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. 1992 Apr;105(4):792–798. doi: 10.1111/j.1476-5381.1992.tb09059.x

Formoterol and salbutamol inhibit bradykinin- and histamine-induced airway microvascular leakage in guinea-pig.

C Advenier 1, Y Qian 1, J D Koune 1, M Molimard 1, M L Candenas 1, E Naline 1
PMCID: PMC1908703  PMID: 1354535

Abstract

1. The effects of the beta 2-adrenoceptor agonists, salbutamol and formoterol, on the increase of microvascular permeability induced by histamine or bradykinin in guinea-pig airways have been studied in vivo. Extravasation of intravenously injected Evans blue dye was used as an index of permeability. The effects of salbutamol and formoterol on the increase in pulmonary airway resistance induced by histamine or bradykinin have also been studied. 2. The increase in pulmonary airway resistance induced by histamine or bradykinin was totally inhibited by salbutamol and formoterol. The ED50 of the two mediators were 0.59 +/- 0.21 (n = 5) and 0.20 +/- 0.14 (n = 5) micrograms kg-1 respectively for salbutamol, and 0.13 +/- 0.12 (n = 6) and 0.02 +/- 0.01 (n = 6) micrograms kg-1 respectively for formoterol. 3. Salbutamol (10 and 30 micrograms kg-1) and formoterol (1 and 10 micrograms kg-1) inhibited the increase of microvascular permeability induced by histamine (30 micrograms kg-1) in the guinea-pig airways. The inhibitory effect was predominant in the trachea and the main bronchi, with a maximum inhibition of 20 to 50%. The two drugs had little or no inhibitory effect on the other structures studied, viz. nasal mucosa, larynx, proximal and distal intrapulmonary airways. 4. Salbutamol and formoterol (1 and 10 micrograms kg-1) abolished the increase in microvascular permeability induced by bradykinin (0.3 micrograms kg-1). This inhibitory effect of two beta-adrenoceptor stimulants was predominant in the trachea and the nasal mucosa where it was observed with 1 microgram kg-1 of the beta-adrenoceptor agonists.(ABSTRACT TRUNCATED AT 250 WORDS)

