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Review

Tumor-intrinsic determinants of immunogenic cell death modalities

ORCID Icon, & ORCID Icon
Article: 1893466 | Received 14 Jan 2021, Accepted 17 Feb 2021, Published online: 02 Mar 2021

References

  • Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science. 2011;331:1565–13.
  • Pfirschke C, Engblom C, Rickelt S, Cortez-Retamozo V, Garris C, Pucci F, Yamazaki T, Poirier-Colame V, Newton A, Redouane Y, et al. Immunogenic chemotherapy sensitizes tumors to checkpoint blockade therapy. Immunity. 2016;44(2):343–354.
  • Casares N, Pequignot MO, Tesniere A, Ghiringhelli F, Roux S, Chaput N, Schmitt E, Hamai A, Hervas-Stubbs S, Obeid M, et al. Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J Exp Med. 2005;202(12):1691–1701.
  • Lhuillier C, Rudqvist NP, Yamazaki T, Zhang T, Charpentier M, Galluzzi L, Dephoure N, Clement CC, Santambrogio L, Zhou XK, et al. Radiotherapy-exposed CD8+ and CD4+ neoantigens enhance tumor control. J Clin Invest. 2021.
  • Workenhe ST, Simmons G, Pol JG, Lichty BD, Halford W, Mossman KL. Immunogenic HSV mediated oncolysis shapes the antitumor immune response and contributes to therapeutic efficacy. Mol Ther. 2014;22:123–131.
  • Alzeibak R, Mishchenko TA, Shilyagina NY, Balalaeva IV, Vedunova MV, Krysko DV. Targeting immunogenic cancer cell death by photodynamic therapy: past, present and future. J Immunother Cancer. 2021;9(1).
  • Coppard C, Hannani D, Humbert M, Gauthier V, Plumas J, Merlin E, Gabert F, Chaperot L. In vitro PUVA treatment triggers calreticulin exposition and HMGB1 release by dying T lymphocytes in GVHD: new insights in extracorporeal photopheresis. J Clin Apher. 2019;34:450–460.
  • Tatsuno K, Yamazaki T, Hanlon D, Han P, Robinson E, Sobolev O, Yurter A, Rivera-Molina F, Arshad N, Edelson RL, et al. Extracorporeal photochemotherapy induces bona fide immunogenic cell death. Cell Death Dis. 2019;10(8):578.
  • Hodi FS, O’Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363(8):711–723.
  • Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, Segal NH, Ariyan CE, Gordon RA, Reed K, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med. 2013;369(2):122–133.
  • Schmid P, Adams S, Rugo HS, Schneeweiss A, Barrios CH, Iwata H, Diéras V, Hegg R, Im S-A, Shaw Wright G, et al. Atezolizumab and nab-paclitaxel in advanced triple-negative breast cancer. N Engl J Med. 2018;379(22):2108–2121.
  • Lévesque S, Le Naour J, Pietrocola F, Paillet J, Kremer M, Castoldi F, Baracco EE, Wang Y, Vacchelli E, Stoll G, et al. A synergistic triad of chemotherapy, immune checkpoint inhibitors, and caloric restriction mimetics eradicates tumors in mice. Oncoimmunology. 2019;8(11):e1657375.
  • Canon J, Rex K, Saiki AY, Mohr C, Cooke K, Bagal D, Gaida K, Holt T, Knutson CG, Koppada N, et al. The clinical KRAS(G12C) inhibitor AMG 510 drives anti-tumour immunity. Nature. 2019;575(7781):217–223.
  • Najafov A, Zervantonakis IK, Mookhtiar AK, Greninger P, March RJ, Egan RK, Luu HS, Stover DG, Matulonis UA, Benes CH, et al. BRAF and AXL oncogenes drive RIPK3 expression loss in cancer. PLoS Biol. 2018;16(8):e2005756.
  • Sallusto F, Cella M, Danieli C, Lanzavecchia A. Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J Exp Med. 1995;182:389–400.
  • Salmon H, Idoyaga J, Rahman A, Leboeuf M, Remark R, Jordan S, Casanova-Acebes M, Khudoynazarova M, Agudo J, Tung N, et al. Expansion and activation of CD103(+) dendritic cell progenitors at the tumor site enhances tumor responses to therapeutic PD-L1 and BRAF inhibition. Immunity. 2016;44(4):924–938.
  • Han P, Hanlon D, Arshad N, Lee JS, Tatsuno K, Robinson E, Filler R, Sobolev O, Cote C, Rivera-Molina F, et al. Platelet P-selectin initiates cross-presentation and dendritic cell differentiation in blood monocytes. Sci Adv. 2020;6(11):eaaz1580.
  • Chen DS, Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity. 2013;39:1–10.
  • Pol JG, Caudana P, Paillet J, Piaggio E, Kroemer G. Effects of interleukin-2 in immunostimulation and immunosuppression. J Exp Med. 2020;217(1).
  • Castro F, Cardoso AP, Gonçalves RM, Serre K, Oliveira MJ. Interferon-gamma at the crossroads of tumor immune surveillance or evasion. Front Immunol. 2018;9:847.
  • Montfort A, Colacios C, Levade T, Andrieu-Abadie N, Meyer N, Ségui B. The TNF paradox in cancer progression and immunotherapy. Front Immunol. 2019;10:1818.
  • Tokunaga R, Zhang W, Naseem M, Puccini A, Berger MD, Soni S, McSkane M, Baba H, Lenz HJ. CXCL9, CXCL10, CXCL11/CXCR3 axis for immune activation - A target for novel cancer therapy. Cancer Treat Rev. 2018;63:40–47.
