Cyclophosphamide-induced cystitis reduces ASIC channel but enhances TRPV1 receptor function in rat bladder sensory neurons

Journal of Neurophysiology

Volumn 110, Issue 2, 2013, Pages 408-417

  Dang, Khoa ^a   Bielefeldt, Klaus ^a   Gebhart, G F ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Acid; ASIC; Bladder sensory neurons; Capsaicin; Cyclophosphamide; Cystitis; pH; Proton; TRPV1 receptors; Visceral hypersensitivity; Whole cell patch clamp

Indexed keywords

1 (5 ISOQUINOLINYL) 3 [4 (TRIFLUOROMETHYL)BENZYL]UREA; ACID SENSING ION CHANNEL; CAPSAICIN; CYCLOPHOSPHAMIDE; MYELOPEROXIDASE; PROTON; VANILLOID RECEPTOR 1; TRPV1 PROTEIN, RAT; VANILLOID RECEPTOR;

ACIDIFICATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLADDER; BLADDER WALL; CELL SIZE; CONTROLLED STUDY; CYSTITIS; ELECTROPHYSIOLOGY; ENZYME ACTIVITY; HIGH TEMPERATURE; HYPERSENSITIVITY; INFLAMMATION; LUMBOSACRAL SPINE; MALE; NERVE CELL PLASTICITY; NONHUMAN; PATCH CLAMP; PH; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SENSORY NERVE CELL; SPINAL GANGLION; THORACOLUMBAR SPINE; ANIMAL; CHEMICALLY INDUCED; DRUG EFFECTS; INNERVATION; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ACID SENSING ION CHANNELS; ANIMALS; CYCLOPHOSPHAMIDE; CYSTITIS; MALE; RATS; RATS, SPRAGUE-DAWLEY; SENSORY RECEPTOR CELLS; TRPV CATION CHANNELS; URINARY BLADDER;

EID: 84880139912     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00945.2012     Document Type: Article

References (85)

