Urothelial and Afferent Mechanisms Inducing Bladder Pain in Interstitial Cystitis

REFERENCES

• Alessandri-Haber N, Yeh JJ, Boyd AE, Parada CA, Chen X, Reichling DB and Levine JD. Hypotonicity induces TRPV4-mediated nociception in rat. Neuron 39: 497–511, 2003.
   PubMed Web of Science ®Google Scholar
• Anderson G, Palermo J, Schilling J, Roth R, Heuser J and Hultgren S. Intracellular bacterial biofilm-like pods in urinary tract infections. Science 301: 105–107, 2003.
   Google Scholar
• Andersson KE and Yoshida M. Antimuscarinics and the overactive detrusor-which is the main mechanism of action? Eur Urol 43: 1–5, 2003.
   PubMed Web of Science ®Google Scholar
• Avelino A, Cruz C, Nagy I and Cruz F. Vanilloid receptor 1 expression in the rat urinary tract. Neuroscience 109: 787–798, 2002.
   PubMed Web of Science ®Google Scholar
• Barrick SR, Lee H, Meyers S, Caterina MJ, Kanai AJ, Zeidel ML, Chopra B, de Groat WC and Birder L. Expression and function of TRPV4 in urinary bladder urothelium. Soc Neurosci Abstr 26: 608.6, 2003.
   Google Scholar
• Beckel J, Barrick SR, Keast JR, Meyers S, Kanai AJ, de Groat WC, Zeidel ML and Birder L. Expression and function of urothelial muscarinic receptors and interactions with bladder nerves. Soc Neurosci Abstr 26: 846.23, 2004.
   Google Scholar
• Beckel JM, Kanai A, Lee SJ, deGroat WC and Birder LA: Expression of functional nicotinic acetylcholine receptors in rat urinary bladder epithelial cells. Am J Physiol, 290: F103-F110, 2006 Bennett DL, Dmietrieva N, Priestley JV, Clary D and McMahon SB. trkA, CGRP and IB4 expression in retrogradely labelled cutaneous and visceral primary sensory neurones in the rat. Neurosci Lett 206: 33–36, 1996.
   Google Scholar
• Birder L, Apodaca G, de Groat WC and Kanai AJ. Adrenergic- and capsaicin-evoked nitric oxide release from urothelium and afferent nerves in urinary bladder. Am J Physiol 275: F226–F229, 1998.
   Google Scholar
• Birder L, Barrick SR, Roppolo JR, Kanai AJ, de Groat WC, Kiss S and Buffington CA. Feline interstitial cystitis results in mechanical hypersensitivity and altered ATP release from bladder urothelium. Am J Physiol 285: F423–F429, 2003.
   Google Scholar
• Birder L, Kanai AJ, de Groat WC, Kiss S, Nealen ML, Burke NE, Dineley KE, Watkins S, Reynolds IJ and Caterina MJ. Vanilloid receptor expression suggests a sensory role for urinary bladder epithelial cells. Proc Natl Acad Sci USA 98: 13396–13401, 2001.
   PubMed Web of Science ®Google Scholar
• Birder L, Nealen ML, Kiss S, de Groat WC, Caterina MJ, WangE,Apodaca G and Kanai AJ. Beta-adrenoceptor agonists stimulate endothelial nitric oxide synthase in rat urinary bladder urothelial cells. J Neurosci 22: 8063–8070, 2002a. Birder L, Nakamura Y, Kiss S, Nealen ML, Barrick SR, Kanai AJ, Wang E, Ruiz WG, de Groat WC, Apodaca G, Watkins S and Caterina MJ. Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat Neurosci 5: 856–860, 2002b. Birder L, Ruan HZ, Chopra B, Xiang Z, Barrick SR, Buffington CA, Roppolo JR, Ford AP, de Groat WC and Burnstock G. Alterations in P2X and P2Y purinergic receptor expression in urinary bladder from normal cats and cats with interstitial cystitis. Am J Physiol 287: F1084-F1091, 2004.
   Web of Science ®Google Scholar
• Birder L, Wolf-Johnston AS, Buffington CA, Roppolo JR, de Groat WC and Kanai AJ. Altered Inducible Nitric Oxide Synthase Expression and Nitric Oxide Production in Urinary Bladder from Cats with Feline Interstitial Cystitis. J Urol 173: 625–629, 2005.
   Google Scholar
• Bladder Research Progress Review Group: Overcoming Bladder Disease. A Strategic Plan for Research. Bethesda, MD, National Institute of Diabetes & Digestive & Kidney Diseases (National Institutes of Health): Chap 8, 2002.
   Google Scholar
• Buffington CA. Visceral pain in humans: lessons from animals. Curr Pain Headache Rep 5: 44–51, 2001.
   PubMedGoogle Scholar
• Buffington CA and Woodworth BE. Excretion of fluorescein in the urine of women with interstitial cystitis. J Urol 158: 786–789, 1997.
   PubMed Web of Science ®Google Scholar
• Buffington CA, Chew DJ and Woodworth BE. Feline interstitial cystitis. J Am Vet Med Assoc 215: 682–687, 1999a. Buffington CA, Chew DJ and Woodworth BE. Interstitial cystitis in humans, and cats? Urology 53: 239–240, 1999b. Burnstock G. Purine-mediated signalling in pain and visceral perception. Trends Pharmacol Sci 22: 182–188, 2001.
