Sensitization of pelvic nerve afferents and mast cell infiltration in the urinary bladder following chronic colonic irritation is mediated by neuropeptides

American Journal of Physiology - Renal Physiology

Volumn 292, Issue 1, 2007, Pages

  Ustinova, Elena E ^a   Gutkin, Dmitriy W ^b   Pezzone, Michael A ^a,c  

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

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

C fiber; Capsaicin; Interstitial cystitis; Irritable bowel syndrome; Mast cell; Trinitrobenzenesulfonic acid

Indexed keywords

CAPSAICIN; NEUROPEPTIDE; TRINITROBENZENESULFONIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLADDER; BLADDER PRESSURE; CELL INFILTRATION; COLITIS; CONTROLLED STUDY; FEMALE; HISTOLOGY; INTERSTITIAL CYSTITIS; IRRITABLE COLON; MAST CELL; NERVE CONDUCTION; NEUROGENIC INFLAMMATION; NOCICEPTIVE STIMULATION; NONHUMAN; PELVIC NERVE; PRIORITY JOURNAL; RAT; SENSITIZATION; SENSORY NERVE;

EID: 33846202164     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00162.2006     Document Type: Article

References (50)

1. Alagiri M, Chottiner S, Ratner V, Slade D, Hanno PM. Interstitial cystitis: unexplained associations with other chronic disease and pain syndromes. Urology 49: 52-57, 1997.
2. Appleyard CB, Wallace JL. Reactivation of hapten-induced colitis and its prevention by anti-inflammatory drugs. Am J Physiol Gastrointest Liver Physiol 269: G119-G125, 1995.
3. Berger RE, Miller JE, Rothman I, Krieger JN, Muller CH. Bladder petechiae after cystoscopy and hydrodistension in men diagnosed with prostate pain. J Urol 159: 83-85, 1998.
4. Cardenas CG, Del Mar LP, Cooper BY, Scroggs RS. 5-HT4 receptors couple positively to tetrodotoxin-insensitive sodium channels in a subpopulation of capsaicin-sensitive rat sensory neurons. J Neurosci 17: 7181-7189, 1997.
5. Christianson JA, Liang R, Ustinova EE, Davis BM, Fraser MO, Pezzone MA. Convergence of bladder and colon sensory innervation occurs at the primary afferent level. Pain. In press. doi-10.1016/j.pain.2006.09.023.
6. Clemens JQ, Meenan RT, Rosetti MC, Gao SY, Calhoun EA. Prevalence and incidence of interstitial cystitis in a managed care population. J Urol 173: 98-102, 2005.
7. de Groat WC, Booth AM. Neural control of penile erection. In: Nervous Control of the Urogenital System, edited by Maggi CA. London: Harwood, 1993, p.467-524.
8. de Groat WC, Booth AM, Oshimura N. Neurophysiology of micturition and its modification in animal models of human disease. In: Nervous Control of the Urogenital System, edited by Maggi CA. London: Harwood, 1993, p. 227-290.
9. de Groat WC, Nadelhaft I, Milne RJ, Booth AM, Morgan C, Thor K. Organization of the sacral parasympathetic reflex pathways to the urinary bladder and large intestine. J Auton Nerv Syst 3: 135-160, 1981.
10. de Groat WC, Roppolo JR, Yoshimura N, Sugaya K. Neural control of the urinary bladder and colon. In: Proceedings 2nd International Symposium, Brain-Gut Interactions, edited by Tache Y, Wingate D, and Burks T. Boca Raton, FL: CRC, 1993, p. 167-190.
11. de Groat WC, Steers WD. Neuroanatomy and neurophysiology of penile erection. In: Contemporary Management of Impotence and Infertility, edited by Tanagho EA, Lue TF, and McClure RD. Baltimore, MD: Williams & Wilkins, 1981, p. 3-27.
12. Dmitrieva N, McMahon SB. Sensitisation of visceral afferents by nerve growth factor in the adult rat. Pain 66: 87-97, 1996.
13. Dmitrieva N, Shelton D, Rice AS, McMahon SB. The role of nerve growth factor in a model of visceral inflammation. Neuroscience 78: 449-459, 1997.
14. Doggweiler-Wiygul R, Blankenship J, MacDiarmid SA. Review on chronic pelvic pain from a urological point of view. World J Urol 19: 160-165, 2001.
15. Elson CO, Sartor RB, Tennyson GS, Riddell RH. Experimental models of inflammatory bowel disease. Gastroenterology 109: 1344-1367, 1995.
16. England S, Bevan S, Docherty RJ. PGE2 modulates the tetrodotoxinresistant sodium current in neonatal rat dorsal root ganglion neurons via the cyclic AMP-protein kinase A cascade. J Physiol 495: 429-440, 1996.
17. Fitzpatrick CC, DeLancey JOL, Elkins TE, McGuire EJ. Vulvar vestibulitis and interstitial cystitis: a disorder of urogenital-derived epithelium? Obstet Gynecol 81: 860-862, 1993.
18. Gebhart GF. Pathobiology of visceral pain: molecular mechanisms and therapeutic implications. IV. Visceral afferent contributions to the pathobiology of visceral pain. Am J Physiol Gastrointest Liver Physiol 278: G834-G838, 2000.
19. Gold MS, Reichling DB, Shuster MJ, Levine JD. Hyperalgesic agents increase a tetrodotoxin-resistant Na+ current in nociceptors. Proc Natl Acad Sci USA 93: 1108-1112, 1996.
20. Häbler HJ, Jänig W, Koltzenburg M. Activation of unmyelinated afferent fibres by mechanical stimuli and inflammation of the urinary bladder in the cat. J Physiol 425: 545-562, 1990.
