Severe, but not mild heat-shock treatment induces immunogenic cell death in cancer cells

References

• Hildebrandt B, Wust P, Ahlers O, Dieing A, Sreenivasa G, Kerner T, Felix R, Riess H. The cellular and molecular basis of hyperthermia. Crit Rev Oncol Hematol 2002; 43:33-56; PMID:12098606; https://doi.org/10.1016/S1040-8428(01)00179-2
   PubMed Web of Science ®Google Scholar
• Mentre P, Hamraoui L, Hui Bon Hoa G, Debey P. Pressure-sensitivity of endoplasmic reticulum membrane and nucleolus as revealed by electron microscopy. Cell Mol Biol 1999; 45:353-62; PMID:10386792; https://doi.org/10.1088/1742-6596/121/1/112003
   PubMed Web of Science ®Google Scholar
• Dudek AM, Garg AD, Krysko DV, De Ruysscher D, Agostinis P. Inducers of immunogenic cancer cell death. Cytokine Growth Factor Rev 2013; 24:319-33; PMID:23391812; https://doi.org/10.1016/j.cytogfr.2013.01.005
   PubMed Web of Science ®Google Scholar
• Kroemer G, Galluzzi L, Kepp O, Zitvogel L. Immunogenic cell death in cancer therapy. Ann Rev Immunol 2013; 31:51-72; PMID:23157435; https://doi.org/10.1146/annurev-immunol-032712-100008
   PubMed Web of Science ®Google Scholar
• Krysko DV, Garg AD, Kaczmarek A, Krysko O, Agostinis P, Vandenabeele P. Immunogenic cell death and DAMPs in cancer therapy. Nat Rev Cancer 2012; 12:860-75; PMID:23151605; https://doi.org/10.1038/nrc3380
   PubMed Web of Science ®Google Scholar
• Adkins I, Fucikova J, Garg AD, Agostinis P, Spisek R. Physical modalities inducing immunogenic tumor cell death for cancer immunotherapy. Oncoimmunology 2014; 3:e968434; PMID:25964865; https://doi.org/10.4161/21624011.2014.968434
   PubMed Web of Science ®Google Scholar
• Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, Perfettini JL, Castedo M, Mignot G, Panaretakis T, Casares N et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 2007; 13:54-61; PMID:17187072; https://doi.org/10.1038/nm1523
   PubMed Web of Science ®Google Scholar
• Bianchi ME. DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukocyte biol 2007; 81:1-5; PMID:17032697; http://doi.org/10.1189/jlb.0306164
   PubMed Web of Science ®Google Scholar
• Matzinger P. The danger model: a renewed sense of self. Science 2002; 296:301-5; PMID:11951032; https://doi.org/10.1126/science.1071059
   PubMed Web of Science ®Google Scholar
• Spisek R, Charalambous A, Mazumder A, Vesole DH, Jagannath S, Dhodapkar MV. Bortezomib enhances dendritic cell (DC)-mediated induction of immunity to human myeloma via exposure of cell surface heat shock protein 90 on dying tumor cells: therapeutic implications. Blood 2007; 109:4839-45; PMID:17299090; https://doi.org/10.1182/blood-2006-10-054221
   PubMed Web of Science ®Google Scholar
• Martins I, Tesniere A, Kepp O, Michaud M, Schlemmer F, Senovilla L, Séror C, Métivier D, Perfettini JL, Zitvogel L, et al. Chemotherapy induces ATP release from tumor cells. Cell Cycle 2009; 8:3723-8; PMID:19855167; https://doi.org/10.4161/cc.8.22.10026
   PubMed Web of Science ®Google Scholar
• Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002; 418:191-5; PMID:12110890; https://doi.org/10.1038/nature00858
   PubMed Web of Science ®Google Scholar
• Tesniere A, Panaretakis T, Kepp O, Apetoh L, Ghiringhelli F, Zitvogel L, Kroemer G. Molecular characteristics of immunogenic cancer cell death. Cell Death Differ 2008; 15:3-12; PMID:18007663; https://doi.org/10.1038/sj.cdd.4402269
   PubMed Web of Science ®Google Scholar
• Kepp O, Galluzzi L, Martins I, Schlemmer F, Adjemian S, Michaud M, Sukkurwala AQ, Menger L, Zitvogel L, Kroemer G. Molecular determinants of immunogenic cell death elicited by anticancer chemotherapy. Cancer Metastasis Rev 2011; 30:61-9; PMID:21249425; https://doi.org/10.1007/s10555-011-9273-4
   PubMed Web of Science ®Google Scholar