   Web of Science ®Google Scholar
• Cardenas CG, Del Mar LP, Cooper BY and Scroggs RS. 5HT4 receptors couple positively to tetrodotoxin-insensitive sodium channels in a subpopulation of capsaicin- sensitive rat sensory neurons. J Neurosci 17: 7181–7189, 1997.
   PubMed Web of Science ®Google Scholar
• Carattino MD, Sheng S and Kleyman TR. Mutations in the pore region modify epithelial sodium channel gating by shear stress. J Cell Biol 280: 4393–4401, 2005.
   Google Scholar
• Caterina MJ. The vanilloid receptor: A molecular gateway to the pain pathway. Ann Rev Neurosci 24: 602–607, 2001.
   Web of Science ®Google Scholar
• Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD and Julius D. The capsaicin receptor: A heat activated ion channel in the pain pathway. Nature 389: 816–824, 1997.
   PubMed Web of Science ®Google Scholar
• Chancellor MB and de Groat WC. Intravesical capsaicin and resiniferatoxin therapy: Spicing up the ways to treat the overactive bladder. J Urol 162: 3–11, 1999.
   PubMed Web of Science ®Google Scholar
• Chancellor MB and Yoshimura N. Treatment of Interstitial Cystitis. Urology 63 (3 Suppl 1): 85-92, 2004.
   Google Scholar
• Chen Y, Varghese R, Chiu P, et al. Urinary substance P is elevated in women with interstitial cystitis. J Urol 161 (4): 26, 1991.
   Google Scholar
• Cheng CL, Ma CP and de Groat WC. The effects of capsaicin on micturition and associated reflexes in the rat. Am J Physiol 265: R132–R138, 1993.
   Google Scholar
• Chess-Williams R. Muscarinic receptors of the urinary bladder: detrusor, urothelial and prejunctional. Auton Autacoid Pharmacol 22: 133–145, 2002.
   PubMedGoogle Scholar
• Chess-Williams R. Potential therapeutic targets for the treatment of detrusor overactivity. Expert Opin Ther Targets 8: 95–106, 2004.
   PubMed Web of Science ®Google Scholar
• Chopra B, Barrick SR, Meyers S, Beckel J, Zeidel ML, Ford AP, de Groat WC and Birder, LA. Expression and function of bradykinin B1/B2 receptors in normal and inflamed rat urinary bladder urothelium. J Physiol 562: 859–871, 2005.
   PubMed Web of Science ®Google Scholar
• Chopra B, de Groat WC, Roppolo JR, Buffington CA, Kanai AJ, Zeidel ML, Ford AP, Nunn P, Daniels D and Birder L. Alterations in stretch mediated prostacyclin release from bladder urothelium in feline interstitial cystitis. The FASEB Journal 18: 399.10, 2003.
   Google Scholar
• Chuang YC, Fraser MO, Yu Y, Chancellor MB, de Groat WC and Yoshimura N. The role of bladder afferent pathways in bladder hyperactivity induced by the intravesical administration of nerve growth factor. J Urol 165: 975–979, 2001.
   Google Scholar
• Chung MK, Lee H and Caterina MJ. Warm temperatures activate TRPV4 in mouse 308 keratinocytes. J Biol Chem 278: 32037-32046, 2003.
   Google Scholar
• Cockayne DA, Hamilton SG, Zhu QM, Dunn PM, Zhong Y, Novakovic S, Malmberg AB, Cain G, Berson A, Kassotakis L, Hedley L, Lachnit WG, Burnstock G, McMahon SB and Ford APDW. Urinary bladder hyporeflexia and reduced pain-related behaviour in P2X(3)-deficient mice. Nature 407: 1011-1015, 2000.
   Google Scholar
• Cox PJ: Cyclophosphamide cystitis-identification of acrolein as the causative agent. Biochem Pharmacol 28: 2045-2049, 1979.
   Google Scholar
• D’Andrea MR, Saban MR, Nguyen NB, Andrade-Gordon P and Saban R. Expression of protease-activated receptor- 1, -2, -3 and -5 in control and experimentally inflamed mouse bladder. Am J Pathol 162: 907–923, 2003.
   PubMed Web of Science ®Google Scholar
• Dang K, Bielefeldt K and Gebhart GF. Gastric ulcers reduce A-type potassium currents in rat gastric sensory ganglion neurons. Am J Physiol Gastrointest Liver Physiol 286: G573–G579, 2004.
   Google Scholar
• Dang K, Bielefeldt K and Gebhart GF. Differential responses of bladder lumbosacral and thoracolumbar dorsal root ganglion neurons to purinergic agonists, protons, and capsaicin. J Neurosci 25: 3973–3984, 2005.
   Google Scholar
• Dattilio A and Vizzard MA. Up-regulation of protease activated receptors in bladder after cyclophosphamide induced cystitis and colocalization with capsaicin receptor (VR1) in bladder nerve fibers. J Urol 173: 635–639, 2005.
   PubMed Web of Science ®Google Scholar
• de Groat WC. Spinal cord projections and neuropeptides in visceral afferent neurons. Prog Brain Res 67: 165–187, 1986.
   PubMed Web of Science ®Google Scholar
• de Groat WC, KawataniM,HisamitsuT,Cheng CL, Ma CP, Thor K, Steers WD and Roppolo JR. Mechanisms underlying the recovery of urinary bladder function following spinal cord injury. J Auton Nerv Syst 30: S71–S78, 1990.
