Sensing of cytosolic LPS through caspy2 pyrin domain mediates noncanonical inflammasome activation in zebrafish

Yang, Dahai; Zheng, Xin; Chen, Shouwen; Wang, Zhuang; Xu, Wenting; Tan, Jinchao; Hu, Tianjian; Hou, Mingyu; Wang, Wenhui; Gu, Zhaoyan; Wang, Qiyao; Zhang, Ruilin; Zhang, Yuanxing; Liu, Qin

doi:10.1038/s41467-018-04984-1

Cited by 56 publications

(51 citation statements)

References 44 publications

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“…However, recently caspy2 has been reported as an intracellular LPS receptor in the zebrafish (26). In this study, no significant response to a standard LPS preparation was detected.…”

Section: Discussioncontrasting

confidence: 61%

Innovation in NLR and TLR sensing drives the MHC-II free Atlantic cod immune system

Jin

Morro

Tørresen

et al. 2020

Preprint

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The genome sequencing of Atlantic cod revealed an immune system absent of specific cell surface toll-like receptors (TLRs), major histocompatibility complex (MHC) class II, invariant chain (CD74) and the CD4 (cluster of differentiation 4) receptor. Despite the loss of these major components considered as critical to vertebrate innate and adaptive immune systems the cod system is fully functional, however the underlying mechanisms of the immune response in cod remain largely unknown. In this study, ex vivo cod macrophages were challenged with various bacterial and viral microbe-associated molecular patterns (MAMP) to identify major response pathways. Cytosolic MAMP-PRR pathways based upon the NOD-like receptors (NLRs) and RIG-I-like receptors (RLRs) were identified as the critical response pathways. Our analyses suggest that internalization of exogenous ligands through scavenger receptors drives both pathways activating transcription factors like NF-kB (Nuclear factor-kappa B) and interferon regulatory factors (IRFs). Further, ligand-dependent differential expression of a unique TLR25 isoform and multiple NLR paralogues suggests (sub)neofunctionalisation toward specific immune defensive strategies. Our results further demonstrate that the unique immune system of the Atlantic cod provides an unprecedented opportunity to explore the evolutionary history of PRR-based signalling in vertebrate immunity.

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“…However, recently caspy2 has been reported as an intracellular LPS receptor in the zebrafish (26). In this study, no significant response to a standard LPS preparation was detected.…”

Section: Discussioncontrasting

confidence: 61%

Innovation in NLR and TLR sensing drives the MHC-II free Atlantic cod immune system

Jin

Morro

Tørresen

et al. 2020

Preprint

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“…Thus, whether noncanonical inflammasome activation exists in zebrafish, and which inflammatory caspases could mediate the noncanonical inflammasome activation to regulate pathogen clearance in fish, remains largely unknown. Very recently, a concurrent work in our laboratory has verified that the caspase‐5‐like‐activity‐dependent pyroptosis in zebrafish induced by E. piscicida 0909I is mediated by zebrafish caspy2 activation, which has the same substrate specificity as caspase‐5, and has also demonstrated the critical role of caspy2 in zebrafish noncanonical inflammasome activation and immune defence (D. Yang et al, ). These data, together with the evidence provided in this work, confirmed the existence of a noncanonical inflammasome pathway in zebrafish.…”

Section: Discussionmentioning

confidence: 88%

Dysregulated haemolysin promotes bacterial outer membrane vesicles-induced pyroptotic-like cell death in zebrafish

Wen

Chen

Jiang

et al. 2019

Cellular Microbiology

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Inflammasomes are important innate immune components in mammals. However, the bacterial factors modulating inflammasome activation in fish, and the mechanisms by which they alter fish immune defences, remain to be investigated. In this work, a mutant of the fish pathogen Edwardsiella piscicida (E. piscicida), called 0909I, was shown to overexpress haemolysin, which could induce a robust pyroptotic-like cell death dependent on caspase-5-like activity during infection in fish nonphagocyte cells. E. piscicida haemolysin was found to mainly associate with bacterial outer membrane vesicles (OMVs), which were internalised into the fish cells via a dynamindependent endocytosis and induced pyroptotic-like cell death. Importantly, bacterial immersion infection of both larvae and adult zebrafish suggested that dysregulated expression of haemolysin alerts the innate immune system and induces intestinal inflammation to restrict bacterial colonisation in vivo. Taken together, these results suggest a critical role of zebrafish innate immunity in monitoring invaded pathogens via detecting the bacterial haemolysin-associated OMVs and initiating pyroptoticlike cell death. These new additions to the understanding of haemolysin-mediated pathogenesis in vivo provide evidence for the existence of noncanonical inflammasome signalling in lower vertebrates. KEYWORDS bacterial outer membrane vesicles, Edwardsiella piscicida, haemolysin, pyroptotic-like cell death, zebrafish intestinal infection

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“…Not finding sex ratio differences in other LPS strains tested or other doses might be explained by the fact that sensitivity to the LPS response depends on the LPS bacterial origin species, serotype, doses, experimental concentrations and the time of duration of the exposure (Novoa et al, 2009). It is known that fish, together with amphibians, are J o u r n a l P r e -p r o o f resistant to the toxic effect of LPS as high doses are required to trigger an immune response when compared to mammals (Berczi et al, 1966;Sepulcre et al, 2009) and these differences were originated by diverse molecular strategies to recognize LPS (Chu and Mazmanian, 2013;Yang et al, 2018).…”

Section: J O U R N a L P R E -P R O O Fmentioning

confidence: 99%

Epigenetic differences in the innate response after immune stimulation during zebrafish sex differentiation

Moraleda-Prados

Caballero‐Huertas

Valdivieso

et al. 2021

Developmental & Comparative Immunology

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Sensing of cytosolic LPS through caspy2 pyrin domain mediates noncanonical inflammasome activation in zebrafish

Cited by 56 publications

References 44 publications

Innovation in NLR and TLR sensing drives the MHC-II free Atlantic cod immune system

Innovation in NLR and TLR sensing drives the MHC-II free Atlantic cod immune system

Dysregulated haemolysin promotes bacterial outer membrane vesicles-induced pyroptotic-like cell death in zebrafish

Epigenetic differences in the innate response after immune stimulation during zebrafish sex differentiation

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