Neuroprotection by transforming growth factor-beta1 involves activation of nuclear factor-kappaB through phosphatidylinositol-3-OH kinase/Akt and mitogen-activated protein kinase-extracellular-signal regulated kinase1,2 signaling pathways

Neuroscience. 2004;123(4):897-906. doi: 10.1016/j.neuroscience.2003.10.037.

Abstract

Prevention of neuronal apoptosis has been introduced as a new therapeutic strategy for neurodegenerative disorders. We have previously reported anti-apoptotic effects of transforming growth factor-beta1 (TGF-beta1), a multifunctional cytokine, in models of cerebral ischemia and in cultured neurons and recently focused on the mechanisms underlying the anti-apoptotic effect of TGF-beta1. The anti-apoptotic transcriptional factor nuclear factor kappa B (NF-kappaB) shows high impact in the cell survival function of multiple cytokines and growth factors. The present study explored whether NF-kappabeta is a target of TGF-beta1 and which signaling pathways involved in the activation of NF-kappabeta are triggered by TGF-beta1. We demonstrated that TGF-beta1 increased the transcriptional activity of NF-kappabeta in cultured hippocampal neurons in a time- and concentration-dependent manner. Furthermore, TGF-beta1 induced translocation of p65/NF-kappabeta to the nucleus and enhanced NF-kappabeta transcriptional activity in the presence of apoptotic stimuli. TGF-beta1-mediated NF-kappabeta activation was blocked by wortmannin and U0126, indicating the involvement of both phosphatidylinositol-3-OH kinase (PI3k)/Akt and mitogen-activated protein kinase (MAPK)/extracellular-signal regulated kinase (Erk)1,2 pathways in the action of TGF-beta1. TGF-beta1 produced a concomitant increase in the phosphorylations of Ikappabeta kinase (IKKalpha/beta) and Ikappabetaalpha with a subsequent degradation of Ikappabetaalpha. Interestingly, the increased phosphorylation of IKKalpha/beta and Ikappabetaalpha was abrogated by wortmannin, but not by U0126, suggesting that PI3k/Akt and MAPK/Erk1,2 pathways triggered by TGF-beta1 regulated the activation of NF-kappabeta through different mechanisms. Of note, wortmannin and U0126, as well as kappabeta-decoy DNA, abolished the anti-apoptotic effect of TGF-beta1, corroborating the notion that both PI3k/Akt and MAPK/Erk1,2 pathways, and NF-kappabeta activity are necessary for the anti-apoptotic activity of TGF-beta1.

Publication types

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

MeSH terms

  • Animals
  • Animals, Newborn
  • Apoptosis / drug effects
  • Apoptosis / physiology
  • Blotting, Western / methods
  • Calcium-Binding Proteins*
  • Cell Count
  • Cells, Cultured
  • Dose-Response Relationship, Drug
  • Drug Interactions
  • Embryo, Mammalian
  • Enzyme Inhibitors / pharmacology
  • Hippocampus / cytology
  • Immunohistochemistry / methods
  • MAP Kinase Signaling System / drug effects*
  • MAP Kinase Signaling System / physiology
  • Membrane Glycoproteins / metabolism
  • Mice
  • Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • Mitogen-Activated Protein Kinases / physiology*
  • NF-kappa B / metabolism*
  • Nerve Tissue Proteins / metabolism
  • Neurons / drug effects
  • Neurons / physiology
  • Neuroprotective Agents / pharmacology*
  • Phosphatidylinositol 3-Kinases / physiology*
  • Phosphoinositide-3 Kinase Inhibitors
  • Phosphorylation / drug effects
  • Protein Serine-Threonine Kinases*
  • Proto-Oncogene Proteins / antagonists & inhibitors
  • Proto-Oncogene Proteins / physiology*
  • Proto-Oncogene Proteins c-akt
  • Rats
  • Rats, Inbred F344
  • Staurosporine / toxicity
  • Synaptotagmin I
  • Synaptotagmins
  • Time Factors
  • Transforming Growth Factor beta / pharmacology*
  • Transforming Growth Factor beta1
  • Tumor Necrosis Factor-alpha / pharmacology

Substances

  • Calcium-Binding Proteins
  • Enzyme Inhibitors
  • Membrane Glycoproteins
  • NF-kappa B
  • Nerve Tissue Proteins
  • Neuroprotective Agents
  • Phosphoinositide-3 Kinase Inhibitors
  • Proto-Oncogene Proteins
  • Synaptotagmin I
  • Tgfb1 protein, mouse
  • Tgfb1 protein, rat
  • Transforming Growth Factor beta
  • Transforming Growth Factor beta1
  • Tumor Necrosis Factor-alpha
  • Synaptotagmins
  • Akt1 protein, rat
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt
  • Mitogen-Activated Protein Kinases
  • Staurosporine