NLRP1-dependent activation of Gasdermin D in neutrophils controls cutaneous leishmaniasis

PLoS Pathog. 2024 Sep 9;20(9):e1012527. doi: 10.1371/journal.ppat.1012527. eCollection 2024 Sep.

Abstract

Intracellular pathogens that replicate in host myeloid cells have devised ways to inhibit the cell's killing machinery. Pyroptosis is one of the host strategies used to reduce the pathogen replicating niche and thereby control its expansion. The intracellular Leishmania parasites can survive and use neutrophils as a silent entry niche, favoring subsequent parasite dissemination into the host. Here, we show that Leishmania mexicana induces NLRP1- and caspase-1-dependent Gasdermin D (GSDMD)-mediated pyroptosis in neutrophils, a process critical to control the parasite-induced pathology. In the absence of GSDMD, we observe an increased number of infected dermal neutrophils two days post-infection. Using adoptive neutrophil transfer in neutropenic mice, we show that pyroptosis contributes to the regulation of the neutrophil niche early after infection. The critical role of neutrophil pyroptosis and its positive influence on the regulation of the disease outcome was further demonstrated following infection of mice with neutrophil-specific deletion of GSDMD. Thus, our study establishes neutrophil pyroptosis as a critical regulator of leishmaniasis pathology.

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Apoptosis Regulatory Proteins / metabolism
  • Gasdermins
  • Intracellular Signaling Peptides and Proteins* / genetics
  • Intracellular Signaling Peptides and Proteins* / metabolism
  • Leishmania mexicana / immunology
  • Leishmaniasis, Cutaneous* / immunology
  • Leishmaniasis, Cutaneous* / metabolism
  • Leishmaniasis, Cutaneous* / parasitology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neutrophils* / immunology
  • Neutrophils* / metabolism
  • Phosphate-Binding Proteins* / metabolism
  • Pyroptosis*

Substances

  • Phosphate-Binding Proteins
  • Gsdmd protein, mouse
  • Intracellular Signaling Peptides and Proteins
  • Apoptosis Regulatory Proteins
  • Adaptor Proteins, Signal Transducing
  • Gasdermins

Grants and funding

This work was supported by grants from the Swiss National Science Foundation (SNSF) 310030_184751 and 310030_184751/2 to FTC and 310030_192523 to PB, and in part by the Intramural Research Program of the NIH (S.K., E.I., S.D.). S.D. is supported by a fellowship from the Indian Council of Medical Research, Government of India (reference number INDO/FRC/452/Y-32/2022-23-IH & HRD, dated 21.02.2023). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.