   PubMedGoogle Scholar
• de Groat WC. Spinal interneurons and preganglionic neurons in sacral autonomic reflex pathways. In: The Emotional Motor System, Progress in Brain Research edited by Holstege G, Bandler R and Saper C, Amsterdam, Elsevier Science Publishers, 1995.
   Google Scholar
• de Groat WC, Nadelhaft I, Milne RJ, Booth AM, Morgan C and Thor K. Organization of the sacral parasympathetic reflex pathways to the urinary bladder and large intestine. J Auton Nerv Syst 3: 135–160, 1981.
   Google Scholar
• Dinis P, Charrua A, Avelino A, Yaqoob M, Bevan S, Nagy I and Cruz F. Anandamide-evoked activation of vanilloid receptor 1 contributes to the development of bladder hyperreflexia and nociceptive transmission to spinal dorsal horn neurons in cystitis. J Neurosci 24: 11253–11263, 2004.
   Google Scholar
• Dmietrieva N and McMahon SB. Sensitization of visceral afferents by nerve growth factor in the adult rat. Pain 66: 87–97, 1996.
   Google Scholar
• Dmitrieva N, Shelton D, Rice ASC, et al. The role of nerve growth factor in a model of visceral inflammation. Neuroscience 78: 449–459, 1997.
   PubMed Web of Science ®Google Scholar
• England S, Bevan S, and Docherty RJ. PGE2 modulates the tetrodotoxin-resistant sodium current in neonatal rat dorsal root ganglion neurones via the cyclic AMPprotein kinase A cascade. J Physiol 495: 429–440, 1996.
   PubMed Web of Science ®Google Scholar
• Fall M, Lindstrom S and Mazieres L. A bladder-to-bladder cooling reflex in the cat. J Physiol 427: 281–300, 1990.
   Google Scholar
• Ferguson DR, Kennedy I and Burton TJ. ATP is released from rabbit urinary bladder epithelial cells by hydrostatic pressure changes-a possible sensory mechanism? J Physiol 505.2: 503–511, 1997.
   Google Scholar
• Fjell J, Cummins TR, Dib-Hajj SD, Fried K, Black JA and Waxman SG. Differential role of GDNF and NGF in the maintenance of two TTX-resistant sodium channels in adult DRG neurons. Mol Brain Res 67: 267–282, 1999.
   PubMedGoogle Scholar
• Ghuang HH, Prescott ED, Kong H, Shields S, Jordt SE, Basbaum AI, Chao MV and Julius D. Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2-mediated inhibition. Nature 411: 957–962, 2001.
   PubMed Web of Science ®Google Scholar
• Gillenwater JY and Wein AJ. Summary of the national institute of arthritis, diabetes, and kidney diseases workshop on interstitial cystitis. J Urol 140: 203–206, 1988.
   PubMed Web of Science ®Google Scholar
• Gold MS, Dastmalchi S and Levine JD. Co-expression of nociceptor properties in dorsal root ganglion neurons from the adult rat in vitro. Neuroscience 71: 265–275, 1996b. Grases F, Ferragut LG and Bosta-Bauza A. Study of the early stages of renal stone formation: Experimental model using urothelium of pig urinary bladder. Urol Res 24: 305–311, 1966.
   Google Scholar
• Habler HJ, Janig W and Koltzenburg M. Activation of unmyelinated afferent fibres by mechanical stimuli and inflammation of the urinary bladder in the cat. J Physiol (Lond) 425: 545–562, 1990.
   Google Scholar
• Han X, Fink MP, Uchiyama T, Yang R and Delude RL. Increased iNOS activity is essential for pulmonary epithelial tight junction dysfunction in endotoxemic mice. Am J Physiol 286: L259–L267, 2004.
   Google Scholar
• Hanno PM, Fritz RW, Mulholland SG and Wein AJ. Heparin-Examination of its antibacterial adsorption properties. Urology 28: 273–276, 1981.
   Google Scholar
• Hanno PM, Landis JR, Matthews-Cook Y, et al. The Interstitial Cystitis Database Study Group: The diagnosis of interstitial cystitis revisited: Lessons learned from the National Institutes of Health Interstitial Cystitis Database study. J Urol 161: 553–557, 1999.
   PubMed Web of Science ®Google Scholar
• Hicks M. The mammalian urinary bladder: An accomodating organ. Biol Rev 50: 215–246, 1975.
   PubMed Web of Science ®Google Scholar
• Hoffman PN, Griffin JW and Price DL. Control of axonal caliber by neurofilament transport. J Cell Biol 99: 705–714, 1984.
   PubMed Web of Science ®Google Scholar
• Hoffman PN, Cleveland DW, Griffin JW, Landes PW, Cowan NJ and Price DL. Neurofilament gene expression: A major determinant of axonal caliber. Proc Natl Acad Sci USA 84: 3472–3476, 1987.
   PubMed Web of Science ®Google Scholar
• Hohenfellner M, Nunues L, Schmidt RA, et al. Interstitial cystitis: Increased sympathetic innervation and related neuropeptide synthesis. J Urol 147: 587–591, 1992.
   PubMed Web of Science ®Google Scholar
• Holm-Bentzen M, Sondergaard I and Hald T. Urinary excretion of a metabolite of histamine (1,4-methylimidazole- acetic-acid) in painful bladder disease. Br J Urol 59: 230–233, 1987.
