TRPA1 mediates bladder hyperalgesia in a mouse model of cystitis

Pain

Volumn 155, Issue 7, 2014, Pages 1280-1287

  Deberry, Jennifer J ^a,b   Schwartz, Erica S ^a   Davis, Brian M ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Bladder; Calcium imaging; Cystitis; Hyperlagesia; TRPA1; TRPV1; Visceromotor reflex

Indexed keywords

ANKYRIN; CAPSAICIN; CYCLOPHOSPHAMIDE; MESSENGER RNA; 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; VANILLOID RECEPTOR 1; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRPA1 PROTEIN, MOUSE; TRPV1 PROTEIN, MOUSE; VANILLOID RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLADDER; CONTROLLED STUDY; CYSTITIS; DEPOLARIZATION; EDEMA; FEMALE; HYPERALGESIA; INFLAMMATION; MAST CELL; MOUSE; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SPINAL GANGLION; ANIMAL; CHEMICALLY INDUCED; DISEASE MODEL; INTERSTITIAL CYSTITIS; METABOLISM;

ANIMALS; CYCLOPHOSPHAMIDE; CYSTITIS, INTERSTITIAL; DISEASE MODELS, ANIMAL; HYPERALGESIA; MICE; TRANSIENT RECEPTOR POTENTIAL CHANNELS; TRPV CATION CHANNELS; URINARY BLADDER;

EID: 84902343834     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2014.03.023     Document Type: Article

References (59)

