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Ecto‐calreticulin in immunogenic chemotherapy
Abstract
Summary:The conventional treatment of cancer relies upon radiotherapy and chemotherapy. Such treatments supposedly mediate their effects via the direct elimination of tumor cells. Nonetheless, there are circumstances in which conventional anti‐cancer therapy can induce a modality of cellular demise that elicits innate and cognate immune responses, which in turn mediate part of the anti‐tumor effect. Although different chemotherapeutic agents may kill tumor cells through an apparently homogeneous apoptotic pathway, they differ in their capacity to stimulate immunogenic cell death. We discovered that the pre‐apoptotic translocation of intracellular calreticulin (endo‐CRT) to the plasma membrane surface (ecto‐CRT) is critical for the recognition and engulfment of dying tumor cells by dendritic cells. Thus, anthracyclines and γ‐irradiation that induce ecto‐CRT cause immunogenic cell death, while other pro‐apoptotic agents (such as mitomycin C and etoposide) induce neither ecto‐CRT nor immunogenic cell death. Depletion of CRT abolishes the immunogenicity of cell death elicited by anthracyclines, while exogenous supply of CRT or enforcement of CRT exposure by pharmacological agents that favor CRT translocation can enhance the immunogenicity of cell death. For optimal anti‐tumor vaccination and immunogenic chemotherapy, the same cells have to expose ecto‐CRT and to succumb to apoptosis; if these events affect different cells, no anti‐tumor immune response is elicited. These results may have far reaching implications for tumor immunology because (i) ecto‐CRT exposure by tumor cells allows for the prediction of therapeutic outcome and because (ii) the re‐establishment of ecto‐CRT may ameliorate the efficacy of chemotherapy.
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“Potential immunogenic signals emanating from dying cells include proteins that appear at the surface of stressed and dying cells (such as calreticulin and heat shock proteins, HSPs), lipid moieties that flip from the inner plasma membrane leaflet to the outer leaflet (such as phosphatidylserine) 38,60, proteins that are released into the supernatant of cells (such as HMGB1) 51, as well as nucleic”
From Immunogenic and tolerogenic cell death (2009) · cites this paper as [38]
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“Both in murine models (17, 18) and in human patients with cancer (20), antitumor immune responses induced by cancer cells undergoing immunogenic cell death are associated with better clinical response.”
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“Calreticulin, thus, has a critical position at the interface between cancer cells and the immune system.(12,35,36) The disclosure of the miR-27a-calreticulin axis and its role in ICD may pave the way for future research aimed to stratify CRC patients on the basis of miR-27a/calreticulin expression levels and design no…”
BackgroundResultInfluentialViral subversion of immunogenic cell death
Kepp, O., Senovilla, L., Galluzzi, L., Panaretakis, T., Schlemmer, F., Madeo, F., Zitvogel, L., & Kroemer, G. (2009) · Cell Cycle · doi:10.4161/cc.8.6.7939 · Cited by 67
Self-citationCalreticulin, a therapeutic target?
Eggleton, P., Bremer, E., Dudek, E., & Michalak, M. (2016) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2016.1164695 · Cited by 64
“There is overwhelming and convincing evidence that CALR may have important extracellular functions, including its pro-immunogenic role in ICD.”
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Cancer and Immune Response: Old and New Evidence for Future Challenges
de la Cruz‐Merino, L., Grande-Pulido, E., Albero, A., & de Villena, M. C. M. (2008) · The Oncologist · doi:10.1634/theoncologist.2008-0166 · Cited by 61
“Other mechanisms that facilitate apoptotic cell antigen presentation to APCs have been reported, such as the translocation of the intracytoplasmic protein calreticulin to the cell surface mediated by anthracyclines [37, 38 ].”
BackgroundViral strategies for the evasion of immunogenic cell death
Galluzzi, L., Kepp, O., Morselli, E., Vitale, I., Senovilla, L., Pinti, M., Zitvogel, L., & Kroemer, G. (2010) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2010.02223.x · Cited by 59
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“41,42 As shown in Figure 10A, pre-treated ID8 cells created in vitro as a tumor vaccine and then injected below the left shoulder of experimental mice.”
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Endoplasmic reticulum Ca2+-homeostasis is altered in small and non-small cell lung cancer cell lines
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“Recently, a role for calreticulin in immunogenic cell death has been proposed [21].”
