Skip to main content
Top
Published in: Cancer and Metastasis Reviews 1/2011

01-03-2011

Molecular determinants of immunogenic cell death elicited by anticancer chemotherapy

Authors: Oliver Kepp, Lorenzo Galluzzi, Isabelle Martins, Frederic Schlemmer, Sandy Adjemian, Mickael Michaud, Abdul Qader Sukkurwala, Laurie Menger, Laurence Zitvogel, Guido Kroemer

Published in: Cancer and Metastasis Reviews | Issue 1/2011

Login to get access

Abstract

The success of some chemo- and radiotherapeutic regimens relies on the induction of immunogenic tumor cell death and on the induction of an anticancer immune response. Cells succumbing to immunogenic cell death undergo specific changes in their surface characteristics and release pro-immunogenic factors according to a defined spatiotemporal pattern. This stimulates antigen presenting cells such as dendritic cells to efficiently take up tumor antigens, process them, and cross-prime cytotoxic T lymphocytes, thus eliciting a tumor-specific cognate immune response. Such a response can also target therapy-resistant tumor (stem) cells, thereby leading, at least in some instances, to tumor eradication. In this review, we shed some light on the molecular identity of the factors that are required for cell death to be perceived as immunogenic. We discuss the intriguing observations that the most abundant endoplasmic reticulum protein, calreticulin, the most abundant intracellular metabolite, ATP, and the most abundant non-histone chromatin-binding protein, HMGB1, can determine whether cell death is immunogenic as they appear on the surface or in the microenvironment of dying cells.
Literature
1.
go back to reference Zitvogel, L., Apetoh, L., Ghiringhelli, F., & Kroemer, G. (2008). Immunological aspects of cancer chemotherapy. Nat Rev Immunol, 8(1), 59–73.PubMedCrossRef Zitvogel, L., Apetoh, L., Ghiringhelli, F., & Kroemer, G. (2008). Immunological aspects of cancer chemotherapy. Nat Rev Immunol, 8(1), 59–73.PubMedCrossRef
2.
go back to reference Savill, J., & Fadok, V. (2000). Corpse clearance defines the meaning of cell death. Nature, 407(6805), 784–788.PubMedCrossRef Savill, J., & Fadok, V. (2000). Corpse clearance defines the meaning of cell death. Nature, 407(6805), 784–788.PubMedCrossRef
3.
4.
go back to reference Kroemer, G., Galluzzi, L., Vandenabeele, P., Abrams, J., Alnemri, E. S., Baehrecke, E. H., et al. (2009). Classification of cell death: recommendations of the nomenclature committee on cell death 2009. Cell Death Differ, 16(1), 3–11.PubMedCrossRef Kroemer, G., Galluzzi, L., Vandenabeele, P., Abrams, J., Alnemri, E. S., Baehrecke, E. H., et al. (2009). Classification of cell death: recommendations of the nomenclature committee on cell death 2009. Cell Death Differ, 16(1), 3–11.PubMedCrossRef
5.
go back to reference Zou, W. (2006). Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol, 6(4), 295–307.PubMedCrossRef Zou, W. (2006). Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol, 6(4), 295–307.PubMedCrossRef
6.
go back to reference Rubio, M. T., Ittelet, D., Raymond, E., Blay, J. Y., Bernard, J., & Chouaib, S. (2004). The immunosuppressive effect of vincristine on allostimulatory potential of human dendritic cells interferes with their function and survival. Int J Oncol, 25(2), 407–412.PubMed Rubio, M. T., Ittelet, D., Raymond, E., Blay, J. Y., Bernard, J., & Chouaib, S. (2004). The immunosuppressive effect of vincristine on allostimulatory potential of human dendritic cells interferes with their function and survival. Int J Oncol, 25(2), 407–412.PubMed
7.
