Skip to main content
PMC home page
Mediators of Inflammation logoLink to Mediators of Inflammation
. 1994;3(3):189–197. doi: 10.1155/S0962935194000268

Neurogenic Inflammation of Guinea-Pig Bladder

D E Bjorling 1,✉, M R Saban 1, R Saban 1
PMCID: PMC2367033  PMID: 18472941

Abstract

Capsaicin, substance P, and ovalbumin, instilled into the bladders of naive and ovalbumin (OVA) sensitized guineapigs caused inflammation, as indicated by increased vascular permeability. Histological changes after exposure to these compounds progressed with time from intense vasodilatation to marginalization of granulocytes followed by interstitial migration of leukocytes. In vitro incubation of guinea-pig bladder tissue with substance P and ovalbumin stimulated release of prostaglandin D2 and leukotrienes. In vitro incubation of bladder tissue with capsaicin, OVA, prostaglandin D2, leukotriene C4, histamine, or calcium ionophore A-23587 all stimulated substance P release. These data suggest that bladder inflammation initiated by a variety of stimuli could lead to a cyclic pattern of release of inflammatory mediators and neuropeptides, which could result in amplification and persistence of cystitis after the inciting cause has subsided.

Full Text

The Full Text of this article is available as a PDF (2.3 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abelli L., Somma V., Maggi C. A., Regoli D., Astolfi M., Parlani M., Rovero P., Conte B., Meli A. Effects of tachykinins and selective tachykinin receptor agonists on vascular permeability in the rat lower urinary tract: evidence for the involvement of NK-1 receptors. J Auton Pharmacol. 1989 Aug;9(4):253–263. doi: 10.1111/j.1474-8673.1989.tb00216.x. [DOI] [PubMed] [Google Scholar]
  2. Abello J., Kaiserlian D., Cuber J. C., Revillard J. P., Chayvialle J. A. Characterization of calcitonin gene-related peptide receptors and adenylate cyclase response in the murine macrophage cell line P388 D1. Neuropeptides. 1991 May;19(1):43–49. doi: 10.1016/0143-4179(91)90072-q. [DOI] [PubMed] [Google Scholar]
  3. Aharony D., Dobson P., Bernstein P. R., Kusner E. J., Krell R. D., Smith J. B. Determination of SRS-A release from guinea-pig lungs by a radioimmunoassay. Biochem Biophys Res Commun. 1983 Dec 16;117(2):574–579. doi: 10.1016/0006-291x(83)91239-1. [DOI] [PubMed] [Google Scholar]
  4. Assem E. S., Ghanem N. S., Abdullah N. A., Repke H., Foreman J. C., Hayes N. A. Substance P and Arg-Pro-Lys-Pro-NH-C12-H25-induced mediator release from different mast cell subtypes of rat and guinea-pig. Immunopharmacology. 1989 Mar-Apr;17(2):119–128. doi: 10.1016/0162-3109(89)90057-x. [DOI] [PubMed] [Google Scholar]
  5. Brokaw J. J., White G. W. Calcitonin gene-related peptide potentiates substance P-induced plasma extravasation in the rat trachea. Lung. 1992;170(2):85–93. doi: 10.1007/BF00175980. [DOI] [PubMed] [Google Scholar]
  6. Christmas T. J., Rode J., Chapple C. R., Milroy E. J., Turner-Warwick R. T. Nerve fibre proliferation in interstitial cystitis. Virchows Arch A Pathol Anat Histopathol. 1990;416(5):447–451. doi: 10.1007/BF01605152. [DOI] [PubMed] [Google Scholar]
  7. Church M. K., Lowman M. A., Robinson C., Holgate S. T., Benyon R. C. Interaction of neuropeptides with human mast cells. Int Arch Allergy Appl Immunol. 1989;88(1-2):70–78. doi: 10.1159/000234752. [DOI] [PubMed] [Google Scholar]
  8. Gu J., Blank M. A., Huang W. M., Islam K. N., McGregor G. P., Christofides N., Allen J. M., Bloom S. R., Polak J. M. Peptide-containing nerves in human urinary bladder. Urology. 1984 Oct;24(4):353–357. doi: 10.1016/0090-4295(84)90209-7. [DOI] [PubMed] [Google Scholar]
  9. HAND J. R. Interstitial cystitis; report of 223 cases (204 women and 19 men). J Urol. 1949 Feb;61(2):291–310. doi: 10.1016/S0022-5347(17)69067-0. [DOI] [PubMed] [Google Scholar]
  10. Holm-Bentzen M., Jacobsen F., Nerstrøm B., Lose G., Kristensen J. K., Pedersen R. H., Krarup T., Feggetter J., Bates P., Barnard R. Painful bladder disease: clinical and pathoanatomical differences in 115 patients. J Urol. 1987 Sep;138(3):500–502. doi: 10.1016/s0022-5347(17)43240-x. [DOI] [PubMed] [Google Scholar]
  11. Kim Y. S., Levin R. M., Wein A. J., Longhurst P. A. Effects of sensitization on the permeability of urothelium in guinea pig urinary bladder. J Urol. 1992 Jan;147(1):270–273. doi: 10.1016/s0022-5347(17)37211-7. [DOI] [PubMed] [Google Scholar]
  12. Kim Y. S., Longhurst P. A., Wein A. J., Levin R. M. Effects of sensitization on female guinea pig urinary bladder function: in vivo and in vitro studies. J Urol. 1991 Aug;146(2):454–457. doi: 10.1016/s0022-5347(17)37823-0. [DOI] [PubMed] [Google Scholar]
  13. Kowalski M. L., Sliwinska-Kowalska M., Kaliner M. A. Neurogenic inflammation, vascular permeability, and mast cells. II. Additional evidence indicating that mast cells are not involved in neurogenic inflammation. J Immunol. 1990 Aug 15;145(4):1214–1221. [PubMed] [Google Scholar]
  14. Kruger J. M., Osborne C. A., Goyal S. M., Wickstrom S. L., Johnston G. R., Fletcher T. F., Brown P. A. Clinical evaluation of cats with lower urinary tract disease. J Am Vet Med Assoc. 1991 Jul 15;199(2):211–216. [PubMed] [Google Scholar]
  15. Lasanen L. T., Tammela T. L., Liesi P., Waris T., Polak J. M. The effect of acute distension on vasoactive intestinal polypeptide (VIP), neuropeptide Y (NPY) and substance P (SP) immunoreactive nerves in the female rat urinary bladder. Urol Res. 1992;20(4):259–263. doi: 10.1007/BF00300255. [DOI] [PubMed] [Google Scholar]
  16. Lundberg J. M., Brodin E., Hua X., Saria A. Vascular permeability changes and smooth muscle contraction in relation to capsaicin-sensitive substance P afferents in the guinea-pig. Acta Physiol Scand. 1984 Feb;120(2):217–227. doi: 10.1111/j.1748-1716.1984.tb00127.x. [DOI] [PubMed] [Google Scholar]
  17. Lundblad L., Lundberg J. M., Anggård A., Zetterström O. Capsaicin pretreatment inhibits the flare component of the cutaneous allergic reaction in man. Eur J Pharmacol. 1985 Jul 31;113(3):461–462. doi: 10.1016/0014-2999(85)90098-6. [DOI] [PubMed] [Google Scholar]
  18. Lundeberg T., Liedberg H., Nordling L., Theodorsson E., Owzarski A., Ekman P. Interstitial cystitis: correlation with nerve fibres, mast cells and histamine. Br J Urol. 1993 Apr;71(4):427–429. doi: 10.1111/j.1464-410x.1993.tb15986.x. [DOI] [PubMed] [Google Scholar]
  19. MacDermott J. P., Charpied G. C., Tesluk H., Stone A. R. Can histological assessment predict the outcome in interstitial cystitis? Br J Urol. 1991 Jan;67(1):44–47. doi: 10.1111/j.1464-410x.1991.tb15068.x. [DOI] [PubMed] [Google Scholar]
  20. Maggi C. A., Abelli L., Giuliani S., Santicioli P., Geppetti P., Somma V., Frilli S., Meli A. The contribution of sensory nerves to xylene-induced cystitis in rats. Neuroscience. 1988 Aug;26(2):709–723. doi: 10.1016/0306-4522(88)90176-5. [DOI] [PubMed] [Google Scholar]
  21. Maggi C. A., Barbanti G., Santicioli P., Beneforti P., Misuri D., Meli A., Turini D. Cystometric evidence that capsaicin-sensitive nerves modulate the afferent branch of micturition reflex in humans. J Urol. 1989 Jul;142(1):150–154. doi: 10.1016/s0022-5347(17)38701-3. [DOI] [PubMed] [Google Scholar]
  22. Maggi C. A., Lecci A., Santicioli P., Del Bianco E., Giuliani S. Cyclophosphamide cystitis in rats: involvement of capsaicin-sensitive primary afferents. J Auton Nerv Syst. 1992 May 15;38(3):201–208. doi: 10.1016/0165-1838(92)90031-b. [DOI] [PubMed] [Google Scholar]
