Neural stem cells traffic functional mitochondria via extracellular vesicles

Neural stem cell (NSC) transplantation induces recovery in animal models of central nervous system (CNS) diseases. Although the replacement of lost endogenous cells was originally proposed as the primary healing mechanism of NSC grafts, it is now clear that transplanted NSCs operate via multiple mec...

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Published inPLoS biology Vol. 19; no. 4; p. e3001166
Main Authors Peruzzotti-Jametti, Luca, Bernstock, Joshua D., Willis, Cory M., Manferrari, Giulia, Rogall, Rebecca, Fernandez-Vizarra, Erika, Williamson, James C., Braga, Alice, van den Bosch, Aletta, Leonardi, Tommaso, Krzak, Grzegorz, Kittel, Ágnes, Benincá, Cristiane, Vicario, Nunzio, Tan, Sisareuth, Bastos, Carlos, Bicci, Iacopo, Iraci, Nunzio, Smith, Jayden A., Peacock, Ben, Muller, Karin H., Lehner, Paul J., Buzas, Edit Iren, Faria, Nuno, Zeviani, Massimo, Frezza, Christian, Brisson, Alain, Matheson, Nicholas J., Viscomi, Carlo, Pluchino, Stefano
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 07.04.2021
Public Library of Science (PLoS)
Subjects
Animals
Annotations
Assembly
ATP synthase
Biochemistry, Molecular Biology
Biological Transport
Biology and Life Sciences
Cell organelles
Cells, Cultured
Cytochrome
Cytochrome b
Cytochrome-c oxidase
Cytochromes
Dehydrogenases
Electron transport chain
Enrichment
Experiments
Extracellular vesicles
Extracellular Vesicles - metabolism
Female
Gene expression
Genomes
Genomics
Green Fluorescent Proteins - genetics
Green Fluorescent Proteins - metabolism
Life Sciences
Localization
Medicine and Health Sciences
Membranes
Mesenchymal Stem Cells - metabolism
Mesenchymal Stem Cells - physiology
Metabolism
Mice
Mice, Inbred C57BL
Mice, Transgenic
Mitochondria
Mitochondria - metabolism
Mitochondrial DNA
Morphology
Multiplexing
NADH
NADH-ubiquinone oxidoreductase
Neural stem cells
Neural Stem Cells - metabolism
Neural Stem Cells - ultrastructure
Neurobiology
Neurons
Neurons and Cognition
Nicotinamide adenine dinucleotide
Ontology
Oxidase
Oxidoreductase
Physiological aspects
Polymerase chain reaction
Proteins
Research and Analysis Methods
Stem cells
Succinate dehydrogenase
Sulfur
Ubiquinone
Ubiquinone oxidoreductase
United Kingdom
Polymerase chain reaction
Phagocytes
Vesicles
Mitochondria
Computer software
Proteomics
Outer membrane proteins
Exosomes
Online AccessGet full text
ISSN1545-7885
1544-9173
1545-7885
DOI10.1371/journal.pbio.3001166

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Abstract Neural stem cell (NSC) transplantation induces recovery in animal models of central nervous system (CNS) diseases. Although the replacement of lost endogenous cells was originally proposed as the primary healing mechanism of NSC grafts, it is now clear that transplanted NSCs operate via multiple mechanisms, including the horizontal exchange of therapeutic cargoes to host cells via extracellular vesicles (EVs). EVs are membrane particles trafficking nucleic acids, proteins, metabolites and metabolic enzymes, lipids, and entire organelles. However, the function and the contribution of these cargoes to the broad therapeutic effects of NSCs are yet to be fully understood. Mitochondrial dysfunction is an established feature of several inflammatory and degenerative CNS disorders, most of which are potentially treatable with exogenous stem cell therapeutics. Herein, we investigated the hypothesis that NSCs release and traffic functional mitochondria via EVs to restore mitochondrial function in target cells. Untargeted proteomics revealed a significant enrichment of mitochondrial proteins spontaneously released by NSCs in EVs. Morphological and functional analyses confirmed the presence of ultrastructurally intact mitochondria within EVs with conserved membrane potential and respiration. We found that the transfer of these mitochondria from EVs to mtDNA-deficient L929 Rho 0 cells rescued mitochondrial function and increased Rho 0 cell survival. Furthermore, the incorporation of mitochondria from EVs into inflammatory mononuclear phagocytes restored normal mitochondrial dynamics and cellular metabolism and reduced the expression of pro-inflammatory markers in target cells. When transplanted in an animal model of multiple sclerosis, exogenous NSCs actively transferred mitochondria to mononuclear phagocytes and induced a significant amelioration of clinical deficits. Our data provide the first evidence that NSCs deliver functional mitochondria to target cells via EVs, paving the way for the development of novel (a)cellular approaches aimed at restoring mitochondrial dysfunction not only in multiple sclerosis, but also in degenerative neurological diseases.
