Immune regulation of 25-hydroxyvitamin D-1alpha-hydroxylase in human monocytic THP1 cells: mechanisms of interferon-gamma-mediated induction

J Clin Endocrinol Metab. 2006 Sep;91(9):3566-74. doi: 10.1210/jc.2006-0678. Epub 2006 Jun 20.

Abstract

Context: 25-Hydroxyvitamin D can be activated to 1,25-dihydroxyvitamin D(3) [1,25(OH)(2)D(3)] by the rate-limiting enzyme 1alpha-hydroxylase in cells of the immune system under control of immune stimuli, such as interferon-gamma (IFNgamma). In pathological situations, such as sarcoidosis, this can lead to systemic excess of 1,25(OH)(2)D(3) and hypercalcemia.

Objective: The aim of this study was to elucidate the intracellular pathways used by the immune system to tightly regulate 1,25(OH)(2)D(3) production in monocytes and macrophages.

Design: Human monocytic THP1-cells were differentiated and activated by IFNgamma and a secondary stimulus, such as lipopolysaccharide or phorbol myristate acetate. 1alpha-Hydroxylase mRNA levels were quantified by real-time RT-PCR. The involvement of different signaling pathways in the regulation of this enzyme was investigated using specific pharmacological inhibitors, whereas phosphorylation of signal transducer and activator of transcription 1alpha and CCAAT/enhancer binding protein beta was investigated by Western blotting.

Results: In undifferentiated monocytic THP1 cells, IFNgamma needs to be combined with a second stimulus, such as lipopolysaccharide, to induce 1alpha-hydroxylase. In contrast, in phorbol myristate acetate-differentiated THP1 macrophages, IFNgamma alone induces 1alpha-hydroxylase and to much higher levels. Many different signaling pathways need to be activated concurrently to allow immune-mediated 1alpha-hydroxylase up-regulation. We show involvement of the Janus kinase-signal transducer and activator of transcription, MAPK, and nuclear factor-kappaB pathways, with a crucial role for the transcription factor CCAAT/enhancer binding protein beta. Furthermore, histone remodeling involving histone deacetylases and histone acetylase p300 is required.

Conclusion: The present findings indicate that IFNgamma-mediated 1,25(OH)(2)D(3) production, as observed in granulomatous diseases such as sarcoidosis, will take place only under conditions where the necessary other signaling pathways are also activated.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 25-Hydroxyvitamin D3 1-alpha-Hydroxylase / genetics
  • 25-Hydroxyvitamin D3 1-alpha-Hydroxylase / immunology*
  • Anthracenes / pharmacology
  • Blotting, Western
  • CCAAT-Enhancer-Binding Protein-beta / genetics
  • CCAAT-Enhancer-Binding Protein-beta / immunology
  • Cell Differentiation / immunology
  • Cell Line
  • Enzyme Induction
  • Flavonoids / pharmacology
  • Humans
  • Imidazoles / pharmacology
  • Interferon-gamma / immunology*
  • Mitogen-Activated Protein Kinases / immunology
  • Monocytes / cytology
  • Monocytes / enzymology
  • Monocytes / immunology*
  • Protein Kinase Inhibitors / pharmacology
  • Pyridines / pharmacology
  • RNA / chemistry
  • RNA / genetics
  • Reverse Transcriptase Polymerase Chain Reaction
  • STAT1 Transcription Factor / genetics
  • STAT1 Transcription Factor / immunology*
  • Signal Transduction
  • Tetradecanoylphorbol Acetate / immunology

Substances

  • Anthracenes
  • CCAAT-Enhancer-Binding Protein-beta
  • Flavonoids
  • Imidazoles
  • Protein Kinase Inhibitors
  • Pyridines
  • STAT1 Transcription Factor
  • pyrazolanthrone
  • RNA
  • Interferon-gamma
  • 25-Hydroxyvitamin D3 1-alpha-Hydroxylase
  • Mitogen-Activated Protein Kinases
  • Tetradecanoylphorbol Acetate
  • SB 203580
  • 2-(2-amino-3-methoxyphenyl)-4H-1-benzopyran-4-one