A novel pathway combining calreticulin exposure and ATP secretion in immunogenic cancer cell death
Open accessAbstract
Surface-exposed calreticulin (ecto-CRT) and secreted ATP are crucial damage-associated molecular patterns (DAMPs) for immunogenic apoptosis. Inducers of immunogenic apoptosis rely on an endoplasmic reticulum (ER)-based (reactive oxygen species (ROS)-regulated) pathway for ecto-CRT induction, but the ATP secretion pathway is unknown. We found that after photodynamic therapy (PDT), which generates ROS-mediated ER stress, dying cancer cells undergo immunogenic apoptosis characterized by phenotypic maturation (CD80(high), CD83(high), CD86(high), MHC-II(high)) and functional stimulation (NO(high), IL-10(absent), IL-1β(high)) of dendritic cells as well as induction of a protective antitumour immune response. Intriguingly, early after PDT the cancer cells displayed ecto-CRT and secreted ATP before exhibiting biochemical signatures of apoptosis, through overlapping PERK-orchestrated pathways that require a functional secretory pathway and phosphoinositide 3-kinase (PI3K)-mediated plasma membrane/extracellular trafficking. Interestingly, eIF2α phosphorylation and caspase-8 signalling are dispensable for this ecto-CRT exposure. We also identified LRP1/CD91 as the surface docking site for ecto-CRT and found that depletion of PERK, PI3K p110α and LRP1 but not caspase-8 reduced the immunogenicity of the cancer cells. These results unravel a novel PERK-dependent subroutine for the early and simultaneous emission of two critical DAMPs following ROS-mediated ER stress.
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CALR knockdown or defects in CALR exposure abolish ability of anthracycline-treated dying cancer cells to establish protective immunity in mice; recombinant CALR confers immunogenic properties to non-immunogenic RCD.
“In line with a key role of CALR in the immunogenicity of RCD, the RNAi-mediated knockdown of CALR as well as natural defects in the CALR exposure pathway reportedly abolish the ability of dying cancer cells succumbing to anthracyclines to establish protective immunity in mice, whereas the exogenous provision of recombinant CALR confers immunogenic properties to otherwise non-immunogenic variants”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [883]
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Pattern Recognition Receptors and the Host Cell Death Molecular Machinery
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DAMPs from Cell Death to New Life
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The hallmarks of cancer immune evasion
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Innate Immune Recognition of Cancer
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New functions of mitochondria associated membranes in cellular signaling
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ROS-induced autophagy in cancer cells assists in evasion from determinants of immunogenic cell death
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Self-citationRole of nonresolving inflammation in hepatocellular carcinoma development and progression
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Many faces of DAMPs in cancer therapy
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Trial watch: Immunogenic cell death induction by anticancer chemotherapeutics
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Self-citationHypoxia-Driven Immune Escape in the Tumor Microenvironment
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Autophagy: shaping the tumor microenvironment and therapeutic response
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Resolvins suppress tumor growth and enhance cancer therapy
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Inducers of immunogenic cancer cell death
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Self-citationAnthracyclines/trastuzumab: new aspects of cardiotoxicity and molecular mechanisms
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Self-citationNanoparticle-Mediated Remodeling of the Tumor Microenvironment to Enhance Immunotherapy
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Crosstalk between ER stress and immunogenic cell death
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Metal-Based Photosensitizers as Inducers of Regulated Cell Death Mechanisms
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Danger Signals Activating the Immune Response after Trauma
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Vitiligo: How do oxidative stress-induced autoantigens trigger autoimmunity?
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The Unfolded Protein Response in Immunogenic Cell Death and Cancer Immunotherapy
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Origin and Consequences of Necroinflammation
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- Authors
- Garg, A. D., Krysko, D. V., Verfaillie, T., Kaczmarek, A., Ferreira, G. B., Marysael, T., Rubio, N., Firczuk, M., Mathieu, C., Roebroek, A. J. M., Annaert, W., Golab, J., de Witte, P., Vandenabeele, P., & Agostinis, P.
- Affiliations
- KU Leuven (BE)
- Vlaams Instituut voor Biotechnologie (BE)
- Corresponding author
- Agostinis, Patrizia
- ORCID
- Venue
- The EMBO Journal
- Published
- 2012-01-17
- Volume
- 31
- Issue
- 5
- Pages
- 1062-1079
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC3298003
- OpenAlex
- W1942176190
- Cited by
- 800
- References
- 76
- Citations by year
- 2026: 43 · 2025: 46 · 2024: 50 · 2023: 80 · 2022: 74 · 2021: 74 · 2020: 72 · 2019: 54 · 2018: 53 · 2017: 45 · 2016: 49 · 2015: 53 · 2014: 46 · 2013: 35 · 2012: 25
- FWCI
- 24.08
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- The EMBO Journal (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Ghent University Academic Bibliography (Ghent University) (submittedVersion)
- Lirias (submittedVersion)
- Funders
- University of Alberta
- European Commission (200767)
- Fundacja na rzecz Nauki Polskiej
- Fonds De La Recherche Scientifique - FNRS
- Fonds Wetenschappelijk Onderzoek (G.0529.08)
- KU Leuven (GOA/11/009)
- Universiteit Gent (01M00709)
- Servier
- Vlaamse regering (BOF09/01M00709)
- European Regional Development Fund (POIG. 01.01.02-00-008/08)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Endoplasmic Reticulum Stress and Disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- calreticulin, ATP release, immunogenic cancer cell death, photodynamic therapy, reactive oxygen species, endoplasmic reticulum stress, PERK, phosphatidylinositol 3-kinase, damage-associated molecular patterns, dendritic cell maturation, antitumor immunity, caspase-8, eIF2α phosphorylation, secretory pathway
- MeSH terms
- CD83 Antigen, Adenosine Triphosphate, Histocompatibility Antigens Class II, Cell Line, Dendritic Cells, Endoplasmic Reticulum, Humans, Immunoglobulins, Membrane Glycoproteins, Neoplasms, Antigens, CD, Cell Death, Photosensitizing Agents, Reactive Oxygen Species, B7-1 Antigen, Calreticulin, B7-2 Antigen
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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