Sex Affects Cognitive Outcomes in HIV-1 Tat Transgenic Mice: Role of CCR5

ASN Neuro. 2025;17(1):2447338. doi: 10.1080/17590914.2024.2447338. Epub 2025 Jan 13.

Abstract

People living with HIV (PLWH) experience HIV-associated neurocognitive disorders (HAND), even though combination antiretroviral therapy (cART) suppresses HIV replication. HIV-1 transactivator of transcription (HIV-1 Tat) contributes to the development of HAND through neuroinflammatory and neurotoxic mechanisms. C-C chemokine 5 receptor (CCR5) is important in immune cell targeting and is a co-receptor for HIV viral entry into CD4+ cells. Notably, CCR5 has been implicated in cognition unrelated to HIV infection. Inhibition of CCR5 has been shown to improve learning and memory. To test whether CCR5 is involved in cognitive changes in HAND, we used a non-infectious, transgenic model in which HIV-1 Tat is inducibly expressed. Well-powered cohorts of male and female mice were placed on a diet containing doxycycline to induce Tat expression for 8-wks. Males showed Tat-mediated deficits in the Barnes maze test of spatial learning and memory; females showed no impairments. Deficits in the males were fully reversed by the CCR5 antagonist, maraviroc (MVC). Tat-mediated deficits were not found in novel object recognition or contextual fear conditioning in either sex. Based on earlier work, we hypothesized that MVC might increase brain-derived neurotrophic factor (BDNF), which is essential in maintaining synaptodendritic function. MVC did increase the mBDNF to proBDNF ratio in males, perhaps contributing to improved cognition.

Keywords: BDNF; Barnes maze; contextual fear conditioning; hippocampus; maraviroc (MVC).

MeSH terms

  • AIDS Dementia Complex / genetics
  • AIDS Dementia Complex / metabolism
  • Animals
  • Brain-Derived Neurotrophic Factor / genetics
  • Brain-Derived Neurotrophic Factor / metabolism
  • CCR5 Receptor Antagonists* / pharmacology
  • CCR5 Receptor Antagonists* / therapeutic use
  • Cognition / drug effects
  • Cognition / physiology
  • Disease Models, Animal
  • Fear / drug effects
  • Fear / physiology
  • Female
  • HIV-1 / genetics
  • Male
  • Maraviroc* / pharmacology
  • Maraviroc* / therapeutic use
  • Maze Learning / drug effects
  • Maze Learning / physiology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic*
  • Receptors, CCR5* / genetics
  • Receptors, CCR5* / metabolism
  • Sex Characteristics
  • tat Gene Products, Human Immunodeficiency Virus / genetics
  • tat Gene Products, Human Immunodeficiency Virus / metabolism

Substances

  • Receptors, CCR5
  • CCR5 protein, mouse
  • Maraviroc
  • CCR5 Receptor Antagonists
  • tat Gene Products, Human Immunodeficiency Virus
  • Brain-Derived Neurotrophic Factor