Neutrophil inflammasomes sense the subcellular delivery route of translocated bacterial effectors and toxins

Oh, Changhoon; Li, Lupeng; Verma, Ashwani Kumar; Reuven, Arianna D.; Miao, Edward A.; Bliska, James B.; Aachoui, Youssef

doi:10.1016/j.celrep.2022.111688

Cited by 11 publications

(39 citation statements)

References 55 publications

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“…73,74 Subsequent studies have verified that neutrophils can assemble functional inflammasome platforms initiated by AIM2, 75 NLRC4, 35,[75][76][77][78][79] NLRP1, 75 NLRP3, 32,34,51,57,75,80,81 and pyrin/ MEFV. 75,78 These are discussed in detail below regarding the differential induction of IL-1β release versus pyroptosis as downstream responses to inflammasome activation in neutrophils. Figure 1 illustrates the major subtypes of inflammasome platforms and their signaling pathways that have been described in neutrophils.…”

Section: Infl Amma Some S and G A S Dermin S A S Criti C Al Reg Ul At...mentioning

confidence: 99%

“…Recent functional studies have demonstrated that human and murine neutrophils express high levels of GSDMD 54,56,75,78,79,99–106 and GSDME 78,102 protein; analyses of the possible expression of the other GSDM proteins in neutrophils have not been reported. Although comprehensive transcriptomic profiling of GSDM family expression in neutrophils has not been reported, our RNA‐Seq analysis of FACS isolated (>99%) murine neutrophil populations revealed high gene expression of GSDME and GSDMD, but no other murine GSDM family members (E. Pearlman and G.R.…”

Section: Inflammasomes and Gasdermins As Critical Regulators Of Pyrop...mentioning

confidence: 99%

“…Oh et al 78 tested the general applicability of this apparent delivery route‐specific induction of neutrophil pyroptosis by caspase‐1 based inflammasome by showing that activation of NLRC4 inflammasomes is coupled to pyroptosis in response to P. aeruginosa , which utilizes contact‐mediated T3SS assembly in the plasma membrane to inject NLRC4‐inducing PAMPs. Conversely, neutrophils resisted pyroptosis when NLRC4 PAMPS are injected via T3SS assembled within phagosomal membranes by internalized Salmonella typhimurium .…”

Section: Neutrophil Inflammasome Signaling Pathways That Facilitate R...mentioning

confidence: 99%

“…Finally, Oh et al 78 described the ability of Yptb‐ΔyopM infection to facilitate NETosis downstream of active pyrin inflammasome assembly and accumulation of pro‐pyroptotic N‐GSDMD pores in the plasma membrane. Similar to the findings of Santoni et al 79 with P. aeruginosa ‐infected neutrophils, PAD4‐mediated H3 histone citrullination was triggered by Ca 2+ influx through the plasma membrane N‐GSDMD pores that accumulated in Yptb‐ΔyopM infected neutrophils.…”

Section: Neutrophil Inflammasome Signaling Pathways That Facilitate R...mentioning

confidence: 99%

“…Studies with GSDMD‐knockout or GSDME‐knockout myeloid cells confirmed that GSDMD, but not GSDME, was required for macrophage death, while the opposite was true for neutrophils. Furthermore, as described in Section 6.2, Oh et al 78 used a Yersinia strain deficient in the YopM virulence factor to drive pyrin‐dependent caspase‐1 signaling responses in wildtype neutrophils versus neutrophils lacking GSDMD, GSDME or both GSDMs. They determined that pyrin‐dependent caspase‐1 induced pyroptosis via two parallel signaling pathways involving accumulation of both N‐GSDMD and N‐GSDME membrane pores and that ablation of both GSDMs was required to suppress release of IL‐1β.…”

Section: Integrated Model For How Different Inflammasome Signaling Pl...mentioning

confidence: 99%

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Pyroptosis in neutrophils: Multimodal integration of inflammasome and regulated cell death signaling pathways

Dubyak

Miller

Pearlman

2023

Immunological Reviews

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Pyroptosis is a proinflammatory mode of lytic cell death mediated by accumulation of plasma membrane (PM) macropores composed of gasdermin-family (GSDM) proteins.It facilitates two major functions in innate immunity: (i) elimination of intracellular replicative niches for pathogenic bacteria; and (ii) non-classical secretion of IL-1 family cytokines that amplify host-beneficial inflammatory responses to microbial infection or tissue damage. Physiological roles for gasdermin D (GSDMD) in pyroptosis and IL-1β release during inflammasome signaling have been extensively characterized in macrophages. This involves cleavage of GSDMD by caspase-1 to generate GSDMD macropores that mediate IL-1β efflux and progression to pyroptotic lysis. Neutrophils, which rapidly accumulate in large numbers at sites of tissue infection or damage, become the predominant local source of IL-1β in coordination with their potent microbiocidal capacity. Similar to macrophages, neutrophils express GSDMD and utilize the same spectrum of diverse inflammasome platforms for caspase-1-mediated cleavage of GSDMD. Distinct from macrophages, neutrophils possess a remarkable capacity to resist progression to GSDMD-dependent pyroptotic lysis to preserve their viability for efficient microbial killing while maintaining GSDMD-dependent mechanisms for export of bioactive IL-1β. Rather, neutrophils employ cell-specific mechanisms to conditionally engage GSDMD-mediated pyroptosis in response to bacterial pathogens that use neutrophils as replicative niches. GSDMD and pyroptosis have also been mechanistically linked to induction of NETosis, a signature neutrophil pathway that expels decondensed nuclear DNA into extracellular compartments for immobilization and killing of microbial pathogens. This review summarizes a rapidly growing number of recent studies that have produced new insights, unexpected mechanistic nuances, and some controversies regarding the regulation of, and roles for, neutrophil inflammasomes, pyroptosis, and GSDMs in diverse innate immune responses.

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Section: Infl Amma Some S and G A S Dermin S A S Criti C Al Reg Ul At...mentioning

confidence: 99%

Section: Inflammasomes and Gasdermins As Critical Regulators Of Pyrop...mentioning

confidence: 99%

Section: Neutrophil Inflammasome Signaling Pathways That Facilitate R...mentioning

confidence: 99%

Section: Neutrophil Inflammasome Signaling Pathways That Facilitate R...mentioning

confidence: 99%

Section: Integrated Model For How Different Inflammasome Signaling Pl...mentioning

confidence: 99%

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Pyroptosis in neutrophils: Multimodal integration of inflammasome and regulated cell death signaling pathways

Dubyak

Miller

Pearlman

2023

Immunological Reviews

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show abstract

Neuronal pyroptosis mediated by STAT3 in early brain injury after subarachnoid hemorrhage

Tang,

Lai,

2024

Brain Research

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Pyroptosis in defense against intracellular bacteria

Dickinson

Coers

et al. 2023

Seminars in Immunology

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Neutrophil inflammasomes sense the subcellular delivery route of translocated bacterial effectors and toxins

Cited by 11 publications

References 55 publications

Pyroptosis in neutrophils: Multimodal integration of inflammasome and regulated cell death signaling pathways

Pyroptosis in neutrophils: Multimodal integration of inflammasome and regulated cell death signaling pathways

Neuronal pyroptosis mediated by STAT3 in early brain injury after subarachnoid hemorrhage

Pyroptosis in defense against intracellular bacteria

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