Immunogenic cell death and DAMPs in cancer therapy

Krysko, Dmitri V.; Garg, Abhishek D.; Kaczmarek, Agnieszka; Krysko, Olga; Agostinis, Patrizia; Vandenabeele, Peter

doi:10.1038/nrc3380

Cited by 3,223Cell death mechanisms and regulationImmunotherapy and Immune ResponsesImmune Response and Inflammation

Immunogenic cell death and DAMPs in cancer therapy

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Krysko, Dmitri V., Garg, Abhishek D., Kaczmarek, Agnieszka, Krysko, Olga, Agostinis, Patrizia, Vandenabeele, Peter·2012·Nature Reviews Cancer

DOI 10.1038/nrc3380

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Abstract

Although it was thought that apoptotic cells, when rapidly phagocytosed, underwent a silent death that did not trigger an immune response, in recent years a new concept of immunogenic cell death (ICD) has emerged. The immunogenic characteristics of ICD are mainly mediated by damage-associated molecular patterns (DAMPs), which include surface-exposed calreticulin (CRT), secreted ATP and released high mobility group protein B1 (HMGB1). Most DAMPs can be recognized by pattern recognition receptors (PRRs). In this Review, we discuss the role of endoplasmic reticulum (ER) stress and reactive oxygen species (ROS) in regulating the immunogenicity of dying cancer cells and the effect of therapy-resistant cancer microevolution on ICD.

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CRT translocation from endoplasmic reticulum to the out-layer of plasma membrane depends on ER stress and is associated with PERK-mediated eIF2α phosphorylation.
“It is known that CRT translocation from endoplasmic reticulum (ER) to the out-layer of plasma membrane depends on an ER stress and associated with ER kinase (PERK)-mediated eIF2α phosphorylation [18, 19].”
From Inhibition of HIF-1α by PX-478 enhances the anti-tumor effect of gemcitabine by inducing immunogenic cell death in pancreatic ductal adenocarcinoma (2015) · cites this paper as [19]
Dying cells can expose or release molecules (DAMPs or alarmins) that alert the organism or colony about a potential threat.
“Such a homeostatic function not only reflects the elimination of useless or potentially dangerous cells, but also the ability of dying cells to expose or release molecules that alert the organism or colony about a potential threat. Such danger signals are commonly referred to as damage-associated molecular patterns (DAMPs) or alarmins [19–22].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [20]

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Köröskényi, K., Duró, E., Pallai, A., Sarang, Z., Kloor, D., Ucker, D. S., Beceiro, S., Castrillo, A., Chawla, A., Ledent, C. A., et al. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1002284 · Cited by 83 · see citing works
Anticancer activities of adenine nucleotides in mice are mediated through expansion of erythrocyte ATP pools.
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Increased expression of HMGB1 is associated with poor prognosis in human bladder cancer
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Mechanisms of induction of apoptosis by anthraquinone anticancer drugs aclarubicin and mitoxantrone in comparison with doxorubicin: Relation to drug cytotoxicity and caspase-3 activation
Koceva‐Chyła, A., Jędrzejczak, M., Skierski, J., et al. (2005) · APOPTOSIS · doi:10.1007/s10495-005-1540-9 · Cited by 79 · see citing works
Targeting Cancer-initiating Cells With Oncolytic Viruses
Cripe, T. P., Wang, P.-Y., Marcato, P., et al. (2009) · Molecular Therapy · doi:10.1038/mt.2009.193 · Cited by 79 · see citing works
Specific Recognition of Apoptotic Cells Reveals a Ubiquitous and Unconventional Innate Immunity
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Differential expression proteomics of human colon cancer
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Functional expression of TLR9 is associated to the metastatic potential of human lung cancer cell
Ren, T., Wen, Z.-K., Liu, Z.-M., Liang, Y.-J., Guo, Z., & Xu, L. (2007) · Cancer Biology & Therapy · doi:10.4161/cbt.6.11.4826 · Cited by 78 · see citing works
Topoisomerase II Is Required for Mitoxantrone to Signal Nuclear Factor κB Activation in HL60 Cells
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Cyclophilin A Is a Damage-Associated Molecular Pattern Molecule That Mediates Acetaminophen-Induced Liver Injury
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Hepatoma-derived Growth Factor Is a Neurotrophic Factor Harbored in the Nucleus
Zhou, Z., Yamamoto, Y., Sugai, F., Yoshida, K., Kishima, Y., Sumi, H., Nakamura, H., & Sakoda, S. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m308650200 · Cited by 72 · see citing works
Subversion of the chemotherapy-induced anticancer immune response by the ecto-ATPase CD39
Michaud, M., Sukkurwala, A. Q., Martins, I., Shen, S., Zitvogel, L., & Kroemer, G. (2012) · OncoImmunology · doi:10.4161/onci.19070 · Cited by 67 · see citing works
Adriamycin-induced modulation of host defenses in tumor-bearing mice.