go back to reference Zitvogel, L., Apetoh, L., Ghiringhelli, F., Andre, F., Tesniere, A., & Kroemer, G. (2008). The anticancer immune response: indispensable for therapeutic success? J Clin Invest, 118(6), 1991–2001.PubMedCrossRef Zitvogel, L., Apetoh, L., Ghiringhelli, F., Andre, F., Tesniere, A., & Kroemer, G. (2008). The anticancer immune response: indispensable for therapeutic success? J Clin Invest, 118(6), 1991–2001.PubMedCrossRef
8.
go back to reference Casares, N., Pequignot, M. O., Tesniere, A., Ghiringhelli, F., Roux, S., Chaput, N., et al. (2005). Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J Exp Med, 202(12), 1691–1701.PubMedCrossRef Casares, N., Pequignot, M. O., Tesniere, A., Ghiringhelli, F., Roux, S., Chaput, N., et al. (2005). Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J Exp Med, 202(12), 1691–1701.PubMedCrossRef
9.
go back to reference Obeid, M., Tesniere, A., Ghiringhelli, F., Fimia, G. M., Apetoh, L., Perfettini, J. L., et al. (2007). Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med, 13(1), 54–61.PubMedCrossRef Obeid, M., Tesniere, A., Ghiringhelli, F., Fimia, G. M., Apetoh, L., Perfettini, J. L., et al. (2007). Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med, 13(1), 54–61.PubMedCrossRef
10.
go back to reference Jung, S., Unutmaz, D., Wong, P., Sano, G., De los Santos, K., Sparwasser, T., et al. (2002). In vivo depletion of cd11c+ dendritic cells abrogates priming of cd8+ t cells by exogenous cell-associated antigens. Immunity, 17(2), 211–220.PubMedCrossRef Jung, S., Unutmaz, D., Wong, P., Sano, G., De los Santos, K., Sparwasser, T., et al. (2002). In vivo depletion of cd11c+ dendritic cells abrogates priming of cd8+ t cells by exogenous cell-associated antigens. Immunity, 17(2), 211–220.PubMedCrossRef
11.
go back to reference Apetoh, L., Ghiringhelli, F., Tesniere, A., Obeid, M., Ortiz, C., Criollo, A., et al. (2007). Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med, 13(9), 1050–1059.PubMedCrossRef Apetoh, L., Ghiringhelli, F., Tesniere, A., Obeid, M., Ortiz, C., Criollo, A., et al. (2007). Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med, 13(9), 1050–1059.PubMedCrossRef
12.
go back to reference Apetoh, L., Ghiringhelli, F., Tesniere, A., Criollo, A., Ortiz, C., Lidereau, R., et al. (2007). The interaction between hmgb1 and tlr4 dictates the outcome of anticancer chemotherapy and radiotherapy. Immunol Rev, 220, 47–59.PubMedCrossRef Apetoh, L., Ghiringhelli, F., Tesniere, A., Criollo, A., Ortiz, C., Lidereau, R., et al. (2007). The interaction between hmgb1 and tlr4 dictates the outcome of anticancer chemotherapy and radiotherapy. Immunol Rev, 220, 47–59.PubMedCrossRef
13.
go back to reference Ghiringhelli, F., Apetoh, L., Tesniere, A., Aymeric, L., Ma, Y., Ortiz, C., et al. (2009). Activation of the nlrp3 inflammasome in dendritic cells induces il-1beta-dependent adaptive immunity against tumors. Nat Med, 15(10), 1170–1178.PubMedCrossRef Ghiringhelli, F., Apetoh, L., Tesniere, A., Aymeric, L., Ma, Y., Ortiz, C., et al. (2009). Activation of the nlrp3 inflammasome in dendritic cells induces il-1beta-dependent adaptive immunity against tumors. Nat Med, 15(10), 1170–1178.PubMedCrossRef
14.
go back to reference Banchereau, J., & Steinman, R. M. (1998). Dendritic cells and the control of immunity. Nature, 392(6673), 245–252.PubMedCrossRef Banchereau, J., & Steinman, R. M. (1998). Dendritic cells and the control of immunity. Nature, 392(6673), 245–252.PubMedCrossRef
15.
