Molecular and Translational Classifications of DAMPs in Immunogenic Cell Death
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
26635802
PubMed Central
PMC4653610
DOI
10.3389/fimmu.2015.00588
Knihovny.cz E-zdroje
- Klíčová slova
- anti-tumor immunity, immunogenicity, immunotherapy, molecular medicine, oncoimmunology, patient prognosis, translational medicine,
- Publikační typ
- časopisecké články MeSH
The immunogenicity of malignant cells has recently been acknowledged as a critical determinant of efficacy in cancer therapy. Thus, besides developing direct immunostimulatory regimens, including dendritic cell-based vaccines, checkpoint-blocking therapies, and adoptive T-cell transfer, researchers have started to focus on the overall immunobiology of neoplastic cells. It is now clear that cancer cells can succumb to some anticancer therapies by undergoing a peculiar form of cell death that is characterized by an increased immunogenic potential, owing to the emission of the so-called "damage-associated molecular patterns" (DAMPs). The emission of DAMPs and other immunostimulatory factors by cells succumbing to immunogenic cell death (ICD) favors the establishment of a productive interface with the immune system. This results in the elicitation of tumor-targeting immune responses associated with the elimination of residual, treatment-resistant cancer cells, as well as with the establishment of immunological memory. Although ICD has been characterized with increased precision since its discovery, several questions remain to be addressed. Here, we summarize and tabulate the main molecular, immunological, preclinical, and clinical aspects of ICD, in an attempt to capture the essence of this phenomenon, and identify future challenges for this rapidly expanding field of investigation.
Biotherapy and Vaccine Unit Institut Pasteur Paris France
Department of Ecological and Biological Sciences Tuscia University Viterbo Italy
Department of Experimental Medicine Sapienza University of Rome Rome Italy
Department of Immunology Medical University of Warsaw Warsaw Poland
Department of Medical Oncology University Hospital Bern Switzerland
Department of Oncology University of Turin Turin Italy
Department of Radiation Oncology Universitätsklinikum Erlangen Erlangen Germany
e Duve Institute Université Catholique de Louvain Brussels Belgium
Faculty of Life Sciences University of Manchester Manchester UK
IRRCS Istituto Scientifico San Raffaele Università Vita Salute San Raffaele Milan Italy
Laboratory of Molecular and Cellular Therapy Vrije Universiteit Brussel Jette Belgium
Sapienza University of Rome Rome Italy
Wellman Center for Photomedicine Massachusetts General Hospital Boston MA USA
Zobrazit více v PubMed
Galluzzi L, Vacchelli E, Bravo-San Pedro JM, Buque A, Senovilla L, Baracco EE, et al. Classification of current anticancer immunotherapies. Oncotarget (2014) 5(24):12472–508.10.18632/oncotarget.2998 PubMed DOI PMC
Kepp O, Tesniere A, Zitvogel L, Kroemer G. The immunogenicity of tumor cell death. Curr Opin Oncol (2009) 21(1):71–6.10.1097/CCO.0b013e32831bc375 PubMed DOI
Garg AD, Dudek AM, Agostinis P. Cancer immunogenicity, danger signals, and DAMPs: what, when, and how? Biofactors (2013) 39(4):355–67.10.1002/biof.1125 PubMed DOI
Blankenstein T, Coulie PG, Gilboa E, Jaffee EM. The determinants of tumour immunogenicity. Nat Rev Cancer (2012) 12(4):307–13.10.1038/nrc3246 PubMed DOI PMC
Garg AD, Nowis D, Golab J, Vandenabeele P, Krysko DV, Agostinis P. Immunogenic cell death, DAMPs and anticancer therapeutics: an emerging amalgamation. Biochim Biophys Acta (2010) 1805(1):53–71.10.1016/j.bbcan.2009.08.003 PubMed DOI
Anguille S, Smits EL, Lion E, van Tendeloo VF, Berneman ZN. Clinical use of dendritic cells for cancer therapy. Lancet Oncol (2014) 15(7):e257–67.10.1016/S1470-2045(13)70585-0 PubMed DOI
Chiang CL, Kandalaft LE, Coukos G. Adjuvants for enhancing the immunogenicity of whole tumor cell vaccines. Int Rev Immunol (2011) 30(2–3):150–82.10.3109/08830185.2011.572210 PubMed DOI
Parish CR. Cancer immunotherapy: the past, the present and the future. Immunol Cell Biol (2003) 81(2):106–13.10.1046/j.0818-9641.2003.01151.x PubMed DOI
Coley WB. The treatment of malignant tumors by repeated inoculations of erysipelas: with a report of ten original cases. Am J Med Sci (1893) 105:487–511.10.1097/00000441-189305000-00001 PubMed DOI
Tsung K, Norton JA. Lessons from Coley’s toxin. Surg Oncol (2006) 15(1):25–8.10.1016/j.suronc.2006.05.002 PubMed DOI
Coulie PG, Van den Eynde BJ, van der Bruggen P, Boon T. Tumour antigens recognized by T lymphocytes: at the core of cancer immunotherapy. Nat Rev Cancer (2014) 14(2):135–46.10.1038/nrc3670 PubMed DOI
Liao SK, Carr DH. Comparative immunogenicity of irradiated, neuraminidase treated, and fused cells of a strain-restricted sarcoma. Z Krebsforsch klin Onkol Cancer Res Clin Oncol (1974) 82(2):133–42. PubMed
Milas L, Withers HR. Nonspecific immunotherapy of malignant tumors. Radiology (1976) 118(1):211–8.10.1148/118.1.211 PubMed DOI
Bogden AE, Esber HJ. Influence of surgery, irradiation, chemotherapy, and immunotherapy on growth of a metastasizing rat mammary adenocarcinoma. Natl Cancer Inst Monogr (1978) (49):97–100. PubMed
Dickson JA, Shah SA. Hyperthermia: the immune response and tumor metastasis. Natl Cancer Inst Monogr (1982) 61:183–92. PubMed
Suit HD, Walker AM. Assessment of the response of tumours to radiation: clinical and experimental studies. Br J Cancer Suppl (1980) 4:1–10. PubMed PMC
Richert L, Or A, Shinitzky M. Promotion of tumor antigenicity in EL-4 leukemia cells by hydrostatic pressure. Cancer Immunol Immunother (1986) 22(2):119–24.10.1007/BF00199125 PubMed DOI PMC
Galluzzi L, Senovilla L, Zitvogel L, Kroemer G. The secret ally: immunostimulation by anticancer drugs. Nat Rev Drug Discov (2012) 11(3):215–33.10.1038/nrd3626 PubMed DOI
Green DR, Ferguson T, Zitvogel L, Kroemer G. Immunogenic and tolerogenic cell death. Nat Rev Immunol (2009) 9(5):353–63.10.1038/nri2545 PubMed DOI PMC
Matzinger P. Tolerance, danger, and the extended family. Annu Rev Immunol (1994) 12:991–1045.10.1146/annurev.iy.12.040194.005015 PubMed DOI
Matzinger P. The danger model: a renewed sense of self. Science (2002) 296(5566):301–5.10.1126/science.1071059 PubMed DOI
