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Decrease in membrane fluidity and traction force induced by silica-coated magnetic nanoparticles

BACKGROUND: Nanoparticles are being increasingly used in biomedical applications owing to their unique physical and chemical properties and small size. However, their biophysical assessment and evaluation of side-effects remain challenging. We addressed this issue by investigating the effects of sil...

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Autores principales: Shin, Tae Hwan, Ketebo, Abdurazak Aman, Lee, Da Yeon, Lee, Seungah, Kang, Seong Ho, Basith, Shaherin, Manavalan, Balachandran, Kwon, Do Hyeon, Park, Sungsu, Lee, Gwang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7802323/
https://www.ncbi.nlm.nih.gov/pubmed/33430909
http://dx.doi.org/10.1186/s12951-020-00765-5
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author Shin, Tae Hwan
Ketebo, Abdurazak Aman
Lee, Da Yeon
Lee, Seungah
Kang, Seong Ho
Basith, Shaherin
Manavalan, Balachandran
Kwon, Do Hyeon
Park, Sungsu
Lee, Gwang
author_facet Shin, Tae Hwan
Ketebo, Abdurazak Aman
Lee, Da Yeon
Lee, Seungah
Kang, Seong Ho
Basith, Shaherin
Manavalan, Balachandran
Kwon, Do Hyeon
Park, Sungsu
Lee, Gwang
author_sort Shin, Tae Hwan
collection PubMed
description BACKGROUND: Nanoparticles are being increasingly used in biomedical applications owing to their unique physical and chemical properties and small size. However, their biophysical assessment and evaluation of side-effects remain challenging. We addressed this issue by investigating the effects of silica-coated magnetic nanoparticles containing rhodamine B isothiocyanate [MNPs@SiO(2)(RITC)] on biophysical aspects, such as membrane fluidity and traction force of human embryonic kidney 293 (HEK293) cells. We further extended our understanding on the biophysical effects of nanoparticles on cells using a combination of metabolic profiling and transcriptomic network analysis. RESULTS: Overdose (1.0 μg/µL) treatment with MNPs@SiO(2)(RITC) induced lipid peroxidation and decreased membrane fluidity in HEK293 cells. In addition, HEK293 cells were morphologically shrunk, and their aspect ratio was significantly decreased. We found that each traction force (measured in micropillar) was increased, thereby increasing the total traction force in MNPs@SiO(2)(RITC)-treated HEK293 cells. Due to the reduction in membrane fluidity and elevation of traction force, the velocity of cell movement was also significantly decreased. Moreover, intracellular level of adenosine triphosphate (ATP) was also decreased in a dose-dependent manner upon treatment with MNPs@SiO(2)(RITC). To understand these biophysical changes in cells, we analysed the transcriptome and metabolic profiles and generated a metabotranscriptomics network, which revealed relationships among peroxidation of lipids, focal adhesion, cell movement, and related genes and metabolites. Furthermore, in silico prediction of the network showed increment in the peroxidation of lipids and suppression of focal adhesion and cell movement. CONCLUSION: Taken together, our results demonstrated that overdose of MNPs@SiO(2)(RITC) impairs cellular movement, followed by changes in the biophysical properties of cells, thus highlighting the need for biophysical assessment of nanoparticle-induced side-effects. [Image: see text]
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spelling pubmed-78023232021-01-13 Decrease in membrane fluidity and traction force induced by silica-coated magnetic nanoparticles Shin, Tae Hwan Ketebo, Abdurazak Aman Lee, Da Yeon Lee, Seungah Kang, Seong Ho Basith, Shaherin Manavalan, Balachandran Kwon, Do Hyeon Park, Sungsu Lee, Gwang J Nanobiotechnology Research BACKGROUND: Nanoparticles are being increasingly used in biomedical applications owing to their unique physical and chemical properties and small size. However, their biophysical assessment and evaluation of side-effects remain challenging. We addressed this issue by investigating the effects of silica-coated magnetic nanoparticles containing rhodamine B isothiocyanate [MNPs@SiO(2)(RITC)] on biophysical aspects, such as membrane fluidity and traction force of human embryonic kidney 293 (HEK293) cells. We further extended our understanding on the biophysical effects of nanoparticles on cells using a combination of metabolic profiling and transcriptomic network analysis. RESULTS: Overdose (1.0 μg/µL) treatment with MNPs@SiO(2)(RITC) induced lipid peroxidation and decreased membrane fluidity in HEK293 cells. In addition, HEK293 cells were morphologically shrunk, and their aspect ratio was significantly decreased. We found that each traction force (measured in micropillar) was increased, thereby increasing the total traction force in MNPs@SiO(2)(RITC)-treated HEK293 cells. Due to the reduction in membrane fluidity and elevation of traction force, the velocity of cell movement was also significantly decreased. Moreover, intracellular level of adenosine triphosphate (ATP) was also decreased in a dose-dependent manner upon treatment with MNPs@SiO(2)(RITC). To understand these biophysical changes in cells, we analysed the transcriptome and metabolic profiles and generated a metabotranscriptomics network, which revealed relationships among peroxidation of lipids, focal adhesion, cell movement, and related genes and metabolites. Furthermore, in silico prediction of the network showed increment in the peroxidation of lipids and suppression of focal adhesion and cell movement. CONCLUSION: Taken together, our results demonstrated that overdose of MNPs@SiO(2)(RITC) impairs cellular movement, followed by changes in the biophysical properties of cells, thus highlighting the need for biophysical assessment of nanoparticle-induced side-effects. [Image: see text] BioMed Central 2021-01-11 /pmc/articles/PMC7802323/ /pubmed/33430909 http://dx.doi.org/10.1186/s12951-020-00765-5 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Shin, Tae Hwan
Ketebo, Abdurazak Aman
Lee, Da Yeon
Lee, Seungah
Kang, Seong Ho
Basith, Shaherin
Manavalan, Balachandran
Kwon, Do Hyeon
Park, Sungsu
Lee, Gwang
Decrease in membrane fluidity and traction force induced by silica-coated magnetic nanoparticles
title Decrease in membrane fluidity and traction force induced by silica-coated magnetic nanoparticles
title_full Decrease in membrane fluidity and traction force induced by silica-coated magnetic nanoparticles
title_fullStr Decrease in membrane fluidity and traction force induced by silica-coated magnetic nanoparticles
title_full_unstemmed Decrease in membrane fluidity and traction force induced by silica-coated magnetic nanoparticles
title_short Decrease in membrane fluidity and traction force induced by silica-coated magnetic nanoparticles
title_sort decrease in membrane fluidity and traction force induced by silica-coated magnetic nanoparticles
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7802323/
https://www.ncbi.nlm.nih.gov/pubmed/33430909
http://dx.doi.org/10.1186/s12951-020-00765-5
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