Local amplification of glucocorticoids by 11 beta-hydroxysteroid dehydrogenase type 1 promotes macrophage phagocytosis of apoptotic leukocytes

J Immunol. 2006 Jun 15;176(12):7605-11. doi: 10.4049/jimmunol.176.12.7605.

Abstract

Glucocorticoids promote macrophage phagocytosis of leukocytes undergoing apoptosis. Prereceptor metabolism of glucocorticoids by 11beta-hydroxysteroid dehydrogenases (11beta-HSDs) modulates cellular steroid action. 11beta-HSD type 1 amplifies intracellular levels of active glucocorticoids in mice by reactivating corticosterone from inert 11-dehydrocorticosterone in cells expressing the enzyme. In this study we describe the rapid (within 3 h) induction of 11beta-HSD activity in cells elicited in the peritoneum by a single thioglycolate injection in mice. Levels remained high in peritoneal cells until resolution. In vitro experiments on mouse macrophages demonstrated that treatment with inert 11-dehydrocorticosterone for 24 h increased phagocytosis of apoptotic neutrophils to the same extent as corticosterone. This effect was dependent upon 11beta-HSD1, as 11beta-HSD1 mRNA, but not 11beta-HSD2 mRNA, was expressed in these cells; 11-dehydrocorticosterone was ineffective in promoting phagocytosis by Hsd11b1(-/-) macrophages, and carbenoxolone, an 11beta-HSD inhibitor, prevented the increase in phagocytosis elicited in wild-type macrophages by 11-dehydrocorticosterone. Importantly, as experimental peritonitis progressed, clearance of apoptotic neutrophils was delayed in Hsd11b1(-/-) mice. These data point to an early role for 11beta-HSD1 in promoting the rapid clearance of apoptotic cells during the resolution of inflammation and indicate a novel target for therapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 11-beta-Hydroxysteroid Dehydrogenase Type 1 / biosynthesis
  • 11-beta-Hydroxysteroid Dehydrogenase Type 1 / deficiency
  • 11-beta-Hydroxysteroid Dehydrogenase Type 1 / genetics
  • 11-beta-Hydroxysteroid Dehydrogenase Type 1 / physiology*
  • 11-beta-Hydroxysteroid Dehydrogenase Type 2 / biosynthesis
  • Animals
  • Apoptosis / genetics
  • Apoptosis / immunology*
  • Ascitic Fluid / enzymology
  • Ascitic Fluid / immunology
  • Ascitic Fluid / pathology
  • Cells, Cultured
  • Corticosterone / metabolism*
  • Corticosterone / physiology
  • Humans
  • Macrophage Activation / genetics
  • Macrophage Activation / immunology
  • Macrophages, Peritoneal / immunology*
  • Macrophages, Peritoneal / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neutrophils / cytology
  • Neutrophils / immunology*
  • Neutrophils / pathology*
  • Peritonitis / enzymology
  • Peritonitis / genetics
  • Peritonitis / immunology
  • Phagocytosis / genetics
  • Phagocytosis / immunology
  • Thioglycolates / administration & dosage
  • Up-Regulation / immunology

Substances

  • Thioglycolates
  • 11-beta-Hydroxysteroid Dehydrogenase Type 1
  • 11-beta-Hydroxysteroid Dehydrogenase Type 2
  • Corticosterone