Inflammation causes a long-term hyperexcitability in the nociceptive sensory neurons of Aplysia

Learn Mem. 1999 May-Jun;6(3):331-40.

Abstract

Nerve injury, tissue damage, and inflammation all cause hyperalgesia. A factor contributing to this increased sensitivity is a long-term (>24 hr) hyperexcitability (LTH) in the sensory neurons that mediate the responses. Using the cluster of nociceptive sensory neurons in Aplysia californica as a model, we are examining how inflammation induces LTH. A general inflammatory response was induced by inserting a gauze pad into the animal Within 4 days, the gauze is enmeshed in an amorphous material that contains hemocytes, which comprise a cellular immune system. Concurrently, LTH appears in both ipsilateral and contralateral sensory neurons. The LTH is manifest as increased action potential discharge to a normalized stimulus. Immunocytochemistry revealed that hemocytes have antigens recognized by antibodies to TGFbeta1, IL-6, and 5HT. When a localized inflammation was elicited on a nerve, hemocytes containing the TGFbeta1 antigen were present near axons within the nerve and those containing the IL-6 were on the surface. Western blots of hemocytes, or of gauze that had induced a foreign body response, contained a 28-kD polypeptide recognized by the anti-TGFbeta1 antibody. Exposure of the nervous system to recombinant human TGFbeta1 elicited increased firing of the nociceptive neurons and a decrease in threshold. The TGFbeta1 also caused an activation of protein kinase C (PKC) in axons but did not affect a kinase that is activated in axons after injury. Our findings, in conjunction with previous results, indicate that a TGFbeta1-homolog can modulate the activity of neurons that respond to noxious stimuli. This system could also contribute to interactions between the immune and nervous systems via regulation of PKC.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Aplysia / physiology*
  • Axonal Transport
  • Cells, Cultured
  • Electrophysiology
  • Hemocytes / chemistry
  • Hemocytes / metabolism
  • Humans
  • Immunohistochemistry
  • Inflammation / pathology*
  • Neurons, Afferent / drug effects
  • Neurons, Afferent / pathology*
  • Nociceptors / drug effects
  • Nociceptors / physiology*
  • Peptides / chemistry
  • Peptides / metabolism
  • Protein Kinase C / metabolism
  • Recombinant Proteins / pharmacology
  • Transforming Growth Factor beta / pharmacology

Substances

  • Peptides
  • Recombinant Proteins
  • Transforming Growth Factor beta
  • Protein Kinase C