Combination of ionising radiation with hyperthermia increases the immunogenic potential of B16-F10 melanoma cells in vitro and in vivo

References

• Scheithauer H, Belka C, Lauber K, Gaipl US. Immunological aspects of radiotherapy. Radiat Oncol 2014;9:185
   PubMed Web of Science ®Google Scholar
• Vatner RE, Cooper BT, Vanpouille-Box C, Demaria S, Formenti SC. Combinations of immunotherapy and radiation in cancer therapy. Front Oncol 2014;4:325
   PubMedGoogle Scholar
• Mace TA, Zhong L, Kokolus KM, Repasky EA. Effector CD8+ T cell IFN-gamma production and cytotoxicity are enhanced by mild hyperthermia. Int J Hyperthermia 2012;28:9–18
   PubMed Web of Science ®Google Scholar
• Datta NR, Grobholz R, Puric E, Bode-Lesniewska B, Lomax N, Khan S, et al. Enhanced tumour regression in a patient of liposarcoma treated with radiotherapy and hyperthermia: Hint for dynamic immunomodulation by hyperthermia. Int J Hyperthermia 2015;31:574–7
   PubMed Web of Science ®Google Scholar
• Repasky EA, Evans SS, Dewhirst MW. Temperature matters! And why it should matter to tumor immunologists. Cancer Immunol Res 2013;1:210–16
   PubMed Web of Science ®Google Scholar
• Frey B, Weiss EM, Rubner Y, Wunderlich R, Ott OJ, Sauer R, et al. Old and new facts about hyperthermia-induced modulations of the immune system. Int J Hyperthermia 2012;28:528–42
   PubMed Web of Science ®Google Scholar
• Toraya-Brown S, Fiering S. Local tumour hyperthermia as immunotherapy for metastatic cancer. Int J Hyperthermia 2014;30:531–39
   PubMed Web of Science ®Google Scholar
• Krawczyk PM, Eppink B, Essers J, Stap J, Rodermond H, Odijk H, et al. Mild hyperthermia inhibits homologous recombination, induces BRCA2 degradation, and sensitizes cancer cells to poly (ADP-ribose) polymerase-1 inhibition. Proc Natl Acad Sci USA 2011;108:9851–6
   PubMed Web of Science ®Google Scholar
• Issels RD. Hyperthermia adds to chemotherapy. Eur J Cancer 2008;44:2546–54
   PubMed Web of Science ®Google Scholar
• van der Zee J. Heating the patient: A promising approach? Ann Oncol 2002;13:1173–84
   PubMed Web of Science ®Google Scholar
• Melcher A, Todryk S, Hardwick N, Ford M, Jacobson M, Vile RG. Tumor immunogenicity is determined by the mechanism of cell death via induction of heat shock protein expression. Nat Med 1998;4:581–7
   PubMed Web of Science ®Google Scholar
• Schilling D, Kuhnel A, Konrad S, Tetzlaff F, Bayer C, Yaglom J, et al. Sensitizing tumor cells to radiation by targeting the heat shock response. Cancer Lett 2015;360:294–301
   PubMed Web of Science ®Google Scholar
• Lauber K, Brix N, Ernst A, Hennel R, Krombach J, Anders H, et al. Targeting the heat shock response in combination with radiotherapy: Sensitizing cancer cells to irradiation-induced cell death and heating up their immunogenicity. Cancer Lett 2015;368:209–29
   PubMed Web of Science ®Google Scholar
• Arnold-Schild D, Hanau D, Spehner D, Schmid C, Rammensee HG, de la Salle H, et al. Cutting edge: Receptor-mediated endocytosis of heat shock proteins by professional antigen-presenting cells. J Immunol 1999;162:3757–60
   PubMed Web of Science ®Google Scholar
• Torigoe T, Tamura Y, Sato N. Heat shock proteins and immunity: Application of hyperthermia for immunomodulation. Int J Hyperthermia 2009;25:610–16
   PubMed Web of Science ®Google Scholar
• Schildkopf P, Frey B, Ott OJ, Rubner Y, Multhoff G, Sauer R, et al. Radiation combined with hyperthermia induces HSP70-dependent maturation of dendritic cells and release of pro-inflammatory cytokines by dendritic cells and macrophages. Radiother Oncol 2011;101:109–15
   PubMed Web of Science ®Google Scholar
• Multhoff G, Botzler C, Wiesnet M, Muller E, Meier T, Wilmanns W, et al. A stress-inducible 72-kDa heat-shock protein (Hsp72) is expressed on the surface of human tumor cells, but not on normal cells. Int J Cancer 1995;61:272–9