  • Kägi D, Ledermann B, Bürki K, Seiler P, Odermatt B, Olsen KJ, Podack ER, Zinkernagel RM, Hengartner H. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature. 1994;369:31–37.
  • Van Den Broek ME, Kägi D, Ossendorp F, Toes R, Vamvakas S, Lutz WK, Melief CJ, Zinkernagel RM, Hengartner H. Decreased tumor surveillance in perforin-deficient mice. J Exp Med. 1996;184:1781–1790.
  • Ghorani E, Reading JL, Henry JY, Massy M, Rosenthal R, Turati V, Joshi K, Furness AJS, Ben AA, Saini SK, et al. The T cell differentiation landscape is shaped by tumour mutations in lung cancer. Nature Cancer. 2020;1(5):546–561.
  • Ozcan M, Janikovits J, Von Knebel Doeberitz M, Kloor M. Complex pattern of immune evasion in MSI colorectal cancer. Oncoimmunology. 2018;7:e1445453.
  • Rooney MS, Shukla SA, Wu CJ, Getz G, Hacohen N. Molecular and genetic properties of tumors associated with local immune cytolytic activity. Cell. 2015;160:48–61.
  • Chen S, Crabill GA, Pritchard TS, McMiller TL, Wei P, Pardoll DM, Pan F, Topalian SL. Mechanisms regulating PD-L1 expression on tumor and immune cells. J Immunother Cancer. 2019;7:305.
  • Labadie BW, Bao R, Luke JJ. Reimagining IDO pathway inhibition in cancer immunotherapy via downstream focus on the tryptophan-kynurenine-aryl hydrocarbon axis. Clin Cancer Res. 2019;25:1462–1471.
  • Garcia-Diaz A, Shin DS, Moreno BH, Saco J, Escuin-Ordinas H, Rodriguez GA, Zaretsky JM, Sun L, Hugo W, Wang X, et al. Interferon receptor signaling pathways regulating PD-L1 and PD-L2 expression. Cell Rep. 2017;19(6):1189–1201.
  • Moon JW, Kong SK, Kim BS, Kim HJ, Lim H, Noh K, Kim Y, Choi JW, Lee JH, Kim YS. IFNγ induces PD-L1 overexpression by JAK2/STAT1/IRF-1 signaling in EBV-positive gastric carcinoma. Sci Rep. 2017;7:17810.
  • Yang B, Liu T, Qu Y, Liu H, Zheng SG, Cheng B, Sun J. Progresses and perspectives of anti-PD-1/PD-L1 antibody therapy in head and neck cancers. Front Oncol. 2018;8:563.
  • Landsberg J, Kohlmeyer J, Renn M, Bald T, Rogava M, Cron M, Fatho M, Lennerz V, Wölfel T, Hölzel M, et al. Melanomas resist T-cell therapy through inflammation-induced reversible dedifferentiation. Nature. 2012;490(7420):412–416.
  • Ribas A, Tumeh PC. Cancer therapy: tumours switch to resist. Nature. 2012;490:347–348.
  • Hoek KS, Eichhoff OM, Schlegel NC, Döbbeling U, Kobert N, Schaerer L, Hemmi S, Dummer R. In vivo switching of human melanoma cells between proliferative and invasive states. Cancer Res. 2008;68:650–656.
  • Hölzel M, Bovier A, Tüting T. Plasticity of tumour and immune cells: a source of heterogeneity and a cause for therapy resistance? Nat Rev Cancer. 2013;13:365–376.
  • Ribas A. Adaptive immune resistance: how cancer protects from immune attack. Cancer Discov. 2015;5:915–919.
  • Vogelstein B, Papadopoulos N, Velculescu VE, Zhou S, Diaz LA Jr., Kinzler KW. Cancer genome landscapes. Science (New York, NY). 2013;339:1546–1558.
  • Reiter JG, Baretti M, Gerold JM, Makohon-Moore AP, Daud A, Iacobuzio-Donahue CA, Azad NS, Kinzler KW, Nowak MA, Vogelstein B. An analysis of genetic heterogeneity in untreated cancers. Nat Rev Cancer. 2019;19:639–650.
  • Zitvogel L, Tesniere A, Kroemer G. Cancer despite immunosurveillance: immunoselection and immunosubversion. Nat Rev Immunol. 2006;6:715–727.
  • Zaretsky JM, Garcia-Diaz A, Shin DS, Escuin-Ordinas H, Hugo W, Hu-Lieskovan S, Torrejon DY, Abril-Rodriguez G, Sandoval S, Barthly L, et al. Mutations associated with acquired resistance to PD-1 blockade in melanoma. N Engl J Med. 2016;375(9):819–829.
  • Li J, Byrne KT, Yan F, Yamazoe T, Chen Z, Baslan T, Richman LP, Lin JH, Sun YH, Rech AJ, et al. Tumor cell-intrinsic factors underlie heterogeneity of immune cell infiltration and response to immunotherapy. Immunity. 2018;49(1):178–93.e7.
  • Gentles AJ, Newman AM, Liu CL, Bratman SV, Feng W, Kim D, Nair VS, Xu Y, Khuong A, Hoang CD, et al. The prognostic landscape of genes and infiltrating immune cells across human cancers. Nat Med. 2015;21:938.
  • Wellenstein MD, De Visser KE. Cancer-cell-intrinsic mechanisms shaping the tumor immune landscape. Immunity. 2018;48:399–416.
  • Elgendy M, Sheridan C, Brumatti G, Martin SJ. Oncogenic Ras-induced expression of Noxa and Beclin-1 promotes autophagic cell death and limits clonogenic survival. Mol Cell. 2011;42:23–35.
  • Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell. 1997;88:593–602.
  • Luo J, Solimini NL, Elledge SJ. Principles of cancer therapy: oncogene and non-oncogene addiction. Cell. 2009;136:823–837.
  • Han C, Liu Z, Zhang Y, Shen A, Dong C, Zhang A, Moore C, Ren Z, Lu C, Cao X, et al. Tumor cells suppress radiation-induced immunity by hijacking caspase 9 signaling. Nat Immunol. 2020;21(5):546–554.
  • Ning X, Wang Y, Jing M, Sha M, Lv M, Gao P, Zhang R, Huang X, Feng JM, Jiang Z. Apoptotic caspases suppress type i interferon production via the cleavage of cGAS, MAVS, and IRF3. Mol Cell. 2019;74:19–31.e7.
  • Rodriguez-Ruiz ME, Buqué A, Hensler M, Chen J, Bloy N, Petroni G, Sato A, Yamazaki T, Fucikova J, Galluzzi L. Apoptotic caspases inhibit abscopal responses to radiation and identify a new prognostic biomarker for breast cancer patients. Oncoimmunology. 2019;8:e1655964.
  • Hanahan D, Weinberg Robert A. Hallmarks of cancer: the next generation. Cell. 2011;144:646–674.
  • Galluzzi L, Buqué A, Kepp O, Zitvogel L, Kroemer G. Immunogenic cell death in cancer and infectious disease. Nat Rev Immunol. 2017;17:97–111.
  • Igney FH, Krammer PH. Death and anti-death: tumour resistance to apoptosis. Nat Rev Cancer. 2002;2:277–288.
  • Xia T, Konno H, Ahn J, Barber GN. Deregulation of STING signaling in colorectal carcinoma constrains DNA damage responses and correlates with tumorigenesis. Cell Rep. 2016;14:282–297.
  • Shi S, Xu C, Fang X, Zhang Y, Li H, Wen W, Yang G. Expression profile of Tolllike receptors in human breast cancer. Mol Med Rep. 2020;21:786–794.
  • Zhu H, Xu W-Y, Hu Z, Zhang H, Shen Y, Lu S, Wei C, Wang Z-G. RNA virus receptor Rig-I monitors gut microbiota and inhibits colitis-associated colorectal cancer. J Exp Clin Cancer Res. 2017;36:2.
  • Ding HF, McGill G, Rowan S, Schmaltz C, Shimamura A, Fisher DE. Oncogene-dependent regulation of caspase activation by p53 protein in a cell-free system. J Biol Chem. 1998;273:28378–28383.
  • Amarante-Mendes GP, Finucane DM, Martin SJ, Cotter TG, Salvesen GS, Green DR. Anti-apoptotic oncogenes prevent caspase-dependent and independent commitment for cell death. Cell Death Differ. 1998;5:298–306.
  • Towers CG, Wodetzki D, Thorburn A. Autophagy and cancer: modulation of cell death pathways and cancer cell adaptations. J Cell Biol. 2019;jcb.201909033.
  • Galluzzi L, Pietrocola F, Bravo-San Pedro JM, Amaravadi RK, Baehrecke EH, Cecconi F, Codogno P, Debnath J, Gewirtz DA, Karantza V, et al. Autophagy in malignant transformation and cancer progression. EMBO J. 2015;34(7):856–880.
  • Young ARJ, Narita M, Ferreira M, Kirschner K, Sadaie M, Darot JFJ, Tavaré S, Arakawa S, Shimizu S, Watt FM, et al. Autophagy mediates the mitotic senescence transition. Genes Dev. 2009;23(7):798–803.
  • Liu H, He Z, Von Rütte T, Yousefi S, Hunger RE, Simon H-U. Down-regulation of autophagy-related protein 5 (ATG5) contributes to the pathogenesis of early-stage cutaneous melanoma. Sci Transl Med. 2013;5:202ra123–202ra123.
  • Green DR, Galluzzi L, Kroemer G. Mitochondria and the autophagy-inflammation-cell death axis in organismal aging. Science (New York, NY). 2011;333:1109–1112.
  • Takahashi Y, Hori T, Cooper TK, Liao J, Desai N, Serfass JM, Young MM, Park S, Izu Y, Wang H-G. Bif-1 haploinsufficiency promotes chromosomal instability and accelerates Myc-driven lymphomagenesis via suppression of mitophagy. Blood. 2013;121:1622–1632.
  • Rodriguez OC, Choudhury S, Kolukula V, Vietsch EE, Catania J, Preet A, Reynoso K, Bargonetti J, Wellstein A, Albanese C, et al. Dietary downregulation of mutant p53 levels via glucose restriction: mechanisms and implications for tumor therapy. Cell Cycle (Georgetown, Tex). 2012;11(23):4436–4446.
  • Choudhury S, Kolukula VK, Preet A, Albanese C, Avantaggiati ML. Dissecting the pathways that destabilize mutant p53: the proteasome or autophagy? Cell Cycle (Georgetown, Tex). 2013;12:1022–1029.
  • Isakson P, Bjørås M, Bøe SO, Simonsen A. Autophagy contributes to therapy-induced degradation of the PML/RARA oncoprotein. Blood. 2010;116:2324–2331.
  • Goussetis DJ, Gounaris E, Wu EJ, Vakana E, Sharma B, Bogyo M, Altman JK, Platanias LC. Autophagic degradation of the BCR-ABL oncoprotein and generation of antileukemic responses by arsenic trioxide. Blood. 2012;120:3555–3562.