1. Y.A. Alpizar, M. Gees, A. Sanchez, A. Apetrei, T. Voets, B. Nilius, and K. Talavera Bimodal effects of cinnamaldehyde and camphor on mouse TRPA1 Pflugers Arch 465 2013 853 864
2. D.A. Andersson, C. Gentry, L. Alenmyr, D. Killander, S.E. Lewis, A. Andersson, B. Bucher, J.L. Galzi, O. Sterner, S. Bevan, E.D. Hogestatt, and P.M. Zygmunt TRPA1 mediates spinal antinociception induced by acetaminophen and the cannabinoid Delta(9)-tetrahydrocannabiorcol Nat Commun 2 2011 551
3. A. Avelino, and F. Cruz TRPV1 (vanilloid receptor) in the urinary tract: expression, function and clinical applications Naunyn Schmiedebergs Arch Pharmacol 373 2006 287 299
4. 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 2004 849 857
5. 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 2006 1269 1282
6. L.A. Birder, Y. Nakamura, S. Kiss, M.L. Nealen, S. Barrick, A.J. Kanai, E. Wang, G. Ruiz, W.C. De Groat, G. Apodaca, S. Watkins, and M.J. Caterina Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1 Nat Neurosci 5 2002 856 860
7. S. Boukalova, F. Touska, L. Marsakova, A. Hynkova, L. Sura, S. Chvojka, I. Dittert, and V. Vlachova Gain-of-function mutations in the transient receptor potential channels TRPV1 and TRPA1: how painful? Physiol Rev 63 2014 S205 S213
8. P. Castroman, and T.J. Ness Vigor of visceromotor responses to urinary bladder distension in rats increases with repeated trials and stimulus intensity Neurosci Lett 306 2001 97 100
9. J.S. Cefalu, M.A. Guillon, L.R. Burbach, Q.M. Zhu, D.Q. Hu, M.J. Ho, A.P. Ford, P.A. Nunn, and D.A. Cockayne Selective pharmacological blockade of the TRPV1 receptor suppresses sensory reflexes of the rodent bladder J Urol 182 2009 776 785
10. F. Cervero Sensory innervation of the viscera: peripheral basis of visceral pain Physiol Rev 74 1994 95 138
11. J.A. Christianson, K. Bielefeldt, S.A. Malin, and B.M. Davis Neonatal colon insult alters growth factor expression and TRPA1 responses in adult mice PAIN® 151 2010 540 549
12. J.A. Christianson, S.L. McIlwrath, H.R. Koerber, and B.M. Davis Transient receptor potential vanilloid 1-immunopositive neurons in the mouse are more prevalent within colon afferents compared to skin and muscle afferents Neuroscience 140 2006 247 257
13. Y.C. Chuang, N. Yoshimura, C.C. Huang, P.H. Chiang, and M.B. Chancellor Intravesical botulinum toxin a administration produces analgesia against acetic acid induced bladder pain responses in rats J Urol 172 2004 1529 1532
14. 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 2008 450 455
15. M.A. Engel, A. Leffler, F. Niedermirtl, A. Babes, K. Zimmermann, M.R. Filipovic, I. Izydorczyk, M. Eberhardt, T.I. Kichko, S.M. Mueller-Tribbensee, M. Khalil, N. Siklosi, C. Nau, I. Ivanovic-Burmazovic, W.L. Neuhuber, C. Becker, M.F. Neurath, and P.W. Reeh TRPA1 and substance P mediate colitis in mice Gastroenterology 141 2011 1346 1358
16. W. Everaerts, M.R. Sepulveda, T. Gevaert, T. Roskams, B. Nilius, and D. De Ridder Where is TRPV1 expressed in the bladder, do we see the real channel? Naunyn Schmiedebergs Arch Pharmacol 379 2009 421 425
17. W. Everaerts, J. Vriens, G. Owsianik, G. Appendino, T. Voets, D. De Ridder, and B. Nilius Functional characterization of transient receptor potential channels in mouse urothelial cells Am J Physiol Renal Physiol 298 2010 F692 F701
18. R.D. Fields, F. Eshete, S. Dudek, N. Ozsarac, and B. Stevens Regulation of gene expression by action potentials: dependence on complexity in cellular information processing Novartis Found Symp 239 2001 160 172
19. 2+ signaling networks in regulating gene expression by action potentials Cell Calcium 37 2005 433 442
20. N.M. Flake, and M.S. Gold Inflammation alters sodium currents and excitability of temporomandibular joint afferents Neurosci Lett 384 2005 294 299
21. N.R. Gavva, J.J. Treanor, A. Garami, L. Fang, S. Surapaneni, A. Akrami, F. Alvarez, A. Bak, M. Darling, A. Gore, G.R. Jang, J.P. Kesslak, L. Ni, M.H. Norman, G. Palluconi, M.J. Rose, M. Salfi, E. Tan, A.A. Romanovsky, C. Banfield, and G. Davar Pharmacological blockade of the vanilloid receptor TRPV1 elicits marked hyperthermia in humans PAIN® 136 2008 202 210
22. G.E. Hardingham, F.J. Arnold, and H. Bading Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity Nat Neurosci 4 2001 261 267
23. S. Holm A simple sequentially rejective multiple test procedure Scand J Stat 6 1979 65 70
24. R.C. Jones 3rd, L. Xu, and G.F. Gebhart The mechanosensitivity of mouse colon afferent fibers and their sensitization by inflammatory mediators require transient receptor potential vanilloid 1 and acid-sensing ion channel 3 J Neurosci 25 2005 10981 10989
25. 2+] with fluorescent indicators Methods Cell Biol 40 1994 155 181
26. B. Kremeyer, F. Lopera, J.J. Cox, A. Momin, F. Rugiero, S. Marsh, C.G. Woods, N.G. Jones, K.J. Paterson, F.R. Fricker, A. Villegas, N. Acosta, N.G. Pineda-Trujillo, J.D. Ramirez, J. Zea, M.W. Burley, G. Bedoya, D.L. Bennett, J.N. Wood, and A. Ruiz-Linares A gain-of-function mutation in TRPA1 causes familial episodic pain syndrome Neuron 66 2010 671 680
27. H.C. Kuo Repeated intravesical onabotulinum toxin A injections are effective in treatment of refractory interstitial cystitis/bladder pain syndrome Int J Clin Pract 67 2013 427 434
28. + channels between the lumbar splanchnic and pelvic nerve innervations of mouse urinary bladder and colon Neuroscience 186 2011 179 187
29. 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 2007 541 545
30. S. Malin, D. Molliver, J.A. Christianson, E.S. Schwartz, P. Cornuet, K.M. Albers, and B.M. Davis TRPV1 and TRPA1 function and modulation are target tissue dependent J Neurosci 31 2011 10516 10528
31. S.A. Malin, B.M. Davis, and D.C. Molliver Production of dissociated sensory neuron cultures and considerations for their use in studying neuronal function and plasticity Nat Protoc 2 2007 152 160
