New insights into the evolutionary dynamic and lineage divergence of gasdermin E in metazoa

Yuan, Zihao; Jiang, Shuai; Qin, Kunpeng; Sun, Li

doi:10.3389/fcell.2022.952015

Cited by 29 publications

(29 citation statements)

References 68 publications

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“…In our tree as others, (Yuan et al, 2022;De Schutter et al, 2021;Angosto-Bazarra et al, 2022;Wang et al, 2023b) the GSDMA protein sequences from mammals separate from those from amphibians, reptiles and birds (Fig. 1).…”

Section: Bird Gsdma Linker Contains a Likely Caspase-1 Cleavage Sitesupporting

confidence: 76%

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Caspase-1 activates gasdermin A in non-mammals

Billman,

Kovacs,

Wei

et al. 2023

Preprint

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Gasdermins oligomerize to form pores in the cell membrane, causing programmed lytic cell death called pyroptosis. Mammals encode five gasdermins that can trigger pyroptosis: GSDMA, B, C, D, and E. Caspase and granzyme proteases cleave the linker regions of and activate GSDMB, C, D, and E, but no endogenous activation pathways are yet known for GSDMA. Here, we perform a comprehensive evolutionary analysis of the gasdermin family and focus on the first gene amplification event that gave rise to mammalGSDMA-Dby studying GSDMA in non-mammal species including amphibians, reptiles, and birds. Remarkably, GSDMA in numerous bird species contains the canonical caspase-1 cleavage site YVAD in the linker. We show that GSDMA from birds, amphibians, and reptiles are all cleaved by caspase-1. Thus, GSDMA was originally cleaved by the host-encoded protease caspase-1. In mammals the caspase-1 cleavage site in GSDMA is disrupted; instead, a new protein, GSDMD, is the target of caspase-1. Mammal caspase-1 uses exosite interactions with the GSDMD C-terminal domain to confer the specificity of this interaction, whereas we show that bird caspase-1 uses a stereotypical tetrapeptide sequence to confer specificity for bird GSDMA. Our results reveal an evolutionarily stable association between caspase-1 and the gasdermin family, albeit a shifting one. Caspase-1 repeatedly changes its target gasdermin over evolutionary time at speciation junctures, initially cleaving GSDME in fish, then GSDMA in amphibians/reptiles/birds, and finally GSDMD in mammals.One Sentence SummaryWe demonstrate that amphibians, reptiles and birds engage pyroptosis using caspase-1 and GS-DMA, filling an evolutionary gap in which caspase-1 cleaves GSDME in fish and GSDMD in mammals.

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Section: Bird Gsdma Linker Contains a Likely Caspase-1 Cleavage Sitesupporting

confidence: 76%

“…Only mammals can encode all six of these genes. Other clades of animals encode fewer gasdermin genes ( Yuan et al, 2022 ; De Schutter et al, 2021 ; Wang et al, 2023b ; Angosto-Bazarra et al, 2022 ). The clades that encode the fewest gasdermins that includes GSDMA are birds and amphibians, which express just GSDMA, GSDME, and PJVK.…”

Section: Introductionmentioning

confidence: 99%

Caspase-1 activates gasdermin A in non-mammals

Billman,

Kovacs,

Wei

et al. 2023

Preprint

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“…milii gsdma/b and Podarcis muralis gsdmb ( S2A Fig ), suggesting that Cmigsdma/b is the common ancestor of vertebrate gsdma and gsdmb . Moreover, in teleost fishes, the intron phase of gsdmea and gsdmeb was the same as that of other vertebrate gsdme , while the intron phase of the recently identified gsdmec was more consistent with gsdma (Figs 1A and S2B ) [ 33 ], suggesting that some of the GSDMEc in teleost fishes may function like a GSDMA rather than a GSDME duplicate. Synteny analysis also suggested the correlation between Anguilla anguilla gsdmec and C .…”

Section: Resultsmentioning

confidence: 97%

“…It is worth noting that high concentration of Z-VAD-FMK (4 μM in this study) did not have a better effect on alleviating amphioxus death upon bacterial infection. Sine CASP cleavage sites usually are member specific and even lineage specific [ 23 , 33 ], generating the peptide inhibitor based on analyzing the cleavage sites is more efficient and may avoid other side effects.…”

Section: Discussionmentioning

confidence: 99%

Characterization of GSDME in amphioxus provides insights into the functional evolution of GSDM-mediated pyroptosis

Wang

Wei

et al. 2023

PLoS Biol

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Members of the gasdermin (GSDM) family are pore-forming effectors that cause membrane permeabilization and pyroptosis, a lytic proinflammatory type of cell death. To reveal the functional evolution of GSDM-mediated pyroptosis at the transition from invertebrates to vertebrates, we conducted functional characterization of amphioxus GSDME (BbGSDME) and found that it can be cleaved by distinct caspase homologs, yielding the N253 and N304 termini with distinct functions. The N253 fragment binds to cell membrane, triggers pyroptosis, and inhibits bacterial growth, while the N304 performs negative regulation of N253-mediated cell death. Moreover, BbGSDME is associated with bacteria-induced tissue necrosis and transcriptionally regulated by BbIRF1/8 in amphioxus. Interestingly, several amino acids that are evolutionarily conserved were found to be important for the function of both BbGSDME and HsGSDME, shedding new lights on the functional regulation of GSDM-mediated inflammation.

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“…Unexpectedly, GSDMEc was identified in perciformes and some primitive ray-finned fishes such as European eel ( Anguilla anguilla ) and reedfish ( Erpetoichthys calabaricus ). However different from GSDMEa and GSDMEb, no obvious caspase recognition site was observed in the linker region of GSDMEc ( 87 ). Whether piscine GSDMEc functions in triggering pyroptosis and bacterial clearance remains to be defined.…”

Section: The Functions Of Inflammasome-associated Effectorsmentioning

confidence: 99%

Emerging mechanisms and functions of inflammasome complexes in teleost fish

Chang

2023

Front. Immunol.

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Inflammasomes are multiprotein complexes, which are assembled in response to a diverse range of exogenous pathogens and endogenous danger signals, leading to produce pro-inflammatory cytokines and induce pyroptotic cell death. Inflammasome components have been identified in teleost fish. Previous reviews have highlighted the conservation of inflammasome components in evolution, inflammasome function in zebrafish infectious and non-infectious models, and the mechanism that induce pyroptosis in fish. The activation of inflammasome involves the canonical and noncanonical pathways, which can play critical roles in the control of various inflammatory and metabolic diseases. The canonical inflammasomes activate caspase-1, and their signaling is initiated by cytosolic pattern recognition receptors. However the noncanonical inflammasomes activate inflammatory caspase upon sensing of cytosolic lipopolysaccharide from Gram-negative bacteria. In this review, we summarize the mechanisms of activation of canonical and noncanonical inflammasomes in teleost fish, with a particular focus on inflammasome complexes in response to bacterial infection. Furthermore, the functions of inflammasome-associated effectors, specific regulatory mechanisms of teleost inflammasomes and functional roles of inflammasomes in innate immune responses are also reviewed. The knowledge of inflammasome activation and pathogen clearance in teleost fish will shed new light on new molecular targets for treatment of inflammatory and infectious diseases.

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New insights into the evolutionary dynamic and lineage divergence of gasdermin E in metazoa

Cited by 29 publications

References 68 publications

Caspase-1 activates gasdermin A in non-mammals

Caspase-1 activates gasdermin A in non-mammals

Characterization of GSDME in amphioxus provides insights into the functional evolution of GSDM-mediated pyroptosis

Emerging mechanisms and functions of inflammasome complexes in teleost fish

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