Antagonism of the transient receptor potential ankyrin 1 (TRPA1) attenuates hyperalgesia and urinary bladder overactivity in cyclophosphamide-induced haemorrhagic cystitis

Chemico-Biological Interactions

Volumn 203, Issue 2, 2013, Pages 440-447

  Meotti, Flavia C ^a,b   Forner, Stefânia ^a   Lima Garcia, Juliana F ^a   Viana, Alice F ^a   Calixto, João B ^a  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Acrolein; Bladder overactivity; Cyclophosphamide; TRPA1; Urotoxicity

Indexed keywords

N (4 ISOPROPYLPHENYL) 2 (1,2,3,6 TETRAHYDRO 1,3 DIMETHYL 2,6 DIOXO 7H PURIN 7 YL)ACETAMIDE; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYSTOMETRY; DRUG TARGETING; FEMALE; HEMORRHAGIC CYSTITIS; HYPERALGESIA; LOCOMOTION; NONHUMAN; OVERACTIVE BLADDER; PAIN THRESHOLD; PROTEIN FUNCTION; RAT; URODYNAMICS;

ACETANILIDES; ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; CYCLOPHOSPHAMIDE; CYSTITIS; FEMALE; HEMORRHAGE; HYPERALGESIA; PURINES; RATS; TRPC CATION CHANNELS; URINARY BLADDER, OVERACTIVE; URODYNAMICS;

RATTUS;

EID: 84875968496     PISSN: 00092797     EISSN: 18727786     Source Type: Journal    
DOI: 10.1016/j.cbi.2013.03.008     Document Type: Article

References (62)