BackgroundProcess of immunogenic cell death caused by disulfiram as the anti-colorectal cancer candidate
You, S.-Y., Rui, W., Chen, S.-T., Chen, H.-C., Liu, X., Huang, J., & Chen, H. (2019) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2019.03.192 · Cited by 51
New insights into metronomic chemotherapy-induced immunoregulation
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Identification of the Rheumatoid Arthritis Shared Epitope Binding Site on Calreticulin
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“). Due to its critical importance for elimination of apoptotic cells”
BackgroundDisruption of the PP1/GADD34 complex induces calreticulin exposure
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“…and calreticulin-exposing cells, and 25 µM was used in the following experiments. these drug concentrations have also been used in previous studies (11,28). primary AMl cells will undergo spontaneous apoptosis during in vitro culture; the degree of apoptosis then shows a wide variation between…”
InfluentialZhang, T., & Herlyn, D. (2008) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-008-0598-y · Cited by 46
“cells by dendritic cells and abolished their immunogenicity in mice [3, 90, 106, 107].”
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Self-citationChimeric Antigen Receptor-Modified T Cells for Solid Tumors: Challenges and Prospects
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Cell Death in the Tumor Microenvironment: Implications for Cancer Immunotherapy
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“One of the principal components of immunogenic cell death appears to be the exposure of a specific eat-me signal, calreticulin (CRT), on the cell surface [87,88].”
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“…been shown to act as critical determinants in PDT-induced immune responses, for example by elevating calreticulin exposure (CRT) to the cancer cell surface [10–12], via heat shock proteins (HSP70 and HSP90) exposure on cancer cells [13–15], or extracellular adenosine triphosphate (ATP) [16, 17].”
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Radiation for Awakening the Dormant Immune System, a Promising Challenge to be Explored
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Roles of Trypanosoma cruzi calreticulin in parasite–host interactions and in tumor growth
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Sensitizing activities of nitric oxide donors for cancer resistance to anticancer therapeutic drugs
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“CRT is a highly conserved endoplasmic reticulum chaperone protein, which upon translocation from the endoplasmic reticulum to the cell surface provides an “eat me” signal; thereby promoting phagocytosis by macrophages and dendritic cells [8].”
Cytotoxicity and immunostimulation: double attack on cancer cells with polymeric therapeutics
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Arginylated Calreticulin at Plasma Membrane Increases Susceptibility of Cells to Apoptosis
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“, upon treatment with anthracyclins (33, 39, 40).”
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“This phenomenon has been described in tumor cells undergoing death in response to anthracyclines, oxaliplatin, cyclophosphamides, or irradiation and results in the induction of specific CD4 and CD8 TLs.(7) Only cells with calreticulin (CRT) at the plasma membrane, which release ATP (adenosine triphosphate)(8) or high-…”
BackgroundStoll, G., Pol, J. G., Soumelis, V., Zitvogel, L., & Kroemer, G. (2018) · OncoImmunology · doi:10.1080/2162402x.2018.1484980 · Cited by 38
Self-citation
Metadata
- Authors
- Obeid, M., Tesniere, A., Panaretakis, T., Tufi, R., Joza, N., Van Endert, P., Ghiringhelli, F., Apetoh, L., Chaput, N., Flament, C., Ullrich, E., De Botton, S., Zitvogel, L., & Kroemer, G.
- Affiliations
- Université Paris-Sud (FR)
- Corresponding author
- Kroemer, Guido
- ORCID
- Venue
- Immunological Reviews
- Publisher
- Wiley
- Published
- 2007-10-30
- Volume
- 220
- Issue
- 1
- Pages
- 22-34
- ISSN
- 0105-2896 (ISSN-L)
- 1600-065X
- OpenAlex
- W1984068314
- Cited by
- 202
- References
- 72
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 5 · 2023: 8 · 2022: 6 · 2021: 17 · 2020: 12 · 2019: 14 · 2018: 12 · 2017: 11 · 2016: 15 · 2015: 11 · 2014: 6 · 2013: 13 · 2012: 8
- FWCI
- 1.20
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Immunological Reviews (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Endoplasmic Reticulum Stress and Disease
- Keywords
- immunogenic cell death, calreticulin, dendritic cells, anthracyclines, gamma irradiation, apoptosis, tumor immunology, cancer immunotherapy, mitomycin C, etoposide
- MeSH terms
- Animals, Cell Membrane, Humans, Neoplasms, Vaccination, Apoptosis, Anthracyclines, Protein Transport, Calreticulin, Mice
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