Abstract
Introduction and hypothesis
The aim of this study was to analyze the mechanism underlying cross-sensitization between the colon and the bladder via activation of transient receptor potential A1 (TRPA1) channels.
Methods
Using female Sprague–Dawley rats, polyethylene catheters were inserted into the colon between two ligations at the levels of 40 and 60 mm rostral to the anus and into the bladder. (1) We examined changes in colon and bladder activity after the application of allyl isothiocyanate (AI, 50 mM, 300 μl), a TRPA1 activator, into the colon or the bladder in an awake condition. Inhibitory effects of the pretreatment with HC-030031 (HC, 3 mg/kg), a TRPA1 inhibitor, on colon-to-bladder cross-sensitization induced by AI instilled in the colon were also investigated. (2) We examined Evans blue (EB) dye extravasation after TRPA1 stimulation in the colon or the bladder to evaluate vascular permeability due to tissue inflammation.
Results
(1) Intercontraction intervals during continuous saline infusion into the bladder (0.04 ml/min) were significantly decreased after the intracolonic AI application, which significantly increased mean intracolonic pressure, indicative of colon-to-bladder cross-sensitization. The AI-induced colon-to-bladder cross-sensitization was completely prevented by the pretreatment with intravenous application of HC. On the other hand, mean intracolonic pressure was significantly decreased after the intravesical AI application, which significantly increased mean intravesical pressure. (2) EB dye extravasation was significantly increased in the AI-treated inflamed organs and also in the bladder following intracolonic AI treatment.
Conclusions
Colon-to-bladder cross-sensitization is mediated via TRPA1 stimulation in the colon, although TRPA1 expressed in the bladder does not seem to participate in bladder-to-colon cross-sensitization.
Similar content being viewed by others
References
Alagiri M, Chottiner S, Ratner V, Slade D, Hanno PM (1997) Interstitial cystitis: unexplained associations with other chronic disease and pain syndromes. Urology 49:52–57
Novi JM, Jeronis S, Srinivas S, Srinivasan R, Morgan MA, Arya LA (2005) Risk of irritable bowel syndrome and depression in women with interstitial cystitis: a case-control study. J Urol 174:937–940
Blanchard EB, Keefer L, Lackner JM, Galovski TE, Krasner S, Sykes MA (2004) The role of childhood abuse in Axis I and Axis II psychiatric disorders and medical disorders of unknown origin among irritable bowel syndrome patients. J Psychosom Res 56:431–436
Berkley KJ (2005) A life of pelvic pain. Physiol Behav 86:272–280
Story GM, Peier AM, Reeve AJ et al (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112:819–829
Suzuki M, Watanabe Y, Oyama Y et al (2003) Localization of mechanosensitive channel TRPV4 in mouse skin. Neurosci Lett 353:189–192
Tsukimi Y, Mizuyachi K, Yamasaki T, Niki T, Hayashi F (2005) Cold response of the bladder in guinea pig: involvement of transient receptor potential channel, TRPM8. Urology 65:406–410
Andersson KE, Gratzke C, Hedlund P (2010) The role of the transient receptor potential (TRP) superfamily of cation-selective channels in the management of the overactive bladder. BJU Int 106:1114–1127
Patapoutian A, Tate S, Woolf CJ (2009) Transient receptor potential channels: targeting pain at the source. Nat Rev Drug Discov 8:55–68
Yamada T, Ugawa S, Ueda T, Ishida Y, Kajita K, Shimada S (2009) Differential localizations of the transient receptor potential channels TRPV4 and TRPV1 in the mouse urinary bladder. J Histochem Cytochem 57:277–287
Liu L, Mansfield KJ, Kristiana I, Vaux KJ, Millard RJ, Burcher E (2007) The molecular basis of urgency: regional difference of vanilloid receptor expression in the human urinary bladder. Neurourol Urodyn 26:433–438
