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. 1994 Sep;113(1):63–68. doi: 10.1111/j.1476-5381.1994.tb16174.x

The involvement of bradykinin B1 and B2 receptor mechanisms in cytokine-induced mechanical hyperalgesia in the rat.

A J Davis 1, M N Perkins 1
PMCID: PMC1510052  PMID: 7812634

Abstract

1. Interleukin-1 beta (IL-1 beta), IL-2 and IL-8 induced a mechanical hyperalgesia following intra-articular (i.artic.) injection into rat knee joints, whereas IL-6 and tumour necrosis factor alpha (TNF-alpha) were without effect. 2. Co-administration of IL-1 receptor antagonist (0.1 micrograms) with IL-1 beta (1 mu), IL-2 (10 mu) or IL-8 (0.1 mu) prevented the subsequent development of the hyperalgesia. 3. Co-administration of desArg9Leu8BK (0.5-5 nmol) with IL-1 beta (1 mu), IL-2 (10 mu) or IL-8 (0.1 mu) reduced the level of hyperalgesia at 1, 4 and 6 h post administration, whereas Hoe 140 (5 pmol) antagonized the hyperalgesia only at the 1 h time point. 4. Intravenous administration of desArg9Leu8BK (10 nmol kg-1) or Hoe 140 (100 pmol kg-1) following IL-1 beta (1 mu), IL-2 (10 mu), or IL-8 (0.1 mu) reversed the subsequent hyperalgesia. 5. Administration of desArg9BK into joints 24 h after pre-treatment with IL-1 beta (1 mu) produced analegsia at low doses (50 pmol) and hyperalgesia at a higher dose (0.5 nmol). Both these effects were blocked by desArg9Leu8BK (0.5 nmol). 6. Administration of desArg9BK (0.5 nmol i.artic.) to animals 24 h after pre-treatment with IL-2 (1-100 mu) or IL-8 (0.1-10 mu) had no effect on the load tolerated by the treated joint. 7. Administration of indomethacin (1 mg kg-1, s.c.) prior to IL-1 beta (1 mu i.artic.) prevented the development of hyperalgesia. Administration of desArg9BK (5 pmol-0.5 nmol, i.artic.) to animals 24 h after indomethacin and IL-1 beta pretreatment had no effect on the load tolerated by the treated joint.(ABSTRACT TRUNCATED AT 250 WORDS)

