Interleukin-1beta inhibits ATP-induced protein kinase B activation in renal mesangial cells by two different mechanisms: the involvement of nitric oxide and ceramide

Br J Pharmacol. 2003 Feb;138(3):461-8. doi: 10.1038/sj.bjp.0705064.

Abstract

1 Extracellular nucleotides, like ATP and UTP, have been shown to activate the protein kinase B (PKB) pathway in mesangial cells. In this study we report that the pro-inflammatory cytokine interleukin-1beta (IL-1beta) inhibits ATP-induced PKB activation. 2 Pretreatment of mesangial cells with IL-1beta leads to a time-dependent decrease of ATP-induced PKB phosphorylation. Maximal inhibition is seen after 6 h of pretreatment. Incubating cells with IL-1beta in the presence of the NO synthase inhibitor, N-monomethyl-L-arginine (L-NMMA), reversed the IL-1beta inhibition of PKB activity. A similar decrease in ATP-evoked PKB activation is obtained when cells were pretreated with the nitric oxide (NO) donor, (Z)-1-[2-Aminoethyl)-N-(2-ammonioethyl)amino]diazen-1-ium-1,2-diolate (Deta-NO), but not with the cell-permeable cGMP analogue, 8-bromo-cGMP. 3 The NO- and IL-1beta-mediated delayed inhibition of PKB activity is completely reversed by the phosphatase inhibitor calyculin A, but not by ocadaic acid, suggesting that NO upregulates a protein phosphatase activity, which most probably belongs to the group of protein phosphatases type 1. 4 In addition, IL-1beta also triggers a short-term and transient inhibitory effect on ATP-induced PKB activation which is maximal after 2-5 min of pre-incubation with IL-1beta. This effect occurs independently of NO generation, because no NO synthase is expressed at that time, and consequently, L-NMMA does not reverse the effect. Rather an involvement of the sphingolipid ceramide is likely, since IL-1beta triggers rapid ceramide formation and incubation of cells with the cell-permeable C6-ceramide blocked ATP-induced PKB phosphorylation. 5 In summary, our data show that IL-1beta exerts both short-term and long-term inhibitory effects on ATP-stimulated PKB activation, the short-term effect probably involves ceramide formation, whereas the long-term effect is due to inducible NO synthase induction and subsequent NO formation. These results reveal a further facet in the mechanisms of ceramide- and NO-induced cell death, i.e. by turning off the survival signal elicited by PKB.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism*
  • Animals
  • Blotting, Western
  • Cells, Cultured
  • Ceramides / metabolism*
  • Dose-Response Relationship, Drug
  • Enzyme Activation
  • Enzyme Induction
  • Enzyme Inhibitors / pharmacology
  • Glomerular Mesangium / cytology
  • Glomerular Mesangium / drug effects
  • Glomerular Mesangium / metabolism*
  • Interleukin-1 / metabolism*
  • Interleukin-1 / pharmacology
  • Marine Toxins
  • Nitric Oxide / metabolism*
  • Nitric Oxide Synthase / biosynthesis
  • Nitric Oxide Synthase Type II
  • Okadaic Acid / pharmacology
  • Oxazoles / pharmacology
  • Protein Serine-Threonine Kinases*
  • Proto-Oncogene Proteins / antagonists & inhibitors
  • Proto-Oncogene Proteins / metabolism*
  • Proto-Oncogene Proteins c-akt
  • Rats

Substances

  • Ceramides
  • Enzyme Inhibitors
  • Interleukin-1
  • Marine Toxins
  • Oxazoles
  • Proto-Oncogene Proteins
  • Okadaic Acid
  • Nitric Oxide
  • calyculin A
  • Adenosine Triphosphate
  • Nitric Oxide Synthase
  • Nitric Oxide Synthase Type II
  • Nos2 protein, rat
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt