadok VA, Henson PM. Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-beta1 secretion and the resolution of inflammation. J Clin Invest 2002;109:41-50.
28. Heit A, Huster KM, Schmitz F, Schiemann M, Busch DH, Wagner H. CpGDNA aided cross-priming by cross-presenting B cells. J Immunol 2004;172:1501-7.
29. Lapointe R, Bellemare-Pelletier A, Housseau F, Thibodeau J, Hwu P. CD40-stimulated B lymphocytes pulsed with tumor antigens are effective antigen-presenting cells that can generate specific T cells. Cancer Res 2003;63:2836-43.
30. Wennhold K, Shimabukuro-Vornhagen A, Theurich S, von Bergwelt- Baildon M. CD40- Activated B cells as antigen-presenting cells: The final sprint toward clinical application. Expert Rev Vaccines 2013;12: 631-7.
31. Barr TA, Brown S, Ryan G, Zhao J, Gray D. TLR-mediated stimulation of APC: distinct cytokine responses of B cells and dendritic cells. Eur J Immunol 2007;37:3040-53.
32. Hanten JA, Vasilakos JP, Riter CL, Neys L, Lipson KE, Alkan SS, et al. Comparison of human B cell activation by TLR7 and TLR9 agonists. BMC Immunol 2008;9:39.
33. Li F, Ravetch JV. Inhibitory Fcgamma receptor engagement drives adjuvant and anti- Tumor activities of agonistic CD40 antibodies. Science 2011;333: 1030-4.
34. White AL, Chan HT, Roghanian A, French RR, Mockridge CI, Tutt AL, et al. Interaction with FcgammaRIIB is critical for the agonistic activity of anti- CD40 monoclonal antibody. J Immunol 2011;187:1754-63.
35. White AL, Dou L, Chan HT, Field VL, Mockridge CI, Moss K, et al. Fcgamma receptor dependency of agonistic CD40 antibody in lymphoma therapy can be overcome through antibody multimerization. J Immunol 2014;193: 1828-35.
36. Richman LP, Vonderheide RH. Role of crosslinking for agonistic CD40 monoclonal antibodies asimmune therapy of cancer. Cancer Immunol Res 2014;2:19-26.
37. Manda K, Glasow A, Paape D, Hildebrandt G. Effects of ionizing radiation on the immune system with special emphasis on the interaction of dendritic and T cells. Front Oncol 2012;2:102.
38. Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A, et al. Tolllike receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007;13:1050-9.
39. Honeychurch J, Melis MH, Dovedi SJ, Mu L, Illidge TM. Immunogenic potential of irradiated lymphoma cells is enhanced by adjuvant immunotherapy and modulation of local macrophage populations. Leuk Lymphoma 2013;54:2008-15.
40. Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, Perfettini JL, et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 2007;13:54-61.
41. Ma Y, Adjemian S, Mattarollo SR, Yamazaki T, Aymeric L, Yang H, et al. Anticancer chemotherapy-induced intratumoral recruitment and differentiation of antigen-presenting cells. Immunity 2013;38:729-41.
42. Schoenberger SP, Toes RE, van der Voort EI, Offringa R, Melief CJ. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 1998;393:480-3.
43. Bennett SR, Carbone FR, Karamalis F, Flavell RA, Miller JF, Heath WR. Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature 1998;393:478-80.
44. Ridge JP, Di Rosa F, Matzinger P. A conditioned dendritic cell can be a temporal bridge between a CD4 T-helper and a T-killer cell. Nature 1998;393:474-8.
45. Gladue RP, Paradis T, Cole SH, Donovan C, Nelson R, Alpert R, et al. The CD40 agonist antibody CP-870, 893 enhances dendritic cell and B-cell activity and promotes anti- Tumor efficacy in SCID-hu mice. Cancer Immunol Immunother 2011;60:1009-17.
46. Boonstra A, Asselin-Paturel C, Gilliet M, Crain C, Trinchieri G, Liu YJ, et al. Flexibility of mouse classical and plasmacytoid-derived dendritic cells in directing T helper type 1 and 2 cell development: dependency on antigen dose and differential toll-like receptor ligation. J ExpMed 2003;197:101-9.
47. Qi H, Denning TL, Soong L. Differential induction of interleukin-10 and interleukin-12 in dendritic cells by microbial toll-like receptor activators and skewing of T-cell cytokine profiles. Infect Immun 2003;71:3337-42.
48. Burnette BC, Liang H, Lee Y, Chlewicki L, Khodarev NN, Weichselbaum RR, et al. The efficacy of radiotherapy relies upon induction of type I interferondependent innate and adaptive immunity. Cancer Res 2011;71:2488-96.
49. Galluzzi L, Vacchelli E, Eggermont A, Fridman WH, Galon J, Sautes-Fridman C, et al. Trial Watch: Experimental Toll-like receptor agonists for cancer therapy. Oncoimmunology 2012;1:699-716.
50. Honeychurch J, Cheadle EJ, Dovedi SJ, Illidge TM. Immuno-regulatory antibodies for the treatment of cancer. Expert Opin Biol Ther 2015; 15:787-801.