   PubMedGoogle Scholar
• Holzer P. TRPV1 and the gut: From a tasty receptor for a painful vanilloid to a key player in hyperalgesia. Eur J Pharmacol 500: 231–241, 2004.
   PubMed Web of Science ®Google Scholar
• Homolya L, Steinberg TH and Boucher RC. Cell to cell communication in response to mechanical stress via bilateral release of ATP and UTP in polarized epithelia. J Cell Biol 150: 1349–1360, 2000.
   PubMed Web of Science ®Google Scholar
• Hu P, Meyers S, Liang FX, Deng FM, Kachar B, Zeidel ML and Sun TT. Role of membrane proteins in permeability barrier function: Uroplakin ablation elevates urothelial permeability. Am J Physiol 283: F1200–F1207, 2002.
   PubMed Web of Science ®Google Scholar
• Hu VY, Zvara P, Dattilio A, Redman TL, Allen SJ, Dawbarn D, Stroemer RP and Vizzard MA. Decrease in bladder overactivity with REN1820 in rats with cyclophosphamide induced cystitis. J Urol 173: 1016–1021, 2005.
   PubMed Web of Science ®Google Scholar
• Hulsebosch CE and Coggeshall RE. An analysis of the axon populations in the nerves to the viscera in the rat. J Comp Neurol 211: 1–10, 1982.
   PubMed Web of Science ®Google Scholar
• Hurst RE. Structure, function and pathology of proteoglycans and glycosaminoglycans in the urinary tract. World J Urol 12: 3–10, 1994.
   PubMed Web of Science ®Google Scholar
• Jackson RL, Busch SJ and Cardin AD. Glycosaminoglycans: molecular properties, protein interactions, and role in physiological processes. Physiol Rev 71: 481–539, 1991.
   PubMed Web of Science ®Google Scholar
• Jaggar SI, Scott HC and Rice AS. Inflammation of the rat urinary bladder is associated with a referred thermal hyperalgesia which is nerve growth factor dependent. Br J Anaesth 83: 442–448, 1999.
   PubMed Web of Science ®Google Scholar
• Jallat-Daloz I, Cognard JL, Badet JM and Regnard J. Neural-epithelial cell interplay: in vitro evidence that vagal mediators increase PGE2 production by human nasal epithelial cells. Allergy Asthma Proc 22: 17–23, 2001.
   PubMed Web of Science ®Google Scholar
• Janig W and Morrison JFB. Functional properties of spinal visceral afferents supplying abdominal and pelvic organs, with special emphasis on visceral nociception. Prog Brain Res 67: 87–114, 1986.
   PubMed Web of Science ®Google Scholar
• Ji RR and Woolf CJ. Neuronal plasticity and signal transduction in nociceptive neurons: implications for the initiation and maintenance of pathological pain. Neurobiol Dis 8: 1–10, 2001.
   PubMed Web of Science ®Google Scholar
• Johansson SL, Ogawa K, and Fall M. The pathology of interstitial cystitis, In: Interstitial Cystitis, edited by Sant GR, Philadelphia, Lippincott-Raven: 143-151, 1997.
   Google Scholar
• Keast JR and de Groat WC. Segmental distribution and peptide content of primary afferent neurons innervating the urogenital organs and colon of male rats. J Comp Neurol 319: 615–623, 1992.
   PubMed Web of Science ®Google Scholar
• Keay S, Warren JW, Zhang CO, Tu LM, Gordon DA and Whitmore KE. Antiproliferative activity is present in bladder but not renal pelvic urine from interstitial cystitis patients. J Urol 162: 1487–1489, 1999.
   PubMed Web of Science ®Google Scholar
• Keay SK, Szekely Z, Conrads TP, Veenstra TD, Barchi JJ, Zhang CO, Koch KR and Michejda CJ. An antiproliferative factor from interstitial cystitis patients is a frizzled 8 protein-related sialoglycopeptide. Proc Natl Acad Sci USA 101: 11803–11808, 2004.
   PubMed Web of Science ®Google Scholar
• Kim JH, Rivas DA, Shenot PJ, Green B, Kennelly M, Erickson JR, O’Leary M, Yoshimura N and Chancellor MB. Intravesical resiniferatoxin for refractory detrusor hyperreflexia: a multicenter, blinded, randomized, placebo-controlled trial. J Spinal Cord Med 26: 358–363, 2003.
   PubMed Web of Science ®Google Scholar
• Lamb K, Gebhart GF and Bielefeldt K. Increased nerve growth factor expression triggers bladder overactivity. J Pain 5: 150–156, 2004.
   PubMed Web of Science ®Google Scholar
• Lantéri-Minet M, Bon K, de Pommery J, et al. Cyclophosphamide cystitis as a model of visceral pain in rats: model elaboration and spinal structures involved as revealed by the expression of c-Fos and Krox-24 proteins. Exp Brain Res 105: 220–232, 1995.
   PubMed Web of Science ®Google Scholar
• Lavelle J, Meyers SA, Ruiz WG, Buffington CA, Zeidel ML and Apodaca G. Urothelial pathophysiological changes in feline interstitial cystitis: A human model. Am J Physiol 278: F540–F553, 2000.
   PubMed Web of Science ®Google Scholar
• Lawson SN, Perry MJ, Prabhakar E and McCarthy PW. Primary sensory neurones: Neurofilament, neuropeptides, and conduction velocity. Brain Res Bull 30: 239–243, 1993.