Maccubbin, D., Wing, K. R., Mace, K. F., et al. (1992) · PubMed · Cited by 65 · see citing works
Nonheritable Cellular Variability Accelerates the Evolutionary Processes of Cancer
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Extracellular heat shock protein HSP90β secreted by MG63 osteosarcoma cells inhibits activation of latent TGF-β1
Suzuki, S., & Kulkarni, A. B. (2010) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2010.06.112 · Cited by 63 · see citing works
Low dose hypericin-PDT induces complete tumor regression in BALB/c mice bearing CT26 colon carcinoma
Šanović, R., Verwanger, T., Hartl, A. J., et al. (2011) · Photodiagnosis and Photodynamic Therapy · doi:10.1016/j.pdpdt.2011.04.003 · Cited by 63 · see citing works
Caspase-8 deficiency facilitates cellular transformation in vitro
Krelin, Y., Zhang, L., Kang, T.-B., et al. (2008) · Cell Death and Differentiation · doi:10.1038/cdd.2008.88 · Cited by 62 · see citing works
Effect of Ionizing Radiation on AP-1 Binding Activity and Basic Fibroblast Growth Factor Gene Expression in Drug-sensitive Human Breast Carcinoma MCF-7 and Multidrug-resistant MCF-7/ADR Cells
Lee, Y. J., Galoforo, S., Berns, C. M., Erdös, G., Gupta, A., Ways, D. K., & Corry, P. M. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.48.28790 · Cited by 60 · see citing works
In Vitro Studies on Erythrosine-Based Photodynamic Therapy of Malignant and Pre-Malignant Oral Epithelial Cells
Garg, A. D., Bose, M., Ahmed, M. I., Bonass, W. A., & Wood, S. R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034475 · Cited by 60 · see citing works
Self-citation
Reactive Carbonyls Are a Major Th2-Inducing Damage-Associated Molecular Pattern Generated by Oxidative Stress
Moghaddam, A. E., Gartlan, K. H., Kong, L., & Sattentau, Q. J. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1003906 · Cited by 60 · see citing works
Functional Analysis of Recombinant Calreticulin Fragment 39–272: Implications for Immunobiological Activities of Calreticulin in Health and Disease
Hong, C., Qiu, X., Li, Y., et al. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1000536 · Cited by 56 · see citing works
Coxsackievirus B3 activates nuclear factor kappa B transcription factor via a phosphatidylinositol-3 kinase/protein kinase B-dependent pathway to improve host cell viability
Esfandiarei, M., Boroomand, S., Suarez, A., Si, X., Rahmani, M., & McManus, B. M. (2007) · Cellular Microbiology · doi:10.1111/j.1462-5822.2007.00964.x · Cited by 53 · see citing works
Amplification of the γ-irradiation-induced cell death pathway by reactive oxygen species in human U937 cells
Kim, E. M., Yang, H. S., Kang, S. W., Ho, J., Lee, S. B., & Um, H. (2008) · Cellular Signalling · doi:10.1016/j.cellsig.2008.01.002 · Cited by 52 · see citing works
The chemotherapeutic drug oxaliplatin differentially affects blood DC function dependent on environmental cues
Tel, J., Hato, S. V., Torensma, R., Buschow, S. I., Figdor, C. G., Lesterhuis, W. J., & de Vries, I. J. M. (2011) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-011-1189-x · Cited by 49 · see citing works
Chemistry of St. John's Wort: Hypericin and Hyperforin
Vollmer, J. J., & Rosenson, J. (2004) · Journal of Chemical Education · doi:10.1021/ed081p1450 · Cited by 46 · see citing works
Loss-of-function alleles ofP2RX7andTLR4fail to affect the response to chemotherapy in non-small cell lung cancer
Vacchelli, E., Galluzzi, L., Rousseau, V., Rigoni, A., Tesnière, A., Delahaye, N., Schlemmer, F., Menger, L., Sukkurwala, A. Q., Adjemian, S., et al. (2012) · OncoImmunology · doi:10.4161/onci.18684 · Cited by 45 · see citing works
T cells are crucial for the anti-metastatic effect of anti-epidermal growth factor receptor antibodies