go back to reference Albert, M. L., Sauter, B., & Bhardwaj, N. (1998). Dendritic cells acquire antigen from apoptotic cells and induce class i-restricted ctls. Nature, 392(6671), 86–89.PubMedCrossRef Albert, M. L., Sauter, B., & Bhardwaj, N. (1998). Dendritic cells acquire antigen from apoptotic cells and induce class i-restricted ctls. Nature, 392(6671), 86–89.PubMedCrossRef
16.
go back to reference Green, D. R., Ferguson, T., Zitvogel, L., & Kroemer, G. (2009). Immunogenic and tolerogenic cell death. Nat Rev Immunol, 9(5), 353–363.PubMedCrossRef Green, D. R., Ferguson, T., Zitvogel, L., & Kroemer, G. (2009). Immunogenic and tolerogenic cell death. Nat Rev Immunol, 9(5), 353–363.PubMedCrossRef
17.
go back to reference Grivennikov, S. I., Greten, F. R., & Karin, M. (2010). Immunity, inflammation, and cancer. Cell, 140(6), 883–899.PubMedCrossRef Grivennikov, S. I., Greten, F. R., & Karin, M. (2010). Immunity, inflammation, and cancer. Cell, 140(6), 883–899.PubMedCrossRef
18.
go back to reference Zitvogel, L., Kepp, O., & Kroemer, G. (2010). Decoding cell death signals in inflammation and immunity. Cell, 140(6), 798–804.PubMedCrossRef Zitvogel, L., Kepp, O., & Kroemer, G. (2010). Decoding cell death signals in inflammation and immunity. Cell, 140(6), 798–804.PubMedCrossRef
19.
go back to reference Zitvogel, L., Mayordomo, J. I., Tjandrawan, T., DeLeo, A. B., Clarke, M. R., Lotze, M. T., et al. (1996). Therapy of murine tumors with tumor peptide-pulsed dendritic cells: dependence on T cells, B7 costimulation, and T helper cell 1-associated cytokines. J Exp Med, 183(1), 87–97.PubMedCrossRef Zitvogel, L., Mayordomo, J. I., Tjandrawan, T., DeLeo, A. B., Clarke, M. R., Lotze, M. T., et al. (1996). Therapy of murine tumors with tumor peptide-pulsed dendritic cells: dependence on T cells, B7 costimulation, and T helper cell 1-associated cytokines. J Exp Med, 183(1), 87–97.PubMedCrossRef
20.
go back to reference Spisek, R., Charalambous, A., Mazumder, A., Vesole, D. H., Jagannath, S., & Dhodapkar, M. V. (2007). 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, 109(11), 4839–4845.PubMedCrossRef Spisek, R., Charalambous, A., Mazumder, A., Vesole, D. H., Jagannath, S., & Dhodapkar, M. V. (2007). 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, 109(11), 4839–4845.PubMedCrossRef
21.
go back to reference Mukhopadhaya, A., Mendecki, J., Dong, X., Liu, L., Kalnicki, S., Garg, M., et al. (2007). Localized hyperthermia combined with intratumoral dendritic cells induces systemic antitumor immunity. Cancer Res, 67(16), 7798–7806.PubMedCrossRef Mukhopadhaya, A., Mendecki, J., Dong, X., Liu, L., Kalnicki, S., Garg, M., et al. (2007). Localized hyperthermia combined with intratumoral dendritic cells induces systemic antitumor immunity. Cancer Res, 67(16), 7798–7806.PubMedCrossRef
22.
go back to reference Didelot, C., Lanneau, D., Brunet, M., Joly, A. L., De Thonel, A., Chiosis, G., et al. (2007). Anti-cancer therapeutic approaches based on intracellular and extracellular heat shock proteins. Curr Med Chem, 14(27), 2839–2847.PubMedCrossRef Didelot, C., Lanneau, D., Brunet, M., Joly, A. L., De Thonel, A., Chiosis, G., et al. (2007). Anti-cancer therapeutic approaches based on intracellular and extracellular heat shock proteins. Curr Med Chem, 14(27), 2839–2847.PubMedCrossRef
23.
