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The Journal of Neuroscience, May 15, 1999, 19(10):4082-4089

Sex Steroid Regulation of the Inflammatory Response: Sympathoadrenal Dependence in the Female Rat

Paul G. Green^{1, 4}, Solbritt Rantapää Dahlqvist⁵, William M. Isenberg^{2, 4}, Holly J. Strausbaugh^{1, 4}, Frederick J.-P. Miao^{1, 4}, and Jon D. Levine^{1, 3, 4}

Departments of ¹ Oral and Maxillofacial Surgery, ² Obstetrics Gynecology and Reproductive Sciences and ³ Medicine, ⁴ Division of Neuroscience and National Institutes of Health Pain Center (UCSF), University of California San Francisco, San Francisco, California 94143-0440, and ⁵ Department of Rheumatology, Umeå University Hospital, SE-901 85, Sweden

To investigate the role of sex steroids in sex differences in the response of rats to the potent inflammatory mediator bradykinin (BK), we evaluated the effect of sex steroid manipulation on the magnitude of BK-induced synovial plasma extravasation (PE). The magnitude of BK-induced PE is markedly less in females. Ovariectomy of female rats increased BK-induced PE, and administration of 17-estradiol to ovariectomized female rats reconstituted the female phenotype. Castration in male rats decreased BK-induced PE, and administration of testosterone or its nonmetabolizable analog dihydrotestosterone reconstituted the male phenotype. The results of these experiments strongly support the role of both male and female sex steroids in sex differences in the inflammatory response.

Because the stress axes are sexually dimorphic and are important in the regulation of the inflammatory response, we evaluated the contribution of the hypothalamic-pituitary-adrenal and the sympathoadrenal axes to sex differences in BK-induced PE. Neither hypophysectomy nor inhibition of corticosteroid synthesis affected BK-induced PE in female or male rats. Adrenal denervation in females produced the same magnitude increase in BK-induced PE as adrenalectomy or ovariectomy, suggesting that the adrenal medullary factor(s) in females may account for the female sex steroid effect on BK-induced PE. Furthermore, we have demonstrated that in female but not male rats, estrogen receptor  immunoreactivity is present on medullary but not cortical cells in the adrenal gland. These data suggest that regulation of the inflammatory response by female sex steroids is strongly dependent on the sympathoadrenal axis, possibly by its action on estrogen receptors on adrenal medullary cells.

Key words: plasma extravasation; inflammation; sex differences; estrogen; testosterone; estrogen receptor; sympathoadrenal axis; hypothalamic-pituitary adrenal axis

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Copyright © 1999 Society for Neuroscience  0270-6474/99/19104082-08$05.00/0

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