1. L.A. Levine, and J.P. Richie Urological complications of cyclophosphamide J. Urol. 141 5 1989 1063 1069
2. D. Nicol Cyclophosphamide and the urinary tract Intern. Med. J. 32 5-6 2002 199 201
3. R.A. Fleming An overview of cyclophosphamide and ifosfamide pharmacology Pharmacotherapy 17 5 Pt. 2 1997 146S 154S
4. P.R. Coggins, R.G. Ravdin, and S.H. Eisman Clinical evaluation of a new alkylating agent: cytoxan (Cyclophosphamide) Cancer 13 1960 1254 1260
5. A. Korkmaz, T. Topal, and S. Oter Pathophysiological aspects of cyclophosphamide and ifosfamide induced hemorrhagic cystitis; implication of reactive oxygen and nitrogen species as well as PARP activation Cell Biol. Toxicol. 23 5 2007 303 312
6. N. Brock, J. Pohl, and J. Stekar Studies on the urotoxicity of oxazaphosphorine cytostatics and its prevention - I. Experimental studies on the urotoxicity of alkylating compounds Eur. J. Cancer 17 6 1981 595 607
7. P.J. Cox Cyclophosphamide cystitis - identification of acrolein as the causative agent Biochem. Pharmacol. 28 13 1979 2045 2049
8. D.M. Bautista, S.E. Jordt, T. Nikai, P.R. Tsuruda, A.J. Read, J. Poblete, E.N. Yamoah, A.I. Basbaum, and D. Julius TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents Cell 124 6 2006 1269 1282
9. L.J. Macpherson, A.E. Dubin, M.J. Evans, F. Marr, P.G. Schultz, B.F. Cravatt, and A. Patapoutian Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines Nature 445 7127 2007 541 545
10. G.M. Story, A.M. Peier, A.J. Reeve, S.R. Eid, J. Mosbacher, T.R. Hricik, T.J. Earley, A.C. Hergarden, D.A. Andersson, S.W. Hwang, P. McIntyre, T. Jegla, S. Bevan, and A. Patapoutian ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures Cell 112 6 2003 819 829
11. E.L. Andrade, F.C. Meotti, and J.B. Calixto TRPA1 antagonists as potential analgesic drugs Pharmacol. Ther. 133 2 2012 189 204
12. P.G. Baraldi, D. Preti, S. Materazzi, and P. Geppetti Transient receptor potential ankyrin 1 (TRPA1) channel as emerging target for novel analgesics and anti-inflammatory agents J. Med. Chem. 53 14 2010 5085 5107
13. K. Nagata, A. Duggan, G. Kumar, and J. Garcia-Anoveros Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing J. Neurosci. 25 16 2005 4052 4061
14. K. Obata, H. Katsura, T. Mizushima, H. Yamanaka, K. Kobayashi, Y. Dai, T. Fukuoka, A. Tokunaga, M. Tominaga, and K. Noguchi TRPA1 induced in sensory neurons contributes to cold hyperalgesia after inflammation and nerve injury J. Clin. Invest. 115 9 2005 2393 2401
15. T. Streng, H.E. Axelsson, P. Hedlund, D.A. Andersson, S.E. Jordt, S. Bevan, K.E. Andersson, E.D. Hogestatt, and P.M. Zygmunt Distribution and function of the hydrogen sulfide-sensitive TRPA1 ion channel in rat urinary bladder Eur. Urol. 53 2 2008 391 399
16. C. Gratzke, T. Streng, E. Waldkirch, K. Sigl, C. Stief, K.E. Andersson, and P. Hedlund Transient receptor potential A1 (TRPA1) activity in the human urethra-evidence for a functional role for TRPA1 in the outflow region Eur. Urol. 55 3 2009 696 704
17. E.L. Andrade, S. Forner, A.F. Bento, D.F. Leite, M.A. Dias, P.C. Leal, J. Koepp, and J.B. Calixto TRPA1 receptor modulation attenuates bladder overactivity induced by spinal cord injury Am. J. Physiol. Renal Physiol. 300 5 2011 F1223 F1234
18. S. Du, I. Araki, H. Kobayashi, H. Zakoji, N. Sawada, and M. Takeda Differential expression profile of cold (TRPA1) and cool (TRPM8) receptors in human urogenital organs Urology 72 2 2008 450 455
19. E.L. Andrade, J. Ferreira, E. Andre, and J.B. Calixto Contractile mechanisms coupled to TRPA1 receptor activation in rat urinary bladder Biochem. Pharmacol. 72 1 2006 104 114
20. S. Du, I. Araki, M. Yoshiyama, T. Nomura, and M. Takeda Transient receptor potential channel A1 involved in sensory transduction of rat urinary bladder through C-fiber pathway Urology 70 4 2007 826 831
21. B.P. Cheppudira, B.M. Girard, S.E. Malley, A. Dattilio, K.C. Schutz, V. May, and M.A. Vizzard Involvement of JAK-STAT signaling/function after cyclophosphamide-induced bladder inflammation in female rats Am. J. Physiol. Renal Physiol. 297 4 2009 F1038 F1044
22. M. Boucher, M. Meen, J.P. Codron, F. Coudore, J.L. Kemeny, and A. Eschalier Cyclophosphamide-induced cystitis in freely-moving conscious rats: behavioral approach to a new model of visceral pain J. Urol. 164 1 2000 203 208