go back to reference Locher, C., Rusakiewicz, S., Tesniere, A., Ghiringhelli, F., Apetoh, L., Kroemer, G., et al. (2009). Witch hunt against tumor cells enhanced by dendritic cells. Ann NY Acad Sci, 1174, 51–60.PubMedCrossRef Locher, C., Rusakiewicz, S., Tesniere, A., Ghiringhelli, F., Apetoh, L., Kroemer, G., et al. (2009). Witch hunt against tumor cells enhanced by dendritic cells. Ann NY Acad Sci, 1174, 51–60.PubMedCrossRef
24.
go back to reference Gardai, S. J., McPhillips, K. A., Frasch, S. C., Janssen, W. J., Starefeldt, A., Murphy-Ullrich, J. E., et al. (2005). Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of lrp on the phagocyte. Cell, 123(2), 321–334.PubMedCrossRef Gardai, S. J., McPhillips, K. A., Frasch, S. C., Janssen, W. J., Starefeldt, A., Murphy-Ullrich, J. E., et al. (2005). Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of lrp on the phagocyte. Cell, 123(2), 321–334.PubMedCrossRef
25.
go back to reference Kepp, O., Gdoura, A., Martins, I., Panaretakis, T., Schlemmer, F., Tesniere, A., et al. (2010). Lysyl tRNA synthetase is required for the translocation of calreticulin to the cell surface in immunogenic death. Cell Cycle, 9(15), 3072–3077.PubMedCrossRef Kepp, O., Gdoura, A., Martins, I., Panaretakis, T., Schlemmer, F., Tesniere, A., et al. (2010). Lysyl tRNA synthetase is required for the translocation of calreticulin to the cell surface in immunogenic death. Cell Cycle, 9(15), 3072–3077.PubMedCrossRef
27.
go back to reference Michalak, M., Corbett, E. F., Mesaeli, N., Nakamura, K., & Opas, M. (1999). Calreticulin: one protein, one gene, many functions. Biochem J, 344(Pt 2), 281–292.PubMedCrossRef Michalak, M., Corbett, E. F., Mesaeli, N., Nakamura, K., & Opas, M. (1999). Calreticulin: one protein, one gene, many functions. Biochem J, 344(Pt 2), 281–292.PubMedCrossRef
28.
go back to reference Johnson, S., Michalak, M., Opas, M., & Eggleton, P. (2001). The ins and outs of calreticulin: from the er lumen to the extracellular space. Trends Cell Biol, 11(3), 122–129.PubMedCrossRef Johnson, S., Michalak, M., Opas, M., & Eggleton, P. (2001). The ins and outs of calreticulin: from the er lumen to the extracellular space. Trends Cell Biol, 11(3), 122–129.PubMedCrossRef
29.
go back to reference Bedard, K., Szabo, E., Michalak, M., & Opas, M. (2005). Cellular functions of endoplasmic reticulum chaperones calreticulin, calnexin, and erp57. Int Rev Cytol, 245, 91–121.PubMedCrossRef Bedard, K., Szabo, E., Michalak, M., & Opas, M. (2005). Cellular functions of endoplasmic reticulum chaperones calreticulin, calnexin, and erp57. Int Rev Cytol, 245, 91–121.PubMedCrossRef
30.
go back to reference Panaretakis, T., Kepp, O., Brockmeier, U., Tesniere, A., Bjorklund, A. C., Chapman, D. C., et al. (2009). Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death. EMBO J, 28(5), 578–590.PubMedCrossRef Panaretakis, T., Kepp, O., Brockmeier, U., Tesniere, A., Bjorklund, A. C., Chapman, D. C., et al. (2009). Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death. EMBO J, 28(5), 578–590.PubMedCrossRef
31.
go back to reference Breckenridge, D. G., Stojanovic, M., Marcellus, R. C., & Shore, G. C. (2003). Caspase cleavage product of bap31 induces mitochondrial fission through endoplasmic reticulum calcium signals, enhancing cytochrome c release to the cytosol. J Cell Biol, 160(7), 1115–1127.PubMedCrossRef Breckenridge, D. G., Stojanovic, M., Marcellus, R. C., & Shore, G. C. (2003). Caspase cleavage product of bap31 induces mitochondrial fission through endoplasmic reticulum calcium signals, enhancing cytochrome c release to the cytosol. J Cell Biol, 160(7), 1115–1127.PubMedCrossRef
32.