21. Jancso G. Pharmacologically induced selective degeneration of chemosensitive primary sensory neurones. Nature 270: 741-43, 1977.
22. Janig W, Koltzenburg M. On the function of spinal primary afferent fibres supplying colon and urinary bladder. J Auton Nerv Syst 30 Suppl: S89-S96, 1990.
23. Letourneau R, Pang X, Sant GR, Theoharides TC. Intragranular activation of bladder mast cells and their association with nerve processes in interstitial cystitis. Brit J Urology 77: 41-54, 1996.
24. Mallory FB. Pathological Technique. Philadelphia, PA: Saunders, 1938, p.195.
25. Malykhina AP, Chao Q, Foreman RD, Akbarali HI. Colonic inflammation increases Na+ currents in bladder sensory neurons. Neuroreport 15: 2601-2605, 2004.
26. Mathias SD, Kuppermann M, Liberman RF, Lipschutz RC, Steege JF. Chronic pelvic pain: prevalence, health-related quality of life, and economic correlates. Obstet Gynecol 87: 321-327, 1996.
27. McCafferty DM, Wallace JL, Sharkey KA. Effects of chemical sympathectomy and sensory nerve ablation on experimental colitis in the rat. Am J Physiol Gastrointest Liver Physiol 272: G272-G280, 1997.
28. McMahon SB, Morrison JFB. Two groups of spinal interneurones that respond to stimulation of the abdominal viscera of the cat. J Physiol 322: 21-34, 1982.
29. Moldwin RM. Similarities between interstitial cystitis and male chronic pelvic pain syndrome. Curr Urol Rep 3: 313-318, 2002.
30. Morris GP, Beck MS, Herridge MS, Depew WT, Szewczuk MR, Wallace JL. Hapten-induced model of chronic inflammation and ulceration in the rat colon. Gastroenterology 96: 795-803, 1989.
31. Newson B, Dahlstrom A, Enerback L, Ahlman H. Suggestive evidence for a direct innervation of mucosal mast cells. Neuroscience 10: 565-570, 1983.
32. Novi JM, Jeronis S, Srinivas S, Srinivasan R, Morgan MA, Arya LA. Risk of irritable bowel syndrome and depression in women with interstitial cystitis: A case-control study. J Urology 174: 937-940, 2005.
33. O'Sullivan M, Clayton N, Breslin NP, Harman I, Bountra C, McLaren A, O'Morain CA. Increased mast cells in the irritable bowel syndrome. Neurogastroenterol Mot 12: 449-457, 2000.
34. Pezzone MA, Liang R, Fraser MO. A model of neural cross-talk and irritation in the pelvis: implications for the overlap of chronic pelvic pain disorders. Gastroenterology 128: 1953-1964, 2005.
35. Prior A, Wilson K, Whorwell PJ, Faragher EB. Irritable bowel syndrome in the gynecological clinic. Survey of 798 new referrals. Dig Dis Sci 34: 1820-1824, 1989.
36. Santos J, Guilarte M, Alonso C, Malagelada JR. Pathogenesis of irritable bowel syndrome: the mast cell connection. Scand J Gastroenterol 40: 129-140, 2005.
37. Shea VK, Cai R, Crepps B, Mason JL, Perl ER. Sensory fibers of the pelvic nerve innervating the rat's urinary bladder. J Neurophysiol 84: 1924-1933, 2000.
38. Spanos C, Pang X, Ligris K, Letourneau R, Alferes L, Alexacos N, Sant GR, Theoharides TC. Stress-induced bladder mast cell activation: Implications for interstitial cystitis. J Urol 157: 669-672, 1997.
39. Spiller RC. Postinfectious irritable bowel syndrome. Gastroenterology 124: 1662-1671, 2003.
40. Stead RH, Dixon MF, Nigel HB, Riddell RH, Bienenstock J. Mast cells are closely apposed to nerves in the human gastrointestinal mucosa. Gastroenterology 97: 575-585, 1989.
41. Szolcsanyi J, Bartho L. Capsaicin-sensitive afferents and their role in gastroprotection: an update. J Physiol Paris 95: 181-188, 2001.
42. Theoharides TC, Cochrane DE. Critical role of mast cells in inflammatory diseases and the effect of acute stress. J Neuroimmunol 146: 1-12, 2004.
43. Theoharides TC, Sant GR. Bladder mast cell activation in interstitial cystitis. Semin Urol 9: 74-87, 1991.
44. Theoharides TC, Sant GR. The role of the mast cell in interstitial cystitis. Urol Clin North Am 21: 41-53, 1994.
45. Ustinova EE, Fraser MO, Pezzone MA. Colonic irritation in the rat sensitizes urinary bladder afferents to mechanical and chemical stimuli: An afferent origin of pelvic organ cross-sensitization. Am J Physiol Renal Physiol 290: F1478-F1487, 2006.
46. Warren JW. Interstitial cystitis as an infectious disease. Urol Clin North Am 21: 31-39, 1994.
47. Weston AP, Biddle WL, Bhatia PS, Miner PB. Terminal ileal mucosal mast cells in irritable bowel syndrome. Dig Dis Sci 38: 1590-1595, 1993.
48. Whorwell PJ, McCallum M, Creed FH, Roberts CT. Non-colonic features of irritable bowel syndrome. Gut 27: 37-40, 1986.
49. Zondervan KT, Yudkin PL, Vessey MP, Dawes MG, Barlow DH, Kennedy SH. Prevalence and incidence of chronic pelvic pain in primary care: evidence from a national general practice database. Br J Obstet Gynaecol 106: 1149-1155, 1999.
50. Zondervan KT, Yudkin PL, Vessey MP, Jenkinson CP, Dawes MG, Barlow DH, Kennedy SH. The community prevalence of chronic pelvic pain in women and associated illness behaviour. Br J Gen Pract 51: 541-547, 2001.