Resurrection of an ancient inflammatory locus reveals switch to caspase-1 specificity on a caspase-4 scaffold.
caspase
cell death
inflammation
interleukin 1
protein evolution
Journal
The Journal of biological chemistry
ISSN: 1083-351X
Titre abrégé: J Biol Chem
Pays: United States
ID NLM: 2985121R
Informations de publication
Date de publication:
06 2022
06 2022
Historique:
received:
24
01
2022
revised:
05
04
2022
accepted:
08
04
2022
pubmed:
16
4
2022
medline:
30
6
2022
entrez:
15
4
2022
Statut:
ppublish
Résumé
Pyroptosis is a mechanism of inflammatory cell death mediated by the activation of the prolytic protein gasdermin D by caspase-1, caspase-4, and caspase-5 in human, and caspase-1 and caspase-11 in mouse. In addition, caspase-1 amplifies inflammation by proteolytic activation of cytokine interleukin-1β (IL-1β). Modern mammals of the order Carnivora lack the caspase-1 catalytic domain but express an unusual version of caspase-4 that can activate both gasdermin D and IL-1β. Seeking to understand the evolutionary origin of this caspase, we utilized the large amount of data available in public databases to perform ancestral sequence reconstruction of an inflammatory caspase of a Carnivora ancestor. We expressed the catalytic domain of this putative ancestor in Escherichia coli, purified it, and compared its substrate specificity on synthetic and protein substrates to extant caspases. We demonstrated that it activates gasdermin D but has reduced ability to activate IL-1β. Our reconstruction suggests that caspase-1 was lost in a Carnivora ancestor, perhaps upon a selective pressure for which the generation of biologically active IL-1β by caspase-1 was detrimental. We speculate that later, a Carnivora encountered selective pressures that required the production of IL-1β, and caspase-4 subsequently gained this activity. This hypothesis would explain why extant Carnivora possess an inflammatory caspase with caspase-1 catalytic function placed on a caspase-4 scaffold.
Identifiants
pubmed: 35427646
pii: S0021-9258(22)00371-4
doi: 10.1016/j.jbc.2022.101931
pmc: PMC9144055
pii:
doi:
Substances chimiques
Interleukin-1beta
0
Phosphate-Binding Proteins
0
Recombinant Proteins
0
Caspases
EC 3.4.22.-
Caspase 1
EC 3.4.22.36
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
101931Subventions
Organisme : NIGMS NIH HHS
ID : K12 GM068524
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM099040
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM127654
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA030199
Pays : United States
Informations de copyright
Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved.
Déclaration de conflit d'intérêts
Conflict of interest The authors declare that they have no conflicts of interest with the contents of this article.
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