Sympathoadrenal‐dependent sexually dimorphic effect of nonhabituating stress on in vivo neutrophil recruitment in the rat

1 Since stress both activates the sympathoadrenal axis and profoundly affects inflammation and inflammatory diseases, many of which are sexually dimorphic, we tested whether the effect of stress on neutrophil recruitment, a primary component of the acute inflammatory response, is sexually dimorphic....

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Veröffentlicht in:British journal of pharmacology 2005-08, Vol.145 (7), p.872-879
Hauptverfasser: Barker, Laura A, Dazin, Paul F, Levine, Jon D, Green, Paul G
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Green, Paul G
description 1 Since stress both activates the sympathoadrenal axis and profoundly affects inflammation and inflammatory diseases, many of which are sexually dimorphic, we tested whether the effect of stress on neutrophil recruitment, a primary component of the acute inflammatory response, is sexually dimorphic. 2 The effect of intermittent sound (over 4 days), a nonhabituating stress, on lipopolysaccharide (LPS)‐induced recruitment of neutrophils was evaluated in vivo in the rat air pouch model. At 24 h following the last stress exposure, LPS‐induced neutrophil recruitment was enhanced in male rats, but not in females. 3 When gonadectomized prepubertally and tested as adults, stress significantly inhibited the magnitude of LPS‐induced neutrophil recruitment in males, while it still had no effect in gonadectomized females. In males, following adrenal denervation, the increase in LPS‐induced neutrophil recruitment produced by stress was prevented. Since these data suggest that the effect of stress is dependent on the sympathoadrenal axis, we tested the hypothesis that catecholamines mediate the stress effects. 4 In male rats, the effect of stress on LPS‐induced neutrophil recruitment was significantly attenuated by continuous administration of the β‐adrenergic receptor antagonist, propranolol (4 mg kg−1 day−1), during sound stress exposure, and administration of isoproterenol (10 nmoles, i.v.) significantly increased neutrophil recruitment in males, an effect that was qualitatively and quantitatively similar to the effect of stress. Propranolol significantly increased neutrophil recruitment in nonstressed female rats, but did not significantly affect neutrophil recruitment in stressed females. 5 These findings indicate a marked male sex hormone‐dependent sexual dimorphism in the sympathoadrenal‐dependent effect of stress on neutrophil migration, a primary component of the inflammatory response, and suggest that the sympathoadrenal axis contributes to this effect via release of epinephrine. British Journal of Pharmacology (2005) 145, 872–879. doi:10.1038/sj.bjp.0706257
doi_str_mv 10.1038/sj.bjp.0706257
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At 24 h following the last stress exposure, LPS‐induced neutrophil recruitment was enhanced in male rats, but not in females. 3 When gonadectomized prepubertally and tested as adults, stress significantly inhibited the magnitude of LPS‐induced neutrophil recruitment in males, while it still had no effect in gonadectomized females. In males, following adrenal denervation, the increase in LPS‐induced neutrophil recruitment produced by stress was prevented. Since these data suggest that the effect of stress is dependent on the sympathoadrenal axis, we tested the hypothesis that catecholamines mediate the stress effects. 4 In male rats, the effect of stress on LPS‐induced neutrophil recruitment was significantly attenuated by continuous administration of the β‐adrenergic receptor antagonist, propranolol (4 mg kg−1 day−1), during sound stress exposure, and administration of isoproterenol (10 nmoles, i.v.) significantly increased neutrophil recruitment in males, an effect that was qualitatively and quantitatively similar to the effect of stress. Propranolol significantly increased neutrophil recruitment in nonstressed female rats, but did not significantly affect neutrophil recruitment in stressed females. 5 These findings indicate a marked male sex hormone‐dependent sexual dimorphism in the sympathoadrenal‐dependent effect of stress on neutrophil migration, a primary component of the inflammatory response, and suggest that the sympathoadrenal axis contributes to this effect via release of epinephrine. 