Mechanistic role for a novel glucocorticoid-KLF11 (TIEG2) protein pathway in stress-induced monoamine oxidase A expression

J Biol Chem. 2012 Jul 13;287(29):24195-206. doi: 10.1074/jbc.M112.373936. Epub 2012 May 24.

Abstract

Chronic stress is a risk factor for psychiatric illnesses, including depressive disorders, and is characterized by increased blood glucocorticoids and brain monoamine oxidase A (MAO A, which degrades monoamine neurotransmitters). This study elucidates the relationship between stress-induced MAO A and the transcription factor Kruppel-like factor 11 (KLF11, also called TIEG2, a member of the Sp/KLF- family), which inhibits cell growth. We report that 1) a glucocorticoid (dexamethasone) increases KLF11 mRNA and protein levels in cultured neuronal cells; 2) overexpressing KLF11 increases levels of MAO A mRNA and enzymatic activity, which is further enhanced by glucocorticoids; in contrast, siRNA-mediated KLF11 knockdown reduces glucocorticoid-induced MAO A expression in cultured neurons; 3) induction of KLF11 and translocation of KLF11 from the cytoplasm to the nucleus are key regulatory mechanisms leading to increased MAO A catalytic activity and mRNA levels because of direct activation of the MAO A promoter via Sp/KLF-binding sites; 4) KLF11 knockout mice show reduced MAO A mRNA and catalytic activity in the brain cortex compared with wild-type mice; and 5) exposure to chronic social defeat stress induces blood glucocorticoids and activates the KLF11 pathway in the rat brain, which results in increased MAO A mRNA and enzymatic activity. Thus, this study reveals for the first time that KLF11 is an MAO A regulator and is produced in response to neuronal stress, which transcriptionally activates MAO A. The novel glucocorticoid-KLF11-MAO A pathway may play a crucial role in modulating distinct pathophysiological steps in stress-related disorders.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis Regulatory Proteins
  • Blotting, Western
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Cell Line, Tumor
  • Cells, Cultured
  • Chromatin Immunoprecipitation
  • Chromatography, High Pressure Liquid
  • Corticosterone / metabolism
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Dexamethasone / metabolism
  • Fluorescent Antibody Technique
  • Gene Expression / drug effects
  • Humans
  • Male
  • Mice
  • Mice, Knockout
  • Monoamine Oxidase / genetics
  • Monoamine Oxidase / metabolism*
  • Radioimmunoassay
  • Rats
  • Rats, Wistar
  • Real-Time Polymerase Chain Reaction
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism*
  • Serotonin / metabolism
  • Stress, Physiological / genetics
  • Stress, Physiological / physiology
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • Apoptosis Regulatory Proteins
  • Cell Cycle Proteins
  • DNA-Binding Proteins
  • KLF11 protein, human
  • KLF11 protein, mouse
  • Repressor Proteins
  • Transcription Factors
  • Serotonin
  • Dexamethasone
  • Monoamine Oxidase
  • Corticosterone