Complementary regulation of caspase-1 and IL-1β reveals additional mechanisms of dampened inflammation in bats

Bats have emerged as unique mammalian vectors harboring a diverse range of highly lethal zoonotic viruses with minimal clinical disease. Despite having sustained complete genomic loss of AIM2, regulation of the downstream inflammasome response in bats is unknown. AIM2 sensing of cytoplasmic DNA trig...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 117; no. 46; pp. 28939 - 28949
Main Authors Goh, Geraldine, Ahn, Matae, Zhu, Feng, Lee, Lim Beng, Luo, Dahai, Irving, Aaron T., Wang, Lin-Fa
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 17.11.2020
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Abstract Bats have emerged as unique mammalian vectors harboring a diverse range of highly lethal zoonotic viruses with minimal clinical disease. Despite having sustained complete genomic loss of AIM2, regulation of the downstream inflammasome response in bats is unknown. AIM2 sensing of cytoplasmic DNA triggers ASC aggregation and recruits caspase-1, the central inflammasome effector enzyme, triggering cleavage of cytokines such as IL-1β and inducing GSDMD-mediated pyroptotic cell death. Restoration of AIM2 in bat cells led to intact ASC speck formation, but intriguingly resulted in a lack of caspase-1 or consequent IL-1β activation. We further identified two residues undergoing positive selection pressures in Pteropus alecto caspase-1 that abrogate its enzymatic function and are crucial in human caspase-1 activity. Functional analysis of another bat lineage revealed a targeted mechanism for loss of Myotis davidii IL-1β cleavage and elucidated an inverse complementary relationship between caspase-1 and IL-1β, resulting in overall diminished signaling across bats of both suborders. Thus we report strategies that additionally undermine downstream inflammasome signaling in bats, limiting an overactive immune response against pathogens while potentially producing an antiinflammatory state resistant to diseases such as atherosclerosis, aging, and neurodegeneration.
AbstractList Bats have emerged as unique mammalian vectors harboring a diverse range of highly lethal zoonotic viruses with minimal clinical disease. Despite having sustained complete genomic loss of AIM2, regulation of the downstream inflammasome response in bats is unknown. AIM2 sensing of cytoplasmic DNA triggers ASC aggregation and recruits caspase-1, the central inflammasome effector enzyme, triggering cleavage of cytokines such as IL-1β and inducing GSDMD-mediated pyroptotic cell death. Restoration of AIM2 in bat cells led to intact ASC speck formation, but intriguingly resulted in a lack of caspase-1 or consequent IL-1β activation. We further identified two residues undergoing positive selection pressures in Pteropus alecto caspase-1 that abrogate its enzymatic function and are crucial in human caspase-1 activity. Functional analysis of another bat lineage revealed a targeted mechanism for loss of Myotis davidii IL-1β cleavage and elucidated an inverse complementary relationship between caspase-1 and IL-1β, resulting in overall diminished signaling across bats of both suborders. Thus we report strategies that additionally undermine downstream inflammasome signaling in bats, limiting an overactive immune response against pathogens while potentially producing an antiinflammatory state resistant to diseases such as atherosclerosis, aging, and neurodegeneration.
Bats have emerged as unique mammalian vectors harboring a diverse range of highly lethal zoonotic viruses with minimal clinical disease. Despite having sustained complete genomic loss of AIM2, regulation of the downstream inflammasome response in bats is unknown. AIM2 sensing of cytoplasmic DNA triggers ASC aggregation and recruits caspase-1, the central inflammasome effector enzyme, triggering cleavage of cytokines such as IL-1β and inducing GSDMD-mediated pyroptotic cell death. Restoration of AIM2 in bat cells led to intact ASC speck formation, but intriguingly resulted in a lack of caspase-1 or consequent IL-1β activation. We further identified two residues undergoing positive selection pressures in caspase-1 that abrogate its enzymatic function and are crucial in human caspase-1 activity. Functional analysis of another bat lineage revealed a targeted mechanism for loss of IL-1β cleavage and elucidated an inverse complementary relationship between caspase-1 and IL-1β, resulting in overall diminished signaling across bats of both suborders. Thus we report strategies that additionally undermine downstream inflammasome signaling in bats, limiting an overactive immune response against pathogens while potentially producing an antiinflammatory state resistant to diseases such as atherosclerosis, aging, and neurodegeneration.