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At 24 h following the last stress exposure, LPS‐induced neutrophil recruitment was enhanced in male rats, but not in females. 3 When gonadectomized prepubertally and tested as adults, stress significantly inhibited the magnitude of LPS‐induced neutrophil recruitment in males, while it still had no effect in gonadectomized females. In males, following adrenal denervation, the increase in LPS‐induced neutrophil recruitment produced by stress was prevented. Since these data suggest that the effect of stress is dependent on the sympathoadrenal axis, we tested the hypothesis that catecholamines mediate the stress effects. 4 In male rats, the effect of stress on LPS‐induced neutrophil recruitment was significantly attenuated by continuous administration of the β‐adrenergic receptor antagonist, propranolol (4 mg kg−1 day−1), during sound stress exposure, and administration of isoproterenol (10 nmoles, i.v.) significantly increased neutrophil recruitment in males, an effect that was qualitatively and quantitatively similar to the effect of stress. Propranolol significantly increased neutrophil recruitment in nonstressed female rats, but did not significantly affect neutrophil recruitment in stressed females. 5 These findings indicate a marked male sex hormone‐dependent sexual dimorphism in the sympathoadrenal‐dependent effect of stress on neutrophil migration, a primary component of the inflammatory response, and suggest that the sympathoadrenal axis contributes to this effect via release of epinephrine. 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At 24 h following the last stress exposure, LPS‐induced neutrophil recruitment was enhanced in male rats, but not in females. 3 When gonadectomized prepubertally and tested as adults, stress significantly inhibited the magnitude of LPS‐induced neutrophil recruitment in males, while it still had no effect in gonadectomized females. In males, following adrenal denervation, the increase in LPS‐induced neutrophil recruitment produced by stress was prevented. Since these data suggest that the effect of stress is dependent on the sympathoadrenal axis, we tested the hypothesis that catecholamines mediate the stress effects. 4 In male rats, the effect of stress on LPS‐induced neutrophil recruitment was significantly attenuated by continuous administration of the β‐adrenergic receptor antagonist, propranolol (4 mg kg−1 day−1), during sound stress exposure, and administration of isoproterenol (10 nmoles, i.v.) significantly increased neutrophil recruitment in males, an effect that was qualitatively and quantitatively similar to the effect of stress. Propranolol significantly increased neutrophil recruitment in nonstressed female rats, but did not significantly affect neutrophil recruitment in stressed females. 5 These findings indicate a marked male sex hormone‐dependent sexual dimorphism in the sympathoadrenal‐dependent effect of stress on neutrophil migration, a primary component of the inflammatory response, and suggest that the sympathoadrenal axis contributes to this effect via release of epinephrine. British Journal of Pharmacology (2005) 145, 872–879. doi:10.1038/sj.bjp.0706257</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>15912135</pmid><doi>10.1038/sj.bjp.0706257</doi><tpages>8</tpages><oa>free_for_read</oa></addata></record>
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subjects Acoustic Stimulation
Adrenal Glands - immunology
Adrenal Glands - innervation
Adrenal medulla
Adrenergic beta-Agonists - pharmacology
Adrenergic beta-Antagonists - pharmacology
Animals
Biological and medical sciences
Female
Flow Cytometry
Gonadal Steroid Hormones - immunology
Inflammation - chemically induced
Inflammation - immunology
Isoproterenol - pharmacology
Lipopolysaccharides
Male
Medical sciences
Neutrophil Infiltration - drug effects
Neutrophil Infiltration - immunology
neutrophils
Orchiectomy
Ovariectomy
Pharmacology. Drug treatments
Propranolol - administration & dosage
Propranolol - pharmacology
Rats
Rats, Sprague-Dawley
sex differences
Sex Factors
Stress, Physiological - etiology
Stress, Physiological - immunology
Sympathetic Nervous System - drug effects
Sympathetic Nervous System - immunology
β‐adrenergic receptor
title Sympathoadrenal‐dependent sexually dimorphic effect of nonhabituating stress on in vivo neutrophil recruitment in the rat
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