go back to reference Kroemer, G., Galluzzi, L., & Brenner, C. (2007). Mitochondrial membrane permeabilization in cell death. Physiol Rev, 87(1), 99–163.PubMedCrossRef Kroemer, G., Galluzzi, L., & Brenner, C. (2007). Mitochondrial membrane permeabilization in cell death. Physiol Rev, 87(1), 99–163.PubMedCrossRef
33.
go back to reference Kepp, O., Senovilla, L., Galluzzi, L., Panaretakis, T., Tesniere, A., Schlemmer, F., et al. (2009). Viral subversion of immunogenic cell death. Cell Cycle, 8(6), 860–869.PubMedCrossRef Kepp, O., Senovilla, L., Galluzzi, L., Panaretakis, T., Tesniere, A., Schlemmer, F., et al. (2009). Viral subversion of immunogenic cell death. Cell Cycle, 8(6), 860–869.PubMedCrossRef
34.
go back to reference Panaretakis, T., Joza, N., Modjtahedi, N., Tesniere, A., Vitale, I., Durchschlag, M., et al. (2008). The co-translocation of erp57 and calreticulin determines the immunogenicity of cell death. Cell Death Differ, 15(9), 1499–1509.PubMedCrossRef Panaretakis, T., Joza, N., Modjtahedi, N., Tesniere, A., Vitale, I., Durchschlag, M., et al. (2008). The co-translocation of erp57 and calreticulin determines the immunogenicity of cell death. Cell Death Differ, 15(9), 1499–1509.PubMedCrossRef
35.
go back to reference Fadok, V. A., Voelker, D. R., Campbell, P. A., Cohen, J. J., Bratton, D. L., & Henson, P. M. (1992). Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol, 148(7), 2207–2216. Fadok, V. A., Voelker, D. R., Campbell, P. A., Cohen, J. J., Bratton, D. L., & Henson, P. M. (1992). Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol, 148(7), 2207–2216.
36.
go back to reference Tyurina, Y. Y., Basova, L. V., Konduru, N. V., Tyurin, V. A., Potapovich, A. I., Cai, P., et al. (2007). Nitrosative stress inhibits the aminophospholipid translocase resulting in phosphatidylserine externalization and macrophage engulfment: implications for the resolution of inflammation. J Biol Chem, 282(11), 8498–8509.PubMedCrossRef Tyurina, Y. Y., Basova, L. V., Konduru, N. V., Tyurin, V. A., Potapovich, A. I., Cai, P., et al. (2007). Nitrosative stress inhibits the aminophospholipid translocase resulting in phosphatidylserine externalization and macrophage engulfment: implications for the resolution of inflammation. J Biol Chem, 282(11), 8498–8509.PubMedCrossRef
37.
go back to reference Tarr, J. M., Young, P. J., Morse, R., Shaw, D. J., Haigh, R., Petrov, P. G., et al. (2010). A mechanism of release of calreticulin from cells during apoptosis. J Mol Biol, 401(5), 799–812.PubMedCrossRef Tarr, J. M., Young, P. J., Morse, R., Shaw, D. J., Haigh, R., Petrov, P. G., et al. (2010). A mechanism of release of calreticulin from cells during apoptosis. J Mol Biol, 401(5), 799–812.PubMedCrossRef
38.
go back to reference Latour, S., Tanaka, H., Demeure, C., Mateo, V., Rubio, M., Brown, E. J., et al. (2001). Bidirectional negative regulation of human T and dendritic cells by cd47 and its cognate receptor signal-regulator protein-alpha: down-regulation of IL-12 responsiveness and inhibition of dendritic cell activation. J Immunol, 167(5), 2547–2554.PubMed Latour, S., Tanaka, H., Demeure, C., Mateo, V., Rubio, M., Brown, E. J., et al. (2001). Bidirectional negative regulation of human T and dendritic cells by cd47 and its cognate receptor signal-regulator protein-alpha: down-regulation of IL-12 responsiveness and inhibition of dendritic cell activation. J Immunol, 167(5), 2547–2554.PubMed
39.
