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The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1985 Jun;75(6):2038–2046. doi: 10.1172/JCI111923

Sympathetic modulation of biochemical and physiological response to immune degranulation in canine bronchial airways in vivo.

E R Garrity, N P Stimler, N M Munoz, J Tallet, A C David, A R Leff
PMCID: PMC425565  PMID: 2409114

Abstract

The effect of sympathetic stimulation on bronchial smooth muscle contractile response after mast cell degranulation with Ascaris suum antigen was studied in 36 natively allergic dogs in situ. Bronchial smooth muscle response was measured isometrically in a single right middle lobe bronchus. A dose of antigen causing maximal release of mediator was administered to the bronchus through the bronchial arterial circulation. Serial plasma histamine concentrations were determined at 15-s intervals after intra-arterial (i.a.) administration of antigen. Samples of blood were obtained simultaneously from right heart and femoral artery, and arteriovenous difference (AVd) in histamine concentration across the bronchus was determined during mast cell degranulation. In nine dogs showing bronchial mast cell degranulation to antigen challenge, bronchial smooth muscle contraction was 22.3 +/- 2.95 g and the mean AVd in histamine concentration across the bronchus was 188 +/- 41.5 ng/ml. Six other dogs having muscarinic blockade with 0.75-1.0 mg/kg intravenous atropine were given i.a. antigen after 1 min of steady-state sympathetic stimulation with intravenous 1,1-dimethyl-4-phenylpiperazinium iodide (DMPP). Sympathetic stimulation during Ascaris suum antigen challenge caused complete inhibition of bronchial smooth muscle contractile response to i.a. antigen (P less than 0.001), and a significant AVd in histamine concentration across the bronchus (9.8 +/- 16.0 ng/ml; P less than 0.01 vs. control) was not detected. Peak plasma histamine concentration in control dogs was 1,138 +/- 237 ng/ml vs. 310 +/- 135 ng/ml in animals receiving sympathetic stimulation (P less than 0.01). In four dogs undergoing systemic anaphylaxis to i.v. antigen, subsequent sympathetic stimulation with i.v. DMPP reduced bronchomotor tone to approximately 70% of base-line control. Exogenously induced sympathetic stimulation can substantially inhibit systemic mast cell degranulation to Ascaris suum antigen in allergic dogs. Maximal stimulation of the sympathetic nervous system causes substantial inhibition of respiratory mast cell secretion of histamine and bronchial smooth muscle contraction to circulating mediator.