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Selected References

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  1. Bathon J. M., Croghan J. E., Goldman D. W., MacGlashan D. W., Proud D. Modulation of kinin responses in human synovium by interleukin-1. Agents Actions Suppl. 1992;38(Pt 2):16–22. [PubMed] [Google Scholar]
  2. Bond A. P., Breipohl G., Worthy K., Campion G., Dieppe P. A., Bhoola K. D. Metabolism and characterisation of kinins and Hoe 140 (kinin antagonist) in the synovial fluid of patients with inflammatory joint diseases. Agents Actions Suppl. 1992;38(Pt 1):582–589. doi: 10.1007/978-3-0348-7321-5_71. [DOI] [PubMed] [Google Scholar]
  3. Bouthillier J., Deblois D., Marceau F. Studies on the induction of pharmacological responses to des-Arg9-bradykinin in vitro and in vivo. Br J Pharmacol. 1987 Oct;92(2):257–264. doi: 10.1111/j.1476-5381.1987.tb11319.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brennan F. M., Zachariae C. O., Chantry D., Larsen C. G., Turner M., Maini R. N., Matsushima K., Feldmann M. Detection of interleukin 8 biological activity in synovial fluids from patients with rheumatoid arthritis and production of interleukin 8 mRNA by isolated synovial cells. Eur J Immunol. 1990 Sep;20(9):2141–2144. doi: 10.1002/eji.1830200938. [DOI] [PubMed] [Google Scholar]
  5. Cahill M., Fishman J. B., Polgar P. Effect of des arginine9-bradykinin and other bradykinin fragments on the synthesis of prostacyclin and the binding of bradykinin by vascular cells in culture. Agents Actions. 1988 Jul;24(3-4):224–231. doi: 10.1007/BF02028275. [DOI] [PubMed] [Google Scholar]
  6. Colditz I. G., Watson D. L. The effect of cytokines and chemotactic agonists on the migration of T lymphocytes into skin. Immunology. 1992 Jun;76(2):272–278. [PMC free article] [PubMed] [Google Scholar]
  7. Cooper W. O., Fava R. A., Gates C. A., Cremer M. A., Townes A. S. Acceleration of onset of collagen-induced arthritis by intra-articular injection of tumour necrosis factor or transforming growth factor-beta. Clin Exp Immunol. 1992 Aug;89(2):244–250. doi: 10.1111/j.1365-2249.1992.tb06939.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cunha F. Q., Poole S., Lorenzetti B. B., Ferreira S. H. The pivotal role of tumour necrosis factor alpha in the development of inflammatory hyperalgesia. Br J Pharmacol. 1992 Nov;107(3):660–664. doi: 10.1111/j.1476-5381.1992.tb14503.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Damas J., Remacle-Volon G. Influence of a long-acting bradykinin antagonist, Hoe 140, on some acute inflammatory reactions in the rat. Eur J Pharmacol. 1992 Jan 28;211(1):81–86. doi: 10.1016/0014-2999(92)90266-7. [DOI] [PubMed] [Google Scholar]
  10. Davis A. J., Perkins M. N. Induction of B1 receptors in vivo in a model of persistent inflammatory mechanical hyperalgesia in the rat. Neuropharmacology. 1994 Jan;33(1):127–133. doi: 10.1016/0028-3908(94)90107-4. [DOI] [PubMed] [Google Scholar]
  11. Davis A., Perkins M. N. The effect of capsaicin and conventional analgesics in two models of monoarthritis in the rat. Agents Actions. 1993;38(Spec No):C10–C12. doi: 10.1007/BF01991121. [DOI] [PubMed] [Google Scholar]
  12. Deblois D., Bouthillier J., Marceau F. Effect of glucocorticoids, monokines and growth factors on the spontaneously developing responses of the rabbit isolated aorta to des-Arg9-bradykinin. Br J Pharmacol. 1988 Apr;93(4):969–977. doi: 10.1111/j.1476-5381.1988.tb11487.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dray A., Patel I. A., Perkins M. N., Rueff A. Bradykinin-induced activation of nociceptors: receptor and mechanistic studies on the neonatal rat spinal cord-tail preparation in vitro. Br J Pharmacol. 1992 Dec;107(4):1129–1134. doi: 10.1111/j.1476-5381.1992.tb13418.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Eisenberg S. P., Evans R. J., Arend W. P., Verderber E., Brewer M. T., Hannum C. H., Thompson R. C. Primary structure and functional expression from complementary DNA of a human interleukin-1 receptor antagonist. Nature. 1990 Jan 25;343(6256):341–346. doi: 10.1038/343341a0. [DOI] [PubMed] [Google Scholar]
  15. Ferreira S. H., Lorenzetti B. B., Bristow A. F., Poole S. Interleukin-1 beta as a potent hyperalgesic agent antagonized by a tripeptide analogue. Nature. 1988 Aug 25;334(6184):698–700. doi: 10.1038/334698a0. [DOI] [PubMed] [Google Scholar]
  16. Follenfant R. L., Nakamura-Craig M., Henderson B., Higgs G. A. Inhibition by neuropeptides of interleukin-1 beta-induced, prostaglandin-independent hyperalgesia. Br J Pharmacol. 1989 Sep;98(1):41–43. doi: 10.1111/j.1476-5381.1989.tb16860.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Forrest M. J., Eiermann G. J., Meurer R., Walakovits L. A., MacIntyre D. E. The role of CD18 in IL-8 induced dermal and synovial inflammation. Br J Pharmacol. 1992 Jun;106(2):287–294. doi: 10.1111/j.1476-5381.1992.tb14330.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Green P. G., Luo J., Heller P., Levine J. D. Modulation of bradykinin-induced plasma extravasation in the rat knee joint by sympathetic co-transmitters. Neuroscience. 1993 Jan;52(2):451–458. doi: 10.1016/0306-4522(93)90171-b. [DOI] [PubMed] [Google Scholar]
