Natural Killer Cells Degenerate Intact Sensory Afferents following Nerve Injury

Cell. 2019 Feb 7;176(4):716-728.e18. doi: 10.1016/j.cell.2018.12.022. Epub 2019 Jan 31.

Abstract

Sensory axons degenerate following separation from their cell body, but partial injury to peripheral nerves may leave the integrity of damaged axons preserved. We show that an endogenous ligand for the natural killer (NK) cell receptor NKG2D, Retinoic Acid Early 1 (RAE1), is re-expressed in adult dorsal root ganglion neurons following peripheral nerve injury, triggering selective degeneration of injured axons. Infiltration of cytotoxic NK cells into the sciatic nerve by extravasation occurs within 3 days following crush injury. Using a combination of genetic cell ablation and cytokine-antibody complex stimulation, we show that NK cell function correlates with loss of sensation due to degeneration of injured afferents and reduced incidence of post-injury hypersensitivity. This neuro-immune mechanism of selective NK cell-mediated degeneration of damaged but intact sensory axons complements Wallerian degeneration and suggests the therapeutic potential of modulating NK cell function to resolve painful neuropathy through the clearance of partially damaged nerves.

Keywords: Wallerian degeneration; autoimmunity; dorsal root ganglia; innate immunity; natural cytotoxicity; neurodegeneration; neuroimmune; neuropathic pain; peripheral neuropathy; sciatic nerve crush.

Publication types

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

MeSH terms

  • Animals
  • Axons
  • Ganglia, Spinal / cytology
  • Ganglia, Spinal / metabolism
  • Killer Cells, Natural / metabolism
  • Killer Cells, Natural / physiology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • NK Cell Lectin-Like Receptor Subfamily K / metabolism
  • Nerve Regeneration
  • Neurons / cytology
  • Neurons, Afferent / immunology
  • Neurons, Afferent / metabolism
  • Nuclear Matrix-Associated Proteins / metabolism*
  • Nuclear Matrix-Associated Proteins / physiology
  • Nucleocytoplasmic Transport Proteins / metabolism*
  • Nucleocytoplasmic Transport Proteins / physiology
  • Pain
  • Peripheral Nerve Injuries / immunology
  • Peripheral Nerve Injuries / metabolism*
  • Peripheral Nervous System Diseases
  • Sciatic Nerve
  • Sensory Receptor Cells / metabolism

Substances

  • Klrk1 protein, mouse
  • NK Cell Lectin-Like Receptor Subfamily K
  • Nuclear Matrix-Associated Proteins
  • Nucleocytoplasmic Transport Proteins
  • Rae1 protein, mouse

Supplementary concepts

  • Neuropathy, Painful