Rapid Inhibitory Effect of Corticosterone on Histamine Release from Rat Peritoneal Mast Cells

Abstract

Glucocorticoids are steroids endowed with powerful anti-inflammatory properties, which are routinely believed to require several hours to take effect through modulation of gene expression. Our recent report has shown that glucocorticoids could inhibit allergic reaction within 10 minutes, which the classical genomic mechanism could not explain. Histamine is thought to be one of major mediators in the allergic reaction, and IgE-mediated histamine release from mast cells plays a pivotal role in allergic diseases. Here, we have determined a rapid effect of corticosterone on histamine release from rat peritoneal mast cells, using fluorometric assay. The results showed that corticosterone could inhibit antigen-induced histamine release from rat peritoneal cells within 15 minutes (p<0.05), which could be mimicked by membrane-impermeable BSA conjugated corticosterone (p<0.05). Neither glucocorticoid nuclear receptor antagonist nor protein synthesis inhibitor could block the rapid action (p<0.05). The study provided evidence that nongenomic mechanism might be involved in rapid effect of glucocorticoids on mast cells in allergic disease.

corticosterone - rapid nongenomic effect - mast cells - histamine

References

• 1 Hirschelmann R, Bekemeier H. Problem and results in testing the possible mode of anti-inflammatory glucocorticoid action in carrageenin rat paw oedema; advertages of local substance injection.  Int J Tiss Reac. 1984;  6 471-475
• 2 Goppelt-Struebe M. Molecular mechanisms involved in the regulation of prostaglandin biosynthesis by glucocorticoids.  Biochem Pharmacol. 1997;  15 1389-1395
• 3 Bames PJ, Karin M. Nuclear factor-κB: A pivotal transcription factor in chronic inflammatory diseases.  N Engl J Med. 1997;  336 1066-1071
• 4 Duval D, Durant S, Homo-Delache F. Non-genomic effects of steroids. Interactions of steroid molecules with membrane structures and functions.  Biochim Biophys Acta. 1983;  737 409-442
• 5 Wehling M. Specific, nongenomic actions of steroid hormones.  Annu Rev Physiol. 1997;  59 365-393
• 6 Buttgereit F, Wehling M, Burmester GR. A new hypothesis of modular glucocorticoid action:steroid treatment of rheumatic disease revisited.  Arthritis Rheum. 1998;  41 761-767
• 7 Zhou J, Kang ZM, Xie QM, Liu C, Lou SJ, Chen YZ, Jiang CL. Rapid nongenomic effect of glucocorticoids on allergic asthma reaction in the guinea pig.  J Endocrinol. 2003;  177 R1-R4
• 8 Ma H, Kovanen PT. IgE-dependent generation of foam cells: an immune mechanism involving degranulation of sensitized mast cells with resultant uptake of LDL by macrophages.  Arterioscler Thromb Vasc Biol. 1995;  15 811-819
• 9 Nemeth A, Rohlich P. Rapid separation of rat peritoneal mast cells with Percoll.  Eur J Cell Biol. 1980;  20 272-275
• 10 Shore PA, Burkhalter A, Cohn VH. A method for the fluorimetric assay of histamine in tissue.  J Pharmacol Exp Ther. 1959;  127 182-186
• 11 Bergendorff A, Uvnas B. Storage of 5-hydroxy-triptamine in rat mast cells. Evidence for an ionic binding to carboxyl groups in a granule heparin-protein complex.  Acta Physiol Scand. 1972;  84 320-331
• 12 Park S, Taub M, Han H. Regulation of phosphate uptake in primary cultured rabbit renal proximal tubule cells by glucocorticoids: evidence for nongenomic as well as genomic mechanisms.  Endocrinology. 2001;  142 710-720
• 13 Blackmore P, Lattanzio F. Cell surface localization of a novel non-genomic progesterone receptor on the head of human sperm.  Biochem Biophys Res Commun. 1991;  181 743-760
• 14 Borski RJ. Nongenomic membrane actions of glucocorticoids in vertebrates. Trends.  Endocrinol Metab. 2000;  11 427-436
• 15 Losel R, Wehling M. Nongenomic actions of steroid hormones.  Nat Rev Mol Cell Biol. 2003;  4 46-56
• 16 Urbach V, Walsh DE, Mainprice B, Bousquet J, Harvey BJ. Rapid non-genomic inhibition of ATP-induced Cl-secretion by dexamethasone in human bronchial epithelium.  AM J Physiol. 2002;  15 869-878
• 17 Ketchell RI, Jensen MW, Lumley P, Wright AM, Allenby MI, O'connor BJ. Rapid effect of inhaled fluticasone propionate on airway responsiveness to adenosine 5'-monophosphate in mild asthma.  J Allergy Clin Immunol. 2002;  110 603-606
• 18 Grosman N, Jensen SM. Influence of glucocorticoids on histamine release and 45calcium uptake by isolated rat mast cells.  Agents Actions. 1984;  14 421-430
• 19 Vendelin J, Laitinen C, Vainio PJ, Nissinen E, Maki T, Eklund KK. Novel sulfhydryl- reactive compounds orazipone and OR-1958 inhibit cytokine production and histamine release in rat and human mast cells.  Int Immunopharmacol. 2005;  5 177-184
• 20 Nadal A, Ropero AB, Fuentes E, Soria B. The plasma membrane estrogen receptor: nuclear or unclear?.  Trends Pharm Sci. 2001;  22 597-599
• 21 Bartholome B, Spies CM, Gaber T, Schuchmann S, Berki T, Kunkel D, Bienert M, Radbruch A, Burmester GR, Lauster R, Scheffold A, Buttgereit F. Membrane glucocorticoid receptors (mGCR) are expressed in normal human peripheral blood mononuclear cells and up-regulated after in vitro stimulation and in patients with rheumatoid arthritis.  FASEB J. 2004;  18 70-80
• 22 Falkenstein E, Norman AW, Wehling M. Mannheim classification of nongenomically initiated (rapid) steroid actions(s).  J Clin Endocrinol Metab. 2000;  85 2072-2075
• 23 Guo Z, Chen YZ, Xu RB, Fu H. Binding characteristics of glucocorticoid receptor in synaptic plasma membrane from rat brain.  Funct Neurol. 1995;  10 183-194
• 24 Wang ZY, Seto H, Fujioka S, Yoshida S, Chory J. BRI1 is a critical component of a plasma-membrane receptor for plant steroids.  Nature. 2001;  401 380-383
• 25 Chen YZ, Qiu J. Pleiotropic signaling pathways in rapid, nongenomic action of glucocorticoid.  Mol Cell Biol Res Commun. 1999;  2 145-149

1 These authors contributed equally to this study.

Correspondence