Land W, Schneeberger H, Schleibner S, Illner WD, Abendroth D, Rutili G, et al. The beneficial effect of human recombinant superoxide dismutase on acute and chronic rejection events in recipients of cadaveric renal transplants. Transplantation (1994) 57(2):211–7.10.1097/00007890-199401001-00010 PubMed DOI
Seong SY, Matzinger P. Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nat Rev Immunol (2004) 4(6):469–78.10.1038/nri1372 PubMed DOI
Rubartelli A, Lotze MT. Inside, outside, upside down: damage-associated molecular-pattern molecules (DAMPs) and redox. Trends Immunol (2007) 28(10):429–36.10.1016/j.it.2007.08.004 PubMed DOI
Li G, Tang D, Lotze MT. Menage a trois in stress: DAMPs, redox and autophagy. Semin Cancer Biol (2013) 23(5):380–90.10.1016/j.semcancer.2013.08.002 PubMed DOI PMC
Garg AD, Martin S, Golab J, Agostinis P. Danger signalling during cancer cell death: origins, plasticity and regulation. Cell Death Differ (2014) 21(1):26–38.10.1038/cdd.2013.48 PubMed DOI PMC
Bianchi ME. DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol (2007) 81(1):1–5.10.1189/jlb.0306164 PubMed DOI
Bondanza A, Zimmermann VS, Rovere-Querini P, Turnay J, Dumitriu IE, Stach CM, et al. Inhibition of phosphatidylserine recognition heightens the immunogenicity of irradiated lymphoma cells in vivo. J Exp Med (2004) 200(9):1157–65.10.1084/jem.20040327 PubMed DOI PMC
Stach CM, Turnay X, Voll RE, Kern PM, Kolowos W, Beyer TD, et al. Treatment with annexin V increases immunogenicity of apoptotic human T-cells in Balb/c mice. Cell Death Differ (2000) 7(10):911–5.10.1038/sj.cdd.4400715 PubMed DOI
Dudek-Peric AM, Ferreira GB, Muchowicz A, Wouters J, Prada N, Martin S, et al. Antitumor immunity triggered by melphalan is potentiated by melanoma cell surface-associated calreticulin. Cancer Res (2015) 75(8):1603–14.10.1158/0008-5472.CAN-14-2089 PubMed DOI
Rondas D, Crevecoeur I, D’Hertog W, Ferreira GB, Staes A, Garg AD, et al. Citrullinated glucose-regulated protein 78 is an autoantigen in type 1 diabetes. Diabetes (2015) 64(2):573–86.10.2337/db14-0621 PubMed DOI
Venereau E, Casalgrandi M, Schiraldi M, Antoine DJ, Cattaneo A, De Marchis F, et al. Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release. J Exp Med (2012) 209(9):1519–28.10.1084/jem.20120189 PubMed DOI PMC
Weyd H, Abeler-Dorner L, Linke B, Mahr A, Jahndel V, Pfrang S, et al. Annexin A1 on the surface of early apoptotic cells suppresses CD8+ T cell immunity. PLoS One (2013) 8(4):e62449.10.1371/journal.pone.0062449 PubMed DOI PMC
Garg AD, Dudek AM, Ferreira GB, Verfaillie T, Vandenabeele P, Krysko DV, et al. ROS-induced autophagy in cancer cells assists in evasion from determinants of immunogenic cell death. Autophagy (2013) 9(9):1292–307.10.4161/auto.25399 PubMed DOI
Garg AD, Krysko DV, Verfaillie T, Kaczmarek A, Ferreira GB, Marysael T, et al. A novel pathway combining calreticulin exposure and ATP secretion in immunogenic cancer cell death. EMBO J (2012) 31(5):1062–79.10.1038/emboj.2011.497 PubMed DOI PMC
Ghiringhelli F, Apetoh L, Tesniere A, Aymeric L, Ma Y, Ortiz C, et al. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat Med (2009) 15(10):1170–8.10.1038/nm.2028 PubMed DOI
Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, Walk SF, et al. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature (2009) 461(7261):282–6.10.1038/nature08296 PubMed DOI PMC
Iwata A, Morgan-Stevenson V, Schwartz B, Liu L, Tupper J, Zhu X, et al. Extracellular BCL2 proteins are danger-associated molecular patterns that reduce tissue damage in murine models of ischemia-reperfusion injury. PLoS One (2010) 5(2):e9103.10.1371/journal.pone.0009103 PubMed DOI PMC
Babelova A, Moreth K, Tsalastra-Greul W, Zeng-Brouwers J, Eickelberg O, Young MF, et al. Biglycan, a danger signal that activates the NLRP3 inflammasome via toll-like and P2X receptors. J Biol Chem (2009) 284(36):24035–48.10.1074/jbc.M109.014266 PubMed DOI PMC
Schaefer L. Extracellular matrix molecules: endogenous danger signals as new drug targets in kidney diseases. Curr Opin Pharmacol (2010) 10(2):185–90.10.1016/j.coph.2009.11.007 PubMed DOI
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(1):54–61.10.1038/nm1523 PubMed DOI
Garg AD, Elsen S, Krysko DV, Vandenabeele P, de Witte P, Agostinis P. Resistance to anticancer vaccination effect is controlled by a cancer cell-autonomous phenotype that disrupts immunogenic phagocytic removal. Oncotarget (2015) 6(29):26841–60.10.18632/oncotarget.4754 PubMed DOI PMC
Koks CA, Garg AD, Ehrhardt M, Riva M, Vandenberk L, Boon L, et al. Newcastle disease virotherapy induces long-term survival and tumor-specific immune memory in orthotopic glioma through the induction of immunogenic cell death. Int J Cancer (2015) 136(5):E313–25.10.1002/ijc.29202 PubMed DOI
Gardai SJ, McPhillips KA, Frasch SC, Janssen WJ, Starefeldt A, Murphy-Ullrich JE, et al. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell (2005) 123(2):321–34.10.1016/j.cell.2005.08.032 PubMed DOI
Garcia Fernandez M, Troiano L, Moretti L, Nasi M, Pinti M, Salvioli S, et al. Early changes in intramitochondrial cardiolipin distribution during apoptosis. Cell Growth Differ (2002) 13(9):449–55. PubMed
Sorice M, Circella A, Cristea IM, Garofalo T, Di Renzo L, Alessandri C, et al. Cardiolipin and its metabolites move from mitochondria to other cellular membranes during death receptor-mediated apoptosis. Cell Death Differ (2004) 11(10):1133–45.10.1038/sj.cdd.4401457 PubMed DOI
Korbelik M, Banath J, Sun J, Canals D, Hannun YA, Separovic D. Ceramide and sphingosine-1-phosphate act as photodynamic therapy-elicited damage-associated molecular patterns: cell surface exposure. Int Immunopharmacol (2014) 20(2):359–65.10.1016/j.intimp.2014.03.016 PubMed DOI PMC
Horino K, Nishiura H, Ohsako T, Shibuya Y, Hiraoka T, Kitamura N, et al. A monocyte chemotactic factor, S19 ribosomal protein dimer, in phagocytic clearance of apoptotic cells. Lab Invest (1998) 78(5):603–17. PubMed
Nishimura T, Horino K, Nishiura H, Shibuya Y, Hiraoka T, Tanase S, et al. Apoptotic cells of an epithelial cell line, AsPC-1, release monocyte chemotactic S19 ribosomal protein dimer. J Biochem (2001) 129(3):445–54.10.1093/oxfordjournals.jbchem.a002876 PubMed DOI
Peter C, Wesselborg S, Lauber K. Role of attraction and danger signals in the uptake of apoptotic and necrotic cells and its immunological outcome. In: Krysko DV, Vandenabeele P, editors. Phagocytosis of Dying Cells. Berlin: Springer Science + Business Media B.V. (2009). p. 63–101.
