Phosphodiesterase 4B mediates extracellular signal-regulated kinase-dependent up-regulation of mucin MUC5AC protein by Streptococcus pneumoniae by inhibiting cAMP-protein kinase A-dependent MKP-1 phosphatase pathway

J Biol Chem. 2012 Jun 29;287(27):22799-811. doi: 10.1074/jbc.M111.337378. Epub 2012 May 18.

Abstract

Otitis media (OM) is the most common childhood bacterial infection and the major cause of conductive hearing loss in children. Mucus overproduction is a hallmark of OM. Streptococcus pneumoniae is the most common gram-positive bacterial pathogen causing OM. Among many mucin genes, MUC5AC has been found to be greatly up-regulated in the middle ear mucosa of human patients with OM. We previously reported that S. pneumoniae up-regulates MUC5AC expression in a MAPK ERK-dependent manner. We also found that MAPK phosphatase-1 (MKP-1) negatively regulates S. pneumoniae-induced ERK-dependent MUC5AC up-regulation. Therapeutic strategies for up-regulating the expression of negative regulators such as MKP-1 may have significant therapeutic potential for treating mucus overproduction in OM. However, the underlying molecular mechanism by which MKP-1 expression is negatively regulated during S. pneumoniae infection is unknown. In this study we show that phosphodiesterase 4B (PDE4B) mediates S. pneumoniae-induced MUC5AC up-regulation by inhibiting the expression of a negative regulator MKP-1, which in turn leads to enhanced MAPK ERK activation and subsequent up-regulation of MUC5AC. PDE4B inhibits MKP-1 expression in a cAMP-PKA-dependent manner. PDE4-specific inhibitor rolipram inhibits S. pneumoniae-induced MUC5AC up-regulation both in vitro and in vivo. Moreover, we show that PDE4B plays a critical role in MUC5AC induction. Finally, topical and post-infection administration of rolipram into the middle ear potently inhibited S. pneumoniae-induced MUC5AC up-regulation. Collectively, these data demonstrate that PDE4B mediates ERK-dependent up-regulation of mucin MUC5AC by S. pneumoniae by inhibiting cAMP-PKA-dependent MKP-1 pathway. This study may lead to novel therapeutic strategy for inhibiting mucus overproduction.

Publication types

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

MeSH terms

  • Animals
  • Cell Line
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Cyclic Nucleotide Phosphodiesterases, Type 4 / genetics
  • Cyclic Nucleotide Phosphodiesterases, Type 4 / metabolism*
  • Dual Specificity Phosphatase 1 / metabolism*
  • Ear, Middle / cytology
  • Ear, Middle / immunology
  • Epithelial Cells / cytology
  • Epithelial Cells / enzymology
  • Epithelial Cells / microbiology
  • Humans
  • MAP Kinase Signaling System / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Mucin 5AC / metabolism*
  • Mucus / metabolism
  • Otitis Media / immunology
  • Otitis Media / metabolism
  • Otitis Media / microbiology
  • Pneumococcal Infections / immunology
  • Pneumococcal Infections / metabolism*
  • Pneumococcal Infections / microbiology
  • RNA, Small Interfering / genetics
  • Respiratory Mucosa / cytology
  • Respiratory Mucosa / immunology
  • Streptococcus pneumoniae / metabolism*
  • Up-Regulation / physiology

Substances

  • MUC5AC protein, human
  • Muc5ac protein, mouse
  • Mucin 5AC
  • RNA, Small Interfering
  • Cyclic AMP-Dependent Protein Kinases
  • DUSP1 protein, human
  • Dual Specificity Phosphatase 1
  • Cyclic Nucleotide Phosphodiesterases, Type 4
  • PDE4B protein, human
  • PDE4B protein, mouse