32. S. Materazzi, R. Nassini, E. Andre, B. Campi, S. Amadesi, M. Trevisani, N.W. Bunnett, R. Patacchini, and P. Geppetti Cox-dependent fatty acid metabolites cause pain through activation of the irritant receptor TRPA1 Proc Natl Acad Sci U S A 105 2008 12045 12050
33. C.R. McNamara, J. Mandel-Brehm, D.M. Bautista, J. Siemens, K.L. Deranian, M. Zhao, N.J. Hayward, J.A. Chong, D. Julius, M.M. Moran, and C.M. Fanger TRPA1 mediates formalin-induced pain Proc Natl Acad Sci U S A 104 2007 13525 13530
34. L. Merrill, B.M. Girard, V. May, and M.A. Vizzard Transcriptional and translational plasticity in rodent urinary bladder TRP channels with urinary bladder inflammation, bladder dysfunction, or postnatal maturation J Mol Neurosci 48 2012 744 756
35. E.M. Messing, and T.A. Stamey Interstitial cystitis: early diagnosis, pathology, and treatment Urology 12 1978 381 392
36. M.M. Moran, M.A. McAlexander, T. Biro, and A. Szallasi Transient receptor potential channels as therapeutic targets Nat Rev Drug Discov 10 2011 601 620
37. T.J. Ness, and H. Elhefni Reliable visceromotor responses are evoked by noxious bladder distention in mice J Urol 171 2004 1704 1708
38. J.C. Nickel, P. Jain, N. Shore, J. Anderson, D. Giesing, H. Lee, G. Kim, K. Daniel, S. White, C. Larrivee-Elkins, J. Lekstrom-Himes, and M. Cima Continuous intravesical lidocaine treatment for interstitial cystitis/bladder pain syndrome: safety and efficacy of a new drug delivery device Sci Transl Med 4 2012 143ra100
39. B. Nilius, G. Appendino, and G. Owsianik The transient receptor potential channel TRPA1: from gene to pathophysiology Pflugers Arch 464 2012 425 458
40. B. Nilius, and G. Owsianik The transient receptor potential family of ion channels Genome Biol 12 2011 218
41. D. Ost, T. Roskams, F. Van Der Aa, and D. De Ridder Topography of the vanilloid receptor in the human bladder: more than just the nerve fibers J Urol 168 2002 293 297
42. X. Pang, M.M. Cotreau-Bibbo, G.R. Sant, and T.C. Theoharides Bladder mast cell expression of high affinity oestrogen receptors in patients with interstitial cystitis Br J Urol 75 1995 154 161
43. M.W. Pfaffl A new mathematical model for relative quantification in real-time RT-PCR Nucleic Acids Res 29 2001 e45
44. R. Pinto, T. Lopes, B. Frias, A. Silva, J.A. Silva, C.M. Silva, C. Cruz, F. Cruz, and P. Dinis Trigonal injection of botulinum toxin A in patients with refractory bladder pain syndrome/interstitial cystitis Eur Urol 58 2010 360 365
45. R. Pinto, T. Lopes, J. Silva, C. Silva, P. Dinis, and F. Cruz Persistent therapeutic effect of repeated injections of onabotulinum toxin a in refractory bladder pain syndrome/interstitial cystitis J Urol 189 2013 548 553
46. J.D. Richardson, and M.R. Vasko Cellular mechanisms of neurogenic inflammation J Pharmacol Exp Ther 302 2002 839 845
47. F.A. Russell, E.S. Fernandes, J.P. Courade, J.E. Keeble, and S.D. Brain Tumour necrosis factor alpha mediates transient receptor potential vanilloid 1-dependent bilateral thermal hyperalgesia with distinct peripheral roles of interleukin-1beta, protein kinase C and cyclooxygenase-2 signalling PAIN® 142 2009 264 274
48. E.S. Schwartz, J.A. Christianson, X. Chen, J.H. La, B.M. Davis, K.M. Albers, and G.F. Gebhart Synergistic role of TRPV1 and TRPA1 in pancreatic pain and inflammation Gastroenterology 140 2011 e1281 e1282
49. C.S. Sherrington The integrative action of the nervous system 1906 Yale University Press New Haven, CT
50. J.H. Shie, H.T. Liu, Y.S. Wang, and H.C. Kuo Immunohistochemical evidence suggests repeated intravesical application of botulinum toxin A injections may improve treatment efficacy of interstitial cystitis/bladder pain syndrome BJU Int 111 2013 638 646
51. 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 2008 391 399
52. A. Sukiennik, D.B. Carr, I. Bonney, J.E. Marchand, H. Wurm, and G.R. Sant The effect of short-term epidural local anesthetic blockade on urinary levels of substance P in interstitial cystitis Anesth Analg 98 2004 846 850
53. T.E. Taylor-Clark, M.A. McAlexander, C. Nassenstein, S.A. Sheardown, S. Wilson, J. Thornton, M.J. Carr, and B.J. Undem Relative contributions of TRPA1 and TRPV1 channels in the activation of vagal bronchopulmonary C-fibres by the endogenous autacoid 4-oxononenal J Physiol 586 2008 3447 3459
54. M. Trevisani, J. Siemens, S. Materazzi, D.M. Bautista, R. Nassini, B. Campi, N. Imamachi, E. Andre, R. Patacchini, G.S. Cottrell, R. Gatti, A.I. Basbaum, N.W. Bunnett, D. Julius, and P. Geppetti 4-Hydroxynonenal, an endogenous aldehyde, causes pain and neurogenic inflammation through activation of the irritant receptor TRPA1 Proc Natl Acad Sci U S A 104 2007 13519 13524
55. M. Trevisani, and A. Szallasi Targeting TRPV1: challenges and issues in pain management Open Drug Discov J 2 2010 37 49
56. W. Vermeulen, J.G. De Man, H.U. De Schepper, H. Bult, T.G. Moreels, P.A. Pelckmans, and B.Y. De Winter Role of TRPV1 and TRPA1 in visceral hypersensitivity to colorectal distension during experimental colitis in rats Eur J Pharmacol 698 2013 404 412
57. T. Yamada, S. Ugawa, T. Ueda, Y. Ishida, K. Kajita, and S. Shimada Differential localizations of the transient receptor potential channels TRPV4 and TRPV1 in the mouse urinary bladder J Histochem Cytochem 57 2009 277 287
58. S. Yu, G. Gao, B.Z. Peterson, and A. Ouyang TRPA1 in mast cell activation-induced long-lasting mechanical hypersensitivity of vagal afferent C-fibers in guinea pig esophagus Am J Physiol Gastrointest Liver Physiol 297 2009 G34 G42
59. W. Yu, W.G. Hill, G. Apodaca, and M.L. Zeidel Expression and distribution of transient receptor potential (TRP) channels in bladder epithelium Am J Physiol Renal Physiol 300 2011 F49 F59 Diseases Diseases