Garrido, G., Lorenzano, P., Sánchez, B., Beausoleil, I., Alonso, D. F., Pérez, R., & Fernandez, L. E. (2007) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-007-0313-4 · Cited by 44 · see citing works
Shikonin inhibits tumor invasion via down‐regulation of NF‐κB‐mediated MMP‐9 expression in human ACC‐M cells
Min, R., Zun, Z., Min, Y., et al. (2010) · Oral Diseases · doi:10.1111/j.1601-0825.2010.01758.x · Cited by 43 · see citing works
Combined modalities of resistance in an oxaliplatin-resistant human gastric cancer cell line with enhanced sensitivity to 5-fluorouracil
Chen, C.-C., Chen, L.-T., Tsou, T., et al. (2007) · British Journal of Cancer · doi:10.1038/sj.bjc.6603866 · Cited by 41 · see citing works
Here, There Be Dragons : Charting Autophagy-Related Alterations in Human Tumors
Lebovitz, C. B., Bortnik, S. B., & Gorski, S. M. (2012) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-11-2465 · Cited by 40 · see citing works
Shikonin Derivatives Protect Immune Organs from Damage and Promote Immune Responses In Vivo in Tumour‐bearing Mice
Su, L., GuangZhi, Y., BaoJie, G., et al. (2011) · Phytotherapy Research · doi:10.1002/ptr.3503 · Cited by 39 · see citing works
The Role of the VPS4A-Exosome Pathway in the Intrinsic Egress Route of a DNA-Binding Anticancer Drug
Chen, V. Y., Posada, M. M., Blazer, L. L., Zhao, T., & Rosania, G. R. (2006) · Pharmaceutical Research · doi:10.1007/s11095-006-9043-0 · Cited by 39 · see citing works
Clearance of dead cells: mechanisms, immune responses and implication in the development of diseases
Krysko, D. V., & Vandenabeele, P. (2010) · APOPTOSIS · doi:10.1007/s10495-010-0524-6 · Cited by 39 · see citing works
Self-citation
Hypericin photoactivation triggers down-regulation of matrix metalloproteinase-9 expression in well-differentiated human nasopharyngeal cancer cells
Du, H., Olivo, M., Mahendran, R., Huang, Q. B., Shen, H., Ong, C. N., & Bay, B. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-7030-1 · Cited by 37 · see citing works
Bax deficiency prolongs cerebellar neurogenesis, accelerates medulloblastoma formation and paradoxically increases both malignancy and differentiation
Garcia, I., Crowther, A., Gama, V., Miller, C. R., Deshmukh, M., & Gershon, T. R. (2012) · Oncogene · doi:10.1038/onc.2012.248 · Cited by 35 · see citing works
Extracellular BCL2 Proteins Are Danger-Associated Molecular Patterns That Reduce Tissue Damage in Murine Models of Ischemia-Reperfusion Injury
Iwata, A., Morgan‐Stevenson, V., Schwartz, B. R., Liu, L., Tupper, J. C., Zhu, X., Harlan, J., & Winn, R. K. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009103 · Cited by 31 · see citing works
Doxorubicin prevents endoplasmic reticulum stress-induced apoptosis
Kim, S., Park, K. M., Kim, N., et al. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.11.040 · Cited by 27 · see citing works
The immunity-related GTPase Irgm3 relieves endoplasmic reticulum stress response during coxsackievirus B3 infection via a PI3K/Akt dependent pathway
Liu, Z., Zhang, H. M., Ji, Y., et al. (2011) · Cellular Microbiology · doi:10.1111/j.1462-5822.2011.01708.x · Cited by 24 · see citing works
Killing of Resistant Cancer Cells with Low Bak by a Combination of an Antimesothelin Immunotoxin and a TRAIL Receptor 2 Agonist Antibody
Du, X., Xiang, L., Mackall, C. L., et al. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-11-1235 · Cited by 24 · see citing works
The n3-polyunsaturated fatty acid docosahexaenoic acid induces immunogenic cell death in human cancer cell lines via pre-apoptotic calreticulin exposure
Molinari, R., D’Eliseo, D., Manzi, L., Zolla, L., Velotti, F., & Merendino, N. (2011) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-011-1074-7 · Cited by 23 · see citing works

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Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018.
