Experimental colitis triggers the release of substance P and calcitonin gene-related peptide in the urinary bladder via TRPV1 signaling pathways

Experimental Neurology

Volumn 225, Issue 2, 2010, Pages 262-273

  Pan, Xiao Qing ^a   Gonzalez, Jessica A ^a   Chang, Shaohua ^a   Chacko, Samuel ^a   Wein, Alan J ^a   Malykhina, Anna P ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cross sensitization; Inflammation; Neuropeptides; Pelvic pain

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; RESINIFERATOXIN; SUBSTANCE P; TRINITROBENZENESULFONIC ACID; VANILLOID RECEPTOR 1; MESSENGER RNA; VANILLOID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLADDER; COLITIS; CONTROLLED STUDY; DESENSITIZATION; DISEASE SEVERITY; DOWN REGULATION; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CHEMICALLY INDUCED; COLON; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; INNERVATION; METABOLISM; SENSORY NERVE CELL; SPRAGUE DAWLEY RAT;

ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; COLITIS; COLON; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; MALE; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION; SUBSTANCE P; TRINITROBENZENESULFONIC ACID; TRPV CATION CHANNELS; URINARY BLADDER;

EID: 77956448154     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2010.05.012     Document Type: Article

References (71)

1. Abelli L., Conte B., Somma V., Maggi C.A., Giuliani S., Meli A. A method for studying pain arising from the urinary bladder in conscious, freely-moving rats. J. Urol. 1989, 141:148-151.
2. Alvarez J., Giuditta A., Koenig E. Protein synthesis in axons and terminals: significance for maintenance, plasticity and regulation of phenotype. With a critique of slow transport theory. Prog. Neurobiol. 2000, 62:1-62.
3. Avelino A., Cruz F. Peptide immunoreactivity and ultrastructure of rat urinary bladder nerve fibers after topical desensitization by capsaicin or resiniferatoxin. Auton. Neurosci. 2000, 86:37-46.
4. Avelino A., Cruz F. TRPV1 (vanilloid receptor) in the urinary tract: expression, function and clinical applications. Naunyn. Schmiedebergs Arch. Pharmacol. 2006, 373:287-299.
5. Avelino A., Cruz C., Nagy I., Cruz F. Vanilloid receptor 1 expression in the rat urinary tract. Neuroscience 2002, 109:787-798.
6. Barreau F., Salvador-Cartier C., Houdeau E., Bueno L., Fioramonti J. Long-term alterations of colonic nerve-mast cell interactions induced by neonatal maternal deprivation in rats. Gut 2008, 57:582-590.
7. Birder L.A., Kanai A.J., de Groat W.C., Kiss S., Nealen M.L., Burke N.E., Dineley K.E., Watkins S., Reynolds I.J., Caterina M.J. Vanilloid receptor expression suggests a sensory role for urinary bladder epithelial cells. Proc. Natl. Acad. Sci. USA 2001, 98:13396-13401.
8. Birder L., de G.W., Mills I., Morrison J., Thor K., Drake M. Neural control of the lower urinary tract: peripheral and spinal mechanisms. Neurourol. Urodyn. 2010, 29:128-139.
9. Blyweert W., Van Der A.F., Ost D., Stagnaro M., De R.D. Interstitial cells of the bladder: the missing link?. BJOG 2004, 111(Suppl 1):57-60.
10. Brady C.A., Gill R.A., Lynch P.T. Preliminary evidence for the metabolism of benzo(a) pyrene by Plantago lanceolata. Environ. Geochem. Health 2003, 25:131-137.
11. Brumovsky P.R., Gebhart G.F. Visceral organ cross-sensitization-an integrated perspective. Auton. Neurosci. 2010, 153:106-115.
12. Bueno L., Fioramonti J. Visceral perception: inflammatory and non-inflammatory mediators. Gut 2002, 51(Suppl 1):i19-i23.
13. Candenas L., Lecci A., Pinto F.M., Patak E., Maggi C.A., Pennefather J.N. Tachykinins and tachykinin receptors: effects in the genitourinary tract. Life Sci. 2005, 76:835-862.
14. Caterina M.J., Julius D. The vanilloid receptor: a molecular gateway to the pain pathway. Annu. Rev. Neurosci. 2001, 24:487-517.
15. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997, 389:816-824.
16. Chen T.Y., Corcos J., Camel M., Ponsot Y., Tu I.M. Prospective, randomized, double-blind study of safety and tolerability of intravesical resiniferatoxin (RTX) in interstitial cystitis (IC). Int. Urogynecol. J. Pelvic Floor Dysfunct. 2005, 16:293-297.
17. Chuang Y.C., Fraser M.O., Yu Y., Chancellor M.B., de Groat W.C., Yoshimura N. The role of bladder afferent pathways in bladder hyperactivity induced by the intravesical administration of nerve growth factor. J. Urol. 2001, 165:975-979.
18. Day I.N., Thompson R.J. UCHL1 (PGP 9.5): neuronal biomarker and ubiquitin system protein. Prog. Neurobiol. 2009, 90(3):327-362.
19. Domotor A., Peidl Z., Vincze A., Hunyady B., Szolcsanyi J., Kereskay L., Szekeres G., Mozsik G. Immunohistochemical distribution of vanilloid receptor, calcitonin-gene related peptide and substance P in gastrointestinal mucosa of patients with different gastrointestinal disorders. Inflammopharmacol. 2005, 13:161-177.
20. Eyden B. Are there myofibroblasts in normal bladder?. Eur. Urol. 2009, 56:427-429.
21. Fowler C.J., Griffiths D., de Groat W.C. The neural control of micturition. Nat. Rev. Neurosci. 2008, 9:453-466.
22. Gabella G., Davis C. Distribution of afferent axons in the bladder of rats. J. Neurocytol. 1998, 27:141-155.
23. Giuditta A., Kaplan B.B., van M.J., Alvarez J., Koenig E. Axonal and presynaptic protein synthesis: new insights into the biology of the neuron. Trends Neurosci. 2002, 25:400-404.
24. Gulbenkian S., Merighi A., Wharton J., Varndell I.M., Polak J.M. Ultrastructural evidence for the coexistence of calcitonin gene-related peptide and substance P in secretory vesicles of peripheral nerves in the guinea pig. J. Neurocytol. 1986, 15:535-542.
25. Holzer P., Maggi C.A. Stimulation and propagation of the ascending enteric reflex contraction: role of tachykinins and acetylcholine. Regul. Pept. 1993, 46:383-385.
26. Hwang S.J., Oh J.M., Valtschanoff J.G. Expression of the vanilloid receptor TRPV1 in rat dorsal root ganglion neurons supports different roles of the receptor in visceral and cutaneous afferents. Brain Res. 2005, 1047:261-266.
27. Kiebler M.A., Bassell G.J. Neuronal RNA granules: movers and makers. Neuron 2006, 51:685-690.
28. Krawisz J.E., Sharon P., Stenson W.F. Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity. Assessment of inflammation in rat and hamster models. Gastroenterology 1984, 87:1344-1350.
29. Le G.P., Nyberg F., Hokfelt T., Terenius L. Calcitonin gene-related peptide is metabolized by an endopeptidase hydrolyzing substance P. Regul. Pept. 1989, 25:277-286.
30. Li D., Ren Y., Xu X., Zou X., Fang L., Lin Q. Sensitization of primary afferent nociceptors induced by intradermal capsaicin involves the peripheral release of calcitonin gene-related Peptide driven by dorsal root reflexes. J. Pain 2008, 9:1155-1168.
31. Lin A.C., Holt C.E. Function and regulation of local axonal translation. Curr. Opin. Neurobiol. 2008, 18:60-68.
32. Lin Q., Wu J., Willis W.D. Dorsal root reflexes and cutaneous neurogenic inflammation after intradermal injection of capsaicin in rats. J. Neurophysiol. 1999, 82:2602-2611.
33. Lin Q., Li D., Xu X., Zou X., Fang L. Roles of TRPV1 and neuropeptidergic receptors in dorsal root reflex-mediated neurogenic inflammation induced by intradermal injection of capsaicin. Mol. Pain 2007, 3:30.
34. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
35. Lundberg J.M., Franco-Cereceda A., Alving K., ay-Goyet P., Lou Y.P. Release of calcitonin gene-related peptide from sensory neurons. Ann. NY Acad. Sci. 1992, 657:187-193.
36. Malykhina A.P. Neural mechanisms of pelvic organ cross-sensitization. Neuroscience 2007, 149:660-672.