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Selected References

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  1. Barnett D. B., Chesrown S. E., Zbinden A. F., Nisam M., Reed B. R., Bourne H. R., Melmon K. L., Gold W. M. Cyclic AMP and cyclic GMP in canine peripheral lung: regulation in vivo. Am Rev Respir Dis. 1978 Oct;118(4):723–733. doi: 10.1164/arrd.1978.118.4.723. [DOI] [PubMed] [Google Scholar]
  2. Beaven M. A., Jacobsen S., Horáková Z. Modification of the enzymatic isotopic assay of histamine and its application to measurement of histamine in tissues, serum and urine. Clin Chim Acta. 1972 Mar;37:91–103. doi: 10.1016/0009-8981(72)90419-6. [DOI] [PubMed] [Google Scholar]
  3. Brown J. K., Leff A. R., Frey M. J., Reed B. R., Lazarus S. C., Shields R., Gold W. M. Characterization of tracheal mast cell reactions in vivo. Inhibition by a beta-adrenergic agonist. Am Rev Respir Dis. 1982 Nov;126(5):842–848. doi: 10.1164/arrd.1982.126.5.842. [DOI] [PubMed] [Google Scholar]
  4. Chiesa A., Dain D., Meyers G. L., Kessler G. F., Gold W. M. Histamine release during antigen inhalation in experimental asthma in dogs. Am Rev Respir Dis. 1975 Feb;111(2):148–156. doi: 10.1164/arrd.1975.111.2.148. [DOI] [PubMed] [Google Scholar]
  5. Drazen J. M. Adrenergic influences on histamine-mediated bronchoconstriction in the guinea pig. J Appl Physiol Respir Environ Exerc Physiol. 1978 Mar;44(3):340–345. doi: 10.1152/jappl.1978.44.3.340. [DOI] [PubMed] [Google Scholar]
  6. Drazen J. M., Schneider M. W. Comparative responses of tracheal spirals and parenchymal strips to histamine and carbachol in vitro. J Clin Invest. 1978 Jun;61(6):1441–1447. doi: 10.1172/JCI109063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Evans G. H., Nies A. S., Shand D. G. The disposition of propranolol. 3. Decreased half-life and volume of distribution as a result of plasma binding in man, monkey, dog and rat. J Pharmacol Exp Ther. 1973 Jul;186(1):114–122. [PubMed] [Google Scholar]
  8. Garrity E. R., Stimler N. P., Munoz N. M., Fried R., Leff A. R. Response of bronchial smooth muscle to mast cell degranulation in situ. J Appl Physiol Respir Environ Exerc Physiol. 1983 Dec;55(6):1803–1810. doi: 10.1152/jappl.1983.55.6.1803. [DOI] [PubMed] [Google Scholar]
  9. Gold W. M., Meyers G. L., Dain D. S., Miller R. L., Bourne H. R. Changes in airway mast cells and histamine caused by antigen aerosol in allergic dogs. J Appl Physiol Respir Environ Exerc Physiol. 1977 Aug;43(2):271–275. doi: 10.1152/jappl.1977.43.2.271. [DOI] [PubMed] [Google Scholar]
  10. Guerzon G. M., Paré P. D., Michoud M. C., Hogg J. C. The number and distribution of mast cells in monkey lungs. Am Rev Respir Dis. 1979 Jan;119(1):59–66. doi: 10.1164/arrd.1979.119.1.59. [DOI] [PubMed] [Google Scholar]
  11. Hendrix S. G., Munoz N. M., Leff A. R. Physiological and pharmacological response of canine bronchial smooth muscle in situ. J Appl Physiol Respir Environ Exerc Physiol. 1983 Jan;54(1):215–224. doi: 10.1152/jappl.1983.54.1.215. [DOI] [PubMed] [Google Scholar]
  12. Hirshman C. A., Downes H., Leon D. A., Peters J. E. Basenji-greyhound dog model of asthma: pulmonary responses after beta-adrenergic blockade. J Appl Physiol Respir Environ Exerc Physiol. 1981 Dec;51(6):1423–1427. doi: 10.1152/jappl.1981.51.6.1423. [DOI] [PubMed] [Google Scholar]
  13. Kaliner M. Human lung tissue and anaphylaxis. I. The role of cyclic GMP as a modulator of the immunologically induced secretory process. J Allergy Clin Immunol. 1977 Sep;60(3):204–211. doi: 10.1016/0091-6749(77)90125-7. [DOI] [PubMed] [Google Scholar]
  14. Kaliner M., Orange R. P., Austen K. F. Immunological release of histamine and slow reacting substance of anaphylaxis from human lung. J Exp Med. 1972 Sep 1;136(3):556–567. doi: 10.1084/jem.136.3.556. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lazarus S. C., Chesrown S. E., Frey M. J., Reed B. R., Mjörndal T. O., Gold W. M. Experimental canine anaphylaxis: cyclic nucleotides, histamine, and lung function. J Appl Physiol Respir Environ Exerc Physiol. 1979 May;46(5):919–926. doi: 10.1152/jappl.1979.46.5.919. [DOI] [PubMed] [Google Scholar]
  16. Leff A. R., Brown J. K., Frey M., Reed B., Gold W. M. Biochemical and physiological effects of compound 48/80 on canine trachea in vivo. J Appl Physiol Respir Environ Exerc Physiol. 1983 Mar;54(3):720–729. doi: 10.1152/jappl.1983.54.3.720. [DOI] [PubMed] [Google Scholar]
  17. Leff A. R., Munoz N. M. Evidence for two subtypes of alpha adrenergic receptors in canine airway smooth muscle. J Pharmacol Exp Ther. 1981 May;217(2):530–535. [PubMed] [Google Scholar]
  18. Leff A. R., Munoz N. M., Hendrix S. G. Comparative distribution of smooth muscle postsynaptic contractile responses in canine trachea and bronchus in vivo. J Pharmacol Exp Ther. 1983 Feb;224(2):259–264. [PubMed] [Google Scholar]
  19. Leff A. R., Munoz N. M., Hendrix S. G. Sympathetic inhibition of histamine-induced contraction of canine trachealis in vivo. J Appl Physiol Respir Environ Exerc Physiol. 1982 Jul;53(1):21–29. doi: 10.1152/jappl.1982.53.1.21. [DOI] [PubMed] [Google Scholar]
  20. Leff A. R., Munoz N. M. Selective autonomic stimulation of canine trachealis with dimethylphenylpiperazinium. J Appl Physiol Respir Environ Exerc Physiol. 1981 Aug;51(2):428–437. doi: 10.1152/jappl.1981.51.2.428. [DOI] [PubMed] [Google Scholar]
  21. Nisam M. R., Zbinden A., Chesrown S., Barnett D., Gold W. M. Distribution oand pharmacological release of histamine in canine lung in vivo. J Appl Physiol Respir Environ Exerc Physiol. 1978 Mar;44(3):455–463. doi: 10.1152/jappl.1978.44.3.455. [DOI] [PubMed] [Google Scholar]
  22. Orange R. P., Austen W. G., Austen K. F. Immunological release of histamine and slow-reacting substance of anaphylaxis from human lung. I. Modulation by agents influencing cellular levels of cyclic 3',5'-adenosine monophosphate. J Exp Med. 1971 Sep 1;134(3 Pt 2):136s–148s. [PubMed] [Google Scholar]
  23. Snyder S. H., Baldessarini R. J., Axelrod J. A sensitive and specific enzymatic isotopic assay for tissue histamine. J Pharmacol Exp Ther. 1966 Sep;153(3):544–549. [PubMed] [Google Scholar]
  24. Sullivan T. J., Parker K. L., Eisen S. A., Parker C. W. Modulation of cyclic AMP in purified rat mast cells. II. Studies on the relationship between intracellular cyclic AMP concentrations and histamine release. J Immunol. 1975 May;114(5):1480–1485. [PubMed] [Google Scholar]

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