Galluzzi, L., Vitale, I., Aaronson, S. A., Abrams, J. M., Adam, D., Agostinis, P., Alnemri, E. S., Altucci, L., Amelio, I., Andrews, D. W., et al. (2018) · Cell Death & Differentiation · doi:10.1038/s41418-017-0012-4 · Cited by 6,680 · see citing works
Self-citation
Immunogenic cell death in cancer and infectious disease
Galluzzi, L., Buqué, A., Kepp, O., Zitvogel, L., & Kroemer, G. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2016.107 · Cited by 3,119 · see citing works
The immune contexture in cancer prognosis and treatment
Fridman, W. H., Zitvogel, L., Sautès–Fridman, C., & Kroemer, G. (2017) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2017.101 · Cited by 2,263 · see citing works
The Tumour Microenvironment after Radiotherapy: Mechanisms of Resistance and Recurrence
Barker, H. E., Paget, J. T. E., Khan, A. A., & Harrington, K. J. (2015) · Nature Reviews Cancer · doi:10.1038/nrc3958 · Cited by 2,144 · see citing works
Somatic <i>CALR</i> Mutations in Myeloproliferative Neoplasms with Nonmutated <i>JAK2</i>
Nangalia, J., Massie, C. E., Baxter, E. J., Nice, F. L., Gundem, G., Wedge, D. C., Avezov, E., Li, J., Kollmann, K., Kent, D. G., et al. (2013) · New England Journal of Medicine · doi:10.1056/nejmoa1312542 · Cited by 1,756 · see citing works
Immunological effects of conventional chemotherapy and targeted anticancer agents
Galluzzi, L., Buqué, A., Kepp, O., Zitvogel, L., & Kroemer, G. (2015) · Cancer Cell · doi:10.1016/j.ccell.2015.10.012 · Cited by 1,530 · see citing works
Necroptosis: The Release of Damage-Associated Molecular Patterns and Its Physiological Relevance
Kaczmarek, A., Vandenabeele, P., & Krysko, D. V. (2013) · Immunity · doi:10.1016/j.immuni.2013.02.003 · Cited by 1,411 · see citing works
Self-citation
Immunostimulation with chemotherapy in the era of immune checkpoint inhibitors
Galluzzi, L., Humeau, J., Buqué, A., Zitvogel, L., & Kroemer, G. (2020) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-020-0413-z · Cited by 1,349 · see citing works
Apoptotic cell clearance: basic biology and therapeutic potential
Poon, I. K. H., Lucas, C. D., Rossi, A. G., & Ravichandran, K. S. (2014) · Nature Reviews Immunology · doi:10.1038/nri3607 · Cited by 1,223 · see citing works
Essential versus accessory aspects of cell death: recommendations of the NCCD 2015
Galluzzi, L., Bravo-San Pedro, J. M., Vitale, I., Aaronson, S. A., Abrams, J. M., Adam, D., Alnemri, E. S., Altucci, L., Andrews, D., Annicchiarico-Petruzzelli, M., et al. (2015) · Cell Death & Differentiation · doi:10.1038/cdd.2014.137 · Cited by 1,002 · see citing works
Self-citation
HMGB1 in health and disease
Kang, R., Chen, R., Zhang, Q., Hou, W., Wu, S., Cao, L., Huang, J., Yu, Y., Fan, X.-G., Yan, Z., et al. (2014) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2014.05.001 · Cited by 956 · see citing works
The Basis of Oncoimmunology
Palucka, A. K., & Coussens, L. M. (2016) · Cell · doi:10.1016/j.cell.2016.01.049 · Cited by 843 · see citing works
Consensus guidelines for the detection of immunogenic cell death
Kepp, O., Senovilla, L., Vitale, I., Vacchelli, E., Adjemian, S., Agostinis, P., Apetoh, L., Aranda, F., Barnaba, V., Bloy, N., et al. (2014) · OncoImmunology · doi:10.4161/21624011.2014.955691 · Cited by 832 · see citing works
Self-citation
Platelets release mitochondria serving as substrate for bactericidal group IIA-secreted phospholipase A2 to promote inflammation
