Some sensory neurons express neuropeptide Y receptors: Potential paracrine inhibition of primary afferent nociceptors following peripheral nerve injury

Patrick W. Mantyh, Clark J. Allen, Scott Rogers, Eric DeMaster, Joseph R. Ghilardi, Tony Mosconi, Lawrence Kruger, Peter J. Mannon, Ian L. Taylor, Steven R. Vigna

Research output: Contribution to journalArticle

66 Scopus citations

Abstract

Neuropeptide Y (NPY) has been suggested to exert antinociceptive actions by inhibiting the release of neurotransmitters from trigeminal and dorsal root ganglia (DRG) neurons, but the site of direct NPY action in vivo and the NPY receptor subtype mediating these effects are unknown. 125I-peptide YY (PYY) was used to localize and characterize NPY receptor binding sites in trigeminal ganglia, DRG, and spinal cord of the rat, rabbit, and monkey. In the rat, rabbit, and monkey, 5-20% of trigeminal ganglia and DRG neurons express NPY binding sites. Unilateral cuff-induced neuropathy or transection of the rat sciatic nerve did not significantly alter the density or number of DRG neurons expressing NPY receptors. A unimodal size distribution for L4 and L5 DRG neurons expressing NPY binding sites in the rat was determined, with a mean cross-sectional area of 947 μm2. In the spinal cord the highest concentration of NPY receptors is found in laminae I, II, V, X, and Onuf's nucleus. Pharmacological experiments using selective Y1 and Y2 receptor antagonists suggest that Y2 is the prominent NPY receptors subtype expressed in trigeminal ganglia neurons, DRG neurons, and spinal cord. Previous studies have demonstrated that a population of large-diameter, presumably myelinated primary afferents express NPY after peripheral nerve injury. NPY released from these injured large-diameter DRG neurons may act in a paracrine fashion to block the transmission of nociceptive information from the small- and medium-diameter DRG neurons that constitutively express NPY receptors. NPY receptors are therefore uniquely positioned to inhibit primary afferent nociceptors directly, especially after peripheral nerve injury.

Original languageEnglish (US)
Pages (from-to)3958-3968
Number of pages11
JournalJournal of Neuroscience
Volume14
Issue number6
DOIs
StatePublished - Jun 1994

Keywords

  • dorsal root ganglion
  • neuropeptide Y
  • neuropeptide Y receptors
  • nociceptor
  • peripheral nerves
  • sensory neurons
  • trigeminal ganglion

ASJC Scopus subject areas

  • Neuroscience(all)

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  • Cite this

    Mantyh, P. W., Allen, C. J., Rogers, S., DeMaster, E., Ghilardi, J. R., Mosconi, T., Kruger, L., Mannon, P. J., Taylor, I. L., & Vigna, S. R. (1994). Some sensory neurons express neuropeptide Y receptors: Potential paracrine inhibition of primary afferent nociceptors following peripheral nerve injury. Journal of Neuroscience, 14(6), 3958-3968. https://doi.org/10.1523/jneurosci.14-06-03958.1994