go back to reference Oldenborg, P. A., Gresham, H. D., & Lindberg, F. P. (2001). Cd47-signal regulatory protein alpha (sirpalpha) regulates fcgamma and complement receptor-mediated phagocytosis. J Exp Med, 193(7), 855–862.PubMedCrossRef Oldenborg, P. A., Gresham, H. D., & Lindberg, F. P. (2001). Cd47-signal regulatory protein alpha (sirpalpha) regulates fcgamma and complement receptor-mediated phagocytosis. J Exp Med, 193(7), 855–862.PubMedCrossRef
40.
go back to reference Castelli, C., Ciupitu, A. M., Rini, F., Rivoltini, L., Mazzocchi, A., Kiessling, R., et al. (2001). Human heat shock protein 70 peptide complexes specifically activate antimelanoma T cells. Cancer Res, 61(1), 222–227.PubMed Castelli, C., Ciupitu, A. M., Rini, F., Rivoltini, L., Mazzocchi, A., Kiessling, R., et al. (2001). Human heat shock protein 70 peptide complexes specifically activate antimelanoma T cells. Cancer Res, 61(1), 222–227.PubMed
41.
go back to reference Gehrmann, M., Liebisch, G., Schmitz, G., Anderson, R., Steinem, C., De Maio, A., et al. (2008). Tumor-specific Hsp70 plasma membrane localization is enabled by the glycosphingolipid Gb3. PLoS ONE, 3(4), e1925.PubMedCrossRef Gehrmann, M., Liebisch, G., Schmitz, G., Anderson, R., Steinem, C., De Maio, A., et al. (2008). Tumor-specific Hsp70 plasma membrane localization is enabled by the glycosphingolipid Gb3. PLoS ONE, 3(4), e1925.PubMedCrossRef
42.
go back to reference Chen, T., Guo, J., Han, C., Yang, M., & Cao, X. (2009). Heat shock protein 70, released from heat-stressed tumor cells, initiates antitumor immunity by inducing tumor cell chemokine production and activating dendritic cells via TLR4 pathway. J Immunol, 182(3), 1449–1459.PubMed Chen, T., Guo, J., Han, C., Yang, M., & Cao, X. (2009). Heat shock protein 70, released from heat-stressed tumor cells, initiates antitumor immunity by inducing tumor cell chemokine production and activating dendritic cells via TLR4 pathway. J Immunol, 182(3), 1449–1459.PubMed
43.
go back to reference Delamarre, L., Couture, R., Mellman, I., & Trombetta, E. S. (2006). Enhancing immunogenicity by limiting susceptibility to lysosomal proteolysis. J Exp Med, 203(9), 2049–2055.PubMedCrossRef Delamarre, L., Couture, R., Mellman, I., & Trombetta, E. S. (2006). Enhancing immunogenicity by limiting susceptibility to lysosomal proteolysis. J Exp Med, 203(9), 2049–2055.PubMedCrossRef
44.
go back to reference Shiratsuchi, A., Watanabe, I., Takeuchi, O., Akira, S., & Nakanishi, Y. (2004). Inhibitory effect of Toll-like receptor 4 on fusion between phagosomes and endosomes/lysosomes in macrophages. J Immunol, 172(4), 2039–2047.PubMed Shiratsuchi, A., Watanabe, I., Takeuchi, O., Akira, S., & Nakanishi, Y. (2004). Inhibitory effect of Toll-like receptor 4 on fusion between phagosomes and endosomes/lysosomes in macrophages. J Immunol, 172(4), 2039–2047.PubMed
45.