Boudreau, L. H., Duchez, A.-C., Cloutier, N., Soulet, D., Martin, N., Bollinger, J., Paré, A., Rousseau, M., Naika, G. S., Lévesque, T., et al. (2014) · Blood · doi:10.1182/blood-2014-05-573543 · Cited by 703 · see citing works
Molecular mechanisms of ATP secretion during immunogenic cell death
Martins, I., Wang, Y., Michaud, M., Ma, Y., Sukkurwala, A. Q., Shen, S., Kepp, O., Métivier, D., Galluzzi, L., Perfettini, J.-L., et al. (2014) · Cell Death & Differentiation · doi:10.1038/cdd.2013.75 · Cited by 563 · see citing works
Nutrition, inflammation and cancer
Zitvogel, L., Pietrocola, F., & Kroemer, G. (2017) · Nature Immunology · doi:10.1038/ni.3754 · Cited by 446 · see citing works
Targeting glutamine metabolism enhances tumor-specific immunity by modulating suppressive myeloid cells
Oh, M.-H., Sun, I.-H., Zhao, L., Leone, R. D., Sun, I.-M., Xu, W., Collins, S. L., Tam, A. J., Blosser, R. L., Patel, C. H., et al. (2020) · Journal of Clinical Investigation · doi:10.1172/jci131859 · Cited by 456 · see citing works
Molecular Mechanisms of Radiation-Induced Cancer Cell Death: A Primer
Sia, J., Szmyd, R., Hau, E., & Gee, H. E. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00041 · Cited by 378 · see citing works
Metal Drugs and the Anticancer Immune Response
Englinger, B., Pirker, C., Heffeter, P., Terenzi, A., Kowol, C. R., Keppler, B. K., & Berger, W. (2019) · Chemical Reviews · doi:10.1021/acs.chemrev.8b00396 · Cited by 355 · see citing works
ROS-induced autophagy in cancer cells assists in evasion from determinants of immunogenic cell death
Garg, A. D., Dudek, A. M., Ferreira, G. B., Verfaillie, T., Vandenabeele, P., Krysko, D. V., Mathieu, C., & Agostinis, P. (2013) · Autophagy · doi:10.4161/auto.25399 · Cited by 305 · see citing works
Self-citation
Metal-based anticancer agents as immunogenic cell death inducers: the past, present, and future
Sen, S., Won, M., Levine, M. S., Noh, Y., Sedgwick, A. C., Kim, J. S., Sessler, J. L., & Arambula, J. F. (2022) · Chemical Society Reviews · doi:10.1039/d1cs00417d · Cited by 297 · see citing works
Gathering brings strength: How organic aggregates boost disease phototheranostics
Qi, J., Ou, H., Liu, Q., & Ding, D. (2021) · Aggregate · doi:10.1002/agt2.25 · Cited by 284 · see citing works
Immunostimulatory nanomedicines synergize with checkpoint blockade immunotherapy to eradicate colorectal tumors
Duan, X., Chan, C., Han, W., Guo, N., Weichselbaum, R. R., & Lin, W. (2019) · Nature Communications · doi:10.1038/s41467-019-09221-x · Cited by 256 · see citing works
Trial watch: TLR3 agonists in cancer therapy
Le Naour, J., Galluzzi, L., Zitvogel, L., Kroemer, G., & Vacchelli, E. (2020) · OncoImmunology · doi:10.1080/2162402x.2020.1771143 · Cited by 239 · see citing works
Dinaciclib induces immunogenic cell death and enhances anti-PD1-mediated tumor suppression
Hossain, D. M. S., Javaid, S., Cai, M., Zhang, C., Sawant, A., Hinton, M., Sathe, M., Grein, J., Blumenschein, W., Pinheiro, E. M., et al. (2018) · Journal of Clinical Investigation · doi:10.1172/jci94586 · Cited by 216 · see citing works
Gastro-intestinal toxicity of chemotherapeutics in colorectal cancer: The role of inflammation
Lee, C. S. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i14.3751 · Cited by 224 · see citing works