   PubMed Web of Science ®Google Scholar
• Gehrmann M, Marienhagen J, Eichholtz-Wirth H, Fritz E, Ellwart J, Jaattela M, et al. Dual function of membrane-bound heat shock protein 70 (Hsp70), Bag-4, and Hsp40: Protection against radiation-induced effects and target structure for natural killer cells. Cell Death Differ 2005;12:38–51
   PubMed Web of Science ®Google Scholar
• Multhoff G, Pockley AG, Schmid TE, Schilling D. The role of heat shock protein 70 (Hsp70) in radiation-induced immunomodulation. Cancer Lett 2015;368:179–84
   PubMed Web of Science ®Google Scholar
• Sottile ML, Losinno AD, Fanelli MA, Cuello-Carrion FD, Montt-Guevara MM, Vargas-Roig LM, et al. Hyperthermia effects on Hsp27 and Hsp72 associations with mismatch repair (MMR) proteins and cisplatin toxicity in MMR-deficient/proficient colon cancer cell lines. Int J Hyperthermia 2015;31:464–75
   PubMed Web of Science ®Google Scholar
• Guzhova IV, Shevtsov MA, Abkin SV, Pankratova KM, Margulis BA. Intracellular and extracellular Hsp70 chaperone as a target for cancer therapy. Int J Hyperthermia 2013;29:399–408
   PubMed Web of Science ®Google Scholar
• Tang D, Kang R, Zeh HJ III, Lotze MT. High-mobility group box 1 and cancer. Biochim Biophys Acta 2010;1799:131–40
   PubMed Web of Science ®Google Scholar
• Ellerman JE, Brown CK, de Vera M, Zeh HJ, Billiar T, Rubartelli A, et al. Masquerader: High mobility group box-1 and cancer. Clin Cancer Res 2007;13:2836–48
   PubMed Web of Science ®Google Scholar
• Gallucci S, Matzinger P. Danger signals: SOS to the immune system. Curr Opin Immunol 2001;13:114–19
   PubMed Web of Science ®Google Scholar
• Bustin M. At the crossroads of necrosis and apoptosis: Signaling to multiple cellular targets by HMGB1. Sci STKE 2002;151:pe39
   Google Scholar
• Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002;418:1915
   Web of Science ®Google Scholar
• Gardella S, Andrei C, Ferrera D, Lotti LV, Torrisi MR, Bianchi ME, et al. The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesicle-mediated secretory pathway. EMBO Rep 2002;3:995–1001
   PubMed Web of Science ®Google Scholar
• Dong Xda E, Ito N, Lotze MT, Demarco RA, Popovic P, Shand SH, et al. High mobility group box I (HMGB1) release from tumor cells after treatment: Implications for development of targeted chemoimmunotherapy. J Immunother 2007;30:596–606
   PubMed Web of Science ®Google Scholar
• Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A, et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007;13:1050–9
   PubMed Web of Science ®Google Scholar
• Park JS, Svetkauskaite D, He Q, Kim JY, Strassheim D, Ishizaka A, et al. Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J Biol Chem 2004;279:7370–7
   PubMed Web of Science ®Google Scholar
• Muckle DS, Dickson JA. Hyperthermia (42 °C) as an adjuvant to radiotherapy and chemotherapy in the treatment of the allogeneic VX2 carcinoma in the rabbit. Br J Cancer 1973;27:307–15
   PubMed Web of Science ®Google Scholar
• Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SA, Behjati S, Biankin AV, et al. Signatures of mutational processes in human cancer. Nature 2013;500:415–21
   PubMed Web of Science ®Google Scholar
• Overgaard J, Gonzalez Gonzalez D, Hulshof MC, Arcangeli G, Dahl O, Mella O, et al. Hyperthermia as an adjuvant to radiation therapy of recurrent or metastatic malignant melanoma. A multicentre randomized trial by the European Society for Hyperthermic Oncology. Int J Hyperthermia 1996;12:3–20
   PubMed Web of Science ®Google Scholar
• Overgaard J, Gonzalez Gonzalez D, Hulshof MC, Arcangeli G, Dahl O, Mella O, et al. Randomised trial of hyperthermia as adjuvant to radiotherapy for recurrent or metastatic malignant melanoma. European Society for Hyperthermic Oncology. Lancet 1995;345:540–3