• Fucikova J, Moserova I, Truxova I, Hermanova I, Vancurova I, Partlova S, Fialova A, Sojka L, Cartron PF, Houska M et al. High hydrostatic pressure induces immunogenic cell death in human tumor cells. Int J Cancer 2014; 135:1165-77; PMID:24500981; https://doi.org/10.1002/ijc.28766
   PubMed Web of Science ®Google Scholar
• Roti Roti JL. Cellular responses to hyperthermia (40–46°C): cell killing and molecular events. Int J Hyperthermia 2008; 24:3-15; PMID:18214765; https://doi.org/10.1080/02656730701769841
   PubMed Web of Science ®Google Scholar
• Milleron RS, Bratton SB. 'Heated' debates in apoptosis. Cell Mol Life Sci 2007; 64:2329-33; PMID:17572850; https://doi.org/10.1007/s00018-007-7135-6
   PubMed Web of Science ®Google Scholar
• Suto R, Srivastava PK. A mechanism for the specific immunogenicity of heat shock protein-chaperoned peptides. Science 1995; 269:1585-8; PMID:7545313; https://doi.org/10.1126/science.7545313
   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; PMID:9585232; https://doi.org/10.1038/nm0598-581
   PubMed Web of Science ®Google Scholar
• Frey B, Weiss EM, Rubner Y, Wunderlich R, Ott OJ, Sauer R, Fietkau R, Gaipl US. Old and new facts about hyperthermia-induced modulations of the immune system. Int J Hyperthermia 2012; 28:528-42; PMID:22690925; https://doi.org/10.3109/02656736.2012.677933
   PubMed Web of Science ®Google Scholar
• Shi H, Cao T, Connolly JE, Monnet L, Bennett L, Chapel S, Bagnis C, Mannoni P, Davoust J, Palucka AK et al. Hyperthermia enhances CTL cross-priming. J Immunol 2006; 176:2134-41; PMID:18539499; https://doi.org/10.4049/jimmunol.176.4.2134
   PubMed Web of Science ®Google Scholar
• Zhang HG, Mehta K, Cohen P, Guha C. Hyperthermia on immune regulation: a temperature's story. Cancer Lett 2008; 271:191-204; PMID:18597930; https://doi.org/10.1016/j.canlet.2008.05.026
   PubMed Web of Science ®Google Scholar
• Feng H, Zeng Y, Graner MW, Katsanis E. Stressed apoptotic tumor cells stimulate dendritic cells and induce specific cytotoxic T cells. Blood 2002; 100:4108-15; PMID:12393401; https://doi.org/10.1182/blood-2002-05-1389
   PubMed Web of Science ®Google Scholar
• Feng H, Zeng Y, Graner MW, Likhacheva A, Katsanis E. Exogenous stress proteins enhance the immunogenicity of apoptotic tumor cells and stimulate antitumor immunity. Blood 2003; 101:245-52; PMID:12393411; https://doi.org/10.1182/blood-2002-05-1580
   PubMed Web of Science ®Google Scholar
• Clark PR, Menoret A. The inducible Hsp70 as a marker of tumor immunogenicity. Cell Stress Chaperones 2001; 6:121-5; PMID:11599573; https://doi.org/10.1379/1466-1268(2001)006<0121:TIHAAM>2.0.CO;2
   PubMed Web of Science ®Google Scholar
• Mise K, Kan N, Okino T, Nakanishi M, Satoh K, Teramura Y, Yamasaki S, Ohgaki K, Tobe T. Effect of heat treatment on tumor cells and antitumor effector cells. Cancer Res 1990; 50:6199-202; PMID:2400985; http://doi.org/10.11501/3057478
   PubMed Web of Science ®Google Scholar
• Takahashi T, Mitsuhashi N, Sakurai H, Niibe H. Modifications of tumor-associated antigen expression on human lung cancer cells by hyperthermia and cytokine. Anticancer Res 1995; 15:2601-6; PMID:8669832; https://doi.org/10.1186/1756-9966-27-5
   PubMed Web of Science ®Google Scholar
• Wong JY, Mivechi NF, Paxton RJ, Williams LE, Beatty BG, Beatty JD, Shively JE. The effects of hyperthermia on tumor carcinoembryonic antigen expression. Int J Radiat Oncol Biol Phys 1989; 17:803-8; PMID:2674083; https://doi.org/10.1016/0360-3016(89)90070-9
   PubMed Web of Science ®Google Scholar
• Zerbini A, Pilli M, Penna A, Pelosi G, Schianchi C, Molinari A, Schivazappa S, Zibera C, Fagnoni FF, Ferrari C et al. Radiofrequency thermal ablation of hepatocellular carcinoma liver nodules can activate and enhance tumor-specific T-cell responses. Cancer Res 2006; 66:1139-46; PMID:16424051; https://doi.org/10.1158/0008-5472.CAN-05-2244