  23. Maggi C. A., Patacchini R., Santicioli P., Giuliani S. Tachykinin antagonists and capsaicin-induced contraction of the rat isolated urinary bladder: evidence for tachykinin-mediated cotransmission. Br J Pharmacol. 1991 Jun;103(2):1535–1541. doi: 10.1111/j.1476-5381.1991.tb09823.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Maggi C. A. The dual function of capsaicin-sensitive sensory nerves in the bladder and urethra. Ciba Found Symp. 1990;151:77–90. doi: 10.1002/9780470513941.ch5. [DOI] [PubMed] [Google Scholar]
  25. McGillis J. P., Mitsuhashi M., Payan D. G. Immunomodulation by tachykinin neuropeptides. Ann N Y Acad Sci. 1990;594:85–94. doi: 10.1111/j.1749-6632.1990.tb40470.x. [DOI] [PubMed] [Google Scholar]
  26. Nadel J. A. Neurogenic inflammation in airways and its modulation by peptidases. Ann N Y Acad Sci. 1992;664:408–414. doi: 10.1111/j.1749-6632.1992.tb39779.x. [DOI] [PubMed] [Google Scholar]
  27. Nielsen K. K., Kromann-Andersen B., Steven K., Hald T. Failure of combined supratrigonal cystectomy and Mainz ileocecocystoplasty in intractable interstitial cystitis: is histology and mast cell count a reliable predictor for the outcome of surgery? J Urol. 1990 Aug;144(2 Pt 1):255–259. doi: 10.1016/s0022-5347(17)39426-0. [DOI] [PubMed] [Google Scholar]
  28. Pascual D. W., Bost K. L., Xu-Amano J., Kiyono H., McGhee J. R. The cytokine-like action of substance P upon B cell differentiation. Reg Immunol. 1992 Mar-Apr;4(2):100–104. [PubMed] [Google Scholar]
  29. Sharkey K. A. Substance P and calcitonin gene-related peptide (CGRP) in gastrointestinal inflammation. Ann N Y Acad Sci. 1992;664:425–442. doi: 10.1111/j.1749-6632.1992.tb39781.x. [DOI] [PubMed] [Google Scholar]
  30. Theoharides T. C., Flaris N., Cronin C. T., Ucci A., Meares E. Mast cell activation in sterile bladder and prostate inflammation. Int Arch Allergy Appl Immunol. 1990;92(3):281–286. doi: 10.1159/000235190. [DOI] [PubMed] [Google Scholar]
  31. Umeda Y., Arisawa M. Characterization of the calcitonin gene-related peptide receptor in mouse T lymphocytes. Neuropeptides. 1989 Nov-Dec;14(4):237–242. doi: 10.1016/0143-4179(89)90052-8. [DOI] [PubMed] [Google Scholar]
  32. Undem B. J., Pickett W. C., Lichtenstein L. M., Adams G. K., 3rd The effect of indomethacin on immunologic release of histamine and sulfidopeptide leukotrienes from human bronchus and lung parenchyma. Am Rev Respir Dis. 1987 Nov;136(5):1183–1187. doi: 10.1164/ajrccm/136.5.1183. [DOI] [PubMed] [Google Scholar]
  33. Vliagoftis H., Dimitriadou V., Boucher W., Rozniecki J. J., Correia I., Raam S., Theoharides T. C. Estradiol augments while tamoxifen inhibits rat mast cell secretion. Int Arch Allergy Immunol. 1992;98(4):398–409. doi: 10.1159/000236217. [DOI] [PubMed] [Google Scholar]
  34. Wozniak A., McLennan G., Betts W. H., Murphy G. A., Scicchitano R. Activation of human neutrophils by substance P: effect on FMLP-stimulated oxidative and arachidonic acid metabolism and on antibody-dependent cell-mediated cytotoxicity. Immunology. 1989 Nov;68(3):359–364. [PMC free article] [PubMed] [Google Scholar]
  35. Yano H., Wershil B. K., Arizono N., Galli S. J. Substance P-induced augmentation of cutaneous vascular permeability and granulocyte infiltration in mice is mast cell dependent. J Clin Invest. 1989 Oct;84(4):1276–1286. doi: 10.1172/JCI114295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Yonehara N., Imai Y., Shibutani T., Inoki R. Participation of substance P in inflammatory responses. Adv Exp Med Biol. 1989;247B:529–534. doi: 10.1007/978-1-4615-9546-5_87. [DOI] [PubMed] [Google Scholar]

Articles from Mediators of Inflammation are provided here courtesy of Wiley

RESOURCES