   PubMed Web of Science ®Google Scholar
• Werthmoller N, Frey B, Wunderlich R, Fietkau R, Gaipl US. Modulation of radiochemoimmunotherapy-induced B16 melanoma cell death by the pan-caspase inhibitor zVAD-fmk induces anti-tumor immunity in a HMGB1-, nucleotide- and T-cell-dependent manner. Cell Death Dis 2015;6:e1761
   PubMed Web of Science ®Google Scholar
• Gaipl US, Kuenkele S, Voll RE, Beyer TD, Kolowos W, Heyder P, et al. Complement binding is an early feature of necrotic and a rather late event during apoptotic cell death. Cell Death Differ 2001;8:327–34
   PubMed Web of Science ®Google Scholar
• Geran RI, Greenberg NH, Macdonald MM, Abbott BJ. Modified protocol for the testing of new synthetics in the L1210 lymphoid leukemia murine model in the DR&D program, DCT, NCI. Natl Cancer Inst Monogr 1977;45:151–3
   PubMedGoogle Scholar
• Gorayski P, Burmeister B, Foote M. Radiotherapy for cutaneous melanoma: Current and future applications. Future Oncol 2015;11:525–34
   PubMed Web of Science ®Google Scholar
• Triantopoulou S, Efstathopoulos E, Platoni K, Uzunoglou N, Kelekis N, Kouloulias V. Radiotherapy in conjunction with superficial and intracavitary hyperthermia for the treatment of solid tumors: Survival and thermal parameters. Clin Transl Oncol 2013;15:95–105
   PubMed Web of Science ®Google Scholar
• Lauber K, Ernst A, Orth M, Herrmann M, Belka C. Dying cell clearance and its impact on the outcome of tumor radiotherapy. Front Oncol 2012;2:116
   PubMedGoogle Scholar
• Rodel F, Frey B, Multhoff G, Gaipl U. Contribution of the immune system to bystander and non-targeted effects of ionizing radiation. Cancer Lett 2015;356:105–13
   PubMed Web of Science ®Google Scholar
• Orth M, Lauber K, Niyazi M, Friedl AA, Li M, Maihofer C, et al. Current concepts in clinical radiation oncology. Radiat Environ Biophys 2014;53:1–29
   PubMed Web of Science ®Google Scholar
• Anvekar RA, Asciolla JJ, Lopez-Rivera E, Floros KV, Izadmehr S, Elkholi R, et al. Sensitization to the mitochondrial pathway of apoptosis augments melanoma tumor cell responses to conventional chemotherapeutic regimens. Cell Death Dis 2012;3:e420
   PubMed Web of Science ®Google Scholar
• Pierce RH, Campbell JS, Pai SI, Brody JD, Kohrt HE. In-situ tumor vaccination: Bringing the fight to the tumor. Hum Vaccin Immunother 2015;11:1901–9
   PubMed Web of Science ®Google Scholar
• Eggermont AM, Maio M, Robert C. Immune checkpoint inhibitors in melanoma provide the cornerstones for curative therapies. Semin Oncol 2015;42:429–35
   PubMed Web of Science ®Google Scholar
• Barker CA, Postow MA. Combinations of radiation therapy and immunotherapy for melanoma: A review of clinical outcomes. Int J Radiat Oncol Biol Phys 2014;88:986–97
   PubMed Web of Science ®Google Scholar
• Dovedi SJ, Adlard AL, Lipowska-Bhalla G, McKenna C, Jones S, Cheadle EJ, et al. Acquired resistance to fractionated radiotherapy can be overcome by concurrent PD-L1 blockade. Cancer Res 2014;74:5458–68
   PubMed Web of Science ®Google Scholar
• Schildkopf P, Frey B, Mantel F, Ott OJ, Weiss EM, Sieber R, et al. Application of hyperthermia in addition to ionizing irradiation fosters necrotic cell death and HMGB1 release of colorectal tumor cells. Biochem Biophys Res Commun 2010;391:1014–20
   PubMed Web of Science ®Google Scholar
• Datta NR, Ordonez SG, Gaipl US, Paulides MM, Crezee H, Gellermann J, et al. Local hyperthermia combined with radiotherapy and-/or chemotherapy: Recent advances and promises for the future. Cancer Treat Rev 2015;41:742–53
   PubMed Web of Science ®Google Scholar
• Mantel F, Frey B, Haslinger S, Schildkopf P, Sieber R, Ott OJ, et al. Combination of ionising irradiation and hyperthermia activates programmed apoptotic and necrotic cell death pathways in human colorectal carcinoma cells. Strahlenther Onkol 2010;186:587–99