AbstractList Neural stem cell (NSC) transplantation induces recovery in animal models of central nervous system (CNS) diseases. Although the replacement of lost endogenous cells was originally proposed as the primary healing mechanism of NSC grafts, it is now clear that transplanted NSCs operate via multiple mechanisms, including the horizontal exchange of therapeutic cargoes to host cells via extracellular vesicles (EVs). EVs are membrane particles trafficking nucleic acids, proteins, metabolites and metabolic enzymes, lipids, and entire organelles. However, the function and the contribution of these cargoes to the broad therapeutic effects of NSCs are yet to be fully understood. Mitochondrial dysfunction is an established feature of several inflammatory and degenerative CNS disorders, most of which are potentially treatable with exogenous stem cell therapeutics. Herein, we investigated the hypothesis that NSCs release and traffic functional mitochondria via EVs to restore mitochondrial function in target cells. Untargeted proteomics revealed a significant enrichment of mitochondrial proteins spontaneously released by NSCs in EVs. Morphological and functional analyses confirmed the presence of ultrastructurally intact mitochondria within EVs with conserved membrane potential and respiration. We found that the transfer of these mitochondria from EVs to mtDNA-deficient L929 Rho(0) cells rescued mitochondrial function and increased Rho(0) cell survival. Furthermore, the incorporation of mitochondria from EVs into inflammatory mononuclear phagocytes restored normal mitochondrial dynamics and cellular metabolism and reduced the expression of pro-inflammatory markers in target cells. When transplanted in an animal model of multiple sclerosis, exogenous NSCs actively transferred mitochondria to mononuclear phagocytes and induced a significant amelioration of clinical deficits. Our data provide the first evidence that NSCs deliver functional mitochondria to target cells via EVs, paving the way for the development of novel (a)cellular approaches aimed at restoring mitochondrial dysfunction not only in multiple sclerosis, but also in degenerative neurological diseases.
Neural stem cell (NSC) transplantation induces recovery in animal models of central nervous system (CNS) diseases. Although the replacement of lost endogenous cells was originally proposed as the primary healing mechanism of NSC grafts, it is now clear that transplanted NSCs operate via multiple mechanisms, including the horizontal exchange of therapeutic cargoes to host cells via extracellular vesicles (EVs). EVs are membrane particles trafficking nucleic acids, proteins, metabolites and metabolic enzymes, lipids, and entire organelles. However, the function and the contribution of these cargoes to the broad therapeutic effects of NSCs are yet to be fully understood. Mitochondrial dysfunction is an established feature of several inflammatory and degenerative CNS disorders, most of which are potentially treatable with exogenous stem cell therapeutics. Herein, we investigated the hypothesis that NSCs release and traffic functional mitochondria via EVs to restore mitochondrial function in target cells. Untargeted proteomics revealed a significant enrichment of mitochondrial proteins spontaneously released by NSCs in EVs. Morphological and functional analyses confirmed the presence of ultrastructurally intact mitochondria within EVs with conserved membrane potential and respiration. We found that the transfer of these mitochondria from EVs to mtDNA-deficient L929 Rho 0 cells rescued mitochondrial function and increased Rho 0 cell survival. Furthermore, the incorporation of mitochondria from EVs into inflammatory mononuclear phagocytes restored normal mitochondrial dynamics and cellular metabolism and reduced the expression of pro-inflammatory markers in target cells. When transplanted in an animal model of multiple sclerosis, exogenous NSCs actively transferred mitochondria to mononuclear phagocytes and induced a significant amelioration of clinical deficits. Our data provide the first evidence that NSCs deliver functional mitochondria to target cells via EVs, paving the way for the development of novel (a)cellular approaches aimed at restoring mitochondrial dysfunction not only in multiple sclerosis, but also in degenerative neurological diseases.
