Synergism of TNF-α and IFN-γ Triggers Inflammatory Cell Death, Tissue Damage, and Mortality in SARS-CoV-2 Infection and Cytokine Shock Syndromes
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Abstract
COVID-19 is characterized by excessive production of pro-inflammatory cytokines and acute lung damage associated with patient mortality. While multiple inflammatory cytokines are produced by innate immune cells during SARS-CoV-2 infection, we found that only the combination of TNF-α and IFN-γ induced inflammatory cell death characterized by inflammatory cell death, PANoptosis. Mechanistically, TNF-α and IFN-γ co-treatment activated the JAK/STAT1/IRF1 axis, inducing nitric oxide production and driving caspase-8/FADD-mediated PANoptosis. TNF-α and IFN-γ caused a lethal cytokine shock in mice that mirrors the tissue damage and inflammation of COVID-19, and inhibiting PANoptosis protected mice from this pathology and death. Furthermore, treating with neutralizing antibodies against TNF-α and IFN-γ protected mice from mortality during SARS-CoV-2 infection, sepsis, hemophagocytic lymphohistiocytosis, and cytokine shock. Collectively, our findings suggest that blocking the cytokine-mediated inflammatory cell death signaling pathway identified here may benefit patients with COVID-19 or other infectious and autoinflammatory diseases by limiting tissue damage/inflammation.
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PANoptosis is involved in the occurrence of cytokine storms (CS) characterized by excessive cytokine production.
“PANoptosis is involved in the occurrence of cytokine storms (CS) characterized by excessive cytokine production.276”
From Inflammation and aging: signaling pathways and intervention therapies (2023) · cites this paper as [276]
The combination of TNF-α and IFN-γ activates the JAK/STAT1/IRF1 signaling pathway, leading to the production of nitric oxide (NO).
“The combination of TNF-α and IFN-γ activates the JAK/STAT1/IRF1 signaling pathway, leading to the production of nitric oxide (NO).”
From Inflammation and aging: signaling pathways and intervention therapies (2023) · cites this paper as [276]
This NO release triggers PANoptosis through the involvement of GSDME (pyroptotic), CASP8/3/7 (apoptotic), and pMLKL (necroptotic) pathways.
“This NO release triggers PANoptosis through the involvement of GSDME (pyroptotic), CASP8/3/7 (apoptotic), and pMLKL (necroptotic) pathways.”
From Inflammation and aging: signaling pathways and intervention therapies (2023) · cites this paper as [276]
In vivo, blocking CS by giving mice anti-TNF-α and anti-IFN-γ antibodies prevents death from SARS-CoV-2 infection, hemophagocytic lymph histiocytosis, and LPS shock (sepsis).
“In vivo, blocking CS by giving mice anti-TNF-α and anti-IFN-γ antibodies prevents death from SARS-CoV-2 infection, hemophagocytic lymph histiocytosis, and LPS shock (sepsis).276”
From Inflammation and aging: signaling pathways and intervention therapies (2023) · cites this paper as [276]
Marked systemic upregulation of TNF α and IFN γ can promote tissue damage.
“While marked systemic upregulation of TNF α and IFN γ can promote tissue damage 50”
From Targeting TBK1 to overcome resistance to cancer immunotherapy (2023) · cites this paper as [50]
In severe COVID-19, concomitant TNF and IFNγ elevation is sufficient to trigger PANoptosis, driving tissue damage and mortality.
“concomitant elevation of TNF and IFNγ as being sufficient to trigger pyroptosis, apoptosis, and necrosis (PANoptosis) driving tissue damage and mortality in severe COVID-19”
From COVID-19 and the human innate immune system (2021) · cites this paper as Karki et al., 2021
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Self-citationIRF8 Regulates Transcription of Naips for NLRC4 Inflammasome Activation
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Inflammation and aging: signaling pathways and intervention therapies
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Wang, Y., & Kanneganti, T.-D. (2021) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2021.07.038 · Cited by 545 · see citing works
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Sun, Y., Revach, O.-Y., Anderson, S., Kessler, E. A., Wolfe, C. H., Jenney, A., Mills, C. E., Robitschek, E. J., Davis, T. G. R., Kim, S., et al. (2023) · Nature · doi:10.1038/s41586-023-05704-6 · Cited by 174 · see citing works
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Cell deaths: Involvement in the pathogenesis and intervention therapy of COVID-19
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- Authors
- Karki, R., Sharma, B. R., Tuladhar, S., Williams, E. P., Zalduondo, L., Samir, P., Zheng, M., Sundaram, B., Banoth, B., Malireddi, R. K. S., Schreiner, P., Neale, G., Vogel, P., Webby, R., Jonsson, C. B., & Kanneganti, T.-D.
- Affiliations
- St. Jude Children's Research Hospital (US)
- University of Tennessee Health Science Center (US)
- Corresponding author
- Kanneganti, Thirumala-Devi
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2021-01
- Volume
- 184
- Issue
- 1
- Pages
- 149-168.e17
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC7674074
- OpenAlex
- W3105908160
- Cited by
- 1,734
- References
- 134
- Citations by year
- 2026: 223 · 2025: 302 · 2024: 318 · 2023: 321 · 2022: 303 · 2021: 249 · 2020: 15
- FWCI
- 29.33
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nd)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Seoul National University Open Repository (Seoul National University) (submittedVersion)
- Funders
- American Lebanese Syrian Associated Charities
- National Institutes of Health (AR056296, AI124346, AI101935, CA253095, 63/106,012, NR-52281)
- RIKEN
- Genentech
- Ministry of Education, Culture, Sports, Science and Technology
- Centers for Disease Control and Prevention
- National Institute of Allergy and Infectious Diseases
- Topics
- Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
- Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
- Keywords
- SARS-CoV-2, COVID-19 pandemic, TNF-α, interferon-gamma, PANoptosis, inflammatory cell death, cytokine storm, nitric oxide, caspase-8, FADD, sepsis, hemophagocytic lymphohistiocytosis, tissue damage, mortality
- MeSH terms
- THP-1 Cells, Cytokine Release Syndrome, COVID-19, Animals, Disease Models, Animal, Female, Humans, Inflammation, Interferon-gamma, Male, Mice, Transgenic, Tumor Necrosis Factor-alpha, Cell Death, Lymphohistiocytosis, Hemophagocytic, Mice, Antibodies, Neutralizing, Human Umbilical Vein Endothelial Cells
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