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Selected References

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  1. AMDUR M. O., MEAD J. Mechanics of respiration in unanesthetized guinea pigs. Am J Physiol. 1958 Feb;192(2):364–368. doi: 10.1152/ajplegacy.1958.192.2.364. [DOI] [PubMed] [Google Scholar]
  2. Abe K., Watanabe N., Kumagai N., Mouri T., Seki T., Yoshinaga K. Circulating kinin in patients with bronchial asthma. Experientia. 1967 Aug 15;23(8):626–627. doi: 10.1007/BF02144161. [DOI] [PubMed] [Google Scholar]
  3. Advenier C., Boissier J. R., Giudicelli J. F. Comparative study of six -adrenoceptive antagonists on airway resistance and heart rate in the guinea-pig. Br J Pharmacol. 1972 Apr;44(4):642–650. doi: 10.1111/j.1476-5381.1972.tb07304.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Andrews P. V., Helme R. D., Thomas K. L. NK-1 receptor mediation of neurogenic plasma extravasation in rat skin. Br J Pharmacol. 1989 Aug;97(4):1232–1238. doi: 10.1111/j.1476-5381.1989.tb12583.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Barnes P. J., Chung K. F., Page C. P. Inflammatory mediators and asthma. Pharmacol Rev. 1988 Mar;40(1):49–84. [PubMed] [Google Scholar]
  6. Baumgarten C. R., Togias A. G., Naclerio R. M., Lichtenstein L. M., Norman P. S., Proud D. Influx of kininogens into nasal secretions after antigen challenge of allergic individuals. J Clin Invest. 1985 Jul;76(1):191–197. doi: 10.1172/JCI111945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Becker A. B., Simons F. E. Formoterol, a new long-acting selective beta 2-adrenergic receptor agonist: double-blind comparison with salbutamol and placebo in children with asthma. J Allergy Clin Immunol. 1989 Dec;84(6 Pt 1):891–895. doi: 10.1016/0091-6749(89)90385-0. [DOI] [PubMed] [Google Scholar]
  8. Beets J. L., Paul W. Actions of locally administered adrenoceptor agonists on increased plasma protein extravasation and blood flow in guinea-pig skin. Br J Pharmacol. 1980 Nov;70(3):461–467. doi: 10.1111/j.1476-5381.1980.tb08724.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Belvisi M. G., Rogers D. F., Barnes P. J. Neurogenic plasma extravasation: inhibition by morphine in guinea pig airways in vivo. J Appl Physiol (1985) 1989 Jan;66(1):268–272. doi: 10.1152/jappl.1989.66.1.268. [DOI] [PubMed] [Google Scholar]
  10. Boschetto P., Roberts N. M., Rogers D. F., Barnes P. J. Effect of antiasthma drugs on microvascular leakage in guinea pig airways. Am Rev Respir Dis. 1989 Feb;139(2):416–421. doi: 10.1164/ajrccm/139.2.416. [DOI] [PubMed] [Google Scholar]
  11. Christiansen S. C., Proud D., Cochrane C. G. Detection of tissue kallikrein in the bronchoalveolar lavage fluid of asthmatic subjects. J Clin Invest. 1987 Jan;79(1):188–197. doi: 10.1172/JCI112782. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chung K. F., Rogers D. F., Barnes P. J., Evans T. W. The role of increased airway microvascular permeability and plasma exudation in asthma. Eur Respir J. 1990 Mar;3(3):329–337. [PubMed] [Google Scholar]
  13. Davis B., Roberts A. M., Coleridge H. M., Coleridge J. C. Reflex tracheal gland secretion evoked by stimulation of bronchial C-fibers in dogs. J Appl Physiol Respir Environ Exerc Physiol. 1982 Oct;53(4):985–991. doi: 10.1152/jappl.1982.53.4.985. [DOI] [PubMed] [Google Scholar]
  14. Dixon C. M., Barnes P. J. Bradykinin-induced bronchoconstriction: inhibition by nedocromil sodium and sodium cromoglycate. Br J Clin Pharmacol. 1989 Jun;27(6):831–836. doi: 10.1111/j.1365-2125.1989.tb03446.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dixon M., Jackson D. M., Richards I. M. The action of sodium cromoglycate on 'C' fibre endings in the dog lung. Br J Pharmacol. 1980 Sep;70(1):11–13. doi: 10.1111/j.1476-5381.1980.tb10898.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Erjefält I., Persson C. G. Inflammatory passage of plasma macromolecules into airway wall and lumen. Pulm Pharmacol. 1989;2(2):93–102. doi: 10.1016/0952-0600(89)90030-6. [DOI] [PubMed] [Google Scholar]
  17. Evans T. W., Rogers D. F., Aursudkij B., Chung K. F., Barnes P. J. Inflammatory mediators involved in antigen-induced airway microvascular leakage in guinea pigs. Am Rev Respir Dis. 1988 Aug;138(2):395–399. doi: 10.1164/ajrccm/138.2.395. [DOI] [PubMed] [Google Scholar]
  18. Frossard N., Barnes P. J. Mu-opioid receptors modulate non-cholinergic constrictor nerves in guinea-pig airways. Eur J Pharmacol. 1987 Sep 23;141(3):519–522. doi: 10.1016/0014-2999(87)90578-4. [DOI] [PubMed] [Google Scholar]