Volcano plots show statistical significance (y axis) vs. fold change (x axis) for 9,951/9,971 cellular proteins quantitated across all 3 biological replicates (no missing values) in the multiplex TMT-based functional proteomic experiment illustrated in a. Proteins annotated with the following GOCC subcellular localisations are highlighted in red: mitochondrial outer membrane (GO:0005741, enriched in EVs); mitochondrial inner membrane (GO: 0005743, enriched in EVs); and mitochondrial matrix (GO:0005759, enriched in EVs). Mitochondrial complex (C) proteins enriched in EVs and encoded in the mitochondrial (upper panel) or nuclear (lower panel) genomes in the multiplex TMT-based functional proteomic experiment include: NADH:ubiquinone oxidoreductase or CI [mtnd2 (ND2 subunit), mtnd5 (ND5 subunit), ndufaf6 (assembly factor 6), ndufa9 (subunit A9), ndufs3 (core subunit S3), ndufb5 (1 beta subcomplex subunit 5)], succinate dehydrogenase or CII [Sdha (Subunit A), sdhd (cytochrome b small subunit), sdhb (iron-sulfur subunit), sdhc (cytochrome b560 subunit)], cytochrome b-c1 or CIII [mt-cyb (cytochrome B), Uqcrfs1 (subunit 5), Uqcrc2 (subunit 2), coq10b (coenzyme Q10B), uqcrq (subunit 8)], cytochrome C oxidase or CIV [mt-co3 (oxidase III), mtco1 (oxidase I), mtco2 (oxidase II), cox15 (subunit 15), cox18 (assembly protein 18), cox6c (subunit 6C), cox5a (subunit 5a)] and ATP synthase or CV [atp5f1 (subunit gamma), atp5s (subunit S), atp5d (subunit delta), atp5h (subunit D)]. The mitochondrial encoded gene mt-ND1 (NADH-ubiquinone oxidoreductase chain 1) was found to be present in EVs, Mito, and NSCs (L929 Rho0 were used as negative controls). (f) Representative protein expression analysis by WB of NSCs, EVs, and isolated mitochondria (Mito). CI, II, II, IV, V, complex I, II, II, IV, V; EV, extracellular vesicle; FDR, false discovery rate; GOCC, Gene Ontology Cellular Component; NSC, neural stem cell; PCR, polymerase chain reaction; TMT, Tandem Mass Tag; WB, western blot. https://doi.org/10.1371/journal.pbio.3001166.g001 Using Gene Ontology Cellular Component (GOCC) annotations, we investigated the subcellular origin of proteins enriched in EVs compared with NSCs (Fig 1B).
Neural stem cell (NSC) transplantation induces recovery in animal models of central nervous system (CNS) diseases. Although the replacement of lost endogenous cells was originally proposed as the primary healing mechanism of NSC grafts, it is now clear that transplanted NSCs operate via multiple mechanisms, including the horizontal exchange of therapeutic cargoes to host cells via extracellular vesicles (EVs). EVs are membrane particles trafficking nucleic acids, proteins, metabolites and metabolic enzymes, lipids, and entire organelles. However, the function and the contribution of these cargoes to the broad therapeutic effects of NSCs are yet to be fully understood. Mitochondrial dysfunction is an established feature of several inflammatory and degenerative CNS disorders, most of which are potentially treatable with exogenous stem cell therapeutics. Herein, we investigated the hypothesis that NSCs release and traffic functional mitochondria via EVs to restore mitochondrial function in target cells. Untargeted proteomics revealed a significant enrichment of mitochondrial proteins spontaneously released by NSCs in EVs. Morphological and functional analyses confirmed the presence of ultrastructurally intact mitochondria within EVs with conserved membrane potential and respiration. We found that the transfer of these mitochondria from EVs to mtDNA-deficient L929 Rho0 cells rescued mitochondrial function and increased Rho0 cell survival. Furthermore, the incorporation of mitochondria from EVs into inflammatory mononuclear phagocytes restored normal mitochondrial dynamics and cellular metabolism and reduced the expression of pro-inflammatory markers in target cells. When transplanted in an animal model of multiple sclerosis, exogenous NSCs actively transferred mitochondria to mononuclear phagocytes and induced a significant amelioration of clinical deficits. Our data provide the first evidence that NSCs deliver functional mitochondria to target cells via EVs, paving the way for the development of novel (a)cellular approaches aimed at restoring mitochondrial dysfunction not only in multiple sclerosis, but also in degenerative neurological