Endocytosis, intracellular fate, accumulation, and agglomeration of titanium dioxide (TiO2) nanoparticles in the rainbow trout liver cell line RTL-W1

Tobias Lammel*, Aiga Mackevica, Bengt R Johansson, Joachim Sturve

*Corresponding author for this work

Research output: Contribution to journalJournal articleResearchpeer-review

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Abstract

There is increasing evidence that titanium dioxide (TiO2) nanoparticles (NPs) present in water or diet can be taken up by fish and accumulate in internal organs including the liver. However, their further fate in the organ is unknown. This study provides new insights into the interaction, uptake mechanism, intracellular trafficking, and fate of TiO2 NPs (Aeroxide® P25) in fish liver parenchymal cells (RTL-W1) in vitro using high-resolution transmission electron microscopy (TEM) and single particle inductively coupled plasma mass spectrometry (spICP-MS) as complementary analytical techniques. The results demonstrate that following their uptake via caveolae-mediated endocytosis, TiO2 NPs were trafficked through different intracellular compartments including early endosomes, multivesicular bodies, and late endosomes/endo-lysosomes, and eventually concentrated inside multilamellar vesicles. TEM and spICP-MS results provide evidence that uptake was nano-specific. Only NPs/NP agglomerates of a specific size range (~ 30-100 nm) were endocytosed; larger agglomerates were excluded from uptake and remained located in the extracellular space/exposure medium. NP number and mass inside cells increased linearly with time and was associated with an increase in particle diameter suggesting intracellular agglomeration/aggregation. No alterations in the expression of genes regulated by the redox balance-sensitive transcription factor Nrf-2 including superoxide dismutase, glutamyl cysteine ligase, glutathione synthetase, glutathione peroxidase, and glutathione S-transferase were observed. This shows that, despite the high intracellular NP burden (~ 3.9 × 102 ng Ti/mg protein after 24 h) and NP-interaction with mitochondria, cellular redox homeostasis was not significantly affected. This study contributes to a better mechanistic understanding of in vitro particokinetics as well as the potential fate and effects of TiO2 NPs in fish liver cells.
Original languageEnglish
JournalEnvironmental science and pollution research international
Volume26
Issue number15
Pages (from-to)15354-15372
ISSN0944-1344
DOIs
Publication statusPublished - 2019

Keywords

  • Bioaccumulation
  • Endocytosis
  • Fish
  • Hepatocyte
  • Particokinetics

Cite this

@article{29f8326cca2d4c438e938a1225c173bf,
title = "Endocytosis, intracellular fate, accumulation, and agglomeration of titanium dioxide (TiO2) nanoparticles in the rainbow trout liver cell line RTL-W1",
abstract = "There is increasing evidence that titanium dioxide (TiO2) nanoparticles (NPs) present in water or diet can be taken up by fish and accumulate in internal organs including the liver. However, their further fate in the organ is unknown. This study provides new insights into the interaction, uptake mechanism, intracellular trafficking, and fate of TiO2 NPs (Aeroxide{\circledR} P25) in fish liver parenchymal cells (RTL-W1) in vitro using high-resolution transmission electron microscopy (TEM) and single particle inductively coupled plasma mass spectrometry (spICP-MS) as complementary analytical techniques. The results demonstrate that following their uptake via caveolae-mediated endocytosis, TiO2 NPs were trafficked through different intracellular compartments including early endosomes, multivesicular bodies, and late endosomes/endo-lysosomes, and eventually concentrated inside multilamellar vesicles. TEM and spICP-MS results provide evidence that uptake was nano-specific. Only NPs/NP agglomerates of a specific size range (~ 30-100 nm) were endocytosed; larger agglomerates were excluded from uptake and remained located in the extracellular space/exposure medium. NP number and mass inside cells increased linearly with time and was associated with an increase in particle diameter suggesting intracellular agglomeration/aggregation. No alterations in the expression of genes regulated by the redox balance-sensitive transcription factor Nrf-2 including superoxide dismutase, glutamyl cysteine ligase, glutathione synthetase, glutathione peroxidase, and glutathione S-transferase were observed. This shows that, despite the high intracellular NP burden (~ 3.9 × 102 ng Ti/mg protein after 24 h) and NP-interaction with mitochondria, cellular redox homeostasis was not significantly affected. This study contributes to a better mechanistic understanding of in vitro particokinetics as well as the potential fate and effects of TiO2 NPs in fish liver cells.",
keywords = "Bioaccumulation, Endocytosis, Fish, Hepatocyte, Particokinetics",
author = "Tobias Lammel and Aiga Mackevica and Johansson, {Bengt R} and Joachim Sturve",
year = "2019",
doi = "10.1007/s11356-019-04856-1",
language = "English",
volume = "26",
pages = "15354--15372",
journal = "Environmental Science and Pollution Research",
issn = "0944-1344",
publisher = "Springer",
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Endocytosis, intracellular fate, accumulation, and agglomeration of titanium dioxide (TiO2) nanoparticles in the rainbow trout liver cell line RTL-W1. / Lammel, Tobias; Mackevica, Aiga; Johansson, Bengt R; Sturve, Joachim.

