SENP1 Promotes Caspase-11 Inflammasome Activation and Aggravates Inflammatory Response in Murine Acute Lung Injury Induced by Lipopolysaccharide

Front Biosci (Landmark Ed). 2024 Nov 21;29(11):397. doi: 10.31083/j.fbl2911397.

Abstract

Background: Infection is the leading cause of acute lung injury (ALI). Macrophages, which are pivotal innate immune cells, play a critical role in mediating inflammatory processes. Intracellular lipopolysaccharide (LPS) from invasive Gram-negative bacteria can activate the caspase-11 inflammasome, leading to the induction of pyroptosis in macrophages. This process subsequently triggers the release of inflammatory cytokines and damage-associated molecular patterns from pyroptotic macrophages, thereby exacerbating inflammatory progression in ALI. However, the precise regulatory mechanisms governing caspase-11 activation is still unclear. Sentrin-specific proteases (SENPs) have been identified as notable targets for their anti-inflammatory properties. Nevertheless, the specific role of SENPs in macrophage pyroptosis during the pathogenesis of ALI remains unknown.

Methods: We used LPS as an endotoxin to induce ALI. We analyzed the expression and location of sentrin-specific protease 1 (SENP1), pulmonary impairment, macrophage infiltration, caspase-11 inflammasome expression and activation, caspase-11 SUMOylation, and inflammatory cytokine secretion.

Results: Upregulated expression of SENP1 in lung tissue and macrophages was observed following LPS stimulation. SENP1 mediates de-SUMOylation and activation of caspase-11 inflammasome in macrophages. Moreover, pharmacological inhibition or genetic deficiency of SENP1 in macrophages significantly improved ALI-related histological damage by reducing the secretion of inflammatory cytokines and suppressing caspase-11-dependent pyroptosis.

Conclusions: Collectively, our findings highlight the involvement of SENP1 in caspase-11 activation and inflammatory progression in macrophages, thereby establishing a scientific foundation for the exploration of novel therapeutic strategies aimed at treating ALI.

Keywords: acute lung injury; caspase-11; inflammation; macrophage; sentrin-specific protease 1.

MeSH terms

  • Acute Lung Injury* / chemically induced
  • Acute Lung Injury* / genetics
  • Acute Lung Injury* / immunology
  • Acute Lung Injury* / metabolism
  • Animals
  • Caspases / metabolism
  • Caspases, Initiator* / genetics
  • Caspases, Initiator* / metabolism
  • Cysteine Endopeptidases* / genetics
  • Cysteine Endopeptidases* / metabolism
  • Cytokines / genetics
  • Cytokines / metabolism
  • Inflammasomes* / metabolism
  • Inflammation / metabolism
  • Lipopolysaccharides*
  • Macrophages / immunology
  • Macrophages / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL*
  • Pyroptosis

Substances

  • Lipopolysaccharides
  • Caspases, Initiator
  • Casp4 protein, mouse
  • Inflammasomes
  • Cysteine Endopeptidases
  • Senp1 protein, mouse
  • Caspases
  • Cytokines