37. Malykhina A.P., Qin C., Greenwood-Van Meerveld B., Foreman R.D., Lupu F., Akbarali H.I. Hyperexcitability of convergent colon and urinary bladder dorsal root ganglion neurons after colonic inflammation: mechanism for pelvic organ cross-talk. Neurogastroenterol. Motil. 2006, 18:936-948.
38. McCloskey K.D. Interstitial cells in the urinary bladder-localization and function. Neurourol. Urodyn. 2010, 29:82-87.
39. Miampamba M., Sharkey K.A. Distribution of calcitonin gene-related peptide, somatostatin, substance P and vasoactive intestinal polypeptide in experimental colitis in rats. Neurogastroenterol. Motil. 1998, 10:315-329.
40. Miranda A., Nordstrom E., Mannem A., Smith C., Banerjee B., Sengupta J.N. The role of transient receptor potential vanilloid 1 in mechanical and chemical visceral hyperalgesia following experimental colitis. Neuroscience 2007, 148:1021-1032.
41. Olerud J.E., Chiu D.S., Usui M.L., Gibran N.S., Ansel J.C. Protein gene product 9.5 is expressed by fibroblasts in human cutaneous wounds. J. Investig. Dermatol. 1998, 111:565-572.
42. Ost D., Roskams T., Van Der A.F., De R.D. Topography of the vanilloid receptor in the human bladder: more than just the nerve fibers. J. Urol. 2002, 168:293-297.
43. Payne C.K., Mosbaugh P.G., Forrest J.B., Evans R.J., Whitmore K.E., Antoci J.P., Perez-Marrero R., Jacoby K., Diokno A.C., O'Reilly K.J., Griebling T.L., Vasavada S.P., Yu A.S., Frumkin L.R. Intravesical resiniferatoxin for the treatment of interstitial cystitis: a randomized, double-blind, placebo controlled trial. J. Urol. 2005, 173:1590-1594.
44. Pothoulakis C., Castagliuolo I., LaMont J.T., Jaffer A., O'Keane J.C., Snider R.M., Leeman S.E. CP-96,345, a substance P antagonist, inhibits rat intestinal responses to clostridium difficile toxin A but not cholera toxin. Proc. Natl. Acad. Sci. USA 1994, 91:947-951.
45. Premkumar L.S., Ahern G.P. Induction of vanilloid receptor channel activity by protein kinase C. Nature 2000, 408:985-990.
46. Price T.J., Flores C.M. Critical evaluation of the colocalization between calcitonin gene-related peptide, substance P, transient receptor potential vanilloid subfamily type 1 immunoreactivities, and isolectin B4 binding in primary afferent neurons of the rat and mouse. J. Pain 2007, 8:263-272.
47. Price T.J., Flores C.M., Cervero F., Hargreaves K.M. The RNA binding and transport proteins staufen and fragile X mental retardation protein are expressed by rat primary afferent neurons and localize to peripheral and central axons. Neuroscience 2006, 141:2107-2116.
48. Qiao L.Y., Grider J.R. Up-regulation of calcitonin gene-related peptide and receptor tyrosine kinase TrkB in rat bladder afferent neurons following TNBS colitis. Exp. Neurol. 2007, 204:667-679.
49. Qin C., Malykhina A.P., Akbarali H.I., Foreman R.D. Cross-organ sensitization of lumbosacral spinal neurons receiving urinary bladder input in rats with inflamed colon. Gastroenterology 2005, 129:1967-1978.
50. Rees H., Sluka K.A., Westlund K.N., Willis W.D. The role of glutamate and GABA receptors in the generation of dorsal root reflexes by acute arthritis in the anaesthetized rat. J. Physiol. 1995, 484(Pt 2):437-445.
51. Reinshagen M., Adler G., Eysselein V.E. Substance P gene expression in acute experimental colitis. Regul. Pept. 1995, 59:53-58.
52. Rigoni M., Trevisani M., Gazzieri D., Nadaletto R., Tognetto M., Creminon C., Davis J.B., Campi B., Amadesi S., Geppetti P., Harrison S. Neurogenic responses mediated by vanilloid receptor-1 (TRPV1) are blocked by the high affinity antagonist, iodo-resiniferatoxin. Br. J. Pharmacol. 2003, 138:977-985.