go back to reference Tesniere, A., Schlemmer, F., Boige, V., Kepp, O., Martins, I., Ghiringhelli, F., et al. (2010). Immunogenic death of colon cancer cells treated with oxaliplatin. Oncogene, 29(4), 482–491.PubMedCrossRef Tesniere, A., Schlemmer, F., Boige, V., Kepp, O., Martins, I., Ghiringhelli, F., et al. (2010). Immunogenic death of colon cancer cells treated with oxaliplatin. Oncogene, 29(4), 482–491.PubMedCrossRef
46.
go back to reference Scaffidi, P., Misteli, T., & Bianchi, M. E. (2002). Release of chromatin protein hmgb1 by necrotic cells triggers inflammation. Nature, 418(6894), 191–195.PubMedCrossRef Scaffidi, P., Misteli, T., & Bianchi, M. E. (2002). Release of chromatin protein hmgb1 by necrotic cells triggers inflammation. Nature, 418(6894), 191–195.PubMedCrossRef
47.
go back to reference Bell, C. W., Jiang, W., Reich, C. F., III, & Pisetsky, D. S. (2006). The extracellular release of hmgb1 during apoptotic cell death. Am J Physiol Cell Physiol, 291(6), C1318–1325.PubMedCrossRef Bell, C. W., Jiang, W., Reich, C. F., III, & Pisetsky, D. S. (2006). The extracellular release of hmgb1 during apoptotic cell death. Am J Physiol Cell Physiol, 291(6), C1318–1325.PubMedCrossRef
48.
go back to reference Andersson, U., Wang, H., Palmblad, K., Aveberger, A. C., Bloom, O., Erlandsson-Harris, H., et al. (2000). High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J Exp Med, 192(4), 565–570.PubMedCrossRef Andersson, U., Wang, H., Palmblad, K., Aveberger, A. C., Bloom, O., Erlandsson-Harris, H., et al. (2000). High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J Exp Med, 192(4), 565–570.PubMedCrossRef
49.
go back to reference Wang, H., Bloom, O., Zhang, M., Vishnubhakat, J. M., Ombrellino, M., Che, J., et al. (1999). HMG-1 as a late mediator of endotoxin lethality in mice. Science, 285(5425), 248–251.PubMedCrossRef Wang, H., Bloom, O., Zhang, M., Vishnubhakat, J. M., Ombrellino, M., Che, J., et al. (1999). HMG-1 as a late mediator of endotoxin lethality in mice. Science, 285(5425), 248–251.PubMedCrossRef
50.
go back to reference Bonaldi, T., Talamo, F., Scaffidi, P., Ferrera, D., Porto, A., Bachi, A., et al. (2003). Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J, 22(20), 5551–5560.PubMedCrossRef Bonaldi, T., Talamo, F., Scaffidi, P., Ferrera, D., Porto, A., Bachi, A., et al. (2003). Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J, 22(20), 5551–5560.PubMedCrossRef
51.
go back to reference Gardella, S., Andrei, C., Ferrera, D., Lotti, L. V., Torrisi, M. R., Bianchi, M. E., et al. (2002). The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesicle-mediated secretory pathway. EMBO Rep, 3(10), 995–1001.PubMedCrossRef Gardella, S., Andrei, C., Ferrera, D., Lotti, L. V., Torrisi, M. R., Bianchi, M. E., et al. (2002). The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesicle-mediated secretory pathway. EMBO Rep, 3(10), 995–1001.PubMedCrossRef
52.
go back to reference Sancho, D., Joffre, O. P., Keller, A. M., Rogers, N. C., Martinez, D., Hernanz-Falcon, P., et al. (2009). Identification of a dendritic cell receptor that couples sensing of necrosis to immunity. Nature, 458(7240), 899–903.PubMedCrossRef Sancho, D., Joffre, O. P., Keller, A. M., Rogers, N. C., Martinez, D., Hernanz-Falcon, P., et al. (2009). Identification of a dendritic cell receptor that couples sensing of necrosis to immunity. Nature, 458(7240), 899–903.PubMedCrossRef
53.
go back to reference Shankaran, V., Ikeda, H., Bruce, A. T., White, J. M., Swanson, P. E., Old, L. J., et al. (2001). IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature, 410(6832), 1107–1111.PubMedCrossRef Shankaran, V., Ikeda, H., Bruce, A. T., White, J. M., Swanson, P. E., Old, L. J., et al. (2001). IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature, 410(6832), 1107–1111.PubMedCrossRef
55.