In: Environmental science and pollution research international, Vol. 26, No. 15, 2019, p. 15354-15372.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Endocytosis, intracellular fate, accumulation, and agglomeration of titanium dioxide (TiO2) nanoparticles in the rainbow trout liver cell line RTL-W1

AU - Lammel, Tobias

AU - Mackevica, Aiga

AU - Johansson, Bengt R

AU - Sturve, Joachim

PY - 2019

Y1 - 2019

N2 - There is increasing evidence that titanium dioxide (TiO2) nanoparticles (NPs) present in water or diet can be taken up by fish and accumulate in internal organs including the liver. However, their further fate in the organ is unknown. This study provides new insights into the interaction, uptake mechanism, intracellular trafficking, and fate of TiO2 NPs (Aeroxide® P25) in fish liver parenchymal cells (RTL-W1) in vitro using high-resolution transmission electron microscopy (TEM) and single particle inductively coupled plasma mass spectrometry (spICP-MS) as complementary analytical techniques. The results demonstrate that following their uptake via caveolae-mediated endocytosis, TiO2 NPs were trafficked through different intracellular compartments including early endosomes, multivesicular bodies, and late endosomes/endo-lysosomes, and eventually concentrated inside multilamellar vesicles. TEM and spICP-MS results provide evidence that uptake was nano-specific. Only NPs/NP agglomerates of a specific size range (~ 30-100 nm) were endocytosed; larger agglomerates were excluded from uptake and remained located in the extracellular space/exposure medium. NP number and mass inside cells increased linearly with time and was associated with an increase in particle diameter suggesting intracellular agglomeration/aggregation. No alterations in the expression of genes regulated by the redox balance-sensitive transcription factor Nrf-2 including superoxide dismutase, glutamyl cysteine ligase, glutathione synthetase, glutathione peroxidase, and glutathione S-transferase were observed. This shows that, despite the high intracellular NP burden (~ 3.9 × 102 ng Ti/mg protein after 24 h) and NP-interaction with mitochondria, cellular redox homeostasis was not significantly affected. This study contributes to a better mechanistic understanding of in vitro particokinetics as well as the potential fate and effects of TiO2 NPs in fish liver cells.

AB - There is increasing evidence that titanium dioxide (TiO2) nanoparticles (NPs) present in water or diet can be taken up by fish and accumulate in internal organs including the liver. However, their further fate in the organ is unknown. This study provides new insights into the interaction, uptake mechanism, intracellular trafficking, and fate of TiO2 NPs (Aeroxide® P25) in fish liver parenchymal cells (RTL-W1) in vitro using high-resolution transmission electron microscopy (TEM) and single particle inductively coupled plasma mass spectrometry (spICP-MS) as complementary analytical techniques. The results demonstrate that following their uptake via caveolae-mediated endocytosis, TiO2 NPs were trafficked through different intracellular compartments including early endosomes, multivesicular bodies, and late endosomes/endo-lysosomes, and eventually concentrated inside multilamellar vesicles. TEM and spICP-MS results provide evidence that uptake was nano-specific. Only NPs/NP agglomerates of a specific size range (~ 30-100 nm) were endocytosed; larger agglomerates were excluded from uptake and remained located in the extracellular space/exposure medium. NP number and mass inside cells increased linearly with time and was associated with an increase in particle diameter suggesting intracellular agglomeration/aggregation. No alterations in the expression of genes regulated by the redox balance-sensitive transcription factor Nrf-2 including superoxide dismutase, glutamyl cysteine ligase, glutathione synthetase, glutathione peroxidase, and glutathione S-transferase were observed. This shows that, despite the high intracellular NP burden (~ 3.9 × 102 ng Ti/mg protein after 24 h) and NP-interaction with mitochondria, cellular redox homeostasis was not significantly affected. This study contributes to a better mechanistic understanding of in vitro particokinetics as well as the potential fate and effects of TiO2 NPs in fish liver cells.

KW - Bioaccumulation

KW - Endocytosis

KW - Fish

KW - Hepatocyte

KW - Particokinetics

U2 - 10.1007/s11356-019-04856-1

DO - 10.1007/s11356-019-04856-1

M3 - Journal article

VL - 26

SP - 15354

EP - 15372

JO - Environmental Science and Pollution Research

JF - Environmental Science and Pollution Research

SN - 0944-1344

IS - 15

ER -