Cystitis-induced bladder pain is Toll-like receptor 4 dependent in a transgenic autoimmune cystitis murine model: a MAPP Research Network animal study

Am J Physiol Renal Physiol. 2019 Jul 1;317(1):F90-F98. doi: 10.1152/ajprenal.00017.2019. Epub 2019 May 15.

Abstract

Altered Toll-like receptor (TLR)4 activation has been identified in several chronic pain conditions but has not been well studied in interstitial cystitis/bladder pain syndrome (IC/BPS). Our previously published human studies indicated that patients with IC/BPS present altered systemic TLR4-mediated inflammatory responses, which were significantly correlated with reported pain severity. In the present study, we sought to determine whether altered TLR4 activation plays a role in pelvic/bladder pain seen in patients with IC/BPS using our validated IC/BPS-like transgenic autoimmune cystitis model (URO-OVA). URO-OVA mice developed responses consistent with pelvic and bladder pain after cystitis induction, which was associated with increased splenocyte production of TLR4-mediated proinflammatory cytokines IL-1β, IL-6, and TNF-α. Increased spinal expression of mRNAs for proinflammatory cytokines IL-6 and TNF-α, glial activation markers CD11b and glial fibrillary acidic protein, and endogenous TLR4 ligand high mobility group box 1 was also observed after cystitis induction. Compared with URO-OVA mice, TLR4-deficient URO-OVA mice developed significantly reduced nociceptive responses, although similar bladder inflammation and voiding dysfunction, after cystitis induction. Intravenous administration of TAK-242 (a TLR4-selective antagonist) significantly attenuated nociceptive responses in cystitis-induced URO-OVA mice, which was associated with reduced splenocyte production of TLR4-mediated IL-1β, IL-6, and TNF-α as well as reduced spinal expression of mRNAs for IL-6, TNF-α, CD11b, glial fibrillary acidic protein, and high mobility group box 1. Our results indicate that altered TLR4 activation plays a critical role in bladder nociception independent of inflammation and voiding dysfunction in the URO-OVA model, providing a potential mechanistic insight and therapeutic target for IC/BPS pain.

Keywords: Multidisciplinary Approach to the Study of Chronic Pelvic Pain; Toll-like receptor 4; cystitis; model; pain.

Publication types

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

MeSH terms

  • Analgesics / pharmacology
  • Animals
  • Autoimmune Diseases / genetics
  • Autoimmune Diseases / immunology
  • Autoimmune Diseases / metabolism*
  • Autoimmune Diseases / physiopathology
  • Cells, Cultured
  • Cystitis, Interstitial / genetics
  • Cystitis, Interstitial / immunology
  • Cystitis, Interstitial / metabolism*
  • Cystitis, Interstitial / physiopathology
  • Cytokines / genetics
  • Cytokines / metabolism
  • Disease Models, Animal
  • Inflammation Mediators / metabolism
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nociceptive Pain / genetics
  • Nociceptive Pain / immunology
  • Nociceptive Pain / metabolism*
  • Nociceptive Pain / physiopathology
  • Ovalbumin / genetics
  • Ovalbumin / immunology
  • Ovalbumin / metabolism
  • Pain Threshold* / drug effects
  • Signal Transduction
  • Spine / immunology
  • Spine / metabolism
  • Spleen / immunology
  • Spleen / metabolism
  • Sulfonamides / pharmacology
  • Toll-Like Receptor 4 / antagonists & inhibitors
  • Toll-Like Receptor 4 / genetics
  • Toll-Like Receptor 4 / immunology
  • Toll-Like Receptor 4 / metabolism*
  • Urinary Bladder / drug effects
  • Urinary Bladder / immunology
  • Urinary Bladder / metabolism*
  • Urinary Bladder / physiopathology
  • Urodynamics

Substances

  • Analgesics
  • Cytokines
  • Inflammation Mediators
  • Sulfonamides
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • ethyl 6-(N-(2-chloro-4-fluorophenyl)sulfamoyl)cyclohex-1-ene-1-carboxylate
  • Ovalbumin