  • Lee IH, Kawai Y, Fergusson MM, Rovira II, Bishop AJR, Motoyama N, Cao L, Finkel T. Atg7 modulates p53 activity to regulate cell cycle and survival during metabolic stress. Science (New York, NY). 2012;336:225–228.
  • Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, Levine B. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature. 1999;402:672–676.
  • Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, Troxel A, Rosen J, Eskelinen EL, Mizushima N, Ohsumi Y, et al. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest. 2003;112(12):1809–1820.
  • Yue Z, Jin S, Yang C, Levine AJ, Heintz N. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci U S A. 2003;100:15077–15082.
  • Mortensen M, Soilleux EJ, Djordjevic G, Tripp R, Lutteropp M, Sadighi-Akha E, Stranks AJ, Glanville J, Knight S, Jacobsen S-EW, et al. The autophagy protein Atg7 is essential for hematopoietic stem cell maintenance. J Exp Med. 2011;208(3):455–467.
  • Strohecker AM, Guo JY, Karsli-Uzunbas G, Price SM, Chen GJ, Mathew R, McMahon M, White E. Autophagy sustains mitochondrial glutamine metabolism and growth of BrafV600E-driven lung tumors. Cancer Discov. 2013;3:1272–1285.
  • Guo JY, Teng X, Laddha SV, Ma S, Van Nostrand SC, Yang Y, Khor S, Chan CS, Rabinowitz JD, White E. Autophagy provides metabolic substrates to maintain energy charge and nucleotide pools in Ras-driven lung cancer cells. Genes Dev. 2016;30:1704–1717.
  • Karsli-Uzunbas G, Guo JY, Price S, Teng X, Laddha SV, Khor S, Kalaany NY, Jacks T, Chan CS, Rabinowitz JD, et al. Autophagy is required for glucose homeostasis and lung tumor maintenance. Cancer Discov. 2014;4(8):914–927.
  • Katheder NS, Khezri R, O’Farrell F, Schultz SW, Jain A, Rahman MM, Schink KO, Theodossiou TA, Johansen T, Juhász G, et al. Microenvironmental autophagy promotes tumour growth. Nature. 2017;541(7637):417–420.
  • Rao S, Yang H, Penninger JM, Kroemer G. Autophagy in non-small cell lung carcinogenesis: a positive regulator of antitumor immunosurveillance. Autophagy. 2014;10:529–531.
  • Yang A, Rajeshkumar NV, Wang X, Yabuuchi S, Alexander BM, Chu GC, Von Hoff DD, Maitra A, Kimmelman AC. Autophagy is critical for pancreatic tumor growth and progression in tumors with p53 alterations. Cancer Discov. 2014;4:905–913.
  • Lazova R, Camp RL, Klump V, Siddiqui SF, Amaravadi RK, Pawelek JM. Punctate LC3B expression is a common feature of solid tumors and associated with proliferation, metastasis, and poor outcome. Clin Cancer Res. 2012;18:370–379.
  • Pietrocola F, Pol J, Kroemer G. Fasting improves anticancer immunosurveillance via autophagy induction in malignant cells. Cell Cycle. 2016;15:3327–3328.
  • Ma Y, Adjemian S, Mattarollo SR, Yamazaki T, Aymeric L, Yang H, Portela Catani JP, Hannani D, Duret H, Steegh K, et al. Anticancer chemotherapy-induced intratumoral recruitment and differentiation of antigen-presenting cells. Immunity. 2013;38(4):729–741.
  • 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:e944047.
  • Pietrocola F, Pol J, Vacchelli E, Rao S, Enot DP, Baracco EE, Levesque S, Castoldi F, Jacquelot N, Yamazaki T, et al. Caloric restriction mimetics enhance anticancer immunosurveillance. Cancer Cell. 2016;30(1):147–160.
  • Uhl M, Kepp O, Jusforgues-Saklani H, Vicencio JM, Kroemer G, Albert ML. Autophagy within the antigen donor cell facilitates efficient antigen cross-priming of virus-specific CD8+ T cells. Cell Death Differ. 2009;16:991–1005.
  • Xu X, Araki K, Li S, Han J-H, Ye L, Tan WG, Konieczny BT, Bruinsma MW, Martinez J, Pearce EL, et al. Autophagy is essential for effector CD8(+) T cell survival and memory formation. Nat Immunol. 2014;15(12):1152–1161.
  • Mgrditchian T, Arakelian T, Paggetti J, Noman MZ, Viry E, Moussay E, Van Moer K, Kreis S, Guerin C, Buart S, et al. Targeting autophagy inhibits melanoma growth by enhancing NK cells infiltration in a CCL5-dependent manner. Proceedings of the National Academy of Sciences of the United States of America 2017;114( 44):E9271–E9.
  • Maiuri MC, Tasdemir E, Criollo A, Morselli E, Vicencio JM, Carnuccio R, Kroemer G. Control of autophagy by oncogenes and tumor suppressor genes. Cell Death Differ. 2009;16:87–93.
  • Morselli E, Galluzzi L, Kepp O, Mariño G, Michaud M, Vitale I, Maiuri MC, Kroemer G. Oncosuppressive functions of autophagy. Antioxid Redox Signal. 2011;14:2251–2269.
  • Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell. 2005;122:927–939.
  • Maiuri MC, Le Toumelin G, Criollo A, Rain J-C, Gautier F, Juin P, Tasdemir E, Pierron G, Troulinaki K, Tavernarakis N, et al. Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J. 2007;26(10):2527–2539.
  • Kang MH, Reynolds CP. Bcl-2 inhibitors: targeting mitochondrial apoptotic pathways in cancer therapy. Clin Cancer Res. 2009;15:1126–1132.