go back to reference Franchi, L., Eigenbrod, T., Munoz-Planillo, R., & Nunez, G. (2009). The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat Immunol, 10(3), 241–247.PubMedCrossRef Franchi, L., Eigenbrod, T., Munoz-Planillo, R., & Nunez, G. (2009). The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat Immunol, 10(3), 241–247.PubMedCrossRef
56.
go back to reference Latz, E. (2010). The inflammasomes: mechanisms of activation and function. Curr Opin Immunol, 22(1), 28–33.PubMedCrossRef Latz, E. (2010). The inflammasomes: mechanisms of activation and function. Curr Opin Immunol, 22(1), 28–33.PubMedCrossRef
57.
go back to reference Martins, I., Tesniere, A., Kepp, O., Michaud, M., Schlemmer, F., Senovilla, L., et al. (2009). Chemotherapy induces ATP release from tumor cells. Cell Cycle, 8(22), 3723–3728.PubMedCrossRef Martins, I., Tesniere, A., Kepp, O., Michaud, M., Schlemmer, F., Senovilla, L., et al. (2009). Chemotherapy induces ATP release from tumor cells. Cell Cycle, 8(22), 3723–3728.PubMedCrossRef
58.
go back to reference Ferrari, D., Pizzirani, C., Adinolfi, E., Lemoli, R. M., Curti, A., Idzko, M., et al. (2006). The P2X7 receptor: a key player in IL-1 processing and release. J Immunol, 176(7), 3877–3883.PubMed Ferrari, D., Pizzirani, C., Adinolfi, E., Lemoli, R. M., Curti, A., Idzko, M., et al. (2006). The P2X7 receptor: a key player in IL-1 processing and release. J Immunol, 176(7), 3877–3883.PubMed
59.
go back to reference Elliott, M. R., Chekeni, F. B., Trampont, P. C., Lazarowski, E. R., Kadl, A., Walk, S. F., et al. (2009). Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature, 461(7261), 282–286.PubMedCrossRef Elliott, M. R., Chekeni, F. B., Trampont, P. C., Lazarowski, E. R., Kadl, A., Walk, S. F., et al. (2009). Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature, 461(7261), 282–286.PubMedCrossRef
60.
go back to reference Stout, C. E., Costantin, J. L., Naus, C. C., & Charles, A. C. (2002). Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem, 277(12), 10482–10488.PubMedCrossRef Stout, C. E., Costantin, J. L., Naus, C. C., & Charles, A. C. (2002). Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem, 277(12), 10482–10488.PubMedCrossRef
61.
go back to reference Zhang, Z., Chen, G., Zhou, W., Song, A., Xu, T., Luo, Q., et al. (2007). Regulated ATP release from astrocytes through lysosome exocytosis. Nat Cell Biol, 9(8), 945–953.PubMedCrossRef Zhang, Z., Chen, G., Zhou, W., Song, A., Xu, T., Luo, Q., et al. (2007). Regulated ATP release from astrocytes through lysosome exocytosis. Nat Cell Biol, 9(8), 945–953.PubMedCrossRef
Metadata
Title
Molecular determinants of immunogenic cell death elicited by anticancer chemotherapy
Authors
Oliver Kepp
Lorenzo Galluzzi
Isabelle Martins
Frederic Schlemmer
Sandy Adjemian
Mickael Michaud
Abdul Qader Sukkurwala
Laurie Menger
Laurence Zitvogel
Guido Kroemer
Publication date
01-03-2011
Publisher
Springer US
Published in
Cancer and Metastasis Reviews / Issue 1/2011
Print ISSN: 0167-7659
Electronic ISSN: 1573-7233
DOI
https://doi.org/10.1007/s10555-011-9273-4

Other articles of this Issue 1/2011

Cancer and Metastasis Reviews 1/2011 Go to the issue

EditorialNotes

Preface

Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine