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Apoptotic Caspases Suppress mtDNA-Induced STING-Mediated Type I IFN Production
Open accessAbstract
Activated caspases are a hallmark of apoptosis induced by the intrinsic pathway, but they are dispensable for cell death and the apoptotic clearance of cells in vivo. This has led to the suggestion that caspases are activated not just to kill but to prevent dying cells from triggering a host immune response. Here, we show that the caspase cascade suppresses type I interferon (IFN) production by cells undergoing Bak/Bax-mediated apoptosis. Bak and Bax trigger the release of mitochondrial DNA. This is recognized by the cGAS/STING-dependent DNA sensing pathway, which initiates IFN production. Activated caspases attenuate this response. Pharmacological caspase inhibition or genetic deletion of caspase-9, Apaf-1, or caspase-3/7 causes dying cells to secrete IFN-β. In vivo, this precipitates an elevation in IFN-β levels and consequent hematopoietic stem cell dysfunction, which is corrected by loss of Bak and Bax. Thus, the apoptotic caspase cascade functions to render mitochondrial apoptosis immunologically silent.
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“In the absence of active caspases, mtDNA released following mitochondrial outer membrane permeabilization triggers type I interferon responses in a cGAS–STING-dependent manner143,144”
From The role of mitochondria in rheumatic diseases (2022) · cites this paper as [144]
Experimental — accuracy not yet measuredIn the citing paper
“These include: (1) the prominent ability of CASP8 to inhibit necroptosis (see above), which is generally associated with the establishment of robust inflammatory responses linked to NF-κB activation [496 925–928]; (2) the capacity of CASP3 to drive PS exposure (see above), which generally supports the phagocytic removal of dying and dead cells while delivering anti-inflammatory signals to”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [932]
In the citing paper
“MtDNA has been reported to activate immunity through two distinct pathways, namely Toll-like receptor 9 (TLR9; Zhang et al, 2010;Oka et al, 2012;Liu et al, 2015), and cGAS activation (White et al, 2014;West et al, 2015).”
From Mitochondrial DNA and TLR9 drive muscle inflammation upon Opa1 deficiency (2018) · cites this paper as White et al, 2014
In the citing paper
“Thus, cytosolic mtDNA activates the DNA sensor cGAS and promotes STING-IRF3-dependent signaling (Rongvaux et al, 2014;White et al, 2014;West et al, 2015).”
From Mitochondrial DNA and TLR9 drive muscle inflammation upon Opa1 deficiency (2018) · cites this paper as White et al, 2014
In the citing paper
“Interestingly, these events were attenuated by caloric restriction (White et al., 2014), an intervention which has been shown to extend lifespan in a plethora of organisms and decrease the burden of senescent cells (Fontana et al., 2018; Mercken et al., 2012).”
From Cytoplasmic DNA: sources, sensing, and role in aging and disease (2021) · cites this paper as White et al., 2014
In the citing paper
“Finally, ABT-737 (an experimental inhibitor of multiple BCL2 family members) is known for its ability to drive robust type I IFN secretion by cancer cells downstream of mtDNA-driven CGAS activation, especially in the context of caspases inhibition (Rongvaux et al., 2014; White et al., 2014).”
From Immunomodulation by targeted anticancer agents (2021) · cites this paper as White et al., 2014
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“…can have pro-or anti-immunogenic effects; apoptosis counteracts the IFN-I response due to caspase-mediated cleavage of cGAS, MAVS, and IRF3, 55,56 necroptosis exerts immunogenic effects due to membrane rupture and the release of damage-associated molecular patterns (DAMPs), 57 while…”
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“Finally, intracellular mtDNA leakage and subsequent activation of inflammation via the DNA sensor, cGAS-STING pathway (Lei et al., 2023; White et al., 2014).”
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BackgroundHUMAN HEMATOPOIETIC STEM CELLS GENERATE EXOSOMES CONTAINING ACTIVE PROTEASOMES BUT NOT CASPASES
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In the Midst of Life—Cell Death: What Is It, What Is It Good for, and How to Study ItPreprint
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“In the absence of these effectors, mitochondria become leaky and mitochondrial DNA is able to activate cytosolic DNA sensors to stimulate IFN production (Rongvaux et al. 2014; White et al. 2014).”
BackgroundJena, K. K., Mehto, S., Nath, P., Chauhan, N. R., Sahu, R., Nayak, T. K., Das, S. K., Dhar, K., Sahoo, P. K., Murmu, K. C., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/815506 · Cited by 1
“The mtDNA or micronuclei induces strong interferon response via cGAS-STING-IRF3 axis leading to autoimmune and auto-inflammatory conditions (Ablasser et al., 2014; Mackenzie et al., 2017; Pisetsky, 2012; West et al., 2015; White et al., 2014).”
BackgroundPreface: Life through death—Key role of cellular suicide for colonial and organismal homeostasis
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Chronic ER stress promotes cGAS/mtDNA-induced autoimmunity via ATF6 in myotonic dystrophy type 2Preprint
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“Interestingly, cytochrome C signalling leads to caspase activation that can attenuate cGAS-STING signalling by cleaving of cGAS, TBK1 and IRF3 to ensure that the immunogenic response is not activated during apoptosis 22 .”
BackgroundMechanical forces drive mitochondrial matrix extrusion and apoptotic pore growthPreprint
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“MIM permeabilization (MIMP) releases immunogenic mitochondrial factors, such as mitochondrial DNA (mtDNA), into the cytosol, which can trigger inflammatory responses under conditions of low caspase activity 26,27 .”
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Control of Cell Survival and Apoptosis
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STING Engages Distinct Antiviral Mechanisms to Restrict RNA Virus and DNA Virus Replication
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STING Mediates Cytosolic Dna-Induced Muc5ac Mrna Expression in Human Bronchial Epithelial CellsPreprint
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“Because caspase-deficiency, and the resulting type I IFN response, alters the fitness of hematopoietic stem cell function in mixed transplantation assays [20, 53], we used donor bone marrow cells from mice in Ifnar1-/- genetic background (Supplementary Figure 3).”
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Preface: Life through death—Key role of cellular suicide for colonial and organismal homeostasis
Spetz, J. K. E., & Galluzzi, L. (2020) · International review of cytology · doi:10.1016/s1937-6448(20)30035-6
Faculty Opinions recommendation of Parkin and PINK1 mitigate STING-induced inflammation.
Schumacher, B. (2018) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.733846349.793551630
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“These changes lead to degenerative changes in the placental villi in pregnant women treated with ART [10]-[12].”
BackgroundRT-PCR-assisted quantification of type I IFN responses in irradiated cancer cells
Galassi, C., Ruan, Y., Sato, A., Jiménez‐Cortegana, C., Klapp, V., Bloy, N., Guilbaud, E., Petroni, G., Buqué, A., Galluzzi, L., et al. (2022) · Methods in cell biology · doi:10.1016/bs.mcb.2022.05.005
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Fancm regulates meiotic double-strand break repair pathway choice in mammalsPreprint
Tsui, V., Lyu, R., Novakovic, S., Stringer, J. M., Dunleavy, J. E. M., Granger, E., Semple, T., Leichter, A. L., Martelotto, L. G., Merriner, D. J., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.16.496499
“600 Sting-/- mice have been described previously [118] and the Sting -/- mice were 601 backcrossed for at least 10 generations on a C57BL/6 background by [119].”
Background
Metadata
- Authors
- White, M. J., McArthur, K., Metcalf, D., Lane, R. M., Cambier, J. C., Herold, M. J., van Delft, M. F., Bedoui, S., Lessene, G., Ritchie, M. E., Huang, D. C. S., & Kile, B. T.
- Affiliations
- The University of Melbourne (AU)
- Walter and Eliza Hall Institute of Medical Research (AU)
- National Jewish Health (US)
- Corresponding author
- White, Michael J.
- Kile, Benjamin T.
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2014-12
- Volume
- 159
- Issue
- 7
- Pages
- 1549-1562
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC4520319
- OpenAlex
- W2028107828
- Cited by
- 983
- References
- 68
- Citations by year
- 2026: 89 · 2025: 88 · 2024: 118 · 2023: 107 · 2022: 111 · 2021: 94 · 2020: 93 · 2019: 61 · 2018: 76 · 2017: 63 · 2016: 39 · 2015: 40
- FWCI
- 21.61
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
- Funders
- National Institute of Allergy and Infectious Diseases (R21AI099346)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
- Keywords
- caspases, apoptosis, type I interferon, STING, cGAS, mitochondrial DNA, Bak, Bax, caspase-9, Apaf-1, caspase-3, caspase-7, interferon-beta, hematopoietic stem cells
- MeSH terms
- STING Protein, Animals, Crosses, Genetic, DNA, Mitochondrial, Female, Hematopoietic Stem Cells, Interferon Type I, Male, Membrane Proteins, Mice, Inbred C57BL, Signal Transduction, Apoptosis, Caspases, Caspase 9
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