  • Furuta S, Hidaka E, Ogata A, Yokota S, Kamata T. Ras is involved in the negative control of autophagy through the class I PI3-kinase. Oncogene. 2004;23:3898–3904.
  • Pasparakis M, Vandenabeele P. Necroptosis and its role in inflammation. Nature. 2015;517:311–320.
  • Seifert L, Werba G, Tiwari S, Giao Ly NN, Alothman S, Alqunaibit D, Avanzi A, Barilla R, Daley D, Greco SH, et al. The necrosome promotes pancreatic oncogenesis via CXCL1 and Mincle-induced immune suppression. Nature. 2016;532(7598):245–249.
  • Yatim N, Jusforgues-Saklani H, Orozco S, Schulz O, Barreira Da Silva R, Reis E Sousa C, Green DR, Oberst A, Albert ML. RIPK1 and NF-kappaB signaling in dying cells determines cross-priming of CD8(+) T cells. Science. 2015;350:328–334.
  • Van Hoecke L, Van Lint S, Roose K, Van Parys A, Vandenabeele P, Grooten J, Tavernier J, De Koker S, Saelens X. Treatment with mRNA coding for the necroptosis mediator MLKL induces antitumor immunity directed against neo-epitopes. Nat Commun. 2018;9:3417.
  • Snyder AG, Hubbard NW, Messmer MN, Kofman SB, Hagan CE, Orozco SL, Chiang K, Daniels BP, Baker D, Oberst A. Intratumoral activation of the necroptotic pathway components RIPK1 and RIPK3 potentiates antitumor immunity. Sci Immunol. 2019;4:eaaw2004.
  • Wang W, Marinis JM, Beal AM, Savadkar S, Wu Y, Khan M, Taunk PS, Wu N, Su W, Wu J, et al. RIP1 kinase drives macrophage-mediated adaptive immune tolerance in pancreatic cancer. Cancer Cell. 2018;34(5):757–74 e7.
  • Koo G-B, Morgan MJ, Lee D-G, Kim W-J, Yoon J-H, Koo JS, Kim SI, Kim SJ, Son MK, Hong SS, et al. Methylation-dependent loss of RIP3 expression in cancer represses programmed necrosis in response to chemotherapeutics. Cell Res. 2015;25(6):707–725.
  • Fukasawa M, Kimura M, Morita S, Matsubara K, Yamanaka S, Endo C, Sakurada A, Sato M, Kondo T, Horii A, et al. Microarray analysis of promoter methylation in lung cancers. J Hum Genet. 2006;51(4):368–374.
  • Nugues AL, El Bouazzati H, Hétuin D, Berthon C, Loyens A, Bertrand E, Jouy N, Idziorek T, Quesnel B. RIP3 is downregulated in human myeloid leukemia cells and modulates apoptosis and caspase-mediated p65/RelA cleavage. Cell Death Dis. 2014;5:e1384–e.
  • Moriwaki K, Bertin J, Gough PJ, Orlowski GM, Chan FK. Differential roles of RIPK1 and RIPK3 in TNF-induced necroptosis and chemotherapeutic agent-induced cell death. Cell Death Dis. 2015;6:e1636–e.
  • Lalaoui N, Brumatti G. Relevance of necroptosis in cancer. Immunol Cell Biol. 2017;95:137–145.
  • Zhang YY, Tabataba H, Liu XY, Wang JY, Yan XG, Farrelly M, Jiang CC, Guo ST, Liu T, Kao H-Y, et al. ACTN4 regulates the stability of RIPK1 in melanoma. Oncogene. 2018;37(29):4033–4045.
  • Park S, Hatanpaa KJ, Xie Y, Mickey BE, Madden CJ, Raisanen JM, Ramnarain DB, Xiao G, Saha D, Boothman DA, et al. The receptor interacting protein 1 Inhibits p53 Induction through NF-κB activation and confers a worse prognosis in glioblastoma. Cancer Res. 2009;69(7):2809–2816.
  • Wang Q, Chen W, Xu X, Li B, He W, Padilla MT, Jang J-H, Nyunoya T, Amin S, Wang X, et al. RIP1 potentiates BPDE-induced transformation in human bronchial epithelial cells through catalase-mediated suppression of excessive reactive oxygen species. Carcinogenesis. 2013;34(9):2119–2128.
  • McCabe KE, Bacos K, Lu D, Delaney JR, Axelrod J, Potter MD, Vamos M, Wong V, Cosford NDP, Xiang R, et al. Triggering necroptosis in cisplatin and IAP antagonist-resistant ovarian carcinoma. Cell Death Dis. 2014;5(10):e1496–e.
  • Fink SL, Cookson BT. Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell Microbiol. 2006;8:1812–1825.
  • Wang Y, Gao W, Shi X, Ding J, Liu W, He H, Wang K, Shao F. Chemotherapy drugs induce pyroptosis through caspase-3 cleavage of a gasdermin. Nature. 2017;547:99.
  • Rogers C, Alnemri ES. Gasdermins: novel mitochondrial pore-forming proteins. Mol Cell Oncol. 2019;6:e1621501.
  • Karki R, Kanneganti T-D. Diverging inflammasome signals in tumorigenesis and potential targeting. Nat Rev Cancer. 2019;19:197–214.
  • Daley D, Mani VR, Mohan N, Akkad N, Pandian GSDB, Savadkar S, Lee KB, Torres-Hernandez A, Aykut B, Diskin B, et al. NLRP3 signaling drives macrophage-induced adaptive immune suppression in pancreatic carcinoma. J Exp Med. 2017;214(6):1711.