Pyroptosis‐Mediated Synergistic Photodynamic and Photothermal Immunotherapy Enabled by a Tumor‐Membrane‐Targeted Photosensitive Dimer
Tang, Y., Bisoyi, H. K., Chen, X., Liu, Z., Chen, X., Zhang, S., & Li, Q. (2023) · Advanced Materials · doi:10.1002/adma.202300232 · Cited by 214 · see citing works
Engineering nanomedicines through boosting immunogenic cell death for improved cancer immunotherapy
Gao, J., Wang, W.-Q., Pei, Q., Lord, M. S., & Yu, H.-J. (2020) · Acta Pharmacologica Sinica · doi:10.1038/s41401-020-0400-z · Cited by 203 · see citing works
Physical modalities inducing immunogenic tumor cell death for cancer immunotherapy
Adkins, I., Fucikova, J., Garg, A. D., Agostinis, P., & Špíšek, R. (2014) · OncoImmunology · doi:10.4161/21624011.2014.968434 · Cited by 200 · see citing works
Self-citation
Biodegradable Hollow Mesoporous Silica Nanoparticles for Regulating Tumor Microenvironment and Enhancing Antitumor Efficiency
Kong, M., Tang, J., Qiao, Q., Wu, T., Qi, Y., Tan, S., Gao, X., & Zhang, Z. (2017) · Theranostics · doi:10.7150/thno.19987 · Cited by 197 · see citing works
Normalization of the tumor microenvironment by harnessing vascular and immune modulation to achieve enhanced cancer therapy
Choi, Y., & Jung, K. (2023) · Experimental & Molecular Medicine · doi:10.1038/s12276-023-01114-w · Cited by 188 · see citing works
Regulated cell death and adaptive stress responses
Galluzzi, L., Bravo-San Pedro, J. M., Kepp, O., & Kroemer, G. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2209-y · Cited by 177 · see citing works
Immunological Mechanisms Underneath the Efficacy of Cancer Therapy
Galluzzi, L., Zitvogel, L., & Kroemer, G. (2016) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-16-0197 · Cited by 175 · see citing works
Prognostic and predictive value of DAMPs and DAMP-associated processes in cancer
Fucikova, J., Moserova, I., Urbanova, L., Bezu, L., Kepp, O., Cremer, I., Salek, C., Strnad, P., Kroemer, G., Galluzzi, L., et al. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00402 · Cited by 159 · see citing works
Current Challenges and Opportunities of Photodynamic Therapy against Cancer
Huis in ‘t Veld, R. V., Heuts, J., Ma, S., Cruz, L. J., Ossendorp, F. A., & Jager, M. J. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15020330 · Cited by 159 · see citing works
Biomembrane-based nanostructures for cancer targeting and therapy: From synthetic liposomes to natural biomembranes and membrane-vesicles
Wang, J., Zhu, M., & Nie, G. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2021.113974 · Cited by 153 · see citing works
Noninvasively immunogenic sonodynamic therapy with manganese protoporphyrin liposomes against triple-negative breast cancer
Chen, H., Liu, L., Ma, A., Yin, T., Chen, Z., Liang, R., Qiu, Y., Zheng, M., & Cai, L. (2021) · Biomaterials · doi:10.1016/j.biomaterials.2020.120639 · Cited by 144 · see citing works
Inhibition of HIF-1α by PX-478 enhances the anti-tumor effect of gemcitabine by inducing immunogenic cell death in pancreatic ductal adenocarcinoma
Zhao, T., Ren, H., Jia, L., Chen, J., Xin, W., Yan, F., Li, J., Wang, X., Gao, S., Qian, D., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.2948 · Cited by 142 · see citing works
“It is known that CRT translocation from endoplasmic reticulum (ER) to the out-layer of plasma membrane depends on an ER stress and associated with ER kinase (PERK)-mediated eIF2α phosphorylation [18, 19].”