23. G.G. Vivancos, W.A. Verri Jr., T.M. Cunha, I.R. Schivo, C.A. Parada, F.Q. Cunha, and S.H. Ferreira An electronic pressure-meter nociception paw test for rats Braz. J. Med. Biol. Res. 37 3 2004 391 399
24. K. Bon, C.A. Lichtensteiger, S.G. Wilson, and J.S. Mogil Characterization of cyclophosphamide cystitis, a model of visceral and referred pain, in the mouse: species and strain differences J. Urol. 170 3 2003 1008 1012
25. L. Klionsky, R. Tamir, B. Gao, W. Wang, D.C. Immke, N. Nishimura, and N.R. Gavva Species-specific pharmacology of Trichloro(sulfanyl)ethyl benzamides as transient receptor potential ankyrin 1 (TRPA1) antagonists Mol. Pain 3 2007 39 48
26. C. Talar-Williams, Y.M. Hijazi, M.M. Walther, W.M. Linehan, C.W. Hallahan, I. Lubensky, G.S. Kerr, G.S. Hoffman, A.S. Fauci, and M.C. Sneller Cyclophosphamide-induced cystitis and bladder cancer in patients with Wegener granulomatosis Ann. Intern. Med. 124 5 1996 477 484
27. T.M. Wong, W. Yeo, L.W. Chan, and T.S. Mok Hemorrhagic pyelitis, ureteritis, and cystitis secondary to cyclophosphamide: case report and review of the literature Gynecol. Oncol. 76 2 2000 223 225
28. M. Boudes, P. Uvin, S. Kerselaers, R. Vennekens, T. Voets, and D. De Ridder Functional characterization of a chronic cyclophosphamide-induced overactive bladder model in mice Neurourol. Urodyn. 30 8 2011 1659 1665
29. L. Arms, and M.A. Vizzard Role for pAKT in rat urinary bladder with cyclophosphamide (CYP)-induced cystitis Am. J. Physiol. Renal Physiol. 301 2 2011 F252 F262
30. P. Geppetti, R. Nassini, S. Materazzi, and S. Benemei The concept of neurogenic inflammation BJU Int. 101 Suppl. 3 2008 2 6
31. V. Stearns, B. Schneider, N.L. Henry, D.F. Hayes, and D.A. Flockhart Breast cancer treatment and ovarian failure: risk factors and emerging genetic determinants Nat. Rev. Cancer 6 11 2006 886 893
32. C.K. Batista, G.A. Brito, M.L. Souza, B.T. Leitao, F.Q. Cunha, and R.A. Ribeiro A model of hemorrhagic cystitis induced with acrolein in mice Braz. J. Med. Biol. Res. 39 11 2006 1475 1481
33. S. Takamoto, N. Sakura, A. Namera, and M. Yashiki Monitoring of urinary acrolein concentration in patients receiving cyclophosphamide and ifosphamide J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 806 1 2004 59 63
34. J.P. Kehrer, and S.S. Biswal The molecular effects of acrolein Toxicol. Sci. 57 1 2000 6 15
35. S.D. Guerios, Z.Y. Wang, K. Boldon, W. Bushman, and D.E. Bjorling Blockade of NGF and trk receptors inhibits increased peripheral mechanical sensitivity accompanying cystitis in rats Am. J. Physiol. Regul. Integr. Comp. Physiol. 295 1 2008 R111 R122
36. S. Studeny, B.P. Cheppudira, S. Meyers, E.M. Balestreire, G. Apodaca, L.A. Birder, K.M. Braas, J.A. Waschek, V. May, and M.A. Vizzard Urinary bladder function and somatic sensitivity in vasoactive intestinal polypeptide (VIP)-/- mice J. Mol. Neurosci. 36 1-3 2008 175 187
37. F. Cattaruzza, I. Spreadbury, M. Miranda-Morales, E.F. Grady, S. Vanner, and N.W. Bunnett Transient receptor potential ankyrin-1 has a major role in mediating visceral pain in mice Am. J. Physiol. Gastrointest. Liver Physiol. 298 3 2010 G81 G91
38. S.M. Brierley, P.A. Hughes, A.J. Page, K.Y. Kwan, C.M. Martin, T.A. O'Donnell, N.J. Cooper, A.M. Harrington, B. Adam, T. Liebregts, G. Holtmann, D.P. Corey, G.Y. Rychkov, and L.A. Blackshaw The ion channel TRPA1 is required for normal mechanosensation and is modulated by algesic stimuli Gastroenterology 137 6 2009 2084 2095
39. K. Lamb, G.F. Gebhart, and K. Bielefeldt Increased nerve growth factor expression triggers bladder overactivity J. Pain 5 3 2004 150 156
40. P.L. Vera, and K.L. Meyer-Siegler Inflammation of the rat prostate evokes release of macrophage migration inhibitory factor in the bladder: evidence for a viscerovisceral reflex J. Urol. 172 6 Pt. 1 2004 2440 2445
41. P. Zvara, and M.A. Vizzard Exogenous overexpression of nerve growth factor in the urinary bladder produces bladder overactivity and altered micturition circuitry in the lumbosacral spinal cord BMC Physiol. 7 2007 9
