IPSE, a parasite-derived, host immunomodulatory infiltrin protein, alleviates resiniferatoxin-induced bladder pain

Mol Pain. 2020 Jan-Dec:16:1744806920970099. doi: 10.1177/1744806920970099.

Abstract

The transient receptor potential cation channel subfamily V member 1 (TRPV1) receptor is an important mediator of nociception and its expression is enriched in nociceptive neurons. TRPV1 signaling has been implicated in bladder pain and is a potential analgesic target. Resiniferatoxin is the most potent known agonist of TRPV1. Acute exposure of the rat bladder to resiniferatoxin has been demonstrated to result in pain-related freezing and licking behaviors that are alleviated by virally encoded IL-4. The interleukin-4-inducing principle of Schistosoma mansoni eggs (IPSE) is a powerful inducer of IL-4 secretion, and is also known to alter host cell transcription through a nuclear localization sequence-based mechanism. We previously reported that IPSE ameliorates ifosfamide-induced bladder pain in an IL-4- and nuclear localization sequence-dependent manner. We hypothesized that pre-administration of IPSE to resiniferatoxin-challenged mice would dampen pain-related behaviors. IPSE indeed lessened resiniferatoxin-triggered freezing behaviors in mice. This was a nuclear localization sequence-dependent phenomenon, since administration of a nuclear localization sequence mutant version of IPSE abrogated IPSE's analgesic effect. In contrast, IPSE's analgesic effect did not seem IL-4-dependent, since use of anti-IL-4 antibody in mice given both IPSE and resiniferatoxin did not significantly affect freezing behaviors. RNA-Seq analysis of resiniferatoxin- and IPSE-exposed bladders revealed differential expression of TNF/NF-κb-related signaling pathway genes. In vitro testing of IPSE uptake by urothelial cells and TRPV1-expressing neuronal cells showed uptake by both cell types. Thus, IPSE's nuclear localization sequence-dependent therapeutic effects on TRPV1-mediated bladder pain may act on TRPV1-expressing neurons and/or may rely upon urothelial mechanisms.

Keywords: Bladder; analgesic; immune modulation; pain; parasite; schistosoma.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Cell Nucleus / drug effects
  • Cell Nucleus / metabolism
  • Diterpenes / adverse effects*
  • Egg Proteins / pharmacology
  • Egg Proteins / therapeutic use*
  • Endocytosis / drug effects
  • Female
  • Gene Expression Profiling
  • Gene Expression Regulation / drug effects
  • Helminth Proteins / pharmacology
  • Helminth Proteins / therapeutic use*
  • Host-Parasite Interactions / immunology*
  • Humans
  • Immunologic Factors / pharmacology
  • Immunologic Factors / therapeutic use*
  • Interleukin-4 / metabolism
  • Mice, Inbred C57BL
  • NF-kappa B / metabolism
  • Neurons / drug effects
  • Neurons / metabolism
  • Nuclear Localization Signals / metabolism
  • Pain / drug therapy*
  • Pain / genetics
  • Parasites / chemistry*
  • Principal Component Analysis
  • Protein Transport / drug effects
  • Signal Transduction / drug effects
  • Tumor Necrosis Factor-alpha / metabolism
  • Urinary Bladder / drug effects
  • Urinary Bladder / pathology*
  • Urothelium / metabolism

Substances

  • Diterpenes
  • Egg Proteins
  • Helminth Proteins
  • IPSE protein, Schistosoma mansoni
  • Immunologic Factors
  • NF-kappa B
  • Nuclear Localization Signals
  • Tumor Necrosis Factor-alpha
  • Interleukin-4
  • resiniferatoxin