BackgroundMethodInfluential
DAMPs, ageing, and cancer: The ‘DAMP Hypothesis’
Huang, J., Xie, Y., Sun, X., Zeh, H. J., Kang, R., Lotze, M. T., & Tang, D. (2015) · Ageing Research Reviews · doi:10.1016/j.arr.2014.10.004 · Cited by 144 · see citing works
Calreticulin exposure by malignant blasts correlates with robust anticancer immunity and improved clinical outcome in AML patients
Fucikova, J., Truxova, I., Hensler, M., Becht, E., Kasikova, L., Moserova, I., Vosahlikova, S., Klouckova, J., Church, S. E., Cremer, I., et al. (2016) · Blood · doi:10.1182/blood-2016-08-731737 · Cited by 135 · see citing works
Chemotherapeutic and targeted drugs-induced immunogenic cell death in cancer models and antitumor therapy: an update review
Zhai, J., Gu, X., Liu, Y., Hu, Y., Jiang, Y., & Zhang, Z. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1152934 · Cited by 131 · see citing works
The presence of LC3B puncta and HMGB1 expression in malignant cells correlate with the immune infiltrate in breast cancer
Ladoire, S., Enot, D., Senovilla, L., Ghiringhelli, F., Poirier-Colame, V., Chaba, K., Semeraro, M., Chaix, M., Penault-Llorca, F., Arnould, L., et al. (2016) · Autophagy · doi:10.1080/15548627.2016.1154244 · Cited by 117 · see citing works
Trial Watch: experimental TLR7/TLR8 agonists for oncological indications
Frega, G., Wu, Q., Le Naour, J., Vacchelli, E., Galluzzi, L., Kroemer, G., & Kepp, O. (2020) · OncoImmunology · doi:10.1080/2162402x.2020.1796002 · Cited by 108 · see citing works
Co-delivery of Dihydroartemisinin and Pyropheophorbide-Iron Elicits Ferroptosis to Potentiate Cancer Immunotherapy
Han, W., Duan, X., Ni, K., Li, Y., Chan, C., & Lin, W. (2022) · Biomaterials · doi:10.1016/j.biomaterials.2021.121315 · Cited by 103 · see citing works
Delivery Strategies for Immune Checkpoint Blockade
Chen, Q., Wang, C., Chen, G., Hu, Q., & Gu, Z. (2018) · Advanced Healthcare Materials · doi:10.1002/adhm.201800424 · Cited by 90 · see citing works
Type I interferons and endoplasmic reticulum stress in health and disease
(2020) · International Review of Cell and Molecular Biology · doi:10.1016/bs.ircmb.2019.10.004 · Cited by 83 · see citing works
Resistance to anticancer vaccination effect is controlled by a cancer cell-autonomous phenotype that disrupts immunogenic phagocytic removal
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Authors: Krysko, D. V., Garg, A. D., Kaczmarek, A., Krysko, O., Agostinis, P., & Vandenabeele, P.
Affiliations: Vlaams Instituut voor Biotechnologie (BE)
KU Leuven (BE)
Ghent University Hospital (BE)
Corresponding author: Krysko, Dmitri V.
Vandenabeele, Peter
ORCID: Krysko, Dmitri V.
Garg, Abhishek D.
Kaczmarek, Agnieszka
Krysko, Olga
Agostinis, Patrizia
Vandenabeele, Peter
Venue: Nature Reviews Cancer
Publisher: Springer Science and Business Media LLC
Published: 2012-11-15
Volume: 12
Issue: 12
Pages: 860-875
ISSN: 1474-175X (ISSN-L)
1474-1768
DOI: 10.1038/nrc3380
OpenAlex: W2067632426
Cited by: 3,223
References: 211
Citations by year: 2026: 353 · 2025: 446 · 2024: 474 · 2023: 483 · 2022: 373 · 2021: 268 · 2020: 209 · 2019: 121 · 2018: 99 · 2017: 87 · 2016: 96 · 2015: 85 · 2014: 77 · 2013: 50
FWCI: 6.18
Type: journal article
Language: en
Open access: green
zenodo.org
Licence: other-oa
www.springer.com/tdm (tdm)
Locations: Nature reviews. Cancer (publishedVersion)
PubMed (publishedVersion)
Ghent University Academic Bibliography (Ghent University) (submittedVersion)
Lirias (submittedVersion)
Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, other-oa)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Keywords: immunogenic cell death, damage-associated molecular patterns, endoplasmic reticulum stress, reactive oxygen species, calreticulin, ATP, HMGB1, pattern recognition receptors, cancer immunotherapy, treatment resistance, cancer cell death
MeSH terms: Adenosine Triphosphate, Animals, Antineoplastic Agents, Endoplasmic Reticulum, Humans, Neoplasms, Phagocytosis, Cell Death, Reactive Oxygen Species, HMGB1 Protein, Calreticulin

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