Pain and itch processing by subpopulations of molecularly diverse spinal and trigeminal projection neurons

Proc Natl Acad Sci U S A. 2021 Jul 13;118(28):e2105732118. doi: 10.1073/pnas.2105732118.

Abstract

A remarkable molecular and functional heterogeneity of the primary sensory neurons and dorsal horn interneurons transmits pain- and or itch-relevant information, but the molecular signature of the projection neurons that convey the messages to the brain is unclear. Here, using retro-TRAP (translating ribosome affinity purification) and RNA sequencing, we reveal extensive molecular diversity of spino- and trigeminoparabrachial projection neurons. Among the many genes identified, we highlight distinct subsets of Cck+ -, Nptx2+ -, Nmb+ -, and Crh+ -expressing projection neurons. By combining in situ hybridization of retrogradely labeled neurons with Fos-based assays, we also demonstrate significant functional heterogeneity, including both convergence and segregation of pain- and itch-provoking inputs into molecularly diverse subsets of NK1R- and non-NK1R-expressing projection neurons.

Keywords: RNA-seq; dorsal horn; itch; pain; projection neurons.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Chloroquine / pharmacology
  • Female
  • Gene Expression Regulation / drug effects
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Neurons / drug effects
  • Neurons / metabolism
  • Neurons / pathology*
  • Pain / complications*
  • Pain / genetics
  • Pain / pathology*
  • Physical Stimulation
  • Pruritus / complications*
  • Pruritus / genetics
  • Pruritus / pathology*
  • RNA / isolation & purification
  • RNA / metabolism
  • Receptors, Neurokinin-1 / metabolism
  • Spinal Cord / pathology*
  • Spinal Cord Dorsal Horn / drug effects
  • Spinal Cord Dorsal Horn / metabolism
  • Trigeminal Nerve / pathology*

Substances

  • Receptors, Neurokinin-1
  • RNA
  • Chloroquine