Reducing age-dependent monocyte-derived macrophage activation contributes to the therapeutic efficacy of NADPH oxidase inhibition in spinal cord injury

Brain Behav Immun. 2019 Feb:76:139-150. doi: 10.1016/j.bbi.2018.11.013. Epub 2018 Nov 16.

Abstract

Objective: The average age at the time of spinal cord injury (SCI) has increased to 43 years old. Middle-aged mice (14 months old, MO) exhibit impaired recovery after SCI with age-dependent increases in reactive oxygen species (ROS) production through NADPH oxidase (NOX) along with pro-inflammatory macrophage activation. Despite these aging differences, clinical therapies are being examined in individuals regardless of age based upon preclinical data generated primarily using young animals (∼4 MO). Our objective is to test the extent to which age affects SCI treatment efficacy. Specifically, we hypothesize that the effectiveness of apocynin, a NOX inhibitor, is age-dependent in SCI.

Methods: Apocynin treatment (5 mg/kg) or vehicle was administered 1 and 6 h after moderate T9 contusion SCI (50kdyn IH) and then daily for 1 week to 4 and 14 MO mice. Locomotor and anatomical recovery was evaluated for 28 days. Monocyte-derived macrophage (MDM) and microglial activation and ROS production were evaluated at 3 and 28 days post-injury.

Results: Apocynin improved functional and anatomical recovery in 14 but not 4 MO SCI mice. Apocynin-mediated recovery was coincident with significant reductions in MDM infiltration and MDM-ROS production in 14 MO SCI mice. Importantly, microglial activation was unaffected by treatment.

Conclusion: These results indicate that apocynin exhibits age-dependent neuroprotective effects by blocking excessive neuroinflammation through NOX-mediated ROS production in MDMs. Further, these data identify age as a critical regulator for SCI treatment efficacy and indicate that pharmacologically reduced macrophage, but not microglia, activation and ROS production reverses age-associated neurological impairments.

Keywords: Age; Apocynin; Macrophage; Microglia; Monocyte; NADPH oxidase; Neuroinflammation; Reactive oxygen species; Spinal cord injury.

Publication types

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

MeSH terms

  • Acetophenones / pharmacology
  • Age Factors
  • Animals
  • Disease Models, Animal
  • Female
  • Inflammation
  • Macrophage Activation / physiology*
  • Macrophages / physiology
  • Mice
  • Mice, Inbred C57BL
  • Microglia / metabolism
  • NADPH Oxidases / metabolism*
  • NADPH Oxidases / physiology
  • Neuroprotective Agents
  • Oxidation-Reduction
  • Oxidative Stress / physiology
  • Reactive Oxygen Species / metabolism
  • Spinal Cord Injuries / immunology
  • Spinal Cord Injuries / physiopathology*

Substances

  • Acetophenones
  • Neuroprotective Agents
  • Reactive Oxygen Species
  • acetovanillone
  • NADPH Oxidases