   PubMed Web of Science ®Google Scholar
• Lazzeri M, Beneforti P, Benaim G, Maggi CA, Lecci A and Turini D. Intravesical capsaicin for treatment of severe bladder pain: A randomized placebo controlled study. J Urol 156: 947–952, 1996.
   PubMed Web of Science ®Google Scholar
• Lazzeri M, Beneforti P, Spinelli M, Zanollo A, Barbagli G and Turini D. Intravesical resiniferatoxin for the treatment of hypersensitive disorder: A randomized placebo controlled study. J Urol 164: 676–679, 2000.
   PubMed Web of Science ®Google Scholar
• Lecci A and Maggi CA. Tachykinins as modulators of the micturition reflex in the central and peripheral nervous system. Regul Pept 101: 1–118, 2001 Lee HY, Bardini M and Burnstock G. Distribution of P2X receptors in the urinary bladder and the ureter of the rat. J Urol 163: 2002–2007, 2000.
   PubMed Web of Science ®Google Scholar
• Lewis SA, Berg JR and Kleine TJ. Modulation of epithelial permeability by extracellular macromolecules. Physiological reviews 75: 561–589, 1995.
   PubMed Web of Science ®Google Scholar
• Lewis SA, Clausen C and Wills NK. Transport-related modulation of the membrane properties of urinary bladder epithelium. Biochim Biophys Acta 1070: 99–110, 1991.
   PubMedGoogle Scholar
• Lewis SA and Hanrahan JW. Apical and basolateral membrane ionic channels in rabbit urinary bladder epithelium. Pflugers Arch 405: S83–S88, 1985.
   PubMed Web of Science ®Google Scholar
• Liedtke W, Choe Y, Marti-Renom MA, Bell AM, Denis CS and Sali A. Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103: 525–535, 2000.
   PubMed Web of Science ®Google Scholar
• Lilly JD and Parsons CL. Bladder surface glycosaminoglycans is a human epithelial permeability factor. Surg Gynecol Obstet 171: 493–496, 1990.
   PubMedGoogle Scholar
• Lowe EM, Anand P, Terenghi G, Williams-Chestnut RE, Sinicropi DV and Osborne JL. Increased nerve growth factor levels in the urinary bladder of women with idiopathic sensory urgency and interstitial cystitis. Br J Urol 79: 572–577, 1997.
   PubMedGoogle Scholar
• Lundberg JM. Pharmacology of cotransmission in the autonomic nervous system: Integrative aspects on amines neuropeptides, adenosine triphosphate, amine acids and nitric oxide. Pharmacol Rev 48: 113–178, 1996.
   PubMed Web of Science ®Google Scholar
• Maggi CA and Conte B. Effect of urethane anesthesia on the micturition reflex in capsaicin -treated rats. J Auton Nerv Syst 30: 247–251, 1990.
   PubMedGoogle Scholar
• Maggi CA. The dual, sensory and efferent function of the capsaicin-sensitive primary sensory nerves in the bladder and urethra. In: The Autonomic Nervous System, Vol. 3, Nervous Control of the Urogenital System, edited by Maggi CA, London, Harwood Academic Publishers: 383–422, 1993.
   Google Scholar
• Malley SE and Vizzard MA. Changes in urinary bladder cytokine mRNA and protein after cyclophosphamideinduced cystitis. Physiol Genomics 9: 5–13, 2002.
   PubMed Web of Science ®Google Scholar
• Mallory B, Steers WD and de Groat WC. Electrophysiological study of micturition reflexes in rats. Am J Physiol 257: R410–R421, 1989.
   Google Scholar
• Moldwin RM and Sant GR. Interstitial cystitis: A pathophysiology and treatment update. Clin Obstet Gynecol 45: 259–272, 2002.
   PubMed Web of Science ®Google Scholar
• Morgan C, Nadelhaft I and de Groat WC. The distribution of visceral primary afferents from the pelvic nerve to Lissauer’s tract and the spinal gray matter and its relationship to the sacral parasympathetic nucleus. J Comp Neurol 201: 415–440, 1981.
   Google Scholar
• Murray E, Malley SE, Qiao LY, Hu VY and Vizzard MA. Cyclophosphamide induced cystitis alters neurotrophin and receptor tyrosine kinase expression in pelvic ganglia and bladder. J Urol 172: 2434–2439, 2004.
   Google Scholar
• Nickel JC, Downey J, Morales, A, Emerson L and Clark J. Relative efficacy of various exogenous glycosaminoglycans in providing a bladder surface permeability barrier. J Urol 160: 612–614, 1998.
   Google Scholar
• Nickel JC. Interstitial cystitis-an elusive clinical target? J Urol 170: 816–817, 2003.
   PubMed Web of Science ®Google Scholar
• Nicol GD, Vasko MR, and Evans AR. Prostaglandins suppress an outward potassium current in embryonic rat sensory neurons. J Neurophysiol 77: 167–176, 1997.
   PubMed Web of Science ®Google Scholar
• Niku SD, Stein PC, Scherz HC and Parsons CL. A new method for cytodestrution of bladder epithelium using protamine sulfate and urea. J Urology152: 1025–1028, 1994.
   Google Scholar
• NIH Publication No.02-3220; National Kidney and Urologic Diseases Information Clearinghouse. Interstitial Cystitis. Bethesda, MD, National Institute of Diabetes and Digestive and Kidney Diseases (National Institutes of Health), 2002.