   PubMed Web of Science ®Google Scholar
• Ito A, Honda H, Kobayashi T. Cancer immunotherapy based on intracellular hyperthermia using magnetite nanoparticles: a novel concept of “heat-controlled necrosis” with heat shock protein expression. Cancer Immunol Immunother 2006; 55:320-8; PMID:16133113; https://doi.org/10.1007/s00262-005-0049-y
   PubMed Web of Science ®Google Scholar
• Hu R, Ma S, Li H, Ke X, Wang G, Wei D, Wang W. Effect of magnetic fluid hyperthermia on lung cancer nodules in a murine model. Oncol Lett 2011; 2:1161-4; PMID:22848282; https://doi.org/10.3892/ol.2011.379
   PubMed Web of Science ®Google Scholar
• Wang H, Zhang L, Shi Y, Javidiparsijani S, Wang G, Li X, Ouyang W, Zhou J, Zhao L, Wang X et al. Abscopal antitumor immune effects of magnet-mediated hyperthermia at a high therapeutic temperature on Walker-256 carcinosarcomas in rats. Oncol Lett 2014; 7:764-70; PMID:24527084; https://doi.org/10.3892/ol.2014.1803
   PubMed Web of Science ®Google Scholar
• Yu Z, Geng J, Zhang M, Zhou Y, Fan Q, Chen J. Treatment of osteosarcoma with microwave thermal ablation to induce immunogenic cell death. Oncotarget 2014; 5:6526-39; PMID:25153727; https://doi.org/10.18632/oncotarget.2310
   PubMed Web of Science ®Google Scholar
• Brusa D, Migliore E, Garetto S, Simone M, Matera L. Immunogenicity of 56°C and UVC-treated prostate cancer is associated with release of HSP70 and HMGB1 from necrotic cells. Prostate 2009; 69:1343-52; PMID:19496055; https://doi.org/10.1002/pros.20981
   PubMed Web of Science ®Google Scholar
• Adkins I, Koberle M, Grobner S, Autenrieth SE, Bohn E, Borgmann S, Autenrieth IB. Y. enterocolitica inhibits antigen degradation in dendritic cells. Microbes Infect 2008; 10:798-806; PMID:18539499; https://doi.org/10.1016/j.micinf.2008.04.014
   PubMed Web of Science ®Google Scholar
• Adkins I, Kamanova J, Kocourkova A, Svedova M, Tomala J, Janova H, Masin J, Chladkova B, Bumba L, Kovar M et al. Bordetella adenylate cyclase toxin differentially modulates toll-like receptor-stimulated activation, migration and T cell stimulatory capacity of dendritic cells. PloS One 2014; 9:e104064; PMID:25084094; https://doi.org/10.1371/journal.pone.0104064
   PubMed Web of Science ®Google Scholar
• Hradilova N, Sadilkova L, Palata O, Mysikova D, Mrazkova H, Lischke R, Spisek R, Adkins I. Generation of dendritic cell-based vaccine using high hydrostatic pressure for non-small cell lung cancer immunotherapy. PLoS One 2017; 12:e0171539; PMID:28187172; https://doi.org/10.1371/journal.pone.0171539
   PubMed Web of Science ®Google Scholar
• Grobner S, Adkins I, Schulz S, Richter K, Borgmann S, Wesselborg S, Ruckdeschel K, Micheau O, Autenrieth IB. Catalytically active Yersinia outer protein P induces cleavage of RIP and caspase-8 at the level of the DISC independently of death receptors in dendritic cells. Apoptosis 2007; 12:1813-25; PMID:17624595; https://doi.org/10.1007/s10495-007-0100-x
   PubMed Web of Science ®Google Scholar
• Fucikova J, Kralikova P, Fialova A, Brtnicky T, Rob L, Bartunkova J, Spísek R. Human tumor cells killed by anthracyclines induce a tumor-specific immune response. Cancer Res 2011; 71:4821-33; PMID:21602432; https://doi.org/10.1158/0008-5472.CAN-11-0950
   PubMed Web of Science ®Google Scholar
• Garg AD, Krysko DV, Verfaillie T, Kaczmarek A, Ferreira GB, Marysael T, Rubio N, Firczuk M, Mathieu C, Roebroek AJ et al. A novel pathway combining calreticulin exposure and ATP secretion in immunogenic cancer cell death. EMBO J 2012; 31:1062-79; PMID:22252128; https://doi.org/10.1038/emboj.2011.497
   PubMed Web of Science ®Google Scholar
