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The Journal of Neuroscience, March 23, 2005, 25(12):3219-3228; doi:10.1523/JNEUROSCI.4486-04.2005

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Cellular/Molecular
Differential Regulation of AMPA Receptor and GABA Receptor Trafficking by Tumor Necrosis Factor-{alpha}

David Stellwagen,1 Eric C. Beattie,2 Jae Y. Seo,2 and Robert C. Malenka1

1Nancy Pritzker Laboratory, Department of Psychiatry and Behavioral Sciences, Stanford Medical School, Palo Alto, California 94305, and 2California Pacific Medical Research Institute, San Francisco, California 94115

The proinflammatory cytokine tumor necrosis factor-{alpha} (TNF{alpha}) causes a rapid exocytosis of AMPA receptors in hippocampal pyramidal cells and is constitutively required for the maintenance of normal surface expression of AMPA receptors. Here we demonstrate that TNF{alpha} acts on neuronal TNFR1 receptors to preferentially exocytose glutamate receptor 2-lacking AMPA receptors through a phosphatidylinositol 3 kinase-dependent process. This increases excitatory synaptic strength while changing the molecular stoichiometry of synaptic AMPA receptors. Conversely, TNF{alpha} causes an endocytosis of GABAA receptors, resulting in fewer surface GABAA receptors and a decrease in inhibitory synaptic strength. These results suggest that TNF{alpha} can regulate neuronal circuit homeostasis in a manner that may exacerbate excitotoxic damage resulting from neuronal insults.

Key words: GABA; receptor; synaptic; glutamate; trafficking; cytokine

Received Nov 1, 2004; revised January 10, 2005; accepted February 17, 2005.




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