   PubMed Web of Science ®Google Scholar
• Meggyeshazi N, Andocs G, Balogh L, Balla P, Kiszner G, Teleki I, et al. DNA fragmentation and caspase-independent programmed cell death by modulated electrohyperthermia. Strahlenther Onkol 2014;190:815–22
   PubMed Web of Science ®Google Scholar
• Ullrich E, Bonmort M, Mignot G, Kroemer G, Zitvogel L. Tumor stress, cell death and the ensuing immune response. Cell Death Differ 2008;15:21–8
   PubMed Web of Science ®Google Scholar
• Gastpar R, Gehrmann M, Bausero MA, Asea A, Gross C, Schroeder JA, et al. Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells. Cancer Res 2005;65:5238–47
   PubMed Web of Science ®Google Scholar
• Liu S, Stolz DB, Sappington PL, Macias CA, Killeen ME, Tenhunen JJ, et al. HMGB1 is secreted by immunostimulated enterocytes and contributes to cytomix-induced hyperpermeability of Caco-2 monolayers. Am J Physiol Cell Physiol 2006;290:C990–9
   PubMed Web of Science ®Google Scholar
• Al-Mayah A, Bright S, Chapman K, Irons S, Luo P, Carter D, et al. The non-targeted effects of radiation are perpetuated by exosomes. Mutat Res 2015;772:38–45
   PubMed Web of Science ®Google Scholar
• Yang Y, Chen Y, Zhang F, Zhao Q and Zhong H. Increased anti-tumour activity by exosomes derived from doxorubicin-treated tumour cells via heat stress. Int J Hyperthermia 2015;31:498–506
   PubMed Web of Science ®Google Scholar
• Breuninger S, Erl J, Knape C, Gunther S, Regel I, Rödel F, et al. Quantitative analysis of liposomal heat shock protein 70 (Hsp70) in the blood of tumor patients using a novel LipHsp70 ELISA. Clin Cell Immunol 2014;5:1–10
   Google Scholar
• Binder DC, Fu YX, Weichselbaum RR. Radiotherapy and immune checkpoint blockade: Potential interactions and future directions. Trends Mol Med 2015;21:463–5
   PubMed Web of Science ®Google Scholar
• Cihoric N, Tsikkinis A, van Rhoon G, Crezee H, Aebersold DM, Bodis S, et al. Hyperthermia-related clinical trials on cancer treatment within the ClinicalTrials.gov registry. Int J Hyperthermia 2015;31:609–14
   PubMed Web of Science ®Google Scholar
• Hurwitz M, Stauffer P. Hyperthermia, radiation and chemotherapy: The role of heat in multidisciplinary cancer care. Semin Oncol 2014;41:714–29
   PubMed Web of Science ®Google Scholar
• Kelleher DK, Vaupel P. No sustained improvement in tumor oxygenation after localized mild hyperthermia. Adv Exp Med Biol 2010;662:393–8
   PubMed Web of Science ®Google Scholar
• Frey B, Rubner Y, Kulzer L, Werthmoller N, Weiss EM, Fietkau R, et al. Antitumor immune responses induced by ionizing irradiation and further immune stimulation. Cancer Immunol Immunother 2014;63:29–36
   PubMed Web of Science ®Google Scholar
• Curtin JF, Liu N, Candolfi M, Xiong W, Assi H, Yagiz K, et al. HMGB1 mediates endogenous TLR2 activation and brain tumor regression. PLoS Med 2009;6:e10
   PubMed Web of Science ®Google Scholar
• Umansky V, Sevko A. Melanoma-induced immunosuppression and its neutralization. Semin Cancer Biol 2012;22:319–26
   PubMed Web of Science ®Google Scholar
• Golden EB, Chhabra A, Chachoua A, Adams S, Donach M, Fenton-Kerimian M, et al. Local radiotherapy and granulocyte-macrophage colony-stimulating factor to generate abscopal responses in patients with metastatic solid tumours: A proof-of-principle trial. Lancet Oncol 2015;16:795–803
   PubMed Web of Science ®Google Scholar
• Twyman-Saint Victor C, Rech AJ, Maity A, Rengan R, Pauken KE, Stelekati E, et al. Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer. Nature 2015;520:373–7
   PubMed Web of Science ®Google Scholar
• Frey B, Gaipl US. Radio-immunotherapy: The focused beam expands. Lancet Oncol 2015;16:742–3
   PubMed Web of Science ®Google Scholar