1. Amaya F, Shimosato G, Nagano M, Ueda M, Hashimoto S, Tanaka Y, Suzuki H, Tanaka M. NGF and GDNF differentially regulate TRPV1 expression that contributes to development of inflammatory thermal hyperalgesia. Eur J Neurosci 20: 2303-2309, 2004.
2. Andrade EL, Ferreira J, André E, Calixto JB. Contractile mechanisms coupled to TRPA1 receptor activation in rat urinary bladder. Biochem Pharmacol 72: 104-114, 2006.
3. Arms L, Girard BM, Malley SE, Vizzard M. Expression and function of CCL2/CCR2 in rat micturition reflexes and somatic sensitivity with urinary bladder inflammation. Am J Physiol Renal Physiol. First published April 17, 2013; doi:10.1152/ajprenal.00139.2013.
4. Avelino A, Cruz C, Nagy I, Cruz F. Vanilloid receptor 1 expression in the rat urinary tract. Neuroscience 109: 787-798, 2002.
5. Bautista DM, Jordt SE, Nikai T, Tsuruda PR, Read AJ, Poblete J, Yamoah EN, Basbaum AI, Julius D. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124: 1269-1282, 2006.
6. +-gated channels in mouse sensory neurons. Proc Natl Acad Sci USA 99: 2338-2343, 2002.
7. Birder LA. Urinary bladder urothelium: molecular sensors of chemical/ thermal/mechanical stimuli. Vascul Pharmacol 45: 221-226, 2006.
8. Bon K, Lanteri-Minet M, Menetrey D, Berkley KJ. Sex, time-of-day and estrous variations in behavioral and bladder histological consequences of cyclophosphamide-induced cystitis in rats. Pain 73: 423-429, 1997.
9. Bon K, Lichtensteiger CA, Wilson SG, Mogil JS. Characterization of cyclophosphamide cystitis, a model of visceral and referred pain, in the mouse: species and strain differences. J Urol 170: 1008-1012, 2003.
10. Boudes M, Uvin P, Kerselaers S, Vennekens R, Voets T, De Ridder D. Functional characterization of a chronic cyclophosphamide-induced overactive bladder model in mice. Neurourol Urodyn 30: 1659-1665, 2011.
11. Brierley SM, Jones RC, Gebhart GF, Blackshaw LA. Splanchnic and pelvic mechanosensory afferents signal different qualities of colonic stimuli in mice. Gastroenterology 127: 166-178, 2004.
12. Burkman RT. Chronic pelvic pain of bladder origin: epidemiology, pathogenesis and quality of life. J Reprod Med 49: 225-229, 2004.
13. Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398: 436-441, 1999.
14. Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288: 306-313, 2000.
15. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 289: 816-824, 1997.
16. Charrua A, Reguenga C, Cordeiro JM, Correiade-Sá P, Paule C, Nagy I, Cruz F, Avelino A. Functional transient receptor potential vanilloid 1 is expressed in human urothelial cells. J Urol 182: 2944-2950, 2009.
17. Chen WH, Hsieh CL, Huang CP, Lin TJ, Tzen JT, Ho TY, Lin YW. Acid-sensing ion channel 3 mediates peripheral anti-hyperalgesia effects of acupuncture in mice inflammatory pain. J Biomed Sci 18: 82, 2011.
18. Chen X, Gebhart GF. Differential purinergic signaling in bladder sensory neurons of naïve and bladder-inflamed mice. Pain 148: 462-472, 2010.
19. Clemens JQ, Link CL, Eggers PW, Kusek JW, Nyberg LM, McKinlay JB. Prevalence of painful bladder symptoms and effect on quality of life in black, Hispanic and white men and women. J Urol 177: 1390-1394, 2007.
20. Clemens JQ, Meenan RT, O'Keeffe Rosetti MC, Brown SO, Gao SY, Calhoun EA. Prevalence of interstitial cystitis symptoms in a managed care population. J Urol 174: 576-580, 2005.
21. Cohen A, Sagron R, Somech E, Segal-Hayoun Y, Zilberberg N. Pain-associated signals, acidosis and lysophosphatidic acid, modulate the neuro-nal K(2P)2.1 channel. Mol Cell Neurosci 40: 382-389, 2009.
22. Correll CC, Phelps PT, Anthes JC, Umland S, Greenfeder S. Cloning and pharmacological characterization of mouse TRPV1. Neurosci Lett 370: 55-60, 2004.
23. Cox PJ. Cyclophosphamide cystitis-identification of acrolein as the causative agent. Biochem Pharmacol 28: 2045-2049, 1979.
24. Cruz F, Guimaraes M, Silva C, Reis M. Suppression of bladder hyperreflexia by intravesical resiniferatoxin. Lancet 350: 640-641, 1997.
25. Dang K, Bielefeldt K, Gebhart GF. Differential responses of bladder lum-bosacral and thoracolumbar dorsal root ganglion neurons to purinergic agonists, protons, and capsaicin. J Neurosci 25: 3973-3984, 2005a.
26. Dang K, Bielefeldt K, Lamb K, Gebhart GF. Gastric ulcers evoke hyper-excitability and enhance P2X receptor function in rat gastric sensory neurons. J Neurophysiol 93: 3112-3119, 2005b.
27. Dang K, Lamb K, Cohen M, Bielefeldt K, Gebhart GF. Cyclophosphamide-induced bladder inflammation sensitizes and enhances P2X receptor function in rat bladder sensory neurons. J Neurophysiol 99: 49-59, 2008.
28. De Ridder D, Chandiramani V, Dasgupta P, Van Poppel H, Baert L, Fowler CJ. Intravesical capsaicin as a treatment for refractory detrusor hyperreflexia: a dual center study with long-term followup. J Urol 158: 2087-2092, 1997.
29. Deval E, Noel J, Lay N, Alloui A, Diochot S, Friend V, Jodar M, Lazdunski M, Lingueglia E. ASIC3, a sensor of acidic and primary inflammatory pain. EMBO J 27: 3047-3055, 2010.
30. Deval E, Gasull X, Noel J, Salinas M, Baron A, Diochot S, Lingueglia E. Acid-sensing ion channels (ASICs): pharmacology and implication in pain. Pharmacol Ther 128: 549-558, 2008.
31. Dinis P, Charrua A, Avelino A, Cruz F. Intravesical resiniferatoxin decreases spinal c-fos expression and increases bladder volume to reflex micturition in rats with chronic inflamed urinary bladders. BJU Int 94: 153-157, 2004.
32. Dray A, Bettaney J, Forster P. Actions of capsaicin on peripheral nociceptors of the neonatal rat spinal cord-tail in vitro: dependence of extracellular ions and independence of second messengers. Br J Pharmacol 101: 727-733, 1990.
33. Du S, Araki I, Yoshiyama M, Nomura T, Takeda M. Transient receptor potential channel A1 involved in sensory transduction of rat urinary bladder through C-fiber pathway. Urology 70: 826-831, 2007.
34. El Kouhen R, Surowy CS, Bianchi BR, Neelands TR, McDonald HA, Niforatos W, Gomtsyan A, Lee CH, Honore P, Sullivan JP, Jarvis MF, Faltynek CR. A-425619 [1-isoquinolin-5-yl-3-(4-trifluoromethyl-benzyl)-urea], a novel and selective transient receptor potential type V1 receptor antagonist, blocks channel activation by vanilloids, heat, and acid. J Pharmacol Exp Ther 314: 400-409, 2005.
35. Friese MA, Craner MJ, Etzensperger R, Vergo S, Wemmie JA, Welsh MJ, Vincent A, Fugger L. Acid-sensing ion channel-1 contributes to axonal degeneration in autoimmune inflammation of the central nervous system. Nat Med 13: 1483-1489, 2007.
36. Gautam M, Benson CJ, Sluka KA. Increased response of muscle sensory neurons to decreases in pH after muscle inflammation. Neuroscience 170: 893-900, 2010.
37. Gunthorpe MJ, Harries MH, Prinjha RK, Davis JB, Randall A. Voltage-and time-dependent properties of the recombinant rat vanilloid receptor (rVR1). J Physiol 525: 747-759, 2000.
38. Hesselager M, Timmermann DB, Ahring PK. pH Dependency and desen-sitization kinetics of heterologously expressed combinations of acid-sensing ion channel subunits. J Biol Chem 279: 11006-11015, 2004.
39. Hiura A. Is thermal nociception only sensed by the capsaicin receptor, TRPV1? Anat Sci Int 84: 122-128, 2009.
40. Holzer P. Acid sensing by visceral afferent neurons. Acta Physiol (Oxf) 201: 63-75, 2011.
41. Jones NG, Slater R, Cadiou H, McNaughton P, McMahon SB. Acid-induced pain and its modulation in humans. J Neurosci 24: 10974-10979, 2004.
42. Kang S, Jang JH, Price MP, Gautam M, Benson CJ, Gong H, Welsh MJ, Brennan TJ. Simultaneous disruption of mouse ASIC1a, ASIC2 and ASIC3 genes enhances cutaneous mechanosensitivity. PLoS One 7: e35225, 2012.
43. Kim S, Kang C, Shin CY, Hwang SW, Yang YD, Shim WS, Park MY, Kim E, Kim M, Kim BM, Cho H, Shin Y, Oh U. TRPV1 recapitulates native capsaicin receptor in sensory neurons in association with Fas-associated factor 1. J Neurosci 26: 2403-2412, 2006.
44. Kobayashi H, Yoshiyama M, Zakoji H, Takeda M, Araki I. Sex differences in the expression profile of acid-sensing ion channels in the mouse urinary bladder: a possible involvement in irritative bladder symptoms. BJU Int 104: 1746-1751, 2009.