  • Saijo Y, Tanaka M, Miki M, Usui K, Suzuki T, Maemondo M, Hong X, Tazawa R, Kikuchi T, Matsushima K, et al. Proinflammatory cytokine IL-1 beta promotes tumor growth of Lewis lung carcinoma by induction of angiogenic factors: in vivo analysis of tumor-stromal interaction. Jl Immunol. 2002;169(1):469–475. Baltimore, Md: 1950.
  • Tu S, Bhagat G, Cui G, Takaishi S, Kurt-Jones EA, Rickman B, Betz KS, Penz-Oesterreicher M, Bjorkdahl O, Fox JG, et al. Overexpression of interleukin-1beta induces gastric inflammation and cancer and mobilizes myeloid-derived suppressor cells in mice. Cancer Cell. 2008;14(5):408–419.
  • Nakamura K, Kassem S, Cleynen A, Chrétien M-L, Guillerey C, Putz EM, Bald T, Förster I, Vuckovic S, Hill GR, et al. Dysregulated IL-18 is a key driver of immunosuppression and a possible therapeutic target in the multiple myeloma microenvironment. Cancer Cell. 2018;33(4):634–48.e5.
  • Terme M, Ullrich E, Aymeric L, Meinhardt K, Desbois M, Delahaye N, Viaud S, Ryffel B, Yagita H, Kaplanski G, et al. IL-18 induces PD-1-dependent immunosuppression in cancer. Cancer Res. 2011;71(16):5393–5399.
  • Kang JS, Bae SY, Kim HR, Kim YS, Kim DJ, Cho BJ, Yang H-K, Hwang Y-I, Kim KJ, Park HS, et al. Interleukin-18 increases metastasis and immune escape of stomach cancer via the downregulation of CD70 and maintenance of CD44. Carcinogenesis. 2009;30(12):1987–1996.
  • Williams TM, Leeth RA, Rothschild DE, Coutermarsh-Ott SL, McDaniel DK, Simmons AE, Heid B, Cecere TE, Allen IC. The NLRP1 inflammasome attenuates colitis and colitis-associated tumorigenesis. Jl Immunol. 2015;194(7):3369–3380. Baltimore, Md: 1950.
  • Allen IC, TeKippe EM, Woodford R-MT, Uronis JM, Holl EK, Rogers AB, Herfarth HH, Jobin C, Ting JPY. The NLRP3 inflammasome functions as a negative regulator of tumorigenesis during colitis-associated cancer. J Exp Med. 2010;207:1045–1056.
  • Zaki MH, Vogel P, Body-Malapel M, Lamkanfi M, Kanneganti T-D. IL-18 production downstream of the Nlrp3 inflammasome confers protection against colorectal tumor formation. Jl Immunol. 2010;185(8):4912–4920. Baltimore, Md: 1950.
  • Wilson JE, Petrucelli AS, Chen L, Koblansky AA, Truax AD, Oyama Y, Rogers AB, Brickey WJ, Wang Y, Schneider M, et al. Inflammasome-independent role of AIM2 in suppressing colon tumorigenesis via DNA-PK and Akt. Nat Med. 2015;21(8):906–913.
  • Kim MS, Lebron C, Nagpal JK, Chae YK, Chang X, Huang Y, Chuang T, Yamashita K, Trink B, Ratovitski EA, et al. Methylation of the DFNA5 increases risk of lymph node metastasis in human breast cancer. Biochem Biophys Res Commun. 2008;370(1):38–43.
  • Zhou Z, He H, Wang K, Shi X, Wang Y, Su Y, Wang Y, Li D, Liu W, Zhang Y, et al. Granzyme A from cytotoxic lymphocytes cleaves GSDMB to trigger pyroptosis in target cells. Science 2020.
  • Zhang Z, Zhang Y, Xia S, Kong Q, Li S, Liu X, Junqueira C, Meza-Sosa KF, Mok TMY, Ansara J, et al. Gasdermin E suppresses tumour growth by activating anti-tumour immunity. Nature. 2020;579(7799):415–420.
  • Akino K, Toyota M, Suzuki H, Imai T, Maruyama R, Kusano M, Nishikawa N, Watanabe Y, Sasaki Y, Abe T, et al. Identification of DFNA5 as a target of epigenetic inactivation in gastric cancer. Cancer Sci. 2007;98(1):88–95.
  • Ibrahim J, Op De Beeck K, Fransen E, Croes L, Beyens M, Suls A, Vanden BW, Peeters M, Van CG. Methylation analysis of Gasdermin E shows great promise as a biomarker for colorectal cancer. Cancer Med. 2019;8:2133–2145.
  • Lu H, Zhang S, Wu J, Chen M, Cai M-C, Fu Y, Li W, Wang J, Zhao X, Yu Z, et al. Molecular targeted therapies elicit concurrent apoptotic and GSDME-dependent pyroptotic tumor cell death. Clin Cancer Res. 2018;24(23):6066–6077.
  • 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(1):54–61.
  • Michaud M, Martins I, Sukkurwala AQ, Adjemian S, Ma Y, Pellegatti P, Shen S, Kepp O, Scoazec M, Mignot G, et al. Autophagy-dependent anticancer immune responses induced by chemotherapeutic agents in mice. Science. 2011;334(6062):1573–1577.
  • Fucikova J, Becht E, Iribarren K, Goc J, Remark R, Damotte D, Alifano M, Devi P, Biton J, Germain C, et al. Calreticulin expression in human non–small cell lung cancers correlates with increased accumulation of antitumor immune cells and favorable prognosis. Cancer Res. 2016;76(7):1746–1756.
