TNF-alpha hyperpolarizes membrane potential and potentiates the response to nicotinic receptor stimulation in cultured rat myenteric neurones

Acta Physiol Scand. 2004 May;181(1):13-22. doi: 10.1111/j.1365-201X.2004.01269.x.

Abstract

Aims: Tumour necrosis factor-alpha (TNF-alpha) plays a central role in the pathophysiology of inflammatory bowel disease. The present experiments were designed to characterize the action of this cytokine on enteric neurones.

Methods: Myenteric ganglia from newborn rats were treated for 20 h with TNF-alpha (100 ng mL(-1)) and studied with the patch-clamp technique.

Results: Control neurones showed a membrane potential of -34.6 +/- 2.2 mV (n = 22), whereas TNF-alpha-treated cells exhibited a membrane potential of -50.8 +/- 3.5 mV (n = 25). The depolarization evoked by carbachol (50 microm) was potentiated from 5.2 +/- 0.7 mV (n = 6) in control neurones to 27.5 +/- 2.0 mV (n = 10) in TNF-alpha-treated cells. This effect was mimicked by 1,1-dimethyl-4-phenylpiperazinium iodide, but not by bethanechol. The changes in basal membrane potential and in the nicotinic receptor response were suppressed by the non-selective cyclooxygenase (COX) inhibitor indomethacin (10 microm), and the COX II-specific inhibitor, nimesulide (100 microm), whereas the COX-I selective inhibitor SC-560 (5 microm) and the proteintyrosinekinase inhibitor genistein (50 microm) only partially inhibited the action of TNF-alpha. Staining of the ganglionic cells with an antibody against the transcription factor STAT5 revealed that TNF-alpha induced a nuclear translocation of STAT5 in non-neuronal cells.

Conclusion: TNF-alpha changes the electrophysiological properties of myenteric neurones via cyclooxygenase metabolites and protein tyrosine phosphorylation; the cells primarily responding to the cytokine seem to be non-neuronal cells in the ganglion culture, which respond with a nuclear STAT5 translocation suggesting an action on gene transcription.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn
  • Bethanechol / pharmacology
  • Carbachol / pharmacology
  • Cells, Cultured
  • Cyclooxygenase Inhibitors / metabolism
  • DNA-Binding Proteins / analysis
  • Dimethylphenylpiperazinium Iodide / pharmacology
  • Enzyme Inhibitors / pharmacology
  • Ganglia, Autonomic / cytology
  • Ganglia, Autonomic / drug effects
  • Genistein / pharmacology
  • Immunohistochemistry / methods
  • Indomethacin / metabolism
  • Intestine, Small / cytology
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Milk Proteins*
  • Muscarinic Agonists / pharmacology
  • Myenteric Plexus / cytology
  • Myenteric Plexus / drug effects
  • Neurons / drug effects
  • Neurons / physiology*
  • Nicotinic Agonists / pharmacology
  • Patch-Clamp Techniques / methods
  • Rats
  • Receptors, Nicotinic / physiology*
  • STAT5 Transcription Factor
  • Trans-Activators / analysis
  • Tumor Necrosis Factor-alpha / physiology*

Substances

  • Cyclooxygenase Inhibitors
  • DNA-Binding Proteins
  • Enzyme Inhibitors
  • Milk Proteins
  • Muscarinic Agonists
  • Nicotinic Agonists
  • Receptors, Nicotinic
  • STAT5 Transcription Factor
  • Trans-Activators
  • Tumor Necrosis Factor-alpha
  • Bethanechol
  • Dimethylphenylpiperazinium Iodide
  • Carbachol
  • Genistein
  • Indomethacin