42. N. Yoshimura, N.E. Bennett, Y. Hayashi, T. Ogawa, O. Nishizawa, M.B. Chancellor, W.C. de Groat, and S. Seki Bladder overactivity and hyperexcitability of bladder afferent neurons after intrathecal delivery of nerve growth factor in rats J. Neurosci. 26 42 2006 10847 10855
43. S.D. Guerios, Z.Y. Wang, and D.E. Bjorling Nerve growth factor mediates peripheral mechanical hypersensitivity that accompanies experimental cystitis in mice Neurosci. Lett. 392 3 2006 193 197
44. K. Bielefeldt, K. Lamb, and G.F. Gebhart Convergence of sensory pathways in the development of somatic and visceral hypersensitivity Am. J. Physiol. Gastrointest. Liver Physiol. 291 4 2006 G658 G665
45. B. Schnegelsberg, T.T. Sun, G. Cain, A. Bhattacharya, P.A. Nunn, A.P. Ford, M.A. Vizzard, and D.A. Cockayne 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 3 2010 R534 R547
46. M.C. Smaldone, Y. Vodovotz, V. Tyagi, D. Barclay, B.J. Philips, N. Yoshimura, M.B. Chancellor, and P. Tyagi Multiplex analysis of urinary cytokine levels in rat model of cyclophosphamide-induced cystitis Urology 73 2 2009 421 426
47. C.D. Cruz, A. Avelino, S.B. McMahon, and F. Cruz Increased spinal cord phosphorylation of extracellular signal-regulated kinases mediates micturition overactivity in rats with chronic bladder inflammation Eur. J. Neurosci. 21 3 2005 773 781
48. K.A. Corrow, and M.A. Vizzard Phosphorylation of extracellular signal-regulated kinases in urinary bladder in rats with cyclophosphamide- induced cystitis Am. J. Physiol. Regul. Integr. Comp. Physiol. 293 1 2007 R125 R134
49. M. Bandell, G.M. Story, S.W. Hwang, V. Viswanath, S.R. Eid, M.J. Petrus, T.J. Earley, and A. Patapoutian Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin Neuron 41 6 2004 849 857
50. Y. Dai, S. Wang, M. Tominaga, S. Yamamoto, T. Fukuoka, T. Higashi, K. Kobayashi, K. Obata, H. Yamanaka, and K. Noguchi Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain J. Clin. Invest. 117 7 2007 1979 1987
51. L. Cruz-Orengo, A. Dhaka, R.J. Heuermann, T.J. Young, M.C. Montana, E.J. Cavanaugh, D. Kim, and G.M. Story Cutaneous nociception evoked by 15-delta PGJ2 via activation of ion channel TRPA1 Mol. Pain 4 2008 30 38
52. S. Wang, Y. Dai, T. Fukuoka, H. Yamanaka, K. Kobayashi, K. Obata, X. Cui, M. Tominaga, and K. Noguchi Phospholipase C and protein kinase a mediate bradykinin sensitization of TRPA1: a molecular mechanism of inflammatory pain Brain 131 Pt. 5 2008 1241 1251
53. F.A. White, and N.M. Wilson Chemokines as pain mediators and modulators Curr. Opin. Anaesthesiol. 21 5 2008 580 585
54. T. Miyamoto, A.E. Dubin, M.J. Petrus, and A. Patapoutian TRPV1 and TRPA1 mediate peripheral nitric oxide-induced nociception in mice PLoS One 4 10 2009 e7596
55. T.E. Taylor-Clark, S. Ghatta, W. Bettner, and B.J. Undem Nitrooleic acid, an endogenous product of nitrative stress, activates nociceptive sensory nerves via the direct activation of TRPA1 Mol. Pharmacol. 75 4 2009 820 829
56. N. Yoshimura, and M.B. Chancellor Neurophysiology of lower urinary tract function and dysfunction Rev. Urol. 5 Suppl. 8 2003 S3 S10
57. N. Yoshimura, and W.C. de Groat Neural control of the lower urinary tract Int. J. Urol. 4 2 1997 111 125
58. B. Chopra, S.R. Barrick, S. Meyers, J.M. Beckel, M.L. Zeidel, A.P. Ford, W.C. de Groat, and L.A. Birder Expression and function of bradykinin B1 and B2 receptors in normal and inflamed rat urinary bladder urothelium J. Physiol. 562 Pt. 3 2005 859 871
59. S.P. Liu, I. Volfson, P. Horan, and R.M. Levin Effects of hypoxia, calcium, carbachol, atropine and tetrodotoxin on the filling of the in-vitro rabbit whole bladder J. Urol. 160 3 Pt. 1 1998 913 919
60. S.A. Buckner, I. Milicic, A.V. Daza, M.J. Coghlan, and M. Gopalakrishnan Spontaneous phasic activity of the pig urinary bladder smooth muscle: characteristics and sensitivity to potassium channel modulators Br. J. Pharmacol. 135 3 2002 639 648
61. W.D. Steer, and J.B. Tuttle Role of ion channels in bladder function and voiding disorders Curr. Bladder Dysfunct. Reports 4 2009 125 131
62. K.E. Andersson, C. Gratzke, and P. Hedlund The role of the transient receptor potential (TRP) superfamily of cation-selective channels in the management of the overactive bladder BJU Int. 106 8 2010 1114 1127