Yamamoto T. Roles of the ribosomal protein S19 dimer and the C5a receptor in pathophysiological functions of phagocytic leukocytes. Pathol Int (2007) 57(1):1–11.10.1111/j.1440-1827.2007.02049.x PubMed DOI
Struck J, Uhlein M, Morgenthaler NG, Furst W, Hoflich C, Bahrami S, et al. Release of the mitochondrial enzyme carbamoyl phosphate synthase under septic conditions. Shock (2005) 23(6):533–8. PubMed
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(12):860–75.10.1038/nrc3380 PubMed DOI
Pullerits R, Bokarewa M, Jonsson IM, Verdrengh M, Tarkowski A. Extracellular cytochrome c, a mitochondrial apoptosis-related protein, induces arthritis. Rheumatology (Oxford) (2005) 44(1):32–9.10.1093/rheumatology/keh406 PubMed DOI
Codina R, Vanasse A, Kelekar A, Vezys V, Jemmerson R. Cytochrome c-induced lymphocyte death from the outside in: inhibition by serum leucine-rich alpha-2-glycoprotein-1. Apoptosis (2010) 15(2):139–52.10.1007/s10495-009-0412-0 PubMed DOI
Yoon KW, Byun S, Kwon E, Hwang SY, Chu K, Hiraki M, et al. Control of signaling-mediated clearance of apoptotic cells by the tumor suppressor p53. Science (2015) 349(6247):1261669.10.1126/science.1261669 PubMed DOI PMC
Kao J, Houck K, Fan Y, Haehnel I, Libutti SK, Kayton ML, et al. Characterization of a novel tumor-derived cytokine. Endothelial-monocyte activating polypeptide II. J Biol Chem (1994) 269(40):25106–19. PubMed
Knies UE, Behrensdorf HA, Mitchell CA, Deutsch U, Risau W, Drexler HC, et al. Regulation of endothelial monocyte-activating polypeptide II release by apoptosis. Proc Natl Acad Sci U S A (1998) 95(21):12322–7.10.1073/pnas.95.21.12322 PubMed DOI PMC
Ahrens S, Zelenay S, Sancho D, Hanc P, Kjaer S, Feest C, et al. F-actin is an evolutionarily conserved damage-associated molecular pattern recognized by DNGR-1, a receptor for dead cells. Immunity (2012) 36(4):635–45.10.1016/j.immuni.2012.03.008 PubMed DOI
Chiba S, Baghdadi M, Akiba H, Yoshiyama H, Kinoshita I, Dosaka-Akita H, et al. Tumor-infiltrating DCs suppress nucleic acid-mediated innate immune responses through interactions between the receptor TIM-3 and the alarmin HMGB1. Nat Immunol (2012) 13(9):832–42.10.1038/ni.2376 PubMed DOI PMC
Zitvogel L, Kepp O, Kroemer G. Decoding cell death signals in inflammation and immunity. Cell (2010) 140(6):798–804.10.1016/j.cell.2010.02.015 PubMed DOI
Pletjushkina OY, Fetisova EK, Lyamzaev KG, Ivanova OY, Domnina LV, Vyssokikh MY, et al. Long-distance apoptotic killing of cells is mediated by hydrogen peroxide in a mitochondrial ROS-dependent fashion. Cell Death Differ (2005) 12(11):1442–4.10.1038/sj.cdd.4401685 PubMed DOI
Garg AD, Nowis D, Golab J, Agostinis P. Photodynamic therapy: illuminating the road from cell death towards anti-tumour immunity. Apoptosis (2010) 15(9):1050–71.10.1007/s10495-010-0479-7 PubMed DOI
Suzuki S, Kulkarni AB. Extracellular heat shock protein HSP90beta secreted by MG63 osteosarcoma cells inhibits activation of latent TGF-beta1. Biochem Biophys Res Commun (2010) 398(3):525–31.10.1016/j.bbrc.2010.06.112 PubMed DOI PMC
Korbelik M, Sun J, Cecic I. Photodynamic therapy-induced cell surface expression and release of heat shock proteins: relevance for tumor response. Cancer Res (2005) 65(3):1018–26. PubMed
Cirone M, Di Renzo L, Lotti LV, Conte V, Trivedi P, Santarelli R, et al. Primary effusion lymphoma cell death induced by bortezomib and AG 490 activates dendritic cells through CD91. PLoS One (2012) 7(3):e31732.10.1371/journal.pone.0031732 PubMed DOI PMC
Zunino B, Rubio-Patino C, Villa E, Meynet O, Proics E, Cornille A, et al. Hyperthermic intraperitoneal chemotherapy leads to an anticancer immune response via exposure of cell surface heat shock protein 90. Oncogene (2015).10.1038/onc.2015.82 PubMed DOI
Zhou Z, Yamamoto Y, Sugai F, Yoshida K, Kishima Y, Sumi H, et al. Hepatoma-derived growth factor is a neurotrophic factor harbored in the nucleus. J Biol Chem (2004) 279(26):27320–6.10.1074/jbc.M308650200 PubMed DOI
Huang H, Evankovich J, Yan W, Nace G, Zhang L, Ross M, et al. Endogenous histones function as alarmins in sterile inflammatory liver injury through toll-like receptor 9 in mice. Hepatology (2011) 54(3):999–1008.10.1002/hep.24501 PubMed DOI PMC
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(9):1050–9.10.1038/nm1622 PubMed DOI
Semino C, Angelini G, Poggi A, Rubartelli A. NK/iDC interaction results in IL-18 secretion by DCs at the synaptic cleft followed by NK cell activation and release of the DC maturation factor HMGB1. Blood (2005) 106(2):609–16.10.1182/blood-2004-10-3906 PubMed DOI
Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature (2002) 418(6894):191–5.10.1038/nature00858 PubMed DOI
Thorburn J, Horita H, Redzic J, Hansen K, Frankel AE, Thorburn A. Autophagy regulates selective HMGB1 release in tumor cells that are destined to die. Cell Death Differ (2009) 16(1):175–83.10.1038/cdd.2008.143 PubMed DOI PMC
Yang D, Postnikov YV, Li Y, Tewary P, de la Rosa G, Wei F. High-mobility group nucleosome-binding protein 1 acts as an alarmin and is critical for lipopolysaccharide-induced immune responses. J Exp Med (2012) 209(1):157–71.10.1084/jem.20101354 PubMed DOI PMC
Cohen I, Rider P, Carmi Y, Braiman A, Dotan S, White MR, et al. Differential release of chromatin-bound IL-1alpha discriminates between necrotic and apoptotic cell death by the ability to induce sterile inflammation. Proc Natl Acad Sci U S A (2010) 107(6):2574–9.10.1073/pnas.0915018107 PubMed DOI PMC
Vanden Berghe T, Kalai M, Denecker G, Meeus A, Saelens X, Vandenabeele P. Necrosis is associated with IL-6 production but apoptosis is not. Cell Signal (2006) 18(3):328–35.10.1016/j.cellsig.2005.05.003 PubMed DOI
Lauber K, Bohn E, Krober SM, Xiao YJ, Blumenthal SG, Lindemann RK, et al. Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell (2003) 113:717–30.10.1016/S0092-8674(03)00422-7 PubMed DOI
Zhang Q, Raoof M, Chen Y, Sumi Y, Sursal T, Junger W, et al. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature (2010) 464(7285):104–7.10.1038/nature08780 PubMed DOI PMC
Collins LV, Hajizadeh S, Holme E, Jonsson IM, Tarkowski A. Endogenously oxidized mitochondrial DNA induces in vivo and in vitro inflammatory responses. J Leukoc Biol (2004) 75(6):995–1000.10.1189/jlb.0703328 PubMed DOI
Galluzzi L, Kepp O, Kroemer G. Mitochondria: master regulators of danger signalling. Nat Rev Mol Cell Biol (2012) 13(12):780–8.10.1038/nrm3479 PubMed DOI
Shi Y, Evans JE, Rock KL. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature (2003) 425(6957):516–21.10.1038/nature01991 PubMed DOI
Carp H. Mitochondrial N-formylmethionyl proteins as chemoattractants for neutrophils. J Exp Med (1982) 155(1):264–75.10.1084/jem.155.1.264 PubMed DOI PMC
Rabiet MJ, Huet E, Boulay F. The N-formyl peptide receptors and the anaphylatoxin C5a receptors: an overview. Biochimie (2007) 89(9):1089–106.10.1016/j.biochi.2007.02.015 PubMed DOI PMC
Czapiga M, Gao JL, Kirk A, Lekstrom-Himes J. Human platelets exhibit chemotaxis using functional N-formyl peptide receptors. Exp Hematol (2005) 33(1):73–84.10.1016/j.exphem.2004.09.010 PubMed DOI