  • Buisseret L, Pommey S, Allard B, Garaud S, Bergeron M, Cousineau I, Ameye L, Bareche Y, Paesmans M, Crown JPA, et al. Clinical significance of CD73 in triple-negative breast cancer: multiplex analysis of a phase III clinical trial. Ann Oncol. 2017;29(4):1056–1062.
  • Coffelt SB, De Visser KE. Immune-mediated mechanisms influencing the efficacy of anticancer therapies. Trends Immunol. 2015;36:198–216.
  • Zitvogel L, Kroemer G. Reply to: chemotherapy response of spontaneous mammary tumors is independent of the adaptive immune system. Nat Med. 2012;18:346.
  • Garg AD, Agostinis P. Editorial: immunogenic cell death in cancer: from benchside research to bedside reality. Front Immunol. 2016;7:110.
  • Salmon H, Remark R, Gnjatic S, Merad M. Host tissue determinants of tumour immunity. Nat Rev Cancer. 2019;19:215–227.
  • Musahl AS, Huang X, Rusakiewicz S, Ntini E, Marsico A, Kroemer G, Kepp O, Ørom UA. A long non-coding RNA links calreticulin-mediated immunogenic cell removal to RB1 transcription. Oncogene. 2015;34:5046–5054.
  • Casey SC, Tong L, Li Y, Do R, Walz S, Fitzgerald KN, Gouw AM, Baylot V, Gütgemann I, Eilers M, et al. MYC regulates the antitumor immune response through CD47 and PD-L1. Science (New York, NY). 2016;352(6282):227–231.
  • Eggleton P, Bremer E, Dudek E, Michalak M. Calreticulin, a therapeutic target? Expert Opin Ther Targets. 2016;20:1137–1147.
  • Michalak M, Corbett EF, Mesaeli N, Nakamura K, Opas M. Calreticulin: one protein, one gene, many functions. Biochem J. 1999;344:281–292.
  • Gardai SJ, McPhillips KA, Frasch SC, Janssen WJ, Starefeldt A, Murphy-Ullrich JE, Bratton DL, Oldenborg P-A, Michalak M, Henson PM. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell. 2005;123:321–334.
  • Sadasivan B, Lehner PJ, Ortmann B, Spies T, Cresswell P. Roles for calreticulin and a novel glycoprotein, tapasin, in the interaction of MHC class I molecules with TAP. Immunity. 1996;5:103–114.
  • Peaper DR, Cresswell P. Regulation of MHC class I assembly and peptide binding. Annu Rev Cell Dev Biol. 2008;24:343–368.
  • Humeau J, Sauvat A, Cerrato G, Xie W, Loos F, Iannantuoni F, Bezu L, Lévesque S, Paillet J, Pol J, et al. Inhibition of transcription by dactinomycin reveals a new characteristic of immunogenic cell stress. EMBO Mol Med. 2020;12(5):e11622.
  • Panaretakis T, Kepp O, Brockmeier U, Tesniere A, Bjorklund A-C, Chapman DC, Durchschlag M, Joza N, Pierron G, Van Endert P, et al. Mechanisms of pro-apoptotic calreticulin exposure in immunogenic cell death. EMBO J. 2009;28(5):578–590.
  • Sukkurwala AQ, Martins I, Wang Y, Schlemmer F, Ruckenstuhl C, Durchschlag M, Michaud M, Senovilla L, Sistigu A, Ma Y, et al. Immunogenic calreticulin exposure occurs through a phylogenetically conserved stress pathway involving the chemokine CXCL8. Cell Death Differ. 2014;21(1):59–68.
  • Garg AD, Krysko DV, Verfaillie T, Kaczmarek A, Ferreira GB, Marysael T, Rubio N, Firczuk M, Mathieu C, Roebroek AJM, et al. A novel pathway combining calreticulin exposure and ATP secretion in immunogenic cancer cell death. EMBO J. 2012;31(5):1062–1079.
  • Kang JS, Dervan PB. A sequence-specific DNA binding small molecule triggers the release of immunogenic signals and phagocytosis in a model of B-cell lymphoma. Q Rev Biophys. 2015;48:453–464.
  • Wemeau M, Kepp O, Tesnière A, Panaretakis T, Flament C, De Botton S, Zitvogel L, Kroemer G, Chaput N. Calreticulin exposure on malignant blasts predicts a cellular anticancer immune response in patients with acute myeloid leukemia. Cell Death Dis. 2010;1:e104–e.
  • Liu X, Kwon H, Li Z, Fu Y-X. Is CD47 an innate immune checkpoint for tumor evasion? J Hematol Oncol. 2017;10:12.
  • Sandilos JK, Chiu Y-H, Chekeni FB, Armstrong AJ, Walk SF, Ravichandran KS, Bayliss DA. Pannexin 1, an ATP release channel, is activated by caspase cleavage of its pore-associated C-terminal autoinhibitory region. J Biol Chem. 2012;287:11303–11311.
  • Ma Y, Aymeric L, Locher C, Mattarollo SR, Delahaye NF, Pereira P, Boucontet L, Apetoh L, Ghiringhelli F, Casares N, 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.
  • Ghiringhelli F, Apetoh L, Tesniere A, Aymeric L, Ma Y, Ortiz C, Vermaelen K, Panaretakis T, Mignot G, Ullrich E, et al. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat Med. 2009;15(10):1170–1178.
  • Allard D, Chrobak P, Allard B, Messaoudi N, Stagg J. Targeting the CD73-adenosine axis in immuno-oncology. Immunol Lett. 2019;205:31–39.
