Immunogenic potential of irradiated lymphoma cells is enhanced by adjuvant immunotherapy and modulation of local macrophage populations

References

• Reits EA, Hodge JW, Herberts CA, et al. Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful antitumor immunotherapy. J Exp Med 2006;203: 1259–1271.
   PubMed Web of Science ®Google Scholar
• Shi Y, Evans JE, Rock KL. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 2003;425:516–521.
   PubMed Web of Science ®Google Scholar
• Gasser S, Orsulic S, Brown EJ, et al. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 2005;436:1186–1190.
   PubMed Web of Science ®Google Scholar
• Casares N, Pequignot MO, Tesniere A, et al. Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J Exp Med 2005;202:1691–1701.
   PubMed Web of Science ®Google Scholar
• Obeid M, Panaretakis T, Joza N, et al. Calreticulin exposure is required for the immunogenicity of gamma-irradiation and UVC light-induced apoptosis. Cell Death Differ 2007;14:1848–1850.
   PubMed Web of Science ®Google Scholar
• Obeid M, Tesniere A, Ghiringhelli F, et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 2007;13: 54–61.
   PubMed Web of Science ®Google Scholar
• Apetoh L, Ghiringhelli F, Tesniere A, et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007;13:1050–1059.
   PubMed Web of Science ®Google Scholar
• Ghiringhelli F, Apetoh L, Tesniere A, et al. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat Med 2009;15:1170–1178.
   PubMed Web of Science ®Google Scholar
• Lugade AA, Moran JP, Gerber SA, et al. Local radiation therapy of B16 melanoma tumors increases the generation of tumor antigen-specific effector cells that traffic to the tumor. J Immunol 2005;174: 7516–7523.
   PubMed Web of Science ®Google Scholar
• Honeychurch J, Glennie MJ, Johnson PW, et al. Anti-CD40 monoclonal antibody therapy in combination with irradiation results in a CD8 T-cell-dependent immunity to B-cell lymphoma. Blood 2003;102:1449–1457.
   PubMed Web of Science ®Google Scholar
• Kroemer G, Zitvogel L. Abscopal but desirable: the contribution of immune responses to the efficacy of radiotherapy. Oncoimmunology 2012;1:407–408.
   PubMed Web of Science ®Google Scholar
• Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 2005;5: 263–274.
   PubMed Web of Science ®Google Scholar
• Green DR, Ferguson T, Zitvogel L, et al. Immunogenic and tolerogenic cell death. Nat Rev Immunol 2009;9:353–363.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Kleinclauss F, Perruche S, Masson E, et al. Intravenous apoptotic spleen cell infusion induces a TGF-beta-dependent regulatory T-cell expansion. Cell Death Differ 2006;13:41–52.
   PubMed Web of Science ®Google Scholar
• Sauter B, Albert ML, Francisco L, et al. Consequences of cell death: exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J Exp Med 2000;191:423–434.
   PubMed Web of Science ®Google Scholar
• Slavin S, Strober S. Spontaneous murine B-cell leukaemia. Nature 1978;272:624–626.
   PubMed Web of Science ®Google Scholar
• Illidge T, Honeychurch J, Howatt W, et al. A new in vivo and in vitro B cell lymphoma model, pi-BCL1. Cancer Biother Radiopharm 2000;15:571–580.
   PubMed Web of Science ®Google Scholar
• Tutt AL, French RR, Illidge TM, et al. Monoclonal antibody therapy of B cell lymphoma: signaling activity on tumor cells appears more important than recruitment of effectors. J Immunol 1998;161:3176–3185.
   PubMed Web of Science ®Google Scholar
• Van Rooijen N, Sanders A. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J Immunol Methods 1994;174:83–93.
   PubMed Web of Science ®Google Scholar
• Miyake Y, Asano K, Kaise H, et al. Critical role of macrophages in the marginal zone in the suppression of immune responses to apoptotic cell-associated antigens. J Clin Invest 2007;117:2268–2278.