Moghaddam AE, Gartlan KH, Kong L, Sattentau QJ. Reactive carbonyls are a major Th2-inducing damage-associated molecular pattern generated by oxidative stress. J Immunol (2011) 187(4):1626–33.10.4049/jimmunol.1003906 PubMed DOI
Miller YI, Choi SH, Wiesner P, Fang L, Harkewicz R, Hartvigsen K, et al. Oxidation-specific epitopes are danger-associated molecular patterns recognized by pattern recognition receptors of innate immunity. Circ Res (2011) 108(2):235–48.10.1161/CIRCRESAHA.110.223875 PubMed DOI PMC
Vandenberk L, Garg AD, Verschuere T, Koks C, Belmans J, Beullens M, et al. Irradiation of necrotic cancer cells employed for pulsing dendritic cells (DCs), potentiates DC vaccine-induced antitumor immunity against high-grade glioma. Oncoimmunology (2015).10.1080/2162402X.2015.1083669 PubMed DOI PMC
Riddell JR, Wang XY, Minderman H, Gollnick SO. Peroxiredoxin 1 stimulates secretion of proinflammatory cytokines by binding to TLR4. J Immunol (2010) 184(2):1022–30.10.4049/jimmunol.0901945 PubMed DOI PMC
Franz S, Herrmann K, Furnrohr BG, Sheriff A, Frey B, Gaipl US, et al. After shrinkage apoptotic cells expose internal membrane-derived epitopes on their plasma membranes. Cell Death Differ (2007) 14(4):733–42.10.1038/sj.cdd.4402066 PubMed DOI
Petrovski G, Zahuczky G, Katona K, Vereb G, Martinet W, Nemes Z, et al. Clearance of dying autophagic cells of different origin by professional and non-professional phagocytes. Cell Death Differ (2007) 14(6):1117–28.10.1038/sj.cdd.4402112 PubMed DOI
Bratton DL, Fadok VA, Richter DA, Kailey JM, Guthrie LA, Henson PM. Appearance of phosphatidylserine on apoptotic cells requires calcium-mediated nonspecific flip-flop and is enhanced by loss of the aminophospholipid translocase. J Biol Chem (1997) 272(42):26159–65.10.1074/jbc.272.42.26159 PubMed DOI
Martin SJ, Reutelingsperger CP, McGahon AJ, Rader JA, van Schie RC, LaFace DM, et al. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J Exp Med (1995) 182(5):1545–56.10.1084/jem.182.5.1545 PubMed DOI PMC
Brouckaert G, Kalai M, Krysko DV, Saelens X, Vercammen D, Ndlovu MN, et al. Phagocytosis of necrotic cells by macrophages is phosphatidylserine dependent and does not induce inflammatory cytokine production. Mol Biol Cell (2004) 15(3):1089–100.10.1091/mbc.E03-09-0668 PubMed DOI PMC
Donato R. RAGE: a single receptor for several ligands and different cellular responses: the case of certain S100 proteins. Curr Mol Med (2007) 7(8):711–24.10.2174/156652407783220688 PubMed DOI
Goh FG, Piccinini AM, Krausgruber T, Udalova IA, Midwood KS. Transcriptional regulation of the endogenous danger signal tenascin-C: a novel autocrine loop in inflammation. J Immunol (2010) 184(5):2655–62.10.4049/jimmunol.0903359 PubMed DOI
Krispin A, Bledi Y, Atallah M, Trahtemberg U, Verbovetski I, Nahari E, et al. Apoptotic cell thrombospondin-1 and heparin-binding domain lead to dendritic-cell phagocytic and tolerizing states. Blood (2006) 108(10):3580–9.10.1182/blood-2006-03-013334 PubMed DOI
Galluzzi L, Bravo-San Pedro JM, Vitale I, Aaronson SA, Abrams JM, Adam D, et al. Essential versus accessory aspects of cell death: recommendations of the NCCD 2015. Cell Death Differ (2015) 22(1):58–73.10.1038/cdd.2014.137 PubMed DOI PMC
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(5):581–7.10.1038/nm0598-581 PubMed DOI
Gough MJ, Melcher AA, Crittenden MR, Sanchez-Perez L, Voellmy R, Vile RG. Induction of cell stress through gene transfer of an engineered heat shock transcription factor enhances tumor immunogenicity. Gene Ther (2004) 11(13):1099–104.10.1038/sj.gt.3302274 PubMed DOI
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(11):4839–45.10.1182/blood-2006-10-054221 PubMed DOI PMC
Casares N, Pequignot MO, Tesniere A, Ghiringhelli F, Roux S, Chaput N, et al. Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J Exp Med (2005) 202(12):1691–701.10.1084/jem.20050915 PubMed DOI PMC
Kroemer G, Galluzzi L, Kepp O, Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol (2013) 31:51–72.10.1146/annurev-immunol-032712-100008 PubMed DOI
Garg AD, Dudek-Peric AM, Romano E, Agostinis P. Immunogenic cell death. Int J Dev Biol (2015) 59:131–40.10.1387/ijdb.150061pa PubMed DOI
Kepp O, Senovilla L, Vitale I, Vacchelli E, Adjemian S, Agostinis P, et al. Consensus guidelines for the detection of immunogenic cell death. Oncoimmunology (2014) 3(9):e955691.10.4161/21624011.2014.955691 PubMed DOI PMC
Dudek AM, Martin S, Garg AD, Agostinis P. Immature, semi-mature, and fully mature dendritic cells: toward a DC-cancer cells interface that augments anticancer immunity. Front Immunol (2014) 4:438.10.3389/fimmu.2013.00438 PubMed DOI PMC
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(4):729–41.10.1016/j.immuni.2013.03.003 PubMed DOI
Zhang JG, Czabotar PE, Policheni AN, Caminschi I, Wan SS, Kitsoulis S, et al. The dendritic cell receptor Clec9A binds damaged cells via exposed actin filaments. Immunity (2012) 36(4):646–57.10.1016/j.immuni.2012.03.009 PubMed DOI
Garnett CT, Palena C, Chakraborty M, Tsang KY, Schlom J, Hodge JW. Sublethal irradiation of human tumor cells modulates phenotype resulting in enhanced killing by cytotoxic T lymphocytes. Cancer Res (2004) 64(21):7985–94.10.1158/0008-5472.CAN-04-1525 PubMed DOI
Hodge JW, Garnett CT, Farsaci B, Palena C, Tsang KY, Ferrone S, et al. Chemotherapy-induced immunogenic modulation of tumor cells enhances killing by cytotoxic T lymphocytes and is distinct from immunogenic cell death. Int J Cancer (2013) 133(3):624–36.10.1002/ijc.28070 PubMed DOI PMC
Gameiro SR, Jammeh ML, Wattenberg MM, Tsang KY, Ferrone S, Hodge JW. Radiation-induced immunogenic modulation of tumor enhances antigen processing and calreticulin exposure, resulting in enhanced T-cell killing. Oncotarget (2014) 5(2):403–16.10.18632/oncotarget.1719 PubMed DOI PMC
Michaud M, Martins I, Sukkurwala AQ, Adjemian S, Ma Y, Pellegatti P, et al. Autophagy-dependent anticancer immune responses induced by chemotherapeutic agents in mice. Science (2011) 334(6062):1573–7.10.1126/science.1208347 PubMed DOI
Garg AD, Dudek AM, Agostinis P. Calreticulin surface exposure is abrogated in cells lacking, chaperone-mediated autophagy-essential gene, LAMP2A. Cell Death Dis (2013) 4:e826.10.1038/cddis.2013.372 PubMed DOI PMC
Martins I, Wang Y, Michaud M, Ma Y, Sukkurwala AQ, Shen S, et al. Molecular mechanisms of ATP secretion during immunogenic cell death. Cell Death Differ (2014) 21(1):79–91.10.1038/cdd.2013.75 PubMed DOI PMC
Kazama H, Ricci JE, Herndon JM, Hoppe G, Green DR, Ferguson TA. Induction of immunological tolerance by apoptotic cells requires caspase-dependent oxidation of high-mobility group box-1 protein. Immunity (2008) 29(1):21–32.10.1016/j.immuni.2008.05.013 PubMed DOI PMC
Jube S, Rivera Z, Bianchi ME, Powers A, Wang E, Pagano IS, et al. Cancer cell secretion of the DAMP protein HMGB1 supports progression in malignant mesothelioma. Cancer Res (2012) 72(13):3290–301.10.1158/0008-5472.CAN-11-3481 PubMed DOI PMC
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(2):215–21.10.1007/s00262-011-1184-2 PubMed DOI PMC
Lancaster GI, Febbraio MA. Exosome-dependent trafficking of HSP70: a novel secretory pathway for cellular stress proteins. J Biol Chem (2005) 280(24):23349–55.10.1074/jbc.M502017200 PubMed DOI