• Garg AD, Krysko DV, Vandenabeele P, Agostinis P. Hypericin-based photodynamic therapy induces surface exposure of damage-associated molecular patterns like HSP70 and calreticulin. Cancer Immunol Immunother 2012; 61:215-21; PMID:22193987; https://doi.org/10.1007/s00262-011-1184-2
   PubMed Web of Science ®Google Scholar
• Panaretakis T, Kepp O, Brockmeier U, Tesniere A, Bjorklund AC, Chapman DC, Durchschlag M, Joza N, Pierron G, van Endert P et al. Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death. EMBO J 2009; 28:578-90; PMID:19165151; https://doi.org/10.1038/emboj.2009.1
   PubMed Web of Science ®Google Scholar
• Tufi R, Panaretakis T, Bianchi K, Criollo A, Fazi B, Di Sano F, Tesniere A, Kepp O, Paterlini-Brechot P, Zitvogel L et al. Reduction of endoplasmic reticulum Ca2+ levels favors plasma membrane surface exposure of calreticulin. Cell Death Differ 2008; 15:274-82; PMID:18034188; https://doi.org/10.1038/sj.cdd.4402275
   PubMed Web of Science ®Google Scholar
• Shellman YG, Howe WR, Miller LA, Goldstein NB, Pacheco TR, Mahajan RL, LaRue SM, Norris DA. Hyperthermia induces endoplasmic reticulum-mediated apoptosis in melanoma and non-melanoma skin cancer cells. J Invest Dermatol 2008; 128:949-56; PMID:17989736; https://doi.org/10.1038/sj.jid.5701114
   PubMed Web of Science ®Google Scholar
• Chen T, Guo J, Han C, Yang M, Cao X. Heat shock protein 70, released from heat-stressed tumor cells, initiates antitumor immunity by inducing tumor cell chemokine production and activating dendritic cells via TLR4 pathway. J Immunol 2009; 182:1449-59; https://doi.org/10.4049/jimmunol.182.3.1449
   PubMed Web of Science ®Google Scholar
• Srivastava PK, Udono H, Blachere NE, Li Z. Heat shock proteins transfer peptides during antigen processing and CTL priming. Immunogenetics 1994; 39:93-8; PMID:8276462; https://doi.org/10.1007/BF00188611
   PubMed Web of Science ®Google Scholar
• Zappasodi R, Pupa SM, Ghedini GC, Bongarzone I, Magni M, Cabras AD, Colombo MP, Carlo-Stella C, Gianni AM, Di Nicola M. Improved clinical outcome in indolent B-cell lymphoma patients vaccinated with autologous tumor cells experiencing immunogenic death. Cancer Res 2010; 70:9062-72; PMID:20884630; https://doi.org/10.1158/0008-5472.CAN-10-1825
   PubMed Web of Science ®Google Scholar
• Bettaieb A, Averill-Bates DA. Thermotolerance induced at a mild temperature of 40°C alleviates heat shock-induced ER stress and apoptosis in HeLa cells. Biochim Biophys Acta 2015; 1853:52-62; PMID:25260982; https://doi.org/10.1016/j.bbamcr.2014.09.016
   PubMed Web of Science ®Google Scholar
• Dutta S, Chiu YC, Probert AW, Wang KK. Selective release of calpain produced alphalI-spectrin (alpha-fodrin) breakdown products by acute neuronal cell death. Biol Chem 2002; 383:785-91; PMID:12108543; https://doi.org/10.1515/BC.2002.082
   PubMed Web of Science ®Google Scholar
• Vanags DM, Porn-Ares MI, Coppola S, Burgess DH, Orrenius S. Protease involvement in fodrin cleavage and phosphatidylserine exposure in apoptosis. J Biol Chem 1996; 271:31075-85; PMID:8940103; https://doi.org/10.1074/jbc.271.49.31075
   PubMed Web of Science ®Google Scholar
• Martins I, Michaud M, Sukkurwala AQ, Adjemian S, Ma Y, Shen S, Kepp O, Menger L, Vacchelli E, Galluzzi L et al. Premortem autophagy determines the immunogenicity of chemotherapy-induced cancer cell death. Autophagy 2012; 8:413-5; PMID:22361584; https://doi.org/10.4161/auto.19009
   PubMed Web of Science ®Google Scholar
• Adkins I, Koberle M, Grobner S, Bohn E, Autenrieth IB, Borgmann S. Yersinia outer proteins E, H, P, and T differentially target the cytoskeleton and inhibit phagocytic capacity of dendritic cells. Int J Med Microbiol 2007; 297:235-44; PMID:17462949; https://doi.org/10.1016/j.ijmm.2007.02.005
   PubMed Web of Science ®Google Scholar