diseases.Neural stem cell (NSC) transplantation induces recovery in animal models of central nervous system (CNS) diseases. Although the replacement of lost endogenous cells was originally proposed as the primary healing mechanism of NSC grafts, it is now clear that transplanted NSCs operate via multiple mechanisms, including the horizontal exchange of therapeutic cargoes to host cells via extracellular vesicles (EVs). EVs are membrane particles trafficking nucleic acids, proteins, metabolites and metabolic enzymes, lipids, and entire organelles. However, the function and the contribution of these cargoes to the broad therapeutic effects of NSCs are yet to be fully understood. Mitochondrial dysfunction is an established feature of several inflammatory and degenerative CNS disorders, most of which are potentially treatable with exogenous stem cell therapeutics. Herein, we investigated the hypothesis that NSCs release and traffic functional mitochondria via EVs to restore mitochondrial function in target cells. Untargeted proteomics revealed a significant enrichment of mitochondrial proteins spontaneously released by NSCs in EVs. Morphological and functional analyses confirmed the presence of ultrastructurally intact mitochondria within EVs with conserved membrane potential and respiration. We found that the transfer of these mitochondria from EVs to mtDNA-deficient L929 Rho0 cells rescued mitochondrial function and increased Rho0 cell survival. Furthermore, the incorporation of mitochondria from EVs into inflammatory mononuclear phagocytes restored normal mitochondrial dynamics and cellular metabolism and reduced the expression of pro-inflammatory markers in target cells. When transplanted in an animal model of multiple sclerosis, exogenous NSCs actively transferred mitochondria to mononuclear phagocytes and induced a significant amelioration of clinical deficits. Our data provide the first evidence that NSCs deliver functional mitochondria to target cells via EVs, paving the way for the development of novel (a)cellular approaches aimed at restoring mitochondrial dysfunction not only in multiple sclerosis, but also in degenerative neurological diseases.
Neural stem cell (NSC) transplantation induces recovery in animal models of central nervous system (CNS) diseases. Although the replacement of lost endogenous cells was originally proposed as the primary healing mechanism of NSC grafts, it is now clear that transplanted NSCs operate via multiple mechanisms, including the horizontal exchange of therapeutic cargoes to host cells via extracellular vesicles (EVs). EVs are membrane particles trafficking nucleic acids, proteins, metabolites and metabolic enzymes, lipids, and entire organelles. However, the function and the contribution of these cargoes to the broad therapeutic effects of NSCs are yet to be fully understood. Mitochondrial dysfunction is an established feature of several inflammatory and degenerative CNS disorders, most of which are potentially treatable with exogenous stem cell therapeutics. Herein, we investigated the hypothesis that NSCs release and traffic functional mitochondria via EVs to restore mitochondrial function in target cells. Untargeted proteomics revealed a significant enrichment of mitochondrial proteins spontaneously released by NSCs in EVs. Morphological and functional analyses confirmed the presence of ultrastructurally intact mitochondria within EVs with conserved membrane potential and respiration. We found that the transfer of these mitochondria from EVs to mtDNA-deficient L929 Rho0 cells rescued mitochondrial function and increased Rho0 cell survival. Furthermore, the incorporation of mitochondria from EVs into inflammatory mononuclear phagocytes restored normal mitochondrial dynamics and cellular metabolism and reduced the expression of pro-inflammatory markers in target cells. When transplanted in an animal model of multiple sclerosis, exogenous NSCs actively transferred mitochondria to mononuclear phagocytes and induced a significant amelioration of clinical deficits. Our data provide the first evidence that NSCs deliver functional mitochondria to target cells via EVs, paving the way for the development of novel (a)cellular approaches aimed at restoring mitochondrial dysfunction not only in multiple sclerosis, but also in degenerative neurological diseases.
Neural stem cell (NSC) transplantation induces recovery in animal models of central nervous system (CNS) diseases. Although the replacement of lost endogenous cells was originally proposed as the primary healing mechanism of NSC grafts, it is now clear that transplanted NSCs operate via multiple mechanisms, including the horizontal exchange of therapeutic cargoes to host cells via extracellular vesicles (EVs). EVs are membrane particles trafficking nucleic acids, proteins, metabolites and metabolic enzymes, lipids, and entire organelles. However, the function and the contribution of these cargoes to the broad therapeutic effects of NSCs are yet to be fully understood. Mitochondrial dysfunction is an established feature of several inflammatory and degenerative CNS disorders, most of which are potentially treatable with exogenous stem cell therapeutics. Herein, we investigated the hypothesis that NSCs release and traffic functional mitochondria via EVs to restore mitochondrial function in target cells. Untargeted proteomics revealed a significant enrichment of mitochondrial proteins spontaneously released by NSCs in EVs. Morphological and functional analyses confirmed the presence of ultrastructurally intact mitochondria within EVs with conserved membrane potential and respiration. We found that the transfer of these mitochondria from EVs to mtDNA-deficient L929 Rho.sup.0 cells rescued mitochondrial function and increased Rho.sup.0 cell survival. Furthermore, the incorporation of mitochondria from EVs into inflammatory mononuclear phagocytes restored normal mitochondrial dynamics and cellular metabolism and reduced the expression of pro-inflammatory markers in target cells. When transplanted in an animal model of multiple sclerosis, exogenous NSCs actively transferred mitochondria to mononuclear phagocytes and induced a significant amelioration of clinical deficits. Our data provide the first evidence that NSCs deliver functional mitochondria to target cells via EVs, paving the way for the development of novel (a)cellular approaches aimed at restoring mitochondrial dysfunction not only in multiple sclerosis, but also in degenerative neurological diseases.
Neural stem cell (NSC) transplantation induces recovery in animal models of central nervous system (CNS) diseases. Although the replacement of lost endogenous cells was originally proposed as the primary healing mechanism of NSC grafts, it is now clear that transplanted NSCs operate via multiple mechanisms, including the horizontal exchange of therapeutic cargoes to host cells via extracellular vesicles (EVs). EVs are membrane particles trafficking nucleic acids, proteins, metabolites and metabolic enzymes, lipids, and entire organelles. However, the function and the contribution of these cargoes to the broad therapeutic effects of NSCs are yet to be fully understood. Mitochondrial dysfunction is an established feature of several inflammatory and degenerative CNS disorders, most of which are potentially treatable with exogenous stem cell therapeutics. Herein, we investigated the hypothesis that NSCs release and traffic functional mitochondria via EVs to restore mitochondrial function in target cells. Untargeted proteomics revealed a significant enrichment of mitochondrial proteins spontaneously released by NSCs in EVs. Morphological and functional analyses confirmed the presence of ultrastructurally intact mitochondria within EVs with conserved membrane potential and respiration. We found that the transfer of these mitochondria from EVs to mtDNA-deficient L929 Rho 0 cells rescued mitochondrial function and increased Rho 0 cell survival. Furthermore, the incorporation of mitochondria from EVs into inflammatory mononuclear phagocytes restored normal mitochondrial dynamics and cellular metabolism and reduced the expression of pro-inflammatory markers in target cells. When transplanted in an animal model of multiple sclerosis, exogenous NSCs actively transferred mitochondria to mononuclear phagocytes and induced a significant amelioration of clinical deficits. Our data provide the first evidence that NSCs deliver functional mitochondria to target cells via EVs, paving the way for the development of novel (a)cellular approaches aimed at restoring mitochondrial dysfunction not only in multiple sclerosis, but also in degenerative neurological diseases. This study shows that neural stem cells are able to transfer functional mitochondria via extracellular vesicles to target cells both in vitro and in vivo, suggesting that functional mitochondrial transfer via extracellular vesicles is a signaling mechanism used by neural stem cells to modulate the physiology and metabolism of target cells.
Volcano plots show statistical significance (y axis) vs. fold change (x axis) for 9,951/9,971 cellular proteins quantitated across all 3 biological replicates (no missing values) in the multiplex TMT-based functional proteomic experiment illustrated in a. Proteins annotated with the following GOCC subcellular localisations are highlighted in red: mitochondrial outer membrane (GO:0005741, enriched in EVs); mitochondrial inner membrane (GO: 0005743, enriched in EVs); and mitochondrial matrix (GO:0005759, enriched in EVs). Mitochondrial complex (C) proteins enriched in EVs and encoded in the mitochondrial (upper panel) or nuclear (lower panel) genomes in the multiplex TMT-based functional proteomic experiment include: NADH:ubiquinone oxidoreductase or CI [mtnd2 (ND2 subunit), mtnd5 (ND5 subunit), ndufaf6 (assembly factor 6), ndufa9 (subunit A9), ndufs3 (core subunit S3), ndufb5 (1 beta subcomplex subunit 5)], succinate dehydrogenase or CII [Sdha (Subunit A), sdhd (cytochrome b small subunit), sdhb (iron-sulfur subunit), sdhc (cytochrome b560 subunit)], cytochrome b-c1 or CIII [mt-cyb (cytochrome B), Uqcrfs1 (subunit 5), Uqcrc2 (subunit 2), coq10b (coenzyme Q10B), uqcrq (subunit 8)], cytochrome C oxidase or CIV [mt-co3 (oxidase III), mtco1 (oxidase I), mtco2 (oxidase II), cox15 (subunit 15), cox18 (assembly protein 18), cox6c (subunit 6C), cox5a (subunit 5a)] and ATP synthase or CV [atp5f1 (subunit gamma), atp5s (subunit S), atp5d (subunit delta), atp5h (subunit D)]. The mitochondrial encoded gene mt-ND1 (NADH-ubiquinone oxidoreductase chain 1) was found to be present in EVs, Mito, and NSCs (L929 Rho0 were used as negative controls). (f) Representative protein expression analysis by WB of NSCs, EVs, and isolated mitochondria (Mito). CI, II, II, IV, V, complex I, II, II, IV, V; EV, extracellular vesicle; FDR, false discovery rate; GOCC, Gene Ontology Cellular Component; NSC, neural stem cell; PCR, polymerase chain reaction; TMT, Tandem Mass Tag; WB, western blot. https://doi.org/10.1371/journal.pbio.3001166.g001 Using Gene Ontology Cellular Component (GOCC) annotations, we investigated the subcellular origin of proteins enriched in EVs compared with NSCs (Fig 1B).
Audience Academic
Author Willis, Cory M.
Faria, Nuno
Bernstock, Joshua D.
Smith, Jayden A.
Braga, Alice
Bastos, Carlos
Buzas, Edit Iren
Tan, Sisareuth
Brisson, Alain
Vicario, Nunzio
Frezza, Christian
Peruzzotti-Jametti, Luca
Benincá, Cristiane
Zeviani, Massimo
Williamson, James C.
Viscomi, Carlo
van den Bosch, Aletta
Rogall, Rebecca
Matheson, Nicholas J.
Krzak, Grzegorz
Fernandez-Vizarra, Erika
Leonardi, Tommaso
Peacock, Ben
Manferrari, Giulia
Kittel, Ágnes
Bicci, Iacopo
Iraci, Nunzio
Lehner, Paul J.
Muller, Karin H.
Pluchino, Stefano
AuthorAffiliation University of Dundee, UNITED KINGDOM
5 NHS Blood and Transplant, Cambridge, United Kingdom
11 Cambridge Innovation Technologies Consulting (CITC) Limited, United Kingdom
12 NanoFCM Co., Ltd, Nottingham, United Kingdom
7 Institute of Experimental Medicine, Eötvös Lorand Research Network, Budapest, Hungary
14 Semmelweis University, Budapest, Hungary
1 Department of Clinical Neurosciences and NIHR Biomedical Research Centre, University of Cambridge, United Kingdom
18 Department of Medicine, University of Cambridge, United Kingdom
2 National Institutes of Health (NINDS/NIH), Bethesda, Maryland, United States of America
6 Center for Genomic Science of IIT@SEMM, Istituto Italiano di Tecnologia (IIT), Milan, Italy
10 Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom
13 Cambridge Advanced Imaging Centre (CAIC), United Kingdom
3 MRC Mitochondrial Biology Unit, University of Cambridge, United Kingdom
17 MRC Cancer Unit, Hutchison/MRC Research Centre, University of Cambridg
AuthorAffiliation_xml – name: 6 Center for Genomic Science of IIT@SEMM, Istituto Italiano di Tecnologia (IIT), Milan, Italy
– name: 5 NHS Blood and Transplant, Cambridge, United Kingdom
– name: 17 MRC Cancer Unit, Hutchison/MRC Research Centre, University of Cambridge, Cambridge United Kingdom
– name: 3 MRC Mitochondrial Biology Unit, University of Cambridge, United Kingdom
– name: 4 Cambridge Institute of Therapeutic Immunology and Infectious Disease (CITIID), University of Cambridge, Cambridge, United Kingdom