Mambula SS, Calderwood SK. Heat shock protein 70 is secreted from tumor cells by a nonclassical pathway involving lysosomal endosomes. J Immunol (2006) 177(11):7849–57.10.4049/jimmunol.177.11.7849 PubMed DOI
Vega VL, Rodriguez-Silva M, Frey T, Gehrmann M, Diaz JC, Steinem C, et al. Hsp70 translocates into the plasma membrane after stress and is released into the extracellular environment in a membrane-associated form that activates macrophages. J Immunol (2008) 180(6):4299–307.10.4049/jimmunol.180.6.4299 PubMed DOI
Kotter B, Frey B, Winderl M, Rubner Y, Scheithauer H, Sieber R, et al. The in vitro immunogenic potential of caspase-3 proficient breast cancer cells with basal low immunogenicity is increased by hypofractionated irradiation. Radiat Oncol (2015) 10(1):197.10.1186/s13014-015-0506-5 PubMed DOI PMC
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(2):272–9.10.1002/ijc.2910610222 PubMed DOI
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(12):5238–47.10.1158/0008-5472.CAN-04-3804 PubMed DOI PMC
Panaretakis T, Kepp O, Brockmeier U, Tesniere A, Bjorklund AC, Chapman DC, et al. Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death. EMBO J (2009) 28(5):578–90.10.1038/emboj.2009.1 PubMed DOI PMC
Madeo F, Durchschlag M, Kepp O, Panaretakis T, Zitvogel L, Frohlich KU, et al. Phylogenetic conservation of the preapoptotic calreticulin exposure pathway from yeast to mammals. Cell Cycle (2009) 8(4):639–42.10.4161/cc.8.4.7794 PubMed DOI
Martin S, Dudek-Peric AM, Maes H, Garg AD, Gabrysiak M, Demirsoy S, et al. Concurrent MEK and autophagy inhibition is required to restore cell death associated danger-signalling in vemurafenib-resistant melanoma cells. Biochem Pharmacol (2015) 93(3):290–304.10.1016/j.bcp.2014.12.003 PubMed DOI
Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, et al. STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res (2015) 43(Database issue):D447–52.10.1093/nar/gku1003 PubMed DOI PMC
Dudek AM, Garg AD, Krysko DV, De Ruysscher D, Agostinis P. Inducers of immunogenic cancer cell death. Cytokine Growth Factor Rev (2013) 24(4):319–33.10.1016/j.cytogfr.2013.01.005 PubMed DOI
Bezu L, Gomes-de-Silva LC, Dewitte H, Breckpot K, Fucikova J, Spisek R, et al. Combinatorial strategies for the induction of immunogenic cell death. Front Immunol (2015) 6:187.10.3389/fimmu.2015.00187 PubMed DOI PMC
Siurala M, Bramante S, Vassilev L, Hirvinen M, Parviainen S, Tahtinen S, et al. Oncolytic adenovirus and doxorubicin-based chemotherapy results in synergistic antitumor activity against soft-tissue sarcoma. Int J Cancer (2015) 136(4):945–54.10.1002/ijc.29048 PubMed DOI
Menger L, Vacchelli E, Adjemian S, Martins I, Ma Y, Shen S, et al. Cardiac glycosides exert anticancer effects by inducing immunogenic cell death. Sci Transl Med (2012) 4(143):143ra99.10.1126/scitranslmed.3003807 PubMed DOI
Panaretakis T, Joza N, Modjtahedi N, Tesniere A, Vitale I, Durchschlag M, et al. The co-translocation of ERp57 and calreticulin determines the immunogenicity of cell death. Cell Death Differ (2008) 15(9):1499–509.10.1038/cdd.2008.67 PubMed DOI
Tufi R, Panaretakis T, Bianchi K, Criollo A, Fazi B, Di Sano F, et al. Reduction of endoplasmic reticulum Ca2+ levels favors plasma membrane surface exposure of calreticulin. Cell Death Differ (2008) 15(2):274–82.10.1038/sj.cdd.4402275 PubMed DOI
Martins I, Kepp O, Schlemmer F, Adjemian S, Tailler M, Shen S, et al. Restoration of the immunogenicity of cisplatin-induced cancer cell death by endoplasmic reticulum stress. Oncogene (2011) 30(10):1147–58.10.1038/onc.2010.500 PubMed DOI
Verfaillie T, Rubio N, Garg AD, Bultynck G, Rizzuto R, Decuypere JP, et al. PERK is required at the ER-mitochondrial contact sites to convey apoptosis after ROS-based ER stress. Cell Death Differ (2012) 19(11):1880–91.10.1038/cdd.2012.74 PubMed DOI PMC
Galluzzi L, Bravo-San Pedro JM, Kroemer G. Organelle-specific initiation of cell death. Nat Cell Biol (2014) 16(8):728–36.10.1038/ncb3005 PubMed DOI
Chaurio RA, Munoz LE, Maueroder C, Janko C, Harrer T, Furnrohr BG, et al. The progression of cell death affects the rejection of allogeneic tumors in immune-competent mice – implications for cancer therapy. Front Immunol (2014) 5:560.10.3389/fimmu.2014.00560 PubMed DOI PMC
Garg AD, Maes H, van Vliet AR, Agostinis P. Targeting the hallmarks of cancer with therapy-induced endoplasmic reticulum (ER) stress. Mol Cell Oncol (2015) 2(1):e975089.10.4161/23723556.2014.975089 PubMed DOI PMC
van Vliet AR, Martin S, Garg AD, Agostinis P. The PERKs of damage-associated molecular patterns mediating cancer immunogenicity: from sensor to the plasma membrane and beyond. Semin Cancer Biol (2015) 33:74–85.10.1016/j.semcancer.2015.03.010 PubMed DOI
Sukkurwala AQ, Adjemian S, Senovilla L, Michaud M, Spaggiari S, Vacchelli E, et al. Screening of novel immunogenic cell death inducers within the NCI mechanistic diversity set. Oncoimmunology (2014) 3:e28473.10.4161/onci.28473 PubMed DOI PMC
Wong DY, Ong WW, Ang WH. Induction of immunogenic cell death by chemotherapeutic platinum complexes. Angew Chem Int Ed Engl (2015) 54(22):6483–7.10.1002/anie.201500934 PubMed DOI
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(11):1301–9.10.1038/nm.3708 PubMed DOI
Ramakrishnan R, Gabrilovich DI. The role of mannose-6-phosphate receptor and autophagy in influencing the outcome of combination therapy. Autophagy (2013) 9(4):615–6.10.4161/auto.23485 PubMed DOI PMC
Kaminski JM, Shinohara E, Summers JB, Niermann KJ, Morimoto A, Brousal J. The controversial abscopal effect. Cancer Treat Rev (2005) 31(3):159–72.10.1016/j.ctrv.2005.03.004 PubMed DOI
Golden EB, Frances D, Pellicciotta I, Demaria S, Helen Barcellos-Hoff M, Formenti SC. Radiation fosters dose-dependent and chemotherapy-induced immunogenic cell death. Oncoimmunology (2014) 3:e28518.10.4161/onci.28518 PubMed DOI PMC
Garrido G, Rabasa A, Sanchez B, Lopez MV, Blanco R, Lopez A, et al. Induction of immunogenic apoptosis by blockade of epidermal growth factor receptor activation with a specific antibody. J Immunol (2011) 187(10):4954–66.10.4049/jimmunol.1003477 PubMed DOI
Bugaut H, Bruchard M, Berger H, Derangere V, Odoul L, Euvrard R, et al. Bleomycin exerts ambivalent antitumor immune effect by triggering both immunogenic cell death and proliferation of regulatory T cells. PLoS One (2013) 8(6):e65181.10.1371/journal.pone.0065181 PubMed DOI PMC
Diaconu I, Cerullo V, Hirvinen ML, Escutenaire S, Ugolini M, Pesonen SK, et al. Immune response is an important aspect of the antitumor effect produced by a CD40L-encoding oncolytic adenovirus. Cancer Res (2012) 72(9):2327–38.10.1158/0008-5472.CAN-11-2975 PubMed DOI
Hemminki O, Parviainen S, Juhila J, Turkki R, Linder N, Lundin J, et al. Immunological data from cancer patients treated with Ad5/3-E2F-Delta24-GMCSF suggests utility for tumor immunotherapy. Oncotarget (2015) 6(6):4467–81.10.18632/oncotarget.2901 PubMed DOI PMC
Sun C, Wang H, Mao S, Liu J, Li S, Wang J. Reactive oxygen species involved in CT26 immunogenic cell death induced by Clostridium difficile toxin B. Immunol Lett (2015) 164(2):65–71.10.1016/j.imlet.2015.02.007 PubMed DOI