  • Robson SC, Sévigny J, Zimmermann H. The E-NTPDase family of ectonucleotidases: structure function relationships and pathophysiological significance. Purinergic Signal. 2006;2:409–430.
  • Sitkovsky MV, Hatfield S, Abbott R, Belikoff B, Lukashev D, Ohta A. Hostile, hypoxia-A2-adenosinergic tumor biology as the next barrier to overcome for tumor immunologists. Cancer Immunol Res. 2014;2:598–605.
  • Stagg J, Divisekera U, McLaughlin N, Sharkey J, Pommey S, Denoyer D, Dwyer KM, Smyth MJ Anti-CD73 antibody therapy inhibits breast tumor growth and metastasis. Proceedings of the National Academy of Sciences of the United States of America 2010;107( 4):1547–1552.
  • Jin D, Fan J, Wang L, Thompson LF, Liu A, Daniel BJ, Shin T, Curiel TJ, Zhang B. CD73 on tumor cells impairs antitumor T-cell responses: a novel mechanism of tumor-induced immune suppression. Cancer Res. 2010;70:2245–2255.
  • Turcotte M, Spring K, Pommey S, Chouinard G, Cousineau I, George J, Chen GM, Gendoo DMA, Haibe-Kains B, Karn T, et al. CD73 is associated with poor prognosis in high-grade serous ovarian cancer. Cancer Res. 2015;75(21):4494–4503.
  • Spychala J, Kitajewski J. Wnt and beta-catenin signaling target the expression of ecto-5ʹ-nucleotidase and increase extracellular adenosine generation. Exp Cell Res. 2004;296:99–108.
  • Reinhardt J, Landsberg J, Schmid-Burgk JL, Ramis BB, Bald T, Glodde N, Lopez-Ramos D, Young A, Ngiow SF, Nettersheim D, et al. MAPK signaling and inflammation link melanoma phenotype switching to induction of CD73 during immunotherapy. Cancer Res. 2017;77(17):4697–4709.
  • Inoue Y, Yoshimura K, Kurabe N, Kahyo T, Kawase A, Tanahashi M, Ogawa H, Inui N, Funai K, Shinmura K, et al. Prognostic impact of CD73 and A2A adenosine receptor expression in non-small-cell lung cancer. Oncotarget. 2017;8(5):8738–8751.
  • Zhu J, Zeng Y, Li W, Qin H, Lei Z, Shen D, Gu D, Huang J-A, Liu Z. CD73/NT5E is a target of miR-30a-5p and plays an important role in the pathogenesis of non-small cell lung cancer. Mol Cancer. 2017;16:34.
  • Young A, Ngiow SF, Madore J, Reinhardt J, Landsberg J, Chitsazan A, Rautela J, Bald T, Barkauskas DS, Ahern E, et al. Targeting adenosine in BRaf-mutant melanoma reduces tumor growth and metastasis. Cancer Res. 2017;77(17):4684–4696.
  • Sims GP, Rowe DC, Rietdijk ST, Herbst R, Coyle AJ. HMGB1 and RAGE in inflammation and cancer. Annu Rev Immunol. 2010;28:367–388.
  • Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature. 2002;418:191–195.
  • Bonaldi T, Talamo F, Scaffidi P, Ferrera D, Porto A, Bachi A, Rubartelli A, Agresti A, Bianchi ME. Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J. 2003;22:5551–5560.
  • Lu B, Antoine DJ, Kwan K, Lundbäck P, Wähämaa H, Schierbeck H, Robinson M, Van Zoelen MAD, Yang H, Li J, et al. JAK/STAT1 signaling promotes HMGB1 hyperacetylation and nuclear translocation. Proceedings of the National Academy of Sciences 2014;111( 8):3068–3073.
  • Wang H, Bloom O, Zhang M, Vishnubhakat JM, Ombrellino M, Che J, Frazier A, Yang H, Ivanova S, Borovikova L, et al. HMG-1 as a late mediator of endotoxin lethality in mice. Science. 1999;285(5425):248–251.
  • Venereau E, Casalgrandi M, Schiraldi M, Antoine DJ, Cattaneo A, De Marchis F, Liu J, Antonelli A, Preti A, Raeli L, et al. Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release. J Exp Med. 2012;209(9):1519–1528.
  • Yang H, Hreggvidsdottir HS, Palmblad K, Wang H, Ochani M, Li J, Lu B, Chavan S, Rosas-Ballina M, Al-Abed Y, et al. A critical cysteine is required for HMGB1 binding to Toll-like receptor 4 and activation of macrophage cytokine release. Proceedings of the National Academy of Sciences 2010;107( 26):11942–11947.
  • LeBlanc PM, Doggett TA, Choi J, Hancock MA, Durocher Y, Frank F, Nagar B, Ferguson TA, Saleh M. An immunogenic peptide in the A-box of HMGB1 protein reverses apoptosis-induced tolerance through RAGE receptor. J Biol Chem. 2014;289:7777–7786.
  • Apetoh L, Ghiringhelli F, Tesniere A, Criollo A, Ortiz C, Lidereau R, Mariette C, Chaput N, Mira JP, Delaloge S, et al. The interaction between HMGB1 and TLR4 dictates the outcome of anticancer chemotherapy and radiotherapy. Immunol Rev. 2007;220:47–59.
  • 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–e.
  • Brusa D, Migliore E, Garetto S, Simone M, Matera L. Immunogenicity of 56 degrees C and UVC-treated prostate cancer is associated with release of HSP70 and HMGB1 from necrotic cells. Prostate. 2009;69:1343–1352.
  • Werthmöller 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–e.