Region-Specific Impact of Repeated Synthetic Cannabinoid Exposure and Withdrawal on Endocannabinoid Signaling, Gliosis, and Inflammatory Markers in the Prefrontal Cortex and Hippocampus

Biomolecules. 2025 Mar 14;15(3):417. doi: 10.3390/biom15030417.

Abstract

Synthetic cannabinoid use raises concerns about its neuroinflammatory effects, including molecular adaptations of the endocannabinoid system (ECS) in the brain. This study investigates the pharmacological effects of 14-day repeated intraperitoneal administration, as well as 14-day administration followed by a 7-day withdrawal period of two synthetic cannabinoids: WIN55,212-2 and HU-210. The study assessed gene expression and protein markers related to the ECS, gliosis, and inflammation in two brain regions critical for cognitive processes and memory-key components of addiction pathways-the prefrontal cortex (PFC) and the hippocampus of rats. Our findings showed that repeated WIN55,212-2 administration induced adaptations in the ECS and reduced IBA1, a glial protein marker, along with inflammatory responses likely mediated through CB2 activity. Notably, regional differences emerged in the hippocampus, where repeated administration of WIN55,212-2 and HU-210 increased IBA1 and inflammatory markers, effects unrelated to CB2 activity. Withdrawal from WIN55,212-2 in the PFC, as well as from both compounds in the hippocampus, decreased IBA1 levels. This was associated with altered protein expression of cannabinoid-synthesizing and degrading enzymes, favoring acylethanolamide synthesis. These findings highlight region-specific effects of synthetic cannabinoids on cannabinoid signaling, gliosis, and inflammation. Further research is needed to elucidate the long-term neurobiological consequences of synthetic cannabinoid use and withdrawal.

Keywords: HU-210; WIN 55,212-2; gliosis; hippocampus; inflammation; legal medicine; neuroanatomy; prefrontal cortex; synthetic cannabinoids; toxicology; withdrawal.

MeSH terms

  • Animals
  • Benzoxazines* / pharmacology
  • Biomarkers / metabolism
  • Calcium-Binding Proteins
  • Cannabinoids* / metabolism
  • Cannabinoids* / pharmacology
  • Endocannabinoids* / metabolism
  • Gliosis* / chemically induced
  • Gliosis* / metabolism
  • Gliosis* / pathology
  • Hippocampus* / drug effects
  • Hippocampus* / metabolism
  • Inflammation / chemically induced
  • Inflammation / metabolism
  • Inflammation / pathology
  • Male
  • Microfilament Proteins / genetics
  • Microfilament Proteins / metabolism
  • Morpholines / pharmacology
  • Naphthalenes / pharmacology
  • Prefrontal Cortex* / drug effects
  • Prefrontal Cortex* / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, Cannabinoid, CB2 / genetics
  • Receptor, Cannabinoid, CB2 / metabolism
  • Signal Transduction* / drug effects

Substances

  • Endocannabinoids
  • Cannabinoids
  • Benzoxazines
  • Naphthalenes
  • (3R)-((2,3-dihydro-5-methyl-3-((4-morpholinyl)methyl)pyrrolo-(1,2,3-de)-1,4-benzoxazin-6-yl)(1-naphthalenyl))methanone
  • Morpholines
  • Aif1 protein, rat
  • Biomarkers
  • Microfilament Proteins
  • Receptor, Cannabinoid, CB2
  • Calcium-Binding Proteins