Paclitaxel-induced cognitive decline was attenuated by necroptosis inhibition

Neuroreport. 2025 Jan 8;36(1):61-69. doi: 10.1097/WNR.0000000000002121. Epub 2024 Dec 4.

Abstract

Anti-cancer agent paclitaxel induces cognitive impairment. Paclitaxel can induce limited neuron apoptosis and wide scope of neuroinflammation, but its precise mechanisms remain unclear. In this study, we determined paclitaxel causes necroptosis, a programmed cell death, via activation of the RIPK1-RIPK3-MLKL signaling pathway in hippocampal neurons (HT22 cells). Flow cytometric analysis, propidium iodide staining, and western blotting techniques were used to evaluate paclitaxel-induced necroptosis. Cell viability was determined using the Cell Counting Kit-8 assay, and the Ca2+ levels were measured using a Fluo-4 AM fluorescent probe. The number of cells positive for both annexin V and propidium iodide staining was significantly higher in paclitaxel-treated than vehicle-treated HT22 cells. Additionally, the nuclei of paclitaxel-treated cells exhibited more diffused necrotic propidium iodide staining than the vehicle-treated cells. The expression of necroptosis-associated proteins, including receptor-interacting protein kinase (RIPK)1, RIPK3, mixed lineage kinase domain-like protein (MLKL), and phosphorylated (p)-MLKL, were increased following paclitaxel treatment. Treating HT22 cells with necrostatin-1, a specific inhibitor for RIPK1, effectively decreased paclitaxel-induced necroptosis through lowering intracellular Ca2+ overload. In addition, administration of necrostatin-1 to paclitaxel-treated mice rescued cognitive impairments, as assessed by novel object recognition and Morris water maze tests. Necrostatin-1 also reduced the increases in necroptosis-associated protein levels of RIPK1, RIPK3, MLKL, and p-MLKL in hippocampal tissue of paclitaxel-treated mice. Paclitaxel induces cognitive deficits through RIPK1-mediated necroptosis. The inhibition of necroptosis may be a potential therapeutic approach to reduce paclitaxel-induced cognitive deficits.

MeSH terms

  • Animals
  • Antineoplastic Agents, Phytogenic / pharmacology
  • Antineoplastic Agents, Phytogenic / toxicity
  • Cell Line
  • Cognitive Dysfunction* / chemically induced
  • Cognitive Dysfunction* / drug therapy
  • Cognitive Dysfunction* / metabolism
  • Hippocampus / drug effects
  • Hippocampus / metabolism
  • Imidazoles / pharmacology
  • Indoles / pharmacology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Necroptosis* / drug effects
  • Neurons / drug effects
  • Neurons / metabolism
  • Paclitaxel* / toxicity
  • Protein Kinases / metabolism
  • Receptor-Interacting Protein Serine-Threonine Kinases* / metabolism

Substances

  • Paclitaxel
  • Receptor-Interacting Protein Serine-Threonine Kinases
  • Ripk1 protein, mouse
  • Protein Kinases
  • Antineoplastic Agents, Phytogenic
  • Indoles
  • necrostatin-1
  • Imidazoles
  • Ripk3 protein, mouse