Bacterial Magnetosomes Release Iron Ions and Induce Regulation of Iron Homeostasis in Endothelial Cells

Magnetosomes (MAGs) extracted from magnetotactic bacteria are well-defined membrane-enveloped single-domain magnetic nanoparticles. Due to their superior magnetic and structural properties, MAGs constitute potential materials that can be manipulated via genetic and chemical engineering for use in bi...

Full description

Bibliographic Details
Main Authors: Wenjia Lai, Dan Li, Qingsong Wang, Yan Ma, Jiesheng Tian, Qiaojun Fang
Format: Article
Language:English
Published: MDPI AG 2022-11-01
Series:Nanomaterials
Subjects:
Online Access:https://www.mdpi.com/2079-4991/12/22/3995
_version_ 1827643909601230848
author Wenjia Lai
Dan Li
Qingsong Wang
Yan Ma
Jiesheng Tian
Qiaojun Fang
author_facet Wenjia Lai
Dan Li
Qingsong Wang
Yan Ma
Jiesheng Tian
Qiaojun Fang
author_sort Wenjia Lai
collection DOAJ
description Magnetosomes (MAGs) extracted from magnetotactic bacteria are well-defined membrane-enveloped single-domain magnetic nanoparticles. Due to their superior magnetic and structural properties, MAGs constitute potential materials that can be manipulated via genetic and chemical engineering for use in biomedical and biotechnological applications. However, the long-term effects exerted by MAGs on cells are of concern in the context of in vivo applications. Meanwhile, it remains relatively unclear which mechanisms are employed by cells to process and degrade MAGs. Hence, a better understanding of MAGs’ degradation and fundamental signal modulations occurring throughout this process is essential. In the current study, we investigated the potential actions of MAGs on endothelial cells over a 10-day period. MAGs were retained in cells and found to gradually gather in the lysosome-like vesicles. Meanwhile, iron-ion release was observed. Proteomics further revealed a potential cellular mechanism underlying MAGs degradation, in which a group of proteins associated with vesicle biogenesis, and lysosomal enzymes, which participate in protein hydrolysis and lipid degradation, were rapidly upregulated. Moreover, the released iron triggered the regulation of the iron metabolic profiles. However, given that the levels of cell oxidative damage were relatively stable, the released iron ions were handled by iron metabolic profiles and incorporated into normal metabolic routes. These results provide insights into the cell response to MAGs degradation that may improve their in vivo applications.
first_indexed 2024-03-09T18:05:41Z
format Article
id doaj.art-169c0a96afab4e3bb326fc8236b5244e
institution Directory Open Access Journal
issn 2079-4991
language English
last_indexed 2024-03-09T18:05:41Z
publishDate 2022-11-01
publisher MDPI AG
record_format Article
series Nanomaterials
spelling doaj.art-169c0a96afab4e3bb326fc8236b5244e2023-11-24T09:27:58ZengMDPI AGNanomaterials2079-49912022-11-011222399510.3390/nano12223995Bacterial Magnetosomes Release Iron Ions and Induce Regulation of Iron Homeostasis in Endothelial CellsWenjia Lai0Dan Li1Qingsong Wang2Yan Ma3Jiesheng Tian4Qiaojun Fang5Division of Nanotechnology Development, National Center for Nanoscience and Technology, Chinese Academy of Sciences, Beijing 100190, ChinaLaboratory of Theoretical and Computational Nanoscience, National Center for Nanoscience and Technology, Chinese Academy of Sciences, Beijing 100190, ChinaState Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing 100871, ChinaAviation Service Department, Yantai Engineering & Technology College, Yantai 264006, ChinaState Key Laboratories for Agrobiotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, ChinaLaboratory of Theoretical and Computational Nanoscience, National Center for Nanoscience and Technology, Chinese Academy of Sciences, Beijing 100190, ChinaMagnetosomes (MAGs) extracted from magnetotactic bacteria are well-defined membrane-enveloped single-domain magnetic nanoparticles. Due to their superior magnetic and structural properties, MAGs constitute potential materials that can be manipulated via genetic and chemical engineering for use in biomedical and biotechnological applications. However, the long-term effects exerted by MAGs on cells are of concern in the context of in vivo applications. Meanwhile, it remains relatively unclear which mechanisms are employed by cells to process and degrade MAGs. Hence, a better understanding of MAGs’ degradation and fundamental signal modulations occurring throughout this process is essential. In the current study, we investigated the potential actions of MAGs on endothelial cells over a 10-day period. MAGs were retained in cells and found to gradually gather in the lysosome-like vesicles. Meanwhile, iron-ion release was observed. Proteomics further revealed a potential cellular mechanism underlying MAGs degradation, in which a group of proteins associated with vesicle biogenesis, and lysosomal enzymes, which participate in protein hydrolysis and lipid degradation, were rapidly upregulated. Moreover, the released iron triggered the regulation of the iron metabolic profiles. However, given that the levels of cell oxidative damage were relatively stable, the released iron ions were handled by iron metabolic profiles and incorporated into normal metabolic routes. These results provide insights into the cell response to MAGs degradation that may improve their in vivo applications.https://www.mdpi.com/2079-4991/12/22/3995magnetosomeendothelial celldegradationquantitative proteomiciron metabolism
spellingShingle Wenjia Lai
Dan Li
Qingsong Wang
Yan Ma
Jiesheng Tian
Qiaojun Fang
Bacterial Magnetosomes Release Iron Ions and Induce Regulation of Iron Homeostasis in Endothelial Cells
Nanomaterials
magnetosome
endothelial cell
degradation
quantitative proteomic
iron metabolism
title Bacterial Magnetosomes Release Iron Ions and Induce Regulation of Iron Homeostasis in Endothelial Cells
title_full Bacterial Magnetosomes Release Iron Ions and Induce Regulation of Iron Homeostasis in Endothelial Cells
title_fullStr Bacterial Magnetosomes Release Iron Ions and Induce Regulation of Iron Homeostasis in Endothelial Cells
title_full_unstemmed Bacterial Magnetosomes Release Iron Ions and Induce Regulation of Iron Homeostasis in Endothelial Cells
title_short Bacterial Magnetosomes Release Iron Ions and Induce Regulation of Iron Homeostasis in Endothelial Cells
title_sort bacterial magnetosomes release iron ions and induce regulation of iron homeostasis in endothelial cells
topic magnetosome
endothelial cell
degradation
quantitative proteomic
iron metabolism
url https://www.mdpi.com/2079-4991/12/22/3995
work_keys_str_mv AT wenjialai bacterialmagnetosomesreleaseironionsandinduceregulationofironhomeostasisinendothelialcells
AT danli bacterialmagnetosomesreleaseironionsandinduceregulationofironhomeostasisinendothelialcells
AT qingsongwang bacterialmagnetosomesreleaseironionsandinduceregulationofironhomeostasisinendothelialcells
AT yanma bacterialmagnetosomesreleaseironionsandinduceregulationofironhomeostasisinendothelialcells
AT jieshengtian bacterialmagnetosomesreleaseironionsandinduceregulationofironhomeostasisinendothelialcells
AT qiaojunfang bacterialmagnetosomesreleaseironionsandinduceregulationofironhomeostasisinendothelialcells