45. Kontani H, Hayashi K. Urinary bladder response to hypogastric nerve stimulation after bilateral resection of the pelvic nerve or spinal cord injury in rats. Int J Urol 4: 394-400, 1997.
46. Lamb K, Gebhart GF, Bielefeldt K. Increased nerve growth factor expression triggers bladder overactivity. J Pain 5: 150-156, 2004.
47. Lanteri-Minet M, Bon K, de Pommery J, Michiels JF, Menetrey D. 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.
48. Liu HT, Tyagi P, Chancellor MB, Kuo HC. Urinary nerve growth factor level is increased in patients with interstitial cystitis/bladder pain syndrome and decreased in responders to treatment. BJU Int 104: 1476-1481, 2009.
49. Macpherson LJ, Dubin AE, Evans MJ, Marr F, Schultz PG, Cravatt BF, Patapoutian A. Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines. Nature 445: 541-545, 2007.
50. Mamet J, Baron A, Lazdunski M, Voilley N. Proinflammatory mediators, stimulators of sensory neuron excitability via the expression of acid-sensing ion channels. J Neurosci 22: 10662-10670, 2002.
51. Mamet J, Lazdunski M, Voilley N. How nerve growth factor drives physiological and inflammatory expressions of acid-sensing ion channel 3 in sensory neurons. J Biol Chem 278: 48907-48913, 2003.
52. Matsuoka PK, Haddad JM, Pacetta AM, Baracat EC. Intravesical treatment of painful bladder syndrome: a systematic review and meta-analysis. Int Urogynecol J 23: 1147-1153, 2012.
53. McLatchie LM, Bevan S. The effects of pH on the interaction between capsaicin and the vanilloid receptor in rat dorsal root ganglia neurons. Br J Pharmacol 132: 899-908, 2001.
54. Meen M, Coudore-Civiale MA, Eschalier A, Boucher M. Involvement of hypogastric and pelvic nerves for conveying cystitis induced nociception in conscious rats. J Urol 166: 318-322, 2001.
55. Mitsui T, Kakizaki H, Matsuura S, Ameda K, Yoshioka M, Koyanagi T. Afferent fibers of the hypogastric nerves are involved in the facilitating effects of chemical bladder irritation in rats. J Neurophysiol 86: 2276-2284, 2001.
56. Mogil JS, Breese NM, Witty MF, Ritchie J, Rainville ML, Ase A, Abbadi N, Stucky CL, Seguela P. Transgenic expression of a dominant-negative ASIC3 subunit leads to increased sensitivity to mechanical and inflammatory stimuli. J Neurosci 25: 9893-9901, 2005.
57. Moss NG, Harrington WW, Tucker MS. Pressure, volume, and chemosen-sitivity in afferent innervation of urinary bladder in rats. Am J Physiol Regul Integr Comp Physiol 272: R695-R703, 1997.
58. Murray E, Malley SE, Qiao LY, Hu VY, Vizzard MA. Cyclophosphamide induced cystitis alters neurotrophin and receptor tyrosine kinase expression in pelvic ganglia and bladder. J Urol 172: 2434-2439, 2004.
59. Nagae M, Hiraga T, Wakabayashi H, Wang L, Iwata K, Yoneda T. Osteoclasts play a part in pain due to the inflammation adjacent to bone. Bone 39: 1107-1115, 2006.
60. Nagae M, Hiraga T, Yoneda T. Acidic microenvironment created by oste-oclasts causes bone pain associated with tumor colonization. J Bone Miner Metab 25: 99-104, 2007.
61. Ness TJ, Powell-Boone T, Cannon R, Lloyd LK, Fillingim RB. Psycho-physical evidence of hypersensitivity in subjects with interstitial cystitis. J Urol 173: 1983-1987, 2005.
62. Nicholas RS, Winter J, Wren P, Bergmann R, Woolf CJ. Peripheral inflammation increases the capsaicin sensitivity of dorsal root ganglion neurons in a nerve growth factor-dependent manner. Neuroscience 91: 1425-1433, 1999.
63. Nickel JC. Interstitial cystitis: a chronic pelvic pain syndrome. Med Clin North Am 88: 467-481, 2004.
64. Oddiah D, Anand P, McMahon SB, Rattray M. Rapid increase of NGF, BDNF and NT-3 mRNAs in inflamed bladder. Neuroreport 9: 1455-1458, 1998.
65. Rashid MH, Inoue M, Bakoshi S, Ueda H. Increased expression of vanilloid receptor 1 on myelinated primary afferent neurons contributes to the anti-hyperalgesic effect of capsaicin cream in diabetic neuropathic pain in mice. J Pharmacol Exp Ther 306: 709-717, 2003.
66. Ruparel NB, Patwardhan AM, Akopian AN, Hargreaves KM. Homologous and heterologous desensitization of capsaicin and mustard oil responses utilize different cellular pathways in nociceptors. Pain 135: 271-279, 2008.
