CCK-8 inhibits LPS-induced IL-1beta production in pulmonary interstitial macrophages by modulating PKA, p38, and NF-kappaB pathway

Shock. 2007 Jun;27(6):678-86. doi: 10.1097/shk.0b013e3180ze26dd.

Abstract

The neuropeptide cholecystokinin octapeptide (CCK-8) inhibits inflammation by downregulating the expression of proinflammatory cytokines, such as tumor necrosis factor alpha and interleukin (IL) 1beta during endotoxin shock. However, the signaling mechanism of CCK-8 action has not yet been clearly elucidated. In this study, we have examined the possible signaling pathways by which CCK-8 inhibits lipopolysaccharide (LPS)-induced IL-1beta production in rat pulmonary interstitial macrophages. In macrophages, LPS is known to activate p38 kinase, which, in turn, activates nuclear factor (NF)-kappaB to induce IL-1beta production. We found that the pretreatment of cells with CCK-8 blocked the LPS-induced p38 kinase, NF-kappaB activation, and IL-1beta production. Furthermore, CCK-8 treatment activated the cyclic adenosine monophosphate-protein kinase A signaling pathway and H-89 (a protein kinase A inhibitor), abrogated the inhibitory effects of CCK-8 on p38 kinase activation and NF-kappaB activation. In addition, we also demonstrate that the specific antagonist to CCK-1 receptor (CCK-1R) and CCK-2 receptor (CCK-2R) abrogate the CCK action, and that the effects of the antagonist specific to CCK-1R is more significant. These results suggest that these responses were mediated through CCK-1R and CCK-2R, and CCK-1R might be the major receptor responsible for the anti-inflammatory effect of CCK-8. Taken together, our results indicate that the stimulation of cyclic adenosine monophosphate-protein kinase A signaling pathway by CCK-8 through CCK-1R and CCK-2R inhibits the LPS-induced activation of p38 kinase and NF-kappaB to block the IL-1beta production in rat pulmonary interstitial macrophages.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cholecystokinin / metabolism
  • Cyclic AMP-Dependent Protein Kinases / metabolism*
  • Female
  • Interleukin-1beta / metabolism*
  • Lipopolysaccharides / metabolism*
  • Lung / metabolism*
  • Macrophages / metabolism*
  • Mice
  • NF-kappa B / metabolism*
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, Cholecystokinin A / metabolism
  • Receptor, Cholecystokinin B / metabolism
  • Sincalide / pharmacology*
  • p38 Mitogen-Activated Protein Kinases / metabolism*

Substances

  • Interleukin-1beta
  • Lipopolysaccharides
  • NF-kappa B
  • Receptor, Cholecystokinin A
  • Receptor, Cholecystokinin B
  • Cholecystokinin
  • Cyclic AMP-Dependent Protein Kinases
  • p38 Mitogen-Activated Protein Kinases
  • Sincalide