   Google Scholar
• Nilsson G, Forsberg-Nilsson, Xiang Z, et al. Human mast cells express functional TrkA and are a source of nerve growth factor. Eur J Immunol 27: 2295–2930, 1997.
   PubMed Web of Science ®Google Scholar
• Nishiguchi J, Hayashi Y, Chancellor MB, de Miguel F. de Groat WC, Kumon H and Yoshimura N. Detrusor overactivity induced by intravesical application of adenosine 5’-triphosphate (ATP) under different delivery conditions in rats. Urology 66: 1332–1337, 2005.
   Google Scholar
• Okragly AJ, Niles AL, Saban R, Schmidt D, Hoffman RL, Warner TF, Moon TD, Uehling DT and Haak- Frendscho M. Elevated tryptase, nerve growth factor, neurotrophin-3 and glial cell line-derived neurotrophic factor levels in the urine of interstitial cystitis and bladder cancer patients. J Urol 161: 438–441, 1999.
   PubMed Web of Science ®Google Scholar
• Otsuka M and Yoshioka K. Neurotransmitter functions of mammalian tachykinins. Physiol Rev 73: 229–308, 1993.
   PubMed Web of Science ®Google Scholar
• Pang X, Marchand J, Sant GR, et al. Increased number of substance P positive fibers in interstitial cystitis. Br J Urol 75: 744–750, 1995.
   PubMedGoogle Scholar
• Parsons CL, Benson G, Childs SJ, et al: A quantitatively controlled method to study prospectively interstitial cystitis and demonstrate the efficacy of pentosanpolysulfate. J Urol 150: 845–848, 1993.
   PubMed Web of Science ®Google Scholar
• Parsons CL, Greenberger M, Gabal L, Bidair M and Barme G. The role of urinary potassium in the pathogenesis and diagnosis of interstitial cystitis. J Urol 159: 1862–1867, 1998.
   Google Scholar
• Payne CK, Mosbaugh PG, Forrest JB, Evans RJ, Whitmore KE, Antoci JP, Perez-Marrero R, Jacoby K, Diokno AC, O’Reilly KJ, Griebling TL, Vasavada SP, Yu AS and Frumkin LR; ICOS RTX Study Group (Resiniferatoxin Treatment for Interstitial Cystitis). Intravesical resiniferatoxin for the treatment of interstitial cystitis: A randomized, double-blind, placebo controlled trial. J Urol 173: 1590–1594, 2005.
   PubMed Web of Science ®Google Scholar
• Qiao LY and Vizzard MA. Up-regulation of phosphorylated CREB but not c-Jun in bladder afferent neurons in dorsal root ganglia after cystitis. J Comp Neurol 469: 262–274, 2004.
   PubMed Web of Science ®Google Scholar
• Qiao LY and Vizzard MA. Cystitis-induced upregulation of tyrosine kinase (TrkA, TrkB) receptor expression and phosphorylation in rat micturition pathways. J Comp Neurol 454: 200–211, 2002.
   PubMed Web of Science ®Google Scholar
• Rong W, Spyer KM and Burnstock G. Activation and sensitisation of low and high threshold afferent fibres mediated by P2X receptors in the mouse urinary bladder. J Physiol 541: 591–600, 2002.
   PubMed Web of Science ®Google Scholar
• Roppolo JR, Tai C,Booth AM, Buffington CA, de Groat WC and Birder LA. Bladder Adelta afferent nerve activity in normal cats and cats with feline interstitial cystitis. J Urol 173: 1011–1015, 2005.
   Google Scholar
• Sant GR, and Theoharides TC. Interstitial cystitis. Curr Opin Urol 9: 297–302, 1999.
   PubMedGoogle Scholar
• Sculptoreanu A and de Groat WC. Protein kinase C is involved in neurokinin receptor modulation of Nand L-type Ca2+ channels in DRG neurons of the adult rat. J Neurophysiol 90: 21–31, 2003.
   PubMed Web of Science ®Google Scholar
• Sculptoreanu A, de Groat WC, Buffington CA and Birder LA. Abnormal excitability in capsaicin-responsive DRG neurons from cats with feline interstitial cystitis. Exp Neurol 193: 437–443, 2005a. Sculptoreanu A, de Groat WC, Buffington CA and Birder LA. Protein kinase C contributes to abnormal capsaicin responses in DRG neurons from cats with feline interstitial cystitis. Neurosci Lett 381: 42–46, 2005b. Seki S, Sasaki K, Igawa Y, Nishizawa O, Chancellor MB, de Groat WC and Yoshimura N. Detrusor overactivity induced by increased levels of nerve growth factor in bladder afferent pathways in rats. Neurourology and Urodynamics 22: 375–377, 2003.
   Web of Science ®Google Scholar
• Sengupta JN, and Gebhart GF. Mechanosensitive properties of pelvic nerve afferent fibers innervating the urinary bladder of the rat. J Neurophysiol 72: 2420–2430, 1994.
   PubMed Web of Science ®Google Scholar
• Smith PR, Mackler SA, Weiser PC, Brooker DR, Ahn YJ, Harte BJ, McNulty KA and Kleyman TR. Expression and localization of epithelial sodium channel in mammalian urinary bladder. Am J Physiol 274: F91–F96, 1998.
   Google Scholar
• Steers WD, Kolbeck S, Creedon D and Tuttle JB. Nerve growth factor in the urinary bladder of the adult regulates neuronal form and function. J Clin Invest 88: 1709–1715, 1991.
