Evaluation of toxicity of halloysite nanotubes and multi-walled carbon nanotubes to endothelial cells in vitro and blood vessels in vivo

Nanotoxicology. 2020 Oct;14(8):1017-1038. doi: 10.1080/17435390.2020.1780642. Epub 2020 Jun 23.

Abstract

Nanomaterials (NMs) with tubular structures, such as halloysite nanotubes (HNTs), have potential applications in biomedicine. Although the biocompatibility of HNTs has been investigated before, the toxicity of HNTs to blood vessels is rarely systemically evaluated. Herein, we compared the toxicity of HNTs and multi-walled carbon nanotubes (MWCNTs) to human umbilical vein endothelial cells (HUVECs) in vitro and blood vessels of mice in vivo. HUVECs internalized HNTs and MWCNTs, but the uptake of HNTs was not obviously changed by clathrin inhibitor. Exposure to NMs decreased cellular viability, activated apoptotic proteins and up-regulated adhesion molecules, including soluble vascular cell adhesion molecule 1 (sVCAM-1) and VCAM-1. As the mechanisms, NMs decreased NO levels, eNOS mRNA and eNOS/p-eNOS proteins. Meanwhile, NMs promoted intracellular ROS and autophagy dysfunction, shown as decreased protein levels of LC3, beclin-1 and ATG5. The eNOS regulator Kruppel-like factor 4 (KLF4) was inhibited, but another eNOS regulator KLF4 was surprisingly up-regulated. Under in vivo conditions, ICR mice intravenously injected with NMs (50 μg/mouse, once a day for 5 days) showed an increased percentage of neutrophils, monocytes and basophils. Meanwhile, autophagy dysfunction, eNOS uncoupling, activation of apoptotic proteins and alteration of KLF proteins were also observed in mouse aortas. All of the toxic effects were more pronounced for MWCNTs in comparison with HNTs based on the same mass concentrations. Our results may provide novel insights about the toxicity of NMs with tubular structures to blood vessels. Considering the toxicological data reported here, HNTs are probably safer nanocarriers compared with MWCNTs.

Keywords: Halloysite nanotubes (HNTs); Kruppel-like factor (KLF); autophagy; blood vessels; multi-walled carbon nanotubes (MWCNTs).

MeSH terms

  • Animals
  • Aorta / drug effects*
  • Aorta / metabolism
  • Aorta / pathology
  • Apoptosis / drug effects
  • Autophagy / drug effects
  • Blood Cell Count
  • Cell Culture Techniques
  • Cell Survival / drug effects
  • Cells, Cultured
  • Clay / chemistry*
  • Endoplasmic Reticulum Stress / drug effects
  • Human Umbilical Vein Endothelial Cells / drug effects*
  • Humans
  • Kruppel-Like Factor 4
  • Kruppel-Like Transcription Factors / metabolism
  • Mice
  • Mice, Inbred ICR
  • Nanotubes / chemistry
  • Nanotubes / toxicity*
  • Nanotubes, Carbon / chemistry
  • Nanotubes, Carbon / toxicity*
  • Nitric Oxide Synthase Type III / metabolism
  • Vascular Cell Adhesion Molecule-1 / metabolism

Substances

  • KLF4 protein, human
  • Klf4 protein, mouse
  • Kruppel-Like Factor 4
  • Kruppel-Like Transcription Factors
  • Nanotubes, Carbon
  • Vascular Cell Adhesion Molecule-1
  • NOS3 protein, human
  • Nitric Oxide Synthase Type III
  • Clay