Miyamoto S, Inoue H, Nakamura T, Yamada M, Sakamoto C, Urata Y, et al. Coxsackievirus B3 Is an oncolytic virus with immunostimulatory properties that is active against lung Adenocarcinoma. Cancer Res (2012) 72(10):2609–21.10.1158/0008-5472.CAN-11-3185 PubMed DOI
Vacchelli E, Eggermont A, Sautes-Fridman C, Galon J, Zitvogel L, Kroemer G, et al. Trial watch: oncolytic viruses for cancer therapy. Oncoimmunology (2013) 2(6):e24612.10.4161/onci.22789 PubMed DOI PMC
Schiavoni G, Sistigu A, Valentini M, Mattei F, Sestili P, Spadaro F, et al. Cyclophosphamide synergizes with type I interferons through systemic dendritic cell reactivation and induction of immunogenic tumor apoptosis. Cancer Res (2011) 71(3):768–78.10.1158/0008-5472.CAN-10-2788 PubMed DOI
Viaud S, Saccheri F, Mignot G, Yamazaki T, Daillere R, Hannani D, et al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science (2013) 342(6161):971–6.10.1126/science.1240537 PubMed DOI PMC
Fucikova J, Moserova I, Truxova I, Hermanova I, Vancurova I, Partlova S, et al. High hydrostatic pressure induces immunogenic cell death in human tumor cells. Int J Cancer (2014) 135(5):1165–77.10.1002/ijc.28766 PubMed DOI
Adkins I, Fucikova J, Garg AD, Agostinis P, Spisek R. Physical modalities inducing immunogenic tumor cell death for cancer immunotherapy. Oncoimmunology (2014) 3:e968434.10.4161/21624011.2014.968434 PubMed DOI PMC
Weiss EM, Meister S, Janko C, Ebel N, Schlucker E, Meyer-Pittroff R, et al. High hydrostatic pressure treatment generates inactivated mammalian tumor cells with immunogeneic features. J Immunotoxicol (2010) 7(3):194–204.10.3109/15476911003657414 PubMed DOI
Garg AD, Agostinis P. ER stress, autophagy and immunogenic cell death in photodynamic therapy-induced anti-cancer immune responses. Photochem Photobiol Sci (2014) 13(3):474–87.10.1039/c3pp50333j PubMed DOI
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(15):6526–39.10.18632/oncotarget.2310 PubMed DOI PMC
Zamarin D, Holmgaard RB, Subudhi SK, Park JS, Mansour M, Palese P, et al. Localized oncolytic virotherapy overcomes systemic tumor resistance to immune checkpoint blockade immunotherapy. Sci Transl Med (2014) 6(226):226ra32.10.1126/scitranslmed.3008095 PubMed DOI PMC
Chen HM, Wang PH, Chen SS, Wen CC, Chen YH, Yang WC, et al. Shikonin induces immunogenic cell death in tumor cells and enhances dendritic cell-based cancer vaccine. Cancer Immunol Immunother (2012) 61(11):1989–2002.10.1007/s00262-012-1258-9 PubMed DOI PMC
Korbelik M, Dougherty GJ. Photodynamic therapy-mediated immune response against subcutaneous mouse tumors. Cancer Res (1999) 59(8):1941–6. PubMed
Krosl G, Korbelik M, Dougherty GJ. Induction of immune cell infiltration into murine SCCVII tumour by photofrin-based photodynamic therapy. Br J Cancer (1995) 71(3):549–55.10.1038/bjc.1995.108 PubMed DOI PMC
Korbelik M, Stott B, Sun J. Photodynamic therapy-generated vaccines: relevance of tumour cell death expression. Br J Cancer (2007) 97(10):1381–7.10.1038/sj.bjc.6604059 PubMed DOI PMC
Korbelik M, Zhang W, Merchant S. Involvement of damage-associated molecular patterns in tumor response to photodynamic therapy: surface expression of calreticulin and high-mobility group box-1 release. Cancer Immunol Immunother (2011) 60(10):1431–7.10.1007/s00262-011-1047-x PubMed DOI PMC
Duewell P, Steger A, Lohr H, Bourhis H, Hoelz H, Kirchleitner SV, et al. RIG-I-like helicases induce immunogenic cell death of pancreatic cancer cells and sensitize tumors toward killing by CD8 T cells. Cell Death Differ (2014) 21(12):1825–37.10.1038/cdd.2014.96 PubMed DOI PMC
West AC, Mattarollo SR, Shortt J, Cluse LA, Christiansen AJ, Smyth MJ, et al. An intact immune system is required for the anticancer activities of histone deacetylase inhibitors. Cancer Res (2013) 73(24):7265–76.10.1158/0008-5472.CAN-13-0890 PubMed DOI
Yang Y, Li XJ, Chen Z, Zhu XX, Wang J, Zhang LB, et al. Wogonin induced calreticulin/annexin A1 exposure dictates the immunogenicity of cancer cells in a PERK/AKT dependent manner. PLoS One (2012) 7(12):e50811.10.1371/journal.pone.0050811 PubMed DOI PMC
Panzarini E, Inguscio V, Fimia GM, Dini L. Rose Bengal acetate photodynamic therapy (RBAc-PDT) induces exposure and release of damage-associated molecular patterns (DAMPs) in human HeLa cells. PLoS One (2014) 9(8):e105778.10.1371/journal.pone.0105778 PubMed DOI PMC
Molinari R, D’Eliseo D, Manzi L, Zolla L, Velotti F, Merendino N. The n3-polyunsaturated fatty acid docosahexaenoic acid induces immunogenic cell death in human cancer cell lines via pre-apoptotic calreticulin exposure. Cancer Immunol Immunother (2011) 60(10):1503–7.10.1007/s00262-011-1074-7 PubMed DOI PMC
D’Eliseo D, Manzi L, Velotti F. Capsaicin as an inducer of damage-associated molecular patterns (DAMPs) of immunogenic cell death (ICD) in human bladder cancer cells. Cell Stress Chaperones (2013) 18(6):801–8.10.1007/s12192-013-0422-2 PubMed DOI PMC
Gilardini Montani MS, D’Eliseo D, Cirone M, Di Renzo L, Faggioni A, Santoni A, et al. Capsaicin-mediated apoptosis of human bladder cancer cells activates dendritic cells via CD91. Nutrition (2015) 31(4):578–81.10.1016/j.nut.2014.05.005 PubMed DOI
Janeway C. Immunobiology: The Immune System in Health and Disease. 6th ed New York, NY: Garland Science; (2005). 823 p.
Fucikova J, Kralikova P, Fialova A, Brtnicky T, Rob L, Bartunkova J, et al. Human tumor cells killed by anthracyclines induce a tumor-specific immune response. Cancer Res (2011) 71(14):4821–33.10.1158/0008-5472.CAN-11-0950 PubMed DOI
Krysko DV, Kaczmarek A, Krysko O, Heyndrickx L, Woznicki J, Bogaert P, et al. TLR-2 and TLR-9 are sensors of apoptosis in a mouse model of doxorubicin-induced acute inflammation. Cell Death Differ (2011) 18(8):1316–25.10.1038/cdd.2011.4 PubMed DOI PMC
Tseng LM, Liu CY, Chang KC, Chu PY, Shiau CW, Chen KF. CIP2A is a target of bortezomib in human triple negative breast cancer cells. Breast Cancer Res (2012) 14(2):R68.10.1186/bcr3175 PubMed DOI PMC
Davies AM, Lara PN, Jr, Mack PC, Gandara DR. Incorporating bortezomib into the treatment of lung cancer. Clin Cancer Res (2007) 13(15 Pt 2):s4647–51.10.1158/1078-0432.CCR-07-0334 PubMed DOI
Huang T, Li S, Li G, Tian Y, Wang H, Shi L, et al. Utility of Clostridium difficile toxin B for inducing anti-tumor immunity. PLoS One (2014) 9(10):e110826.10.1371/journal.pone.0110826 PubMed DOI PMC
Bravim F, de Freitas JM, Fernandes AA, Fernandes PM. High hydrostatic pressure and the cell membrane: stress response of Saccharomyces cerevisiae. Ann N Y Acad Sci (2010) 1189:127–32.10.1111/j.1749-6632.2009.05182.x PubMed DOI
Senovilla L, Vitale I, Martins I, Tailler M, Pailleret C, Michaud M, et al. An immunosurveillance mechanism controls cancer cell ploidy. Science (2012) 337(6102):1678–84.10.1126/science.1224922 PubMed DOI
Korbelik M. Cancer vaccines generated by photodynamic therapy. Photochem Photobiol Sci (2011) 10(5):664–9.10.1039/c0pp00343c PubMed DOI
Garg AD, Krysko DV, Vandenabeele P, Agostinis P. DAMPs and PDT-mediated photo-oxidative stress: exploring the unknown. Photochem Photobiol Sci (2011) 10(5):670–80.10.1039/c0pp00294a PubMed DOI
Chen J, Xie J, Jiang Z, Wang B, Wang Y, Hu X. Shikonin and its analogs inhibit cancer cell glycolysis by targeting tumor pyruvate kinase-M2. Oncogene (2011) 30(42):4297–306.10.1038/onc.2011.137 PubMed DOI