67. Saban MR, Davis CA, Avelino A, Cruz F, Maier J, Bjorling DE, Sferra TJ, Hurst RE, Saban R. VEGF signaling mediates bladder neuroplasticity and inflammation in response to BCG. BMC Physiol 11: 16, 2011.
68. Schnegelsberg B, Sun TT, Cain G, Bhattacharya A, Nunn PA, Ford AP, Vizzard MA, Cockayne DA. Overexpression of NGF in mouse urothelium leads to neuronal hyperinnervation, pelvic sensitivity, and changes in urinary bladder function. Am J Physiol Regul Integr Comp Physiol 298: R534-R547, 2010.
69. Seo HS, Roh DH, Yoon SY, Kang SY, Moon JY, Kim HW, Han HJ, Chung JM, Beitz AJ, Lee JH. Peripheral acid-sensing ion channels and P2X receptors contribute to mechanical allodynia in a rodent thrombus-induced ischemic pain model. J Pain 11: 718-727, 2010.
70. Shimosato G, Amaya F, Ueda M, Tanaka Y, Decosterd I, Tanaka M. Peripheral inflammation induces up-regulation of TRPV2 expression in rat DRG. Pain 119: 225-232, 2005.
71. Simonetti M, Fabbro A, D'Arco M, Zweyer M, Nistri A, Giniatullin R, Fabbretti E. Comparison of P2X and TRPV1 receptors in ganglia or primary culture of trigeminal neurons and their modulation by NGF or serotonin. Mol Pain 2: 11, 2006.
72. Smith GD, Gunthorpe MJ, Kelsell RE, Hayes PD, Reilly P, Facer P, Wright JE, Jerman JC, Walhin JP, Ooi L, Egerton J, Charles KJ, Smart D, Randall AD, Anand P, Davis JB. TRPV3 is a temperature-sensitive vanilloid receptor-like protein. Nature 418: 186-190, 2002.
73. Staniland AA, McMahon SB. Mice lacking acid-sensing ion channels (ASIC) 1 or 2, but not ASIC3, show increased pain behaviour in the formalin test. Eur J Pain 13: 554-563, 2009.
74. Streng T, Axelsson HE, Hedlund P, Andersson DA, Jordte SE, Bevan S, Andersson KE, Högestätt ED, Zygmunt PM. Distribution and function of the hydrogen sulfide-sensitive TRPA1 ion channel in rat urinary bladder. Eur Urol 53: 391-400, 2008.
75. Tamura S, Morikawa Y, Senba E. TRPV2, a capsaicin receptor homologue, is expressed predominantly in the neurotrophin-3-dependent subpopulation of primary sensory neurons. Neuroscience 130: 223-228, 2005.
76. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, Raumann BE, Basbaum AI, Julius D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21: 531-543, 1998.
77. Voilley N, de Weille J, Mamet J, Lazdunski M. Nonsteroid anti-inflammatory drugs inhibit both the activity and the inflammation-induced expression of acid-sensing ion channels in nociceptors. J Neurosci 21: 8026-8033, 2001.
78. Walder RY, Rasmussen LA, Rainier JD, Light AR, Wemmie JA, Sluka KA. ASIC1 and ASIC3 play different roles in the development of hyperal-gesia after inflammatory muscle injury. J Pain 11: 210-218, 2010.
79. Xu L, Gebhart GF. Characterization of mouse lumbar splanchnic and pelvic nerve urinary bladder mechanosensory afferents. J Neurophysiol 99: 244-253, 2008.
80. Xue Q, Jong B, Chen T, Schumacher MA. Transcription of rat TRPV1 utilizes a dual promoter system that is positively regulated by nerve growth factor. J Neurochem 101: 212-222, 2007.
81. Yen YT, Tu PH, Chen CJ, Lin YW, Hsieh ST, Chen CC. Role of acid-sensing ion channel 3 in sub-acute-phase inflammation. Mol Pain 5: 1, 2009.
82. Yoshimura N, Bennett NE, Hayashi Y, Ogawa T, Nishizawa O, Chancellor MB, de Groat WC, Seki S. Bladder overactivity and hyperexcitability of bladder afferent neurons after intrathecal delivery of nerve growth factor in rats. J Neurosci 26: 10847-10855, 2006.
83. Yoshimura N, de Groat WC. Increased excitability of afferent neurons innervating rat urinary bladder after chronic bladder inflammation. J Neu-rosci 19: 4644-4653, 1999.
84. Zhang X, Huang J, McNaughton PA. NGF rapidly increases membrane expression of TRPV1 heat-gated ion channels. EMBO J 24: 4211-4223, 2005.
85. Zhu Y, Colak T, Shenoy M, Liu L, Pai R, Li C, Mehta K, Pasricha PJ. Nerve growth factor modulates TRPV1 expression and function and mediates pain in chronic pancreatitis. Gastroenterology 141: 370-377, 2011.