  19. Fuller R. W., Dixon C. M., Cuss F. M., Barnes P. J. Bradykinin-induced bronchoconstriction in humans. Mode of action. Am Rev Respir Dis. 1987 Jan;135(1):176–180. doi: 10.1164/arrd.1987.135.1.176. [DOI] [PubMed] [Google Scholar]
  20. Geppetti P., Maggi C. A., Perretti F., Frilli S., Manzini S. Simultaneous release by bradykinin of substance P- and calcitonin gene-related peptide immunoreactivities from capsaicin-sensitive structures in guinea-pig heart. Br J Pharmacol. 1988 Jun;94(2):288–290. doi: 10.1111/j.1476-5381.1988.tb11528.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ichinose M., Barnes P. J. Bradykinin-induced airway microvascular leakage and bronchoconstriction are mediated via a bradykinin B2 receptor. Am Rev Respir Dis. 1990 Nov;142(5):1104–1107. doi: 10.1164/ajrccm/142.5.1104. [DOI] [PubMed] [Google Scholar]
  22. Ichinose M., Barnes P. J. The effect of peptidase inhibitors on bradykinin-induced bronchoconstriction in guinea-pigs in vivo. Br J Pharmacol. 1990 Sep;101(1):77–80. doi: 10.1111/j.1476-5381.1990.tb12092.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ichinose M., Belvisi M. G., Barnes P. J. Bradykinin-induced bronchoconstriction in guinea pig in vivo: role of neural mechanisms. J Pharmacol Exp Ther. 1990 May;253(2):594–599. [PubMed] [Google Scholar]
  24. Jin L. S., Seeds E., Page C. P., Schachter M. Inhibition of bradykinin-induced bronchoconstriction in the guinea-pig by a synthetic B2 receptor antagonist. Br J Pharmacol. 1989 Jun;97(2):598–602. doi: 10.1111/j.1476-5381.1989.tb11991.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kaufman M. P., Coleridge H. M., Coleridge J. C., Baker D. G. Bradykinin stimulates afferent vagal C-fibers in intrapulmonary airways of dogs. J Appl Physiol Respir Environ Exerc Physiol. 1980 Mar;48(3):511–517. doi: 10.1152/jappl.1980.48.3.511. [DOI] [PubMed] [Google Scholar]
  26. Laitinen L. A., Laitinen A., Widdicombe J. Effects of inflammatory and other mediators on airway vascular beds. Am Rev Respir Dis. 1987 Jun;135(6 Pt 2):S67–S70. doi: 10.1164/arrd.1987.135.6P2.S67. [DOI] [PubMed] [Google Scholar]
  27. Lyon R. A., Weisshaar P. S., Phipps R. J. Identification and characterization of B2 bradykinin receptors in sheep nasal turbinate membranes. Pulm Pharmacol. 1990;3(4):209–214. doi: 10.1016/0952-0600(90)90019-f. [DOI] [PubMed] [Google Scholar]
  28. Löfdahl C. G., Svedmyr N. Formoterol fumarate, a new beta 2-adrenoceptor agonist. Acute studies of selectivity and duration of effect after inhaled and oral administration. Allergy. 1989 May;44(4):264–271. doi: 10.1111/j.1398-9995.1989.tb01068.x. [DOI] [PubMed] [Google Scholar]
  29. Malo J. L., Cartier A., Trudeau C., Ghezzo H., Gontovnick L. Formoterol, a new inhaled beta-2 adrenergic agonist, has a longer blocking effect than albuterol on hyperventilation-induced bronchoconstriction. Am Rev Respir Dis. 1990 Nov;142(5):1147–1152. doi: 10.1164/ajrccm/142.5.1147. [DOI] [PubMed] [Google Scholar]
  30. Naclerio R. M., Proud D., Lichtenstein L. M., Kagey-Sobotka A., Hendley J. O., Sorrentino J., Gwaltney J. M. Kinins are generated during experimental rhinovirus colds. J Infect Dis. 1988 Jan;157(1):133–142. doi: 10.1093/infdis/157.1.133. [DOI] [PubMed] [Google Scholar]
  31. Newball H. H., Keiser H. R., Pisano J. J. Bradykinin and human airways. Respir Physiol. 1975 Jul;24(2):139–146. doi: 10.1016/0034-5687(75)90108-5. [DOI] [PubMed] [Google Scholar]
  32. Norris A. A., Leeson M. E., Jackson D. M., Holroyde M. C. Modulation of neurogenic inflammation in rat trachea. Pulm Pharmacol. 1990;3(4):180–184. doi: 10.1016/0952-0600(90)90014-a. [DOI] [PubMed] [Google Scholar]
  33. Persson C. G., Erjefält I. Terbutaline and adrenaline inhibit leakage of fluid and protein in guinea-pig lung. Eur J Pharmacol. 1979 Apr 15;55(2):199–201. doi: 10.1016/0014-2999(79)90392-3. [DOI] [PubMed] [Google Scholar]
  34. Persson C. G. Leakage of macromolecules from the tracheobronchial microcirculation. Am Rev Respir Dis. 1987 Jun;135(6 Pt 2):S71–S75. doi: 10.1164/arrd.1987.135.6P2.S71. [DOI] [PubMed] [Google Scholar]
  35. Polosa R., Holgate S. T. Comparative airway response to inhaled bradykinin, kallidin, and [des-Arg9]bradykinin in normal and asthmatic subjects. Am Rev Respir Dis. 1990 Dec;142(6 Pt 1):1367–1371. doi: 10.1164/ajrccm/142.6_Pt_1.1367. [DOI] [PubMed] [Google Scholar]
