α2δ1-mediated maladaptive sensory plasticity disrupts adipose tissue homeostasis following spinal cord injury

Cell Rep Med. 2024 May 21;5(5):101525. doi: 10.1016/j.xcrm.2024.101525. Epub 2024 Apr 24.

Abstract

Spinal cord injury (SCI) increases the risk of cardiometabolic disorders, including hypertension, dyslipidemia, and insulin resistance. Not only does SCI lead to pathological expansion of adipose tissue, but it also leads to ectopic lipid accumulation in organs integral to glucose and insulin metabolism. The pathophysiological changes that underlie adipose tissue dysfunction after SCI are unknown. Here, we find that SCI exacerbates lipolysis in epididymal white adipose tissue (eWAT). Whereas expression of the α2δ1 subunit of voltage-gated calcium channels increases in calcitonin gene-related peptide-positive dorsal root ganglia neurons that project to eWAT, conditional deletion of the gene encoding α2δ1 in these neurons normalizes eWAT lipolysis after SCI. Furthermore, α2δ1 pharmacological blockade through systemic administration of gabapentin also normalizes eWAT lipolysis after SCI, preventing ectopic lipid accumulation in the liver. Thus, our study provides insight into molecular causes of maladaptive sensory processing in eWAT, facilitating the development of strategies to reduce metabolic and cardiovascular complications after SCI.

Keywords: dorsal root ganglia neurons; epididymal white adipose tissue; gabapentin; lipolysis; spinal cord injury; α2δ1.

MeSH terms

  • Adipose Tissue / metabolism
  • Adipose Tissue, White* / metabolism
  • Animals
  • Calcitonin Gene-Related Peptide / genetics
  • Calcitonin Gene-Related Peptide / metabolism
  • Ganglia, Spinal / metabolism
  • Ganglia, Spinal / pathology
  • Homeostasis*
  • Lipolysis* / drug effects
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Neuronal Plasticity / drug effects
  • Neurons / metabolism
  • Neurons / pathology
  • Spinal Cord Injuries* / metabolism
  • Spinal Cord Injuries* / pathology
  • Spinal Cord Injuries* / physiopathology

Substances

  • Calcitonin Gene-Related Peptide