Cited by 800Endoplasmic Reticulum Stress and DiseaseCell death mechanisms and regulationImmunotherapy and Immune Responses

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A novel pathway combining calreticulin exposure and ATP secretion in immunogenic cancer cell death

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Garg, Abhishek D, Krysko, Dmitri V, Verfaillie, Tom, Kaczmarek, Agnieszka, Ferreira, Gabriela B, Marysael, Thierry, Rubio, Noemi, Firczuk, Malgorzata, Mathieu, Chantal, Roebroek, Anton J M, Annaert, Wim, Golab, Jakub, de Witte, Peter, Vandenabeele, Peter, Agostinis, Patrizia·2012·The EMBO Journal

DOI 10.1038/emboj.2011.497PMC PMC3298003

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Abstract

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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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: Garg, Abhishek D
Krysko, Dmitri V
Verfaillie, Tom
Kaczmarek, Agnieszka
Mathieu, Chantal
Roebroek, Anton J M
Annaert, Wim
Vandenabeele, Peter
Agostinis, Patrizia
Venue: The EMBO Journal
Publisher: Springer Science and Business Media LLC
Published: 2012-01-17
Volume: 31
Issue: 5
Pages: 1062-1079
ISSN: 0261-4189 (ISSN-L)
1460-2075
DOI: 10.1038/emboj.2011.497
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: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
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

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A novel pathway combining calreticulin exposure and ATP secretion in immunogenic cancer cell death

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