Pain hypersensitivity is dependent on autophagy protein Beclin 1 in males but not females

Cell Rep. 2024 Jun 25;43(6):114293. doi: 10.1016/j.celrep.2024.114293. Epub 2024 May 29.

Abstract

Chronic pain is associated with alterations in fundamental cellular processes. Here, we investigate whether Beclin 1, a protein essential for initiating the cellular process of autophagy, is involved in pain processing and is targetable for pain relief. We find that monoallelic deletion of Becn1 increases inflammation-induced mechanical hypersensitivity in male mice. However, in females, loss of Becn1 does not affect inflammation-induced mechanical hypersensitivity. In males, intrathecal delivery of a Beclin 1 activator, tat-beclin 1, reverses inflammation- and nerve injury-induced mechanical hypersensitivity and prevents mechanical hypersensitivity induced by brain-derived neurotrophic factor (BDNF), a mediator of inflammatory and neuropathic pain. Pain signaling pathways converge on the enhancement of N-methyl-D-aspartate receptors (NMDARs) in spinal dorsal horn neurons. The loss of Becn1 upregulates synaptic NMDAR-mediated currents in dorsal horn neurons from males but not females. We conclude that inhibition of Beclin 1 in the dorsal horn is critical in mediating inflammatory and neuropathic pain signaling pathways in males.

Keywords: BDNF; Beclin 1; CP: Cell biology; CP: Neuroscience; NMDA receptors; autophagy; pain; sex differences.

MeSH terms

  • Animals
  • Autophagy*
  • Beclin-1* / metabolism
  • Brain-Derived Neurotrophic Factor / metabolism
  • Female
  • Hyperalgesia / metabolism
  • Hyperalgesia / pathology
  • Inflammation / metabolism
  • Inflammation / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Neuralgia / metabolism
  • Neuralgia / pathology
  • Posterior Horn Cells / metabolism
  • Posterior Horn Cells / pathology
  • Receptors, N-Methyl-D-Aspartate / metabolism
  • Signal Transduction

Substances

  • Beclin-1
  • Receptors, N-Methyl-D-Aspartate
  • Brain-Derived Neurotrophic Factor
  • Becn1 protein, mouse