A nitric oxide/Ca(2+)/calmodulin/ERK1/2 mitogen-activated protein kinase pathway is involved in the mitogenic effect of IL-1beta in human astrocytoma cells

Br J Pharmacol. 2008 Apr;153(8):1706-17. doi: 10.1038/bjp.2008.40. Epub 2008 Feb 25.

Abstract

Background and purpose: Evidence is accumulating to support a role for interleukin-1beta (IL-1beta) in astrocyte proliferation. However, the mechanism by which this cytokine modulates this process is not fully elucidated.

Experimental approach: In this study we used human astrocytoma U-373MG cells to investigate the role of nitric oxide (NO), intracellular Ca(2+) concentration ([Ca(2+)](i)), and extracellular signal-regulated protein kinase (ERK) in the signalling pathway mediating IL-1beta-induced astrocyte proliferation.

Key results: Low IL-1beta concentrations induced dose-dependent ERK activation which paralleled upregulation of cell division, whereas higher concentrations gradually reversed both these responses by promoting apoptosis. Pretreatment with the nonspecific NOS inhibitor, N-omega-nitro-l-arginine methyl ester (L-NAME) or the selective iNOS inhibitor, N-[[3-(aminomethyl)phenyl]methyl]-ethanimidamide dihydrochloride (1400W), antagonized ERK activation and cell proliferation induced by IL-1beta. Inhibition of cGMP formation by the guanylate cyclase inhibitor, 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one (ODQ), partially inhibited ERK activation and cell division. Functionally blocking Ca(2+) release from endoplasmic reticulum with ryanodine or 2-aminoethoxydiphenylborane (2-APB), inhibiting calmodulin (CaM) activity with N-(6-aminohexyl)-5-chloro-1-naphthalenesulphonamide hydrochloride (W7) or MAPK kinase activity with 1,4-diamino-2,3-dicyano-1,4-bis[2-aminophenylthiol]butadiene (U0126) downregulated IL-1beta-induced ERK activation as well as cell proliferation. The cytokine induced a transient and time-dependent increase in intracellular NO levels which preceded elevation in [Ca(2+)](i).

Conclusions and implications: These data identified the NO/Ca(2+)/CaM/ERK signalling pathway as a novel mechanism mediating the mitogenic effect of IL-1beta in human astrocytes. As astrocyte proliferation is a hallmark of reactive astrogliosis, our results reveal a new potential target for therapeutic intervention in neuroinflammatory disorders.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Astrocytoma / metabolism
  • Calcium / metabolism
  • Calmodulin / metabolism
  • Cell Proliferation / drug effects
  • Cells, Cultured
  • Dose-Response Relationship, Drug
  • Gene Expression Regulation*
  • Humans
  • Interleukin-1beta / physiology*
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Mitosis / physiology
  • Nitric Oxide / metabolism
  • Signal Transduction*
  • Time Factors

Substances

  • Calmodulin
  • Interleukin-1beta
  • Nitric Oxide
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Calcium