  19. Haley J. E., Dickenson A. H., Schachter M. Electrophysiological evidence for a role of bradykinin in chemical nociception in the rat. Neurosci Lett. 1989 Feb 13;97(1-2):198–202. doi: 10.1016/0304-3940(89)90163-8. [DOI] [PubMed] [Google Scholar]
  20. Heapy C. G., Shaw J. S., Farmer S. C. Differential sensitivity of antinociceptive assays to the bradykinin antagonist Hoe 140. Br J Pharmacol. 1993 Jan;108(1):209–213. doi: 10.1111/j.1476-5381.1993.tb13464.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hirano T., Matsuda T., Turner M., Miyasaka N., Buchan G., Tang B., Sato K., Shimizu M., Maini R., Feldmann M. Excessive production of interleukin 6/B cell stimulatory factor-2 in rheumatoid arthritis. Eur J Immunol. 1988 Nov;18(11):1797–1801. doi: 10.1002/eji.1830181122. [DOI] [PubMed] [Google Scholar]
  22. Lerner U. H., Brunius G., Modeer T. On the signal transducing mechanisms involved in the synergistic interaction between interleukin-1 and bradykinin on prostaglandin biosynthesis in human gingival fibroblasts. Biosci Rep. 1992 Aug;12(4):263–271. doi: 10.1007/BF01122798. [DOI] [PubMed] [Google Scholar]
  23. Lerner U. H., Modéer T. Bradykinin B1 and B2 receptor agonists synergistically potentiate interleukin-1-induced prostaglandin biosynthesis in human gingival fibroblasts. Inflammation. 1991 Dec;15(6):427–436. doi: 10.1007/BF00923340. [DOI] [PubMed] [Google Scholar]
  24. McFadden R. G., Vickers K. E. Bradykinin augments the in vitro migration of nonsensitized lymphocytes. Clin Invest Med. 1989 Aug;12(4):247–253. [PubMed] [Google Scholar]
  25. Perkins M. N., Campbell E., Dray A. Antinociceptive activity of the bradykinin B1 and B2 receptor antagonists, des-Arg9, [Leu8]-BK and HOE 140, in two models of persistent hyperalgesia in the rat. Pain. 1993 May;53(2):191–197. doi: 10.1016/0304-3959(93)90080-9. [DOI] [PubMed] [Google Scholar]
  26. Petitclerc E., Abel S., deBlois D., Poubelle P. E., Marceau F. Effects of interleukin-1 receptor antagonist on three types of responses to interleukin-1 in rabbit isolated blood vessels. J Cardiovasc Pharmacol. 1992 May;19(5):821–829. [PubMed] [Google Scholar]
  27. Regoli D., Marceau F., Barabé J. De novo formation of vascular receptors for bradykinin. Can J Physiol Pharmacol. 1978 Aug;56(4):674–677. doi: 10.1139/y78-109. [DOI] [PubMed] [Google Scholar]
  28. Remick D. G., DeForge L. E., Sullivan J. F., Showell H. J. Profile of cytokines in synovial fluid specimens from patients with arthritis. Interleukin 8 (IL-8) and IL-6 correlate with inflammatory arthritides. Immunol Invest. 1992 Jul;21(4):321–327. doi: 10.3109/08820139209069371. [DOI] [PubMed] [Google Scholar]
  29. Salmon J. A., Simmons P. M., Moncada S. The effects of BW755C and other anti-inflammatory drugs on eicosanoid concentrations and leukocyte accumulation in experimentally-induced acute inflammation. J Pharm Pharmacol. 1983 Dec;35(12):808–813. doi: 10.1111/j.2042-7158.1983.tb02901.x. [DOI] [PubMed] [Google Scholar]
  30. Siebeck M., Whalley E. T., Hoffmann H., Weipert J., Fritz H. The hypotensive response to des-Arg9-bradykinin increases during E. coli septicemia in the pig. Adv Exp Med Biol. 1989;247B:389–393. doi: 10.1007/978-1-4615-9546-5_64. [DOI] [PubMed] [Google Scholar]
  31. Steranka L. R., Manning D. C., DeHaas C. J., Ferkany J. W., Borosky S. A., Connor J. R., Vavrek R. J., Stewart J. M., Snyder S. H. Bradykinin as a pain mediator: receptors are localized to sensory neurons, and antagonists have analgesic actions. Proc Natl Acad Sci U S A. 1988 May;85(9):3245–3249. doi: 10.1073/pnas.85.9.3245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Tiffany C. W., Burch R. M. Bradykinin stimulates tumor necrosis factor and interleukin-1 release from macrophages. FEBS Lett. 1989 Apr 24;247(2):189–192. doi: 10.1016/0014-5793(89)81331-6. [DOI] [PubMed] [Google Scholar]
  33. Wirth K. J., Wiemer G., Schölkens B. A. DesArg10[Hoe 140] is a potent B1 bradykinin antagonist. Agents Actions Suppl. 1992;38(Pt 2):406–413. [PubMed] [Google Scholar]
  34. Wirth K., Hock F. J., Albus U., Linz W., Alpermann H. G., Anagnostopoulos H., Henk S., Breipohl G., König W., Knolle J. Hoe 140 a new potent and long acting bradykinin-antagonist: in vivo studies. Br J Pharmacol. 1991 Mar;102(3):774–777. doi: 10.1111/j.1476-5381.1991.tb12249.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Yocum D. E., Esparza L., Dubry S., Benjamin J. B., Volz R., Scuderi P. Characteristics of tumor necrosis factor production in rheumatoid arthritis. Cell Immunol. 1989 Aug;122(1):131–145. doi: 10.1016/0008-8749(89)90154-8. [DOI] [PubMed] [Google Scholar]
  36. Zini J. M., Schmaier A. H., Cines D. B. Bradykinin regulates the expression of kininogen binding sites on endothelial cells. Blood. 1993 Jun 1;81(11):2936–2946. [PubMed] [Google Scholar]
  37. deBlois D., Bouthillier J., Marceau F. Pharmacological modulation of the up-regulated responses to des-Arg9-bradykinin in vivo and in vitro. Immunopharmacology. 1989 May-Jun;17(3):187–198. doi: 10.1016/0162-3109(89)90047-7. [DOI] [PubMed] [Google Scholar]

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