Lipid Coating Modulates Effects of Nanoceria on Oxidative Metabolism in Human Embryonic Lung Fibroblasts: A Case of Cardiolipin

The unique redox properties of nanoscale cerium dioxide determine its diverse application in biology and medicine as a regulator of oxidative metabolism. Lipid modifiers of the nanoparticle surface change their biochemical properties and bioavailability. Complexes with lipids can be formed upon cont...

Full description

Saved in:
Bibliographic Details
Main Authors: Elena V. Proskurnina, Madina M. Sozarukova, Elizaveta S. Ershova, Ekaterina A. Savinova, Larisa V. Kameneva, Natalia N. Veiko, Maria A. Teplonogova, Vladimir P. Saprykin, Vladimir K. Ivanov, Svetlana V. Kostyuk
Format: Article
Language:English
Published: MDPI AG 2025-01-01
Series:Biomolecules
Subjects:
Online Access:https://www.mdpi.com/2218-273X/15/1/53
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1832588911148269568
author Elena V. Proskurnina
Madina M. Sozarukova
Elizaveta S. Ershova
Ekaterina A. Savinova
Larisa V. Kameneva
Natalia N. Veiko
Maria A. Teplonogova
Vladimir P. Saprykin
Vladimir K. Ivanov
Svetlana V. Kostyuk
author_facet Elena V. Proskurnina
Madina M. Sozarukova
Elizaveta S. Ershova
Ekaterina A. Savinova
Larisa V. Kameneva
Natalia N. Veiko
Maria A. Teplonogova
Vladimir P. Saprykin
Vladimir K. Ivanov
Svetlana V. Kostyuk
author_sort Elena V. Proskurnina
collection DOAJ
description The unique redox properties of nanoscale cerium dioxide determine its diverse application in biology and medicine as a regulator of oxidative metabolism. Lipid modifiers of the nanoparticle surface change their biochemical properties and bioavailability. Complexes with lipids can be formed upon contact of the nanoparticles with the membrane. The effects of lipid coating on nanoceria have not been studied yet. Here, we assessed the effect of bare and cardiolipin-coated CeO<sub>2</sub> on the expression of oxidative metabolism genes in human embryonic lung fibroblasts. Cell viability, mitochondrial activity, intracellular reactive oxygen species, NOX4, NRF2, and NF-κB expression, oxidative DNA damage/repair, autophagy, and cell proliferation were studied. We used an MTT assay, fluorescence microscopy, real-time reverse transcription polymerase chain reaction, and flow cytometry. At a concentration of 1.5 μM, bare and cardiolipin-coated nanoceria penetrated into cells within 1–3 h. Cell survival, mitochondrial activity, and the proliferative effect were similar for bare and cardiolipin-coated nanoceria. Intracellular ROS, activation of NOX4, NRF2, and NF-kB, DNA oxidative damage, and DNA break/repair were different. Cardiolipin-coated nanoceria induced intracellular oxidative stress and short-term activation of these genes and DNA damage/break/repair. Unlike bare nanoceria, cardiolipin-coated nanoceria induced autophagy. Thus, the effects of cardiolipin-coated nanoceria are determined by both the nanoceria itself and cardiolipin. Presumably, the differences in properties are due to lipid peroxidation of cardiolipin. This effect needs to be taken into account when developing nanoceria-based drugs targeting mitochondria.
format Article
id doaj-art-7f05191c18a548eb8f6274738da476e3
institution Kabale University
issn 2218-273X
language English
publishDate 2025-01-01
publisher MDPI AG
record_format Article
series Biomolecules
spelling doaj-art-7f05191c18a548eb8f6274738da476e32025-01-24T13:25:00ZengMDPI AGBiomolecules2218-273X2025-01-011515310.3390/biom15010053Lipid Coating Modulates Effects of Nanoceria on Oxidative Metabolism in Human Embryonic Lung Fibroblasts: A Case of CardiolipinElena V. Proskurnina0Madina M. Sozarukova1Elizaveta S. Ershova2Ekaterina A. Savinova3Larisa V. Kameneva4Natalia N. Veiko5Maria A. Teplonogova6Vladimir P. Saprykin7Vladimir K. Ivanov8Svetlana V. Kostyuk9Research Centre for Medical Genetics, ul. Moskvorechye 1, Moscow 115522, RussiaKurnakov Institute of General and Inorganic Chemistry of the Russian Academy of Sciences, Leninskii Prospect 31, Moscow 119071, RussiaResearch Centre for Medical Genetics, ul. Moskvorechye 1, Moscow 115522, RussiaResearch Centre for Medical Genetics, ul. Moskvorechye 1, Moscow 115522, RussiaResearch Centre for Medical Genetics, ul. Moskvorechye 1, Moscow 115522, RussiaResearch Centre for Medical Genetics, ul. Moskvorechye 1, Moscow 115522, RussiaKurnakov Institute of General and Inorganic Chemistry of the Russian Academy of Sciences, Leninskii Prospect 31, Moscow 119071, RussiaFaculty of Biotechnology and Fisheries, K.G. Razumovsky Moscow State University of Technologies and Management, Zemlyanoy Val Str. 73, Moscow 109004, RussiaKurnakov Institute of General and Inorganic Chemistry of the Russian Academy of Sciences, Leninskii Prospect 31, Moscow 119071, RussiaResearch Centre for Medical