Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death
Open accessAbstract
Systemic anticancer chemotherapy is immunosuppressive and mostly induces nonimmunogenic tumor cell death. Here, we show that even in the absence of any adjuvant, tumor cells dying in response to anthracyclins can elicit an effective antitumor immune response that suppresses the growth of inoculated tumors or leads to the regression of established neoplasia. Although both antracyclins and mitomycin C induced apoptosis with caspase activation, only anthracyclin-induced immunogenic cell death was immunogenic. Caspase inhibition by Z-VAD-fmk or transfection with the baculovirus inhibitor p35 did not inhibit doxorubicin (DX)-induced cell death, yet suppressed the immunogenicity of dying tumor cells in several rodent models of neoplasia. Depletion of dendritic cells (DCs) or CD8+T cells abolished the immune response against DX-treated apoptotic tumor cells in vivo. Caspase inhibition suppressed the capacity of DX-killed cells to be phagocytosed by DCs, yet had no effect on their capacity to elicit DC maturation. Freshly excised tumors became immunogenic upon DX treatment in vitro, and intratumoral inoculation of DX could trigger the regression of established tumors in immunocompetent mice. These results delineate a procedure for the generation of cancer vaccines and the stimulation of anti-neoplastic immune responses in vivo.
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During radiotherapy or chemotherapy, immune responses may be biased toward tumor antigens rather than normal self-antigens.
“Consequently, during radiotherapy or chemotherapy in which the tumor cells are induced to die, immune responses may be biased towards a response against the tumor antigens rather than normal self-antigens, to which the immune system has been tolerized 7,27,28.”
From Immunogenic and tolerogenic cell death (2009) · cites this paper as [7]
CRT exposure strongly correlates with immunogenicity; anthracyclin-treated dying tumor cells exposing CRT can vaccinate against cancer and lose immunogenicity upon CRT depletion or neutralization.
“This feature strongly correlates with immunogenicity, and anthracyclin-treated dying tumor cells that expose CRT can be used to vaccinate against cancer, yet lose their immunogenicity upon siRNA-mediated depletion or antibody-mediated neutralization of CRT.”
From Immunogenic and tolerogenic cell death (2009) · cites this paper as [7]
Absorbing CRT to live tumor cells does not suffice to render them immunogenic, meaning additional factors are essential for immunogenicity.
“However, the absorbance of CRT to live tumor cells does not suffice to render them immunogenic 7, meaning that additional factors are essential for immunogenicity.”
From Immunogenic and tolerogenic cell death (2009) · cites this paper as [7]
There are subcategories of cell death, such as immunogenic versus non-immunogenic apoptosis, and subtle differences in cell surface composition and secreted products determine whether death is immunogenic.
“In an effort to reconcile these different data, it has been proposed that there are subcategories of cell death (such as immunogenic versus non-immunogenic apoptosis) and that subtle differences in the composition of the cell surface and/or in the products, which could include DAMPs, that are secreted by the dying cells determine whether the death of the cell is immunogenic or not7.”
From Immunogenic and tolerogenic cell death (2009) · cites this paper as [7]
Anthracyclins, but not mitomycin C or etoposide, cause tumor cells to expose a CRT-ERp57 complex at a pre-apoptotic stage, facilitating DC uptake.
“Similarly, in response to some chemotherapeutic agents, such as anthracyclins, but not others, such as mitomycin C or etoposide, tumor cells expose complexes that are formed by the chaperone calreticulin (CRT) and the disulfide isomerase ERp57 on their cell surface. The exposure of this complex occurs at a pre-apoptotic stage and facilitates the uptake of dying cells by DC 7,39.”
From Immunogenic and tolerogenic cell death (2009) · cites this paper as [7]
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- Authors
- Casares, N., Pequignot, M. O., Tesniere, A., Ghiringhelli, F., Roux, S., Chaput, N., Schmitt, E., Hamai, A., Hervas-Stubbs, S., Obeid, M., Coutant, F., Métivier, D., Pichard, E., Aucouturier, P., Pierron, G., Garrido, C., Zitvogel, L., & Kroemer, G.
- Affiliations
- 1Centre National de la Recherche Scientifique UMR8125, Institut Gustave Roussy, F-94805 Villejuif, France
- 2Institut National de la Santé et de la Recherche Medicale (INSERM) Immunology Unit, Institut Gustave Roussy, F-94805 Villejuif, France
- Inserm (FR)
- 4Unite de Biologie des Regulations Immunitaires, INSERM E 352, Institut Pasteur, 75724 Paris, Cedex 15, France
- 5Institut André Lwoff, UPR-1983, Laboratoire Replication de l'ADN et Ultrastructure du Noyau, 94801 Villejuif, France
- 6INSERM U712, Hopital Saint-Antoine, Paris, France
- Centre National de la Recherche Scientifique (FR)
- Venue
- The Journal of Experimental Medicine
- Publisher
- Rockefeller University Press
- Published
- 2005-12-19
- Volume
- 202
- Issue
- 12
- Pages
- 1691-1701
- ISSN
- 0022-1007 (ISSN-L)
- 1540-9538
- PMC
- PMC2212968
- OpenAlex
- W2142153200
- Cited by
- 1,512
- References
- 57
- Citations by year
- 2026: 60 · 2025: 98 · 2024: 105 · 2023: 143 · 2022: 120 · 2021: 108 · 2020: 129 · 2019: 82 · 2018: 71 · 2017: 79 · 2016: 64 · 2015: 60 · 2014: 49 · 2013: 62 · 2012: 49
- FWCI
- 12.41
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Experimental Medicine (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- Funders
- Styrelsen för Internationellt Utvecklingssamarbete
- Sidaction
- Fondation pour la Recherche Médicale
- Institut Gustave-Roussy
- 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
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Keywords
- immunogenic cell death, doxorubicin, anthracyclines, caspase activation, apoptosis, cancer cell death, dendritic cells, CD8+ T cells, cancer vaccines, tumor regression, mitomycin C, z-VAD-fmk, p35, phagocytosis, DC maturation, antitumor immunity
- MeSH terms
- Amino Acid Chloromethyl Ketones, Animals, Antibiotics, Antineoplastic, Dendritic Cells, Doxorubicin, Neoplasms, Vaccination, Viral Proteins, Immunoblotting, Mitomycin, Apoptosis, CD8-Positive T-Lymphocytes, Caspases, In Situ Nick-End Labeling, Cell Line, Tumor, Mice, Rats, Caspase Inhibitors
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