– name: University of Dundee, UNITED KINGDOM
– name: 15 HCEMM Kft HU, Budapest, Hungary
– name: 1 Department of Clinical Neurosciences and NIHR Biomedical Research Centre, University of Cambridge, United Kingdom
– name: 9 UMR-CBMN CNRS-Université de Bordeaux-IPB, France
– name: 11 Cambridge Innovation Technologies Consulting (CITC) Limited, United Kingdom
– name: 18 Department of Medicine, University of Cambridge, United Kingdom
– name: 16 ELKH-SE, Budapest, Hungary
– name: 14 Semmelweis University, Budapest, Hungary
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– name: 10 Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom
– name: 7 Institute of Experimental Medicine, Eötvös Lorand Research Network, Budapest, Hungary
– name: 8 Department of Biomedical and Biotechnological Sciences (BIOMETEC), University of Catania, Italy
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2021 Peruzzotti-Jametti et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Keywords Polymerase chain reaction
Phagocytes
Vesicles
Mitochondria
Computer software
Proteomics
Outer membrane proteins
Exosomes
Language English
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I have read the journal’s policy and the authors of this manuscript have the following competing interests: SP is co-founder, CSO and shareholder (>5%) of CITC Ltd. and iSTEM Therapeutics Litd., and co-founder and Non-executive Director at asitia Therapeutics Ltd.; LPJ is shareholder of CITC Ltd.; JAS is a Project Manager and Senior Research Associate at CITC Ltd. and Director of Research of iSTEM Therapeutics Ltd.; BP is an employee of NanoFCM and his contributions to this paper were made as part of their employment.
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  year: 2021
  text: 20210407
  day: 7
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
– name: San Francisco
– name: San Francisco, CA USA
PublicationTitle PLoS biology
PublicationTitleAlternate PLoS Biol
PublicationYear 2021
Publisher Public Library of Science
Public Library of Science (PLoS)
Publisher_xml – name: Public Library of Science
– name: Public Library of Science (PLoS)
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Snippet Neural stem cell (NSC) transplantation induces recovery in animal models of central nervous system (CNS) diseases. Although the replacement of lost endogenous...
Volcano plots show statistical significance (y axis) vs. fold change (x axis) for 9,951/9,971 cellular proteins quantitated across all 3 biological replicates...
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SubjectTerms Animals
Annotations
Assembly
ATP synthase
Biochemistry, Molecular Biology
Biological Transport
Biology and Life Sciences
Cell organelles
Cells, Cultured
Cytochrome
Cytochrome b
Cytochrome-c oxidase
Cytochromes
Dehydrogenases
Electron transport chain
Enrichment
Experiments
Extracellular vesicles
Extracellular Vesicles - metabolism
Female
Gene expression
Genomes
Genomics
Green Fluorescent Proteins - genetics
Green Fluorescent Proteins - metabolism
Life Sciences
Localization
Medicine and Health Sciences
Membranes
Mesenchymal Stem Cells - metabolism
Mesenchymal Stem Cells - physiology
Metabolism
Mice
Mice, Inbred C57BL
Mice, Transgenic
Mitochondria
Mitochondria - metabolism
Mitochondrial DNA
Morphology
Multiplexing
NADH
NADH-ubiquinone oxidoreductase
Neural stem cells
Neural Stem Cells - metabolism
Neural Stem Cells - ultrastructure
Neurobiology
Neurons
Neurons and Cognition
Nicotinamide adenine dinucleotide
Ontology
Oxidase
Oxidoreductase
Physiological aspects
Polymerase chain reaction
Proteins
Research and Analysis Methods
Stem cells
Succinate dehydrogenase
Sulfur
Ubiquinone
Ubiquinone oxidoreductase
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Title Neural stem cells traffic functional mitochondria via extracellular vesicles
URI https://www.ncbi.nlm.nih.gov/pubmed/33826607
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https://www.proquest.com/docview/2510265241
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https://doaj.org/article/62e32062ab904101a16fc0e8ef20d45c
http://dx.doi.org/10.1371/journal.pbio.3001166
Volume 19
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