Tsai CF, Yeh WL, Huang SM, Tan TW, Lu DY. Wogonin induces reactive oxygen species production and cell apoptosis in human glioma cancer cells. Int J Mol Sci (2012) 13(8):9877–92.10.3390/ijms13089877 PubMed DOI PMC
Sanovic R, Verwanger T, Hartl A, Krammer B. Low dose hypericin-PDT induces complete tumor regression in BALB/c mice bearing CT26 colon carcinoma. Photodiagnosis Photodyn Ther (2011) 8(4):291–6.10.1016/j.pdpdt.2011.04.003 PubMed DOI
Garg AD, Krysko DV, Vandenabeele P, Agostinis P. The emergence of phox-ER stress induced immunogenic apoptosis. OncoImmunology (2012) 1(5):787–9.10.4161/onci.19750 PubMed DOI PMC
Liu Z, Zhang HM, Yuan J, Ye X, Taylor GA, Yang D. The immunity-related GTPase Irgm3 relieves endoplasmic reticulum stress response during Coxsackievirus B3 infection via a PI3K/Akt dependent pathway. Cell Microbiol (2012) 14(1):133–46.10.1111/j.1462-5822.2011.01708.x PubMed DOI PMC
Bian J, Wang K, Kong X, Liu H, Chen F, Hu M, et al. Caspase- and p38-MAPK-dependent induction of apoptosis in A549 lung cancer cells by Newcastle disease virus. Arch Virol (2011) 156(8):1335–44.10.1007/s00705-011-0987-y PubMed DOI
Garg AD, De Ruysscher D, Agostinis P. Immunological metagene signatures derived from immunogenic cancer cell death associate with improved survival of patients with lung, breast or ovarian malignancies: a large-scale meta-analysis. Oncoimmunology (2015).10.1080/2162402X.2015.1069938 PubMed DOI PMC
Galluzzi L, Kepp O, Kroemer G. Enlightening the impact of immunogenic cell death in photodynamic cancer therapy. EMBO J (2012) 31(5):1055–7.10.1038/emboj.2012.2 PubMed DOI PMC
Galluzzi L, Pietrocola F, Bravo-San Pedro JM, Amaravadi RK, Baehrecke EH, Cecconi F, et al. Autophagy in malignant transformation and cancer progression. EMBO J (2015) 34(7):856–80.10.15252/embj.201490784 PubMed DOI PMC
Mattarollo SR, Loi S, Duret H, Ma Y, Zitvogel L, Smyth MJ. Pivotal role of innate and adaptive immunity in anthracycline chemotherapy of established tumors. Cancer Res (2011) 71(14):4809–20.10.1158/0008-5472.CAN-11-0753 PubMed DOI
Lin TJ, Lin HT, Chang WT, Mitapalli SP, Hsiao PW, Yin SY, et al. Shikonin-enhanced cell immunogenicity of tumor vaccine is mediated by the differential effects of DAMP components. Mol Cancer (2015) 14:174.10.1186/s12943-015-0435-9 PubMed DOI PMC
Ma Y, Aymeric L, Locher C, Mattarollo SR, Delahaye NF, Pereira P, et al. Contribution of IL-17-producing gamma delta T cells to the efficacy of anticancer chemotherapy. J Exp Med (2011) 208(3):491–503.10.1084/jem.20100269 PubMed DOI PMC
Yang H, Yamazaki T, Pietrocola F, Zhou H, Zitvogel L, Ma Y, et al. STAT3 inhibition enhances the therapeutic efficacy of immunogenic chemotherapy by stimulating type 1 interferon production by cancer cells. Cancer Res (2015) 75(18):3812–22.10.1158/0008-5472.CAN-15-1122 PubMed DOI
Ciampricotti M, Hau CS, Doornebal CW, Jonkers J, de Visser KE. Chemotherapy response of spontaneous mammary tumors is independent of the adaptive immune system. Nat Med (2012) 18(3):344–6.10.1038/nm.2652 PubMed DOI
Gould SE, Junttila MR, de Sauvage FJ. Translational value of mouse models in oncology drug development. Nat Med (2015) 21(5):431–9.10.1038/nm.3853 PubMed DOI
Tesniere A, Schlemmer F, Boige V, Kepp O, Martins I, Ghiringhelli F, et al. Immunogenic death of colon cancer cells treated with oxaliplatin. Oncogene (2010) 29(4):482–91.10.1038/onc.2009.356 PubMed DOI
Hannesdottir L, Tymoszuk P, Parajuli N, Wasmer MH, Philipp S, Daschil N, et al. Lapatinib and doxorubicin enhance the Stat1-dependent antitumor immune response. Eur J Immunol (2013) 43(10):2718–29.10.1002/eji.201242505 PubMed DOI
Michaud M, Xie X, Bravo-San Pedro JM, Zitvogel L, White E, Kroemer G. An autophagy-dependent anticancer immune response determines the efficacy of melanoma chemotherapy. Oncoimmunology (2014) 3(7):e944047.10.4161/21624011.2014.944047 PubMed DOI PMC
Demaria S, Santori FR, Ng B, Liebes L, Formenti SC, Vukmanovic S. Select forms of tumor cell apoptosis induce dendritic cell maturation. J Leukoc Biol (2005) 77(3):361–8.10.1189/jlb.0804478 PubMed DOI
Schumacher LY, Vo DD, Garban HJ, Comin-Anduix B, Owens SK, Dissette VB, et al. Immunosensitization of tumor cells to dendritic cell-activated immune responses with the proteasome inhibitor bortezomib (PS-341, Velcade). J Immunol (2006) 176(8):4757–65.10.4049/jimmunol.176.8.4757 PubMed DOI
Chang CL, Hsu YT, Wu CC, Yang YC, Wang C, Wu TC, et al. Immune mechanism of the antitumor effects generated by bortezomib. J Immunol (2012) 189(6):3209–20.10.4049/jimmunol.1103826 PubMed DOI
van der Most RG, Currie AJ, Mahendran S, Prosser A, Darabi A, Robinson BW, et al. Tumor eradication after cyclophosphamide depends on concurrent depletion of regulatory T cells: a role for cycling TNFR2-expressing effector-suppressor T cells in limiting effective chemotherapy. Cancer Immunol Immunother (2009) 58(8):1219–28.10.1007/s00262-008-0628-9 PubMed DOI PMC
Obeid M, Panaretakis T, Joza N, Tufi R, Tesniere A, van Endert P, et al. Calreticulin exposure is required for the immunogenicity of gamma-irradiation and UVC light-induced apoptosis. Cell Death Differ (2007) 14(10):1848–50.10.1038/sj.cdd.4402201 PubMed DOI
Carr-Brendel V, Markovic D, Smith M, Taylor-Papadimitriou J, Cohen EP. Immunity to breast cancer in mice immunized with X-irradiated breast cancer cells modified to secrete IL-12. J Immunother (1999) 22(5):415–22.10.1097/00002371-199909000-00005 PubMed DOI
Strome SE, Voss S, Wilcox R, Wakefield TL, Tamada K, Flies D, et al. Strategies for antigen loading of dendritic cells to enhance the antitumor immune response. Cancer Res (2002) 62(6):1884–9. PubMed
Prasad SJ, Farrand KJ, Matthews SA, Chang JH, McHugh RS, Ronchese F. Dendritic cells loaded with stressed tumor cells elicit long-lasting protective tumor immunity in mice depleted of CD4+CD25+ regulatory T cells. J Immunol (2005) 174(1):90–8.10.4049/jimmunol.174.1.90 PubMed DOI
Yang H, Zhou P, Huang H, Chen D, Ma N, Cui QC, et al. Shikonin exerts antitumor activity via proteasome inhibition and cell death induction in vitro and in vivo. Int J Cancer (2009) 124(10):2450–9.10.1002/ijc.24195 PubMed DOI PMC
Sharma P, Allison JP. The future of immune checkpoint therapy. Science (2015) 348(6230):56–61.10.1126/science.aaa8172 PubMed DOI
Viney M, Lazarou L, Abolins S. The laboratory mouse and wild immunology. Parasite Immunol (2015) 37(5):267–73.10.1111/pim.12150 PubMed DOI
Davis MM. A prescription for human immunology. Immunity (2008) 29(6):835–8.10.1016/j.immuni.2008.12.003 PubMed DOI PMC
Mestas J, Hughes CC. Of mice and not men: differences between mouse and human immunology. J Immunol (2004) 172(5):2731–8.10.4049/jimmunol.172.5.2731 PubMed DOI
Tubiana M. Klaas Breur medal lecture 1985. The growth and progression of human tumors: implications for management strategy. Radiother Oncol (1986) 6(3):167–84.10.1016/S0167-8140(86)80151-7 PubMed DOI
Klein CA. Parallel progression of primary tumours and metastases. Nat Rev Cancer (2009) 9(4):302–12.10.1038/nrc2627 PubMed DOI