  36. Polosa R., Lai C. K., Robinson C., Holgate S. T. The influence of cyclooxygenase inhibition on the loss of bronchoconstrictor response to repeated bradykinin challenge in asthma. Eur Respir J. 1990 Sep;3(8):914–921. [PubMed] [Google Scholar]
  37. Proud D., Reynolds C. J., Lacapra S., Kagey-Sobotka A., Lichtenstein L. M., Naclerio R. M. Nasal provocation with bradykinin induces symptoms of rhinitis and a sore throat. Am Rev Respir Dis. 1988 Mar;137(3):613–616. doi: 10.1164/ajrccm/137.3.613. [DOI] [PubMed] [Google Scholar]
  38. Proud D., Togias A., Naclerio R. M., Crush S. A., Norman P. S., Lichtenstein L. M. Kinins are generated in vivo following nasal airway challenge of allergic individuals with allergen. J Clin Invest. 1983 Nov;72(5):1678–1685. doi: 10.1172/JCI111127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Regoli D., Barabé J. Pharmacology of bradykinin and related kinins. Pharmacol Rev. 1980 Mar;32(1):1–46. [PubMed] [Google Scholar]
  40. Rhoden K. J., Meldrum L. A., Barnes P. J. Inhibition of cholinergic neurotransmission in human airways by beta 2-adrenoceptors. J Appl Physiol (1985) 1988 Aug;65(2):700–705. doi: 10.1152/jappl.1988.65.2.700. [DOI] [PubMed] [Google Scholar]
  41. Rogers D. F., Belvisi M. G., Aursudkij B., Evans T. W., Barnes P. J. Effects and interactions of sensory neuropeptides on airway microvascular leakage in guinea-pigs. Br J Pharmacol. 1988 Dec;95(4):1109–1116. doi: 10.1111/j.1476-5381.1988.tb11745.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Rogers D. F., Boschetto P., Barnes P. J. Plasma exudation. Correlation between Evans blue dye and radiolabeled albumin in guinea pig airways in vivo. J Pharmacol Methods. 1989 Jul;21(4):309–315. doi: 10.1016/0160-5402(89)90068-5. [DOI] [PubMed] [Google Scholar]
  43. Rogers D. F., Dijk S., Barnes P. J. Bradykinin-induced plasma exudation in guinea-pig airways: involvement of platelet activating factor. Br J Pharmacol. 1990 Nov;101(3):739–745. doi: 10.1111/j.1476-5381.1990.tb14150.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Saria A., Lundberg J. M., Skofitsch G., Lembeck F. Vascular protein linkage in various tissue induced by substance P, capsaicin, bradykinin, serotonin, histamine and by antigen challenge. Naunyn Schmiedebergs Arch Pharmacol. 1983 Nov;324(3):212–218. doi: 10.1007/BF00503897. [DOI] [PubMed] [Google Scholar]
  45. Saria A., Martling C. R., Yan Z., Theodorsson-Norheim E., Gamse R., Lundberg J. M. Release of multiple tachykinins from capsaicin-sensitive sensory nerves in the lung by bradykinin, histamine, dimethylphenyl piperazinium, and vagal nerve stimulation. Am Rev Respir Dis. 1988 Jun;137(6):1330–1335. doi: 10.1164/ajrccm/137.6.1330. [DOI] [PubMed] [Google Scholar]
  46. Simonsson B. G., Skoogh B. E., Bergh N. P., Andersson R., Svedmyr N. In vivo and in vitro effect of bradykinin on bronchial motor tone in normal subjects and patients with airways obstruction. Respiration. 1973;30(4):378–388. doi: 10.1159/000193051. [DOI] [PubMed] [Google Scholar]
  47. Tokuyama K., Lötvall J. O., Löfdahl C. G., Barnes P. J., Chung K. F. Inhaled formoterol inhibits histamine-induced airflow obstruction and airway microvascular leakage. Eur J Pharmacol. 1991 Jan 25;193(1):35–39. doi: 10.1016/0014-2999(91)90197-x. [DOI] [PubMed] [Google Scholar]
  48. Udaka K., Takeuchi Y., Movat H. Z. Simple method for quantitation of enhanced vascular permeability. Proc Soc Exp Biol Med. 1970 Apr;133(4):1384–1387. doi: 10.3181/00379727-133-34695. [DOI] [PubMed] [Google Scholar]
  49. Ueda N., Muramatsu I., Fujiwara M. Capsaicin and bradykinin-induced substance P-ergic responses in the iris sphincter muscle of the rabbit. J Pharmacol Exp Ther. 1984 Aug;230(2):469–473. [PubMed] [Google Scholar]
  50. Vermeire P. A., Vanhoutte P. M. Inhibitory effects of catecholamine in isolated canine bronchial smooth muscle. J Appl Physiol Respir Environ Exerc Physiol. 1979 Apr;46(4):787–791. doi: 10.1152/jappl.1979.46.4.787. [DOI] [PubMed] [Google Scholar]
  51. Wallin A., Melander B., Rosenhall L., Sandström T., Wåhlander L. Formoterol, a new long acting beta 2 agonist for inhalation twice daily, compared with salbutamol in the treatment of asthma. Thorax. 1990 Apr;45(4):259–261. doi: 10.1136/thx.45.4.259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Williams T. J. Oedema and vasodilatation in inflammation: the relevance of prostaglandins. Postgrad Med J. 1977 Nov;53(625):660–662. doi: 10.1136/pgmj.53.625.660. [DOI] [PMC free article] [PubMed] [Google Scholar]

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