TRPA1 Influences Staphylococcus aureus Skin Infection in Mice and Associates with HIF-1a and MAPK Pathway Modulation

Int J Mol Sci. 2024 Sep 14;25(18):9933. doi: 10.3390/ijms25189933.

Abstract

Infections caused by methicillin-resistant Staphylococcus aureus (MRSA) are a major public health burden. Emerging antibiotic resistance has heightened the need for new treatment approaches for MRSA infection such as developing novel antimicrobial agents and enhancing the host's defense response. The thermo-ion channels Transient Receptor Potential (TRP-) A1 and V1 have been identified as modulators of S. aureus quorum sensing in cell culture models. However, their effects on in vivo infection control are unknown. In this study, we investigated the therapeutic effect of natural TRP ion channel inhibitors on MRSA skin infection in mice. While deletion of TRPV1 did not affect lesion size or inflammatory markers, TRPA1-/- mice demonstrated significantly reduced infection severity and abscess size. Treatment with natural inhibitors of TRPA1 with or without blockade of TRPV1 also reduced abscess size. Tissue transcriptomic data coupled with immunohistochemistry revealed that TRPA1 inhibition impacted heat shock protein expression (HSP), modulated the HIF-1a and MAPK pathways, and reduced IL4 expression. Additionally, metabolomics data showed an impact on purine and glycosaminoglycan pathways. Multi-omic integration of transcriptomic and metabolic data revealed that diacylglycerol metabolism was the likely bridge between metabolic and immunological impacts. Our findings suggest that TRPA1 antagonism could provide a promising and cost-effective therapeutic approach for reducing the severity of MRSA infection, and presents a novel underlying molecular mechanism.

Keywords: MRSA; TRPA1; TRPV1; metabolomics; staphylococcus aureus.

MeSH terms

  • Animals
  • Hypoxia-Inducible Factor 1, alpha Subunit* / genetics
  • Hypoxia-Inducible Factor 1, alpha Subunit* / metabolism
  • MAP Kinase Signaling System / drug effects
  • Methicillin-Resistant Staphylococcus aureus* / drug effects
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Staphylococcal Infections / metabolism
  • Staphylococcal Infections / microbiology
  • Staphylococcal Skin Infections* / drug therapy
  • Staphylococcal Skin Infections* / metabolism
  • Staphylococcal Skin Infections* / microbiology
  • Staphylococcal Skin Infections* / pathology
  • TRPA1 Cation Channel* / genetics
  • TRPA1 Cation Channel* / metabolism
  • TRPV Cation Channels / genetics
  • TRPV Cation Channels / metabolism

Substances

  • TRPA1 Cation Channel
  • Trpa1 protein, mouse
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Hif1a protein, mouse
  • TRPV1 protein, mouse
  • TRPV Cation Channels