   Google Scholar
• Steers WD, Mackway AM, Ciambotti J and de Groat WC. Alterations in neural pathways to the urinary bladder of the rat in response to streptozotocin-induced diabetes. J Auton Nerv Syst 47: 83–94, 1994.
   Google Scholar
• Steers WD, Creedon DJ and Tuttle JB. Immunity to nerve growth factor prevents afferent plasticity following urinary bladder hypertrophy. J Urol 155: 379–385, 1996.
   PubMed Web of Science ®Google Scholar
• Steers WD and Tuttle JB. Neurogenic inflammation and nerve growth factor: possible roles in interstitial cystitis. In: Interstitial cystitis, edited by Sant GR, Philadelphia, Lippincott-Raven: 67–75, 1997.
   Google Scholar
• Stein RJ, Santos S, Nagatomi J, Hayashi Y, Minnery BS, Xavier M, Patel AS, Nelson JB, Futrell WJ, Yoshimura N, Chancellor MB and deMiguel F. Cool (TRPM8) and hot (TRPV1) receptors in the bladder and male genital tract.JUrol 172: 1175–1178, 2004.
   Google Scholar
• Stewart T, Beyak MJ and Vanner S. Ileitis modulates potassium and sodium currents in guinea pig dorsal root ganglia sensory neurons. J Physiol (London) 552: 797–807, 2003.
   Google Scholar
• Studeny S, Torabi A and Vizzard MA. P2X2 and P2X3 Receptor Expression in Postnatal and Adult Rat Urinary Bladder and Lumbosacral Spinal Cord. Am J Physiol Regul Integr Comp Physiol 289: R1155-R1168, 2005.
   Google Scholar
• Sun Y and Chai TC. Up-regulation of P2X3 receptor during stretch of bladder urothelial cells from patients with interstitial cystitis. J Urol 171: 448–452, 2004.
   PubMed Web of Science ®Google Scholar
• Sun Y, Keay S, DeDeyne PG and Chai TC. Augmented stretch activated adenosine triphosphate release from bladder uroepithelial cells in patients with interstitial cystitis. J Urol 166: 1951–1956, 2001.
   Google Scholar
• Szallasi A. Vanilloid receptor ligands: hopes and realities for the future. Drugs Aging 18: 561–573, 2001.
   PubMed Web of Science ®Google Scholar
• Szallasi A and Fowler CJ. After a decade of intravesical vanilloid therapy: still more questions than answers. Lancet Neurol 1: 167–172, 2002.
   PubMed Web of Science ®Google Scholar
• Tempest HV, Dixon AK, Turner WH, Elneil S, Sellers LA and Ferguson DR. P2X and P2Y receptor expression in human bladder urothelium and changes in interstitial cystitis. BJU Int 93: 1344–1388, 2004.
   PubMed Web of Science ®Google Scholar
• Theoharides TC and Sant GR. New agents for the medical treatment of interstitial cystitis. Exp Opin Invest Drugs 10: 521–546, 2001.
   PubMed Web of Science ®Google Scholar
• Theoharides TC, Kempuraj D and Sant GR: Mast cell involvement in interstitial cystitis: a review of human and experimental evidence. Urology 57(Suppl 6A): 47–55, 2001.
   Google Scholar
• Thor KB, Hisamitsu T, Roppolo JR, Tuttle P, Nagel J and de Groat WC. Selective inhibitory effects of ethylketocyclazocine on reflex pathways to the external urethral sphincter of the cat. J Pharmacol Exp Ther 248: 1018–1025, 1989.
   Google Scholar
• Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H,Skinner K, Raumann BE, BasbaumAI and Julius D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21: 531–543, 1998.
   Google Scholar
• Tominaga M, Wada M and Masu M. Potentiation of capsaicin receptor activation by metabotropic ATP receptors: A possible mechanism for ATP-evoked pain and hypersensitivity. Proc Natl Acad Sci USA 29: 820–825, 2001.
   Google Scholar
• Truschel ST, Ruiz WG, Kanai AJ, Kiss S, Meyers S, Apodaca G, de Groat WC, Maggi CA, Zeidel ML and Birder L. Involvement of nitric oxide (NO) in bladder afferent and urothelial abnormalities following chronic spinal cord injury. Soc Neurosci Abstr 24: 842.9, 2001.
   Google Scholar
• Tsavaler L, Shapero MH, Morkowski S and Laus R. Trp-p8, a novel prostate-specific gene, is up-regulated in prostate cancer and other malignancies and shares high homology with transient receptor potential calcium channel proteins. Cancer Res 61: 3760–3769, 2001.
   Google Scholar
• Tzan CJ, Berg JR and Lewis SA. Effect of protamine sulfate on thepermeability properties of the mammalian urinary bladder.Jmembrane Biology 133: 227–242, 1993.
   Google Scholar
• Tzan CJ, Berg JR and Lewis SA. Mammalian urinary bladder permeability is altered by cationic proteins: modulation by divalent cations. Am J Physiol (Cell Physiol) 267: C1013–C1026, 1994.
   Web of Science ®Google Scholar
• Vera PL and Nadelhaft I. Conduction velocity distribution of afferent fibers innervating the rat urinary bladder. Brain Res 520: 83–89, 1990.
   PubMed Web of Science ®Google Scholar
• Vizzard MA, Erdman SL and de Groat WC. Increased expression of neuronal nitric oxide synthase in bladder afferent pathways following chronic bladder irritation. J Comp Neurol 370: 191–202, 1996.