Akbar A, Yiangou Y, Facer P, Walters JR, Anand P, Ghosh S (2008) Increased capsaicin receptor TRPV1-expressing sensory fibres in irritable bowel syndrome and their correlation with abdominal pain. Gut 57:923–929
Asfaw TS, Hypolite J, Northington GM, Arya LA, Wein AJ, Malykhina AP (2011) Acute colonic inflammation triggers detrusor instability via activation of TRPV1 receptors in a rat model of pelvic organ cross-sensitization. Am J Physiol Regul Integr Comp Physiol 300:R1392–R1400
Malykhina AP (2007) Neural mechanisms of pelvic organ cross-sensitization. Neuroscience 149:660–672
Jordt SE, Bautista DM, Chuang HH et al (2004) Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427:260–265
Brierley SM, Hughes PA, Page AJ et al (2009) The ion channel TRPA1 is required for normal mechanosensation and is modulated by algesic stimuli. Gastroenterology 137:2084–2095
Bautista DM, Jordt SE, Nikai T et al (2006) TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124:1269–1282
Satoh J, Yamakage M (2009) Desflurane induces airway contraction mainly by activating transient receptor potential A1 of sensory C-fibers. J Anesth 23:620–623
Peng HY, Chen GD, Tung KC et al (2009) Colon mustard oil instillation induced cross-organ reflex sensitization on the pelvic-urethra reflex activity in rats. Pain 142:75–88
Winnard KP, Dmitrieva N, Berkley KJ (2006) Cross-organ interactions between reproductive, gastrointestinal, and urinary tracts: modulation by estrous stage and involvement of the hypogastric nerve. Am J Physiol Regul Integr Comp Physiol 291:R1592–R1601
Andrade EL, Ferreira J, André E, Calixto JB (2006) Contractile mechanisms coupled to TRPA1 receptor activation in rat urinary bladder. Biochem Pharmacol 72:104–114
Du S, Araki I, Kobayashi H, Zakoji H, Sawada N, Takeda M (2008) Differential expression profile of cold (TRPA1) and cool (TRPM8) receptors in human urogenital organs. Urology 72:450–455
Furuta A, Suzuki Y, Hayashi N, Egawa S, Yoshimura N (2012) Transient receptor potential A1 receptor-mediated neural cross-talk and afferent sensitization induced by oxidative stress: implication for the pathogenesis of interstitial cystitis/bladder pain syndrome. Int J Urol 19:429–436
Julius D, Basbaum AI (2001) Molecular mechanisms of nociception. Nature 413:203–210
Malykhina AP, Qin C, Greenwood-van Meerveld B, Foreman RD, Lupu F, Akbarali HI (2006) Hyperexcitability of convergent colon and bladder dorsal root ganglion neurons after colonic inflammation: mechanism for pelvic organ cross-talk. Neurogastroenterol Motil 18:936–948
Christianson JA, Liang R, Ustinova EE, Davis BM, Fraser MO, Pezzone MA (2007) Convergence of bladder and colon sensory innervation occurs at the primary afferent level. Pain 128:235–243
de Groat WC (2006) Integrative control of the lower urinary tract: preclinical perspective. Br J Pharmacol 147(Suppl 2):S25–S40
Rouzade-Dominguez ML, Miselis R, Valentino RJ (2003) Central representation of bladder and colon revealed by dual transsynaptic tracing in the rat: substrates for pelvic visceral coordination. Eur J Neurosci 18:3311–3324
La JH, Schwartz ES, Gebhart GF (2011) Differences in the expression of transient receptor potential channel V1, transient receptor potential channel A1 and mechanosensitive two pore-domain K+ channels between the lumbar splanchnic and pelvic nerve innervations of mouse urinary bladder and colon. Neuroscience 186:179–187
Acknowledgments
This study was supported by Department of Defense grant W81XWH-12-1-0565.
Conflicts of interest
None.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Furuta, A., Suzuki, Y., Naruoka, T. et al. Cross-sensitization mechanisms between colon and bladder via transient receptor potential A1 stimulation in rats. Int Urogynecol J 25, 1575–1581 (2014). https://doi.org/10.1007/s00192-014-2405-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00192-014-2405-y