Yamazaki T, Hannani D, Poirier-Colame V, Ladoire S, Locher C, Sistigu A, et al. Defective immunogenic cell death of HMGB1-deficient tumors: compensatory therapy with TLR4 agonists. Cell Death Differ (2014) 21(1):69–78.10.1038/cdd.2013.72 PubMed DOI PMC
Loi S, Pommey S, Haibe-Kains B, Beavis PA, Darcy PK, Smyth MJ, et al. CD73 promotes anthracycline resistance and poor prognosis in triple negative breast cancer. Proc Natl Acad Sci U S A (2013) 110(27):11091–6.10.1073/pnas.1222251110 PubMed DOI PMC
Shalapour S, Font-Burgada J, Di Caro G, Zhong Z, Sanchez-Lopez E, Dhar D, et al. Immunosuppressive plasma cells impede T-cell-dependent immunogenic chemotherapy. Nature (2015) 521(7550):94–8.10.1038/nature14395 PubMed DOI PMC
De Boo S, Kopecka J, Brusa D, Gazzano E, Matera L, Ghigo D, et al. iNOS activity is necessary for the cytotoxic and immunogenic effects of doxorubicin in human colon cancer cells. Mol Cancer (2009) 8:108.10.1186/1476-4598-8-108 PubMed DOI PMC
Riganti C, Castella B, Kopecka J, Campia I, Coscia M, Pescarmona G, et al. Zoledronic acid restores doxorubicin chemosensitivity and immunogenic cell death in multidrug-resistant human cancer cells. PLoS One (2013) 8(4):e60975.10.1371/journal.pone.0060975 PubMed DOI PMC
Stoll G, Enot D, Mlecnik B, Galon J, Zitvogel L, Kroemer G. Immune-related gene signatures predict the outcome of neoadjuvant chemotherapy. Oncoimmunology (2014) 3(1):e27884.10.4161/onci.27884 PubMed DOI PMC
Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer (2012) 12(4):252–64.10.1038/nrc3239 PubMed DOI PMC
Galon J, Angell HK, Bedognetti D, Marincola FM. The continuum of cancer immunosurveillance: prognostic, predictive, and mechanistic signatures. Immunity (2013) 39(1):11–26.10.1016/j.immuni.2013.07.008 PubMed DOI
Fridman WH, Pages F, Sautes-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer (2012) 12(4):298–306.10.1038/nrc3245 PubMed DOI
Zitvogel L, Tesniere A, Kroemer G. Cancer despite immunosurveillance: immunoselection and immunosubversion. Nat Rev Immunol (2006) 6(10):715–27.10.1038/nri1936 PubMed DOI
Ladoire S, Penault-Llorca F, Senovilla L, Dalban C, Enot D, Locher C, et al. Combined evaluation of LC3B puncta and HMGB1 expression predicts residual risk of relapse after adjuvant chemotherapy in breast cancer. Autophagy (2015) 11(10):1878–90.10.1080/15548627.2015.1082022 PubMed DOI PMC
Kacerovska D, Pizinger K, Majer F, Smid F. Photodynamic therapy of nonmelanoma skin cancer with topical Hypericum perforatum extract – a pilot study. Photochem Photobiol (2008) 84(3):779–85.10.1111/j.1751-1097.2007.00260.x PubMed DOI
Rook AH, Wood GS, Duvic M, Vonderheid EC, Tobia A, Cabana B. A phase II placebo-controlled study of photodynamic therapy with topical hypericin and visible light irradiation in the treatment of cutaneous T-cell lymphoma and psoriasis. J Am Acad Dermatol (2010) 63(6):984–90.10.1016/j.jaad.2010.02.039 PubMed DOI
Koren H, Schenk GM, Jindra RH, Alth G, Ebermann R, Kubin A, et al. Hypericin in phototherapy. J Photochem Photobiol B (1996) 36(2):113–9.10.1016/S1011-1344(96)07357-5 PubMed DOI
Alecu M, Ursaciuc C, Halalau F, Coman G, Merlevede W, Waelkens E, et al. Photodynamic treatment of basal cell carcinoma and squamous cell carcinoma with hypericin. Anticancer Res (1998) 18(6B):4651–4. PubMed
Liikanen I, Koski A, Merisalo-Soikkeli M, Hemminki O, Oksanen M, Kairemo K, et al. Serum HMGB1 is a predictive and prognostic biomarker for oncolytic immunotherapy. Oncoimmunology (2015) 4(3):e989771.10.4161/2162402X.2014.989771 PubMed DOI PMC
Agostinis P, Berg K, Cengel KA, Foster TH, Girotti AW, Gollnick SO, et al. Photodynamic therapy of cancer: an update. CA Cancer J Clin (2011) 61(4):250–81.10.3322/caac.20114 PubMed DOI PMC
Suzuki Y, Mimura K, Yoshimoto Y, Watanabe M, Ohkubo Y, Izawa S, et al. Immunogenic tumor cell death induced by chemoradiotherapy in patients with esophageal squamous cell carcinoma. Cancer Res (2012) 72(16):3967–76.10.1158/0008-5472.CAN-12-0851 PubMed DOI
Zappasodi R, Pupa SM, Ghedini GC, Bongarzone I, Magni M, Cabras AD, et al. Improved clinical outcome in indolent B-cell lymphoma patients vaccinated with autologous tumor cells experiencing immunogenic death. Cancer Res (2010) 70(22):9062–72.10.1158/0008-5472.CAN-10-1825 PubMed DOI
Baitsch L, Fuertes-Marraco SA, Legat A, Meyer C, Speiser DE. The three main stumbling blocks for anticancer T cells. Trends Immunol (2012) 33(7):364–72.10.1016/j.it.2012.02.006 PubMed DOI
Redmond WL, Sherman LA. Peripheral tolerance of CD8 T lymphocytes. Immunity (2005) 22(3):275–84.10.1016/j.immuni.2005.01.010 PubMed DOI
Cole DK, Pumphrey NJ, Boulter JM, Sami M, Bell JI, Gostick E, et al. Human TCR-binding affinity is governed by MHC class restriction. J Immunol (2007) 178(9):5727–34.10.4049/jimmunol.178.9.5727 PubMed DOI
Schmid DA, Irving MB, Posevitz V, Hebeisen M, Posevitz-Fejfar A, Sarria JC, et al. Evidence for a TCR affinity threshold delimiting maximal CD8 T cell function. J Immunol (2010) 184(9):4936–46.10.4049/jimmunol.1000173 PubMed DOI
Zehn D, Bevan MJ. T cells with low avidity for a tissue-restricted antigen routinely evade central and peripheral tolerance and cause autoimmunity. Immunity (2006) 25(2):261–70.10.1016/j.immuni.2006.06.009 PubMed DOI PMC
Baumgaertner P, Jandus C, Rivals JP, Derre L, Lovgren T, Baitsch L, et al. Vaccination-induced functional competence of circulating human tumor-specific CD8 T-cells. Int J Cancer (2012) 130(11):2607–17.10.1002/ijc.26297 PubMed DOI
Gubin MM, Artyomov MN, Mardis ER, Schreiber RD. Tumor neoantigens: building a framework for personalized cancer immunotherapy. J Clin Invest (2015) 125(9):3413–21.10.1172/JCI80008 PubMed DOI PMC
Schumacher TN, Schreiber RD. Neoantigens in cancer immunotherapy. Science (2015) 348(6230):69–74.10.1126/science.aaa4971 PubMed DOI
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(7547):373–7.10.1038/nature14292 PubMed DOI PMC
Ochsenbein AF, Klenerman P, Karrer U, Ludewig B, Pericin M, Hengartner H, et al. Immune surveillance against a solid tumor fails because of immunological ignorance. Proc Natl Acad Sci U S A (1999) 96(5):2233–8.10.1073/pnas.96.5.2233 PubMed DOI PMC
Chu-Yuan H, Jing P, Yi-Sheng W, He-Ping P, Hui Y, Chu-Xiong Z, et al. The impact of chemotherapy-associated neutrophil/lymphocyte counts on prognosis of adjuvant chemotherapy in colorectal cancer. BMC Cancer (2013) 13:177.10.1186/1471-2407-13-177 PubMed DOI PMC
Inoges S, Rodriguez-Calvillo M, Zabalegui N, Lopez-Diaz de Cerio A, Villanueva H, Soria E, et al. Clinical benefit associated with idiotypic vaccination in patients with follicular lymphoma. J Natl Cancer Inst (2006) 98(18):1292–301.10.1093/jnci/djj358 PubMed DOI
Kakarla S, Gottschalk S. CAR T cells for solid tumors: armed and ready to go? Cancer J (2014) 20(2):151–5.10.1097/PPO.0000000000000032 PubMed DOI PMC
Consensus guidelines for the definition, detection and interpretation of immunogenic cell death
Trial watch: chemotherapy-induced immunogenic cell death in immuno-oncology
Induction of Tolerance and Immunity by Dendritic Cells: Mechanisms and Clinical Applications
Trial Watch: Toll-like receptor agonists in cancer immunotherapy
Trial watch: Peptide-based vaccines in anticancer therapy
Trial Watch: Immunostimulation with recombinant cytokines for cancer therapy