   PubMed Web of Science ®Google Scholar
• Vizzard MA and Boyle MM. Increased expression of growth-associated protein (GAP-43) in lower urinary tract pathways following cyclophosphamide (CYP)- induced cystitis. Brain Res 844: 174–187, 1999.
   PubMed Web of Science ®Google Scholar
• Vizzard MA. Up-regulation of pituitary adenylate cyclase- activating polypeptide in urinary bladder pathways after chronic cystitis. J Comp Neurol 420: 335–348, 2000a. Vizzard MA. Alterations in spinal cord Fos protein expression induced by bladder stimulation following cystitis. Am J Physiol Regul Integr Comp Physiol 278: R1027-R1039, 2000b. Vizzard MA. Alterations in neuropeptide expression in lumbosacral bladder pathways following chronic cystitis. J Chem Neuroanat 21: 125–138, 2001.
   Web of Science ®Google Scholar
• Wang E, Lee JM, Johnson JP, Kleyman T, Bridges R and Apodaca G. Hydrostatic pressure-regulated ion transport in bladder uoepithelium. Am J Physiol 285: F651–F663, 2003.
   Google Scholar
• Wang EC, Lee JM, Ruiz WG, Balestreire EM, von Bodungen M, Barrick S, Cockayne DA, Birder LA and Apodaca GA. ATP and purinergic receptor-dependent membrane traffic in bladder umbrella cells. J Clin Investigation 115: 2412–2422, 2005.
   PubMed Web of Science ®Google Scholar
• Warren JW. Interstitial cystitis as an infectious disease. Urol Clin North Am 21: 31–39, 1994.
   PubMed Web of Science ®Google Scholar
• Wen J and Morrison JF. The effects of high urinary potassium concentration on pelvic nerve mechanoreceptors and ‗silent‘ afferents from the rat bladder. Adv Exp Med Biol 385: 237–239, 1995.
   PubMedGoogle Scholar
• Westropp J and Buffington CA. In vivo models of interstitial cystitis. J Urol 167: 694–702, 2002.
   PubMed Web of Science ®Google Scholar
• Wolf-Johnston AS, Beckel JM, Barrick SR, Kanai AJ, de Groat WC and Birder L. Induction of urinary cystitis results in increased expression of nerve growth factor and its receptors. Soc Neurosci Abstr 27: 742.16, 2004.
   Google Scholar
• Wolf-Johnston AS, Buffington CA, Roppol o JR, Tai C, Kanai AJ, de Groat WC and Birder L. Increased NGF and TRPV1 expression in urinary bladder and sensory neurons from cats with feline interstitial cystitis. Soc Neurosci Abst 27: 608.4, 2003.
   Google Scholar
• Woolf CJ and Salter MW. Neuronal plasticity: Increasing the gain in pain. Science 288: 1765–1769, 2000.
   PubMed Web of Science ®Google Scholar
• Yiangou Y, Facer P, Ford A, Brady C, Wiseman O, Fowler CJ and Anand P. Capsaicin receptor VR1 and ATP-gated ion channel P2X3 in human urinary bladder. BJU Int 87: 774–977, 2001.
   PubMed Web of Science ®Google Scholar
• Yoshimura N, White G, Weight FF and de Groat WC. Different types of Na+ and K+ currents in rat dorsal root ganglion neurons innervating the urinary bladder. J Physiol 494: 1–16, 1996.
   PubMed Web of Science ®Google Scholar
• Yoshimura N and de Groat WC. Plasticity of Na+ channels in afferent neurones innervating rat urinary bladder following spinal cord injury. J Physiol 503: 269–276, 1997.
   PubMed Web of Science ®Google Scholar
• Yoshimura N and de Groat WC. Neural control of lower urinary tract. Int J Urol 4: 101–115, 1997.
   PubMedGoogle Scholar
• Yoshimura N, Erdman SL, Snider MW and de Groat WC. Effects of spinal cord injury on neurofilament immunoreactivity and capsaicin sensitivity in rat dorsal root ganglion neurons innervating the urinary bladder. Neuroscience 83: 633–643, 1998.
   PubMed Web of Science ®Google Scholar
• Yoshimura N. Bladder afferent pathway and spinal cord injury: possible mechanisms inducing hyperreflexia of the urinary bladder. Prog Neurobiol 57: 583–606, 1999.
   PubMed Web of Science ®Google Scholar
• Yoshimura N and de Groat WC. Increased excitability of afferent neurons innervating rat urinary bladder following chronic bladder inflammation. J Neurosci 19: 4644–4653, 1999.
   Google Scholar
• Yoshimura N, Seki S, Chancellor MB, de Groat WC and Ueda T. Targeting afferent hyperexcitability for therapy of the painful bladder syndrome. Urology 59 (5 Suppl 1): 61–67, 2002.
   Google Scholar
• Yoshimura N, Seki S, Erickson KA, Erickson VL, Chancellor MB and de Groat WC. Histological and electrical properties of rat dorsal root ganglion neurons innervating the lower urinary tract. J Neurosci 23: 4355–4361, 2003.
   PubMed Web of Science ®Google Scholar
• Zhong Y, Banning AS, Cockayne DA, Ford AP, Burnstock G and McMahon SB. Bladder and cutaneous sensory neurons of the rat express different functional P2X receptors. Neuroscience 120: 667–675, 2003.
   PubMed Web of Science ®Google Scholar