   PubMed Web of Science ®Google Scholar
• Castiglioni P, Martin-Fontecha A, Milan G, et al. Apoptosis-dependent subversion of the T-lymphocyte epitope hierarchy in lymphoma cells. Cancer Res 2002;62:1116–1122.
   PubMed Web of Science ®Google Scholar
• Bennett SR, Carbone FR, Karamalis F, et al. Help for cytotoxic- T-cell responses is mediated by CD40 signalling. Nature 1998;393: 478–480.
   PubMed Web of Science ®Google Scholar
• 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;393:474–478.
   PubMed Web of Science ®Google Scholar
• Schoenberger SP, Toes RE, van der Voort EI, et al. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 1998;393:480–483.
   PubMed Web of Science ®Google Scholar
• Albert ML, Sauter B, Bhardwaj N. Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature 1998;392:86–89.
   PubMed Web of Science ®Google Scholar
• French RR, Chan HT, Tutt AL, et al. CD40 antibody evokes a cytotoxic T-cell response that eradicates lymphoma and bypasses T-cell help. Nat Med 1999;5:548–553.
   PubMed Web of Science ®Google Scholar
• Barr TA, Carlring J, Heath AW. Co-stimulatory agonists as immunological adjuvants. Vaccine 2006;24:3399–3407.
   PubMed Web of Science ®Google Scholar
• Johansen P, Storni T, Rettig L, et al. Antigen kinetics determines immune reactivity. Proc Natl Acad Sci USA 2008;105:5189–5194.
   PubMed Web of Science ®Google Scholar
• Fadok VA, Bratton DL, Rose DM, et al. A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 2000;405:85–90.
   PubMed Web of Science ®Google Scholar
• Park D, Tosello-Trampont AC, Elliott MR, et al. BAI1 is an engulfment receptor for apoptotic cells upstream of the ELMO/Dock180/Rac module. Nature 2007;450:430–434.
   PubMed Web of Science ®Google Scholar
• Park SY, Jung MY, Kim HJ, et al. Rapid cell corpse clearance by stabilin-2, a membrane phosphatidylserine receptor. Cell Death Differ 2008;15:192–201.
   PubMed Web of Science ®Google Scholar
• Miyanishi M, Tada K, Koike M, et al. Identification of Tim4 as a phosphatidylserine receptor. Nature 2007;450:435–439.
   PubMed Web of Science ®Google Scholar
• Gardai SJ, McPhillips KA, Frasch SC, et al. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 2005;123:321–334.
   PubMed Web of Science ®Google Scholar
• Bondanza A, Zimmermann VS, Rovere-Querini P, et al. Inhibition of phosphatidylserine recognition heightens the immunogenicity of irradiated lymphoma cells in vivo. J Exp Med 2004; 200:1157–1165.
   PubMed Web of Science ®Google Scholar
• Delamarre L, Pack M, Chang H, et al. Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 2005;307:1630–1634.
   PubMed Web of Science ®Google Scholar
• Rovere P, Sabbadini MG, Vallinoto C, et al. Delayed clearance of apoptotic lymphoma cells allows cross-presentation of intracellular antigens by mature dendritic cells. J Leukoc Biol 1999;66: 345–349.
   PubMed Web of Science ®Google Scholar
• Heath WR, Carbone FR. Cross-presentation, dendritic cells, tolerance and immunity. Annu Rev Immunol 2001;19:47–64.
   PubMed Web of Science ®Google Scholar
• Soiffer R, Hodi FS, Haluska F, et al. Vaccination with irradiated, autologous melanoma cells engineered to secrete granulocyte-macrophage colony-stimulating factor by adenoviral-mediated gene transfer augments antitumor immunity in patients with metastatic melanoma. J Clin Oncol 2003;21:3343–3350.
   PubMed Web of Science ®Google Scholar
• Luo Y, Zhou H, Krueger J, et al. Targeting tumor-associated macrophages as a novel strategy against breast cancer. J Clin Invest 2006;116:2132–2141.
   PubMed Web of Science ®Google Scholar