53. Saban M.R., Backer J.M., Backer M.V., Maier J., Fowler B., Davis C.A., Simpson C., Wu X.R., Birder L., Freeman M.R., Soker S., Hurst R.E., Saban R. VEGF receptors and neuropilins are expressed in the urothelial and neuronal cells in normal mouse urinary bladder and are upregulated in inflammation. Am. J. Physiol. Ren. Physiol. 2008, 295:F60-F72.
54. Schmid H.A. Effect of glutamate and angiotensin II on whole cell currents and release of nitric oxide in the rat subfornical organ. Amino Acids 1998, 14:113-119.
55. Smet P.J., Edyvane K.A., Jonavicius J., Marshall V.R. Neuropeptides and neurotransmitter-synthesizing enzymes in intrinsic neurons of the human urinary bladder. J. Neurocytol. 1996, 25:112-124.
56. Smet P.J., Moore K.H., Jonavicius J. Distribution and colocalization of calcitonin gene-related peptide, tachykinins, and vasoactive intestinal peptide in normal and idiopathic unstable human urinary bladder. Lab. Investig. 1997, 77:37-49.
57. Stein R.J., Santos S., Nagatomi J., Hayashi Y., Minnery B.S., Xavier M., Patel A.S., Nelson J.B., Futrell W.J., Yoshimura N., Chancellor M.B., De M.F. Cool (TRPM8) and hot (TRPV1) receptors in the bladder and male genital tract. J. Urol. 2004, 172:1175-1178.
58. Steward O., Schuman E.M. Compartmentalized synthesis and degradation of proteins in neurons. Neuron 2003, 40:347-359.
59. 2+ is involved in the mechanism of distinct substance P release in cultured rat dorsal root ganglion neurons. Naunyn-Schmiedebergs Arch. Pharmacol. 2008, 377:325-332.
60. Tang H.B., Inoue A., Oshita K., Nakata Y. Sensitization of vanilloid receptor 1 induced by bradykinin via the activation of second messenger signaling cascades in rat primary afferent neurons. Eur. J. Pharmacol. 2004, 498:37-43.
61. Tang H.B., Inoue A., Iwasa M., Hide I., Nakata Y. Substance P release evoked by capsaicin or potassium from rat cultured dorsal root ganglion neurons is conversely modulated with bradykinin. J. Neurochem. 2006, 97:1412-1418.
62. Tang H.B., Li Y.S., Arihiro K., Nakata Y. Activation of the neurokinin-1 receptor by substance P triggers the release of substance P from cultured adult rat dorsal root ganglion neurons. Mol. Pain 2007, 3:42.
63. Thompson R.J., Doran J.F., Jackson P., Dhillon A.P., Rode J. PGP 9.5-a new marker for vertebrate neurons and neuroendocrine cells. Brain Res. 1983, 278:224-228.
64. Ustinova E.E., Fraser M.O., Pezzone M.A. Cross-talk and sensitization of bladder afferent nerves. Neurourol. Urodyn. 2010, 29:77-81.
65. Warsame A.A., Gustafsson H., Olgart L., Brodin E., Stiller C.O., Taylor B.K. Capsaicin-evoked substance P release in rat dorsal horn increases after peripheral inflammation: a microdialysis study. Neurosci. Lett. 2004, 368:226-230.
66. Wesselmann U. Neurogenic inflammation and chronic pelvic pain. World J. Urol. 2001, 19:180-185.
67. Willis D., Li K.W., Zheng J.Q., Chang J.H., Smit A., Kelly T., Merianda T.T., Sylvester J., van M.J., Twiss J.L. Differential transport and local translation of cytoskeletal, injury-response, and neurodegeneration protein mRNAs in axons. J. Neurosci. 2005, 25:778-791.
68. Wilson P.O., Barber P.C., Hamid Q.A., Power B.F., Dhillon A.P., Rode J., Day I.N., Thompson R.J., Polak J.M. The immunolocalization of protein gene product 9.5 using rabbit polyclonal and mouse monoclonal antibodies. Br. J. Exp. Pathol. 1988, 69:91-104.
69. Winston J., Shenoy M., Medley D., Naniwadekar A., Pasricha P.J. The vanilloid receptor initiates and maintains colonic hypersensitivity induced by neonatal colon irritation in rats. Gastroenterology 2007, 132:615-627.
70. Wiseman O.J., Fowler C.J., Landon D.N. The role of the human bladder lamina propria myofibroblast. BJU Int. 2003, 91:89-93.
71. Zheng J.Q., Kelly T.K., Chang B., Ryazantsev S., Rajasekaran A.K., Martin K.C., Twiss J.L. A functional role for intra-axonal protein synthesis during axonal regeneration from adult sensory neurons. J. Neurosci. 2001, 21:9291-9303.