Genetics, ul. Moskvorechye 1, Moscow 115522, RussiaThe unique redox properties of nanoscale cerium dioxide determine its diverse application in biology and medicine as a regulator of oxidative metabolism. Lipid modifiers of the nanoparticle surface change their biochemical properties and bioavailability. Complexes with lipids can be formed upon contact of the nanoparticles with the membrane. The effects of lipid coating on nanoceria have not been studied yet. Here, we assessed the effect of bare and cardiolipin-coated CeO<sub>2</sub> on the expression of oxidative metabolism genes in human embryonic lung fibroblasts. Cell viability, mitochondrial activity, intracellular reactive oxygen species, NOX4, NRF2, and NF-κB expression, oxidative DNA damage/repair, autophagy, and cell proliferation were studied. We used an MTT assay, fluorescence microscopy, real-time reverse transcription polymerase chain reaction, and flow cytometry. At a concentration of 1.5 μM, bare and cardiolipin-coated nanoceria penetrated into cells within 1–3 h. Cell survival, mitochondrial activity, and the proliferative effect were similar for bare and cardiolipin-coated nanoceria. Intracellular ROS, activation of NOX4, NRF2, and NF-kB, DNA oxidative damage, and DNA break/repair were different. Cardiolipin-coated nanoceria induced intracellular oxidative stress and short-term activation of these genes and DNA damage/break/repair. Unlike bare nanoceria, cardiolipin-coated nanoceria induced autophagy. Thus, the effects of cardiolipin-coated nanoceria are determined by both the nanoceria itself and cardiolipin. Presumably, the differences in properties are due to lipid peroxidation of cardiolipin. This effect needs to be taken into account when developing nanoceria-based drugs targeting mitochondria.https://www.mdpi.com/2218-273X/15/1/53cardiolipin-coated nanoceriaoxidative metabolism genesoxidative DNA damagecell proliferationautophagyhuman embryonic lung fibroblasts
spellingShingle Elena V. Proskurnina
Madina M. Sozarukova
Elizaveta S. Ershova
Ekaterina A. Savinova
Larisa V. Kameneva
Natalia N. Veiko
Maria A. Teplonogova
Vladimir P. Saprykin
Vladimir K. Ivanov
Svetlana V. Kostyuk
Lipid Coating Modulates Effects of Nanoceria on Oxidative Metabolism in Human Embryonic Lung Fibroblasts: A Case of Cardiolipin
Biomolecules
cardiolipin-coated nanoceria
oxidative metabolism genes
oxidative DNA damage
cell proliferation
autophagy
human embryonic lung fibroblasts
title Lipid Coating Modulates Effects of Nanoceria on Oxidative Metabolism in Human Embryonic Lung Fibroblasts: A Case of Cardiolipin
title_full Lipid Coating Modulates Effects of Nanoceria on Oxidative Metabolism in Human Embryonic Lung Fibroblasts: A Case of Cardiolipin
title_fullStr Lipid Coating Modulates Effects of Nanoceria on Oxidative Metabolism in Human Embryonic Lung Fibroblasts: A Case of Cardiolipin
title_full_unstemmed Lipid Coating Modulates Effects of Nanoceria on Oxidative Metabolism in Human Embryonic Lung Fibroblasts: A Case of Cardiolipin
title_short Lipid Coating Modulates Effects of Nanoceria on Oxidative Metabolism in Human Embryonic Lung Fibroblasts: A Case of Cardiolipin
title_sort lipid coating modulates effects of nanoceria on oxidative metabolism in human embryonic lung fibroblasts a case of cardiolipin
topic cardiolipin-coated nanoceria
oxidative metabolism genes
oxidative DNA damage
cell proliferation
autophagy
human embryonic lung fibroblasts
url https://www.mdpi.com/2218-273X/15/1/53
work_keys_str_mv AT elenavproskurnina lipidcoatingmodulateseffectsofnanoceriaonoxidativemetabolisminhumanembryoniclungfibroblastsacaseofcardiolipin
AT madinamsozarukova lipidcoatingmodulateseffectsofnanoceriaonoxidativemetabolisminhumanembryoniclungfibroblastsacaseofcardiolipin
AT elizavetasershova lipidcoatingmodulateseffectsofnanoceriaonoxidativemetabolisminhumanembryoniclungfibroblastsacaseofcardiolipin
AT ekaterinaasavinova lipidcoatingmodulateseffectsofnanoceriaonoxidativemetabolisminhumanembryoniclungfibroblastsacaseofcardiolipin
AT larisavkameneva lipidcoatingmodulateseffectsofnanoceriaonoxidativemetabolisminhumanembryoniclungfibroblastsacaseofcardiolipin
AT natalianveiko lipidcoatingmodulateseffectsofnanoceriaonoxidativemetabolisminhumanembryoniclungfibroblastsacaseofcardiolipin
AT mariaateplonogova lipidcoatingmodulateseffectsofnanoceriaonoxidativemetabolisminhumanembryoniclungfibroblastsacaseofcardiolipin
AT vladimirpsaprykin lipidcoatingmodulateseffectsofnanoceriaonoxidativemetabolisminhumanembryoniclungfibroblastsacaseofcardiolipin
AT vladimirkivanov lipidcoatingmodulateseffectsofnanoceriaonoxidativemetabolisminhumanembryoniclungfibroblastsacaseofcardiolipin
AT svetlanavkostyuk lipidcoatingmodulateseffectsofnanoceriaonoxidativemetabolisminhumanembryoniclungfibroblastsacaseofcardiolipin