Minocycline prevents early age-related cognitive decline in a mouse model of intellectual disability caused by ZBTB18/RP58 haploinsufficiency

J Neuroinflammation. 2024 Oct 12;21(1):260. doi: 10.1186/s12974-024-03217-1.

Abstract

Haploinsufficiency of the transcriptional repressor ZBTB18/RP58 is associated with intellectual disability. However, the mechanisms causing this disability are unknown, and preventative measures and treatments are not available. Here, we assessed multiple behaviors in Zbtb18/Rp58 heterozygous-knockout mice, and examined local field potentials, DNA fragmentation, mitochondrial morphology, and performed histochemical and transcriptome analyses in the hippocampus to evaluate chronic inflammation. In wild-type mice, object location memory was present at a similar level at 2 and 4-5 months of age, and became impaired at 12-18 months. In contrast, Zbtb18/Rp58 heterozygous-knockout mice displayed early onset impairments in object location memory by 4-5 months of age. These mice also exhibited earlier accumulation of DNA and mitochondrial damage, and activated microglia in the dentate gyrus, which are associated with defective DNA repair. Notably, chronic minocycline therapy, which has neuroprotective and anti-inflammatory effects, attenuated age-related phenotypes, including accumulation of DNA damage, increased microglial activation, and impairment of object location memory. Our results suggest that Zbtb18/Rp58 activity is required for DNA repair and its reduction results in DNA and mitochondrial damage, increased activation of microglia, and inflammation, leading to accelerated declines in cognitive functions. Minocycline has potential as a therapeutic agent for the treatment of ZBTB18/RP58 haploinsufficiency-associated cognitive dysfunction.

Keywords: Cognitive decline; DNA damage; DNA repair; Inflammation; Intellectual disability; ZBTB18/RP58.

MeSH terms

  • Aging / drug effects
  • Aging / genetics
  • Aging / metabolism
  • Animals
  • Cognitive Dysfunction* / genetics
  • Cognitive Dysfunction* / metabolism
  • Cognitive Dysfunction* / pathology
  • Cognitive Dysfunction* / prevention & control
  • Disease Models, Animal*
  • Haploinsufficiency*
  • Hippocampus / drug effects
  • Hippocampus / metabolism
  • Hippocampus / pathology
  • Intellectual Disability* / genetics
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Minocycline* / pharmacology
  • Minocycline* / therapeutic use
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism

Substances

  • Minocycline
  • Repressor Proteins