Bats have been shown to dampen several key upstream pathogen and danger-associated molecular patterns, yet much of the downstream signaling is yet unknown. Here, we identify residues in caspase-1 which are critical for enzymatic activity and have been targeted for inhibition in Pteropus bats. Further, we discover cleavage-site flanking residues which lead to loss of IL-1β cleavage in Myotis bats. Thus, we report an inverse relationship between caspase-1 function and IL-1β cleavage, resulting in a consistent reduction of downstream signaling by the inflammasome across bats within the two suborders. In sum, we confirm that bats have targeted the inflammasome pathway at multiple levels and via heterogeneous strategies to reduce proinflammatory responses, thus mitigating potential immune-mediated tissue damage and disease. Bats have emerged as unique mammalian vectors harboring a diverse range of highly lethal zoonotic viruses with minimal clinical disease. Despite having sustained complete genomic loss of AIM2, regulation of the downstream inflammasome response in bats is unknown. AIM2 sensing of cytoplasmic DNA triggers ASC aggregation and recruits caspase-1, the central inflammasome effector enzyme, triggering cleavage of cytokines such as IL-1β and inducing GSDMD-mediated pyroptotic cell death. Restoration of AIM2 in bat cells led to intact ASC speck formation, but intriguingly resulted in a lack of caspase-1 or consequent IL-1β activation. We further identified two residues undergoing positive selection pressures in Pteropus alecto caspase-1 that abrogate its enzymatic function and are crucial in human caspase-1 activity. Functional analysis of another bat lineage revealed a targeted mechanism for loss of Myotis davidii IL-1β cleavage and elucidated an inverse complementary relationship between caspase-1 and IL-1β, resulting in overall diminished signaling across bats of both suborders. Thus we report strategies that additionally undermine downstream inflammasome signaling in bats, limiting an overactive immune response against pathogens while potentially producing an antiinflammatory state resistant to diseases such as atherosclerosis, aging, and neurodegeneration.
Author Lee, Lim Beng
Ahn, Matae
Luo, Dahai
Zhu, Feng
Wang, Lin-Fa
Goh, Geraldine
Irving, Aaron T.
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Keywords bats
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IL-1β
caspase-1
inflammasome
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Author contributions: G.G., M.A., A.T.I., and L.-F.W. conceived the study; M.A., A.T.I., and L.-F.W. provided resources and materials; G.G., L.B.L., and M.A. performed experiments; G.G., M.A., F.Z., and D.L. analyzed the data; and G.G., M.A., D.L., A.T.I., and L.-F.W. wrote the manuscript with input from all authors.
1G.G. and M.A. contributed equally to this work.
Edited by Vishva M. Dixit, Genentech, San Francisco, CA, and approved September 14, 2020 (received for review February 21, 2020)
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Snippet Bats have emerged as unique mammalian vectors harboring a diverse range of highly lethal zoonotic viruses with minimal clinical disease. Despite having...
Bats have been shown to dampen several key upstream pathogen and danger-associated molecular patterns, yet much of the downstream signaling is yet unknown....
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SubjectTerms Aging
Animals
Arteriosclerosis
Atherosclerosis
Biological Sciences
Caspase 1 - metabolism
Caspase-1
Cell death
Chiroptera
Chiroptera - genetics
Chiroptera - immunology
Cleavage
Cytokines
Cytokines - metabolism
Deoxyribonucleic acid
DNA
DNA-Binding Proteins
Functional analysis
Genomics
HEK293 Cells
Humans
IL-1β
Immune response
Inflammasomes
Inflammasomes - metabolism
Inflammation - metabolism
Interleukin-1beta - metabolism
Macrophages - metabolism
Neurodegeneration
Positive selection
Pyroptosis
Signal Transduction
Signaling
Viruses
Zoonoses
Title Complementary regulation of caspase-1 and IL-1β reveals additional mechanisms of dampened inflammation in bats
URI https://www.jstor.org/stable/26971019
https://www.ncbi.nlm.nih.gov/pubmed/33106404
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https://pubmed.ncbi.nlm.nih.gov/PMC7682399
Volume 117
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