Extracellular vesicles in metabolic disease

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Abstract

Extracellular vesicles (EVs) are submicron-sized lipid envelopes that are produced and released from a parent cell and can be taken up by a recipient cell. EVs are capable of mediating cellular signalling by carrying nucleic acids, proteins, lipids and cellular metabolites between cells and organs. Metabolic dysfunction is associated with changes in plasma concentrations of EVs as well as alterations in their EV cargo. Since EVs can act as messengers between parent and recipient cells, they could be involved in cell-to-cell and organ-to-organ communication in metabolic diseases. Recent literature has shown that EVs are produced by cells within metabolic tissues, such as adipose tissue, pancreas, muscle and liver. These vesicles have therefore been proposed as a novel intercellular communication mode in systemic metabolic regulation. In this review, we will describe and discuss the current literature that investigates the role of adipose-derived EVs in the regulation of obesity-associated metabolic disease. We will particularly focus on the EV-dependent communication between adipocytes, the vasculature and immune cells in type 2 diabetes.

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Most cited references 43

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Plant-Derived Exosomal MicroRNAs Shape the Gut Microbiota

Yun L Teng, Yi Ren, Mohammed S. Sayed … (2018)

The gut microbiota can be altered by dietary interventions to prevent and treat various diseases. However, the mechanisms by which food products modulate commensals remain largely unknown. We demonstrate that plant-derived e xosomes- l ike n anoparticles (ELNs) are taken up by the gut microbiota and contain RNAs that alter microbiome composition and host physiology. Ginger ELNs (GELNs) are preferentially taken up by Lactobacillaceae in a GELN lipid-dependent manner and contain microRNAs that target various genes in Lactobacillus rhamnosus (LGG). Among these, GELN mdo-miR7267-3p-mediated targeting of the LGG monooxygenase ycnE yields increased indole-3-carboxaldehyde (I3A). GELN RNAs or I3A, a ligand for aryl hydrocarbon receptor (AHR), are sufficient to induce production of IL-22, which is linked to barrier function improvement. These functions of GELN RNAs can ameliorate mouse colitis via IL-22-dependent mechanisms. These findings reveal how plant products and their effects on the microbiome may be used to target specific host processes to alleviate disease. Teng et al. show that exosomes-like nanoparticles (ELNs) from edible plants such as ginger are preferentially taken up by gut bacteria in an ELN lipid dependent manner. ELN RNAs regulate gut microbiota composition and localization as well as host physiology, notably enhancing gut barrier function to alleviate colitis.

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Local proliferation of macrophages contributes to obesity-associated adipose tissue inflammation.

Shinya U Amano, Jessica Cohen, Pranitha Vangala … (2014)

Adipose tissue (AT) of obese mice and humans accumulates immune cells, which secrete cytokines that can promote insulin resistance. AT macrophages (ATMs) are thought to originate from bone-marrow-derived monocytes, which infiltrate the tissue from the circulation. Here, we show that a major fraction of macrophages unexpectedly undergo cell division locally within AT, as detected by Ki67 expression and 5-ethynyl-2'-deoxyuridine incorporation. Macrophages within the visceral AT (VAT), but not those in other tissues (including liver and spleen), displayed increased proliferation in obesity. Importantly, depletion of blood monocytes had no impact on ATM content, whereas their proliferation in situ continued. Treatment with monocyte chemotactic protein 1 (MCP-1) induced macrophage cell division in AT explants, whereas mcp-1 deficiency in vivo decreased ATM proliferation. These results reveal that, in addition to blood monocyte recruitment, in situ proliferation driven by MCP-1 is an important process by which macrophages accumulate in the VAT in obesity. Copyright © 2014 Elsevier Inc. All rights reserved.

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Macrophage-dependent clearance of systemically administered B16BL6-derived exosomes from the blood circulation in mice

Takafumi Imai, Yuki Takahashi, Makiya Nishikawa … (2015)

Previous studies using B16BL6-derived exosomes labelled with gLuc–lactadherin (gLuc-LA), a fusion protein of Gaussia luciferase (a reporter protein) and lactadherin (an exosome-tropic protein), showed that the exosomes quickly disappeared from the systemic circulation after intravenous injection in mice. In the present study, the mechanism of rapid clearance of intravenously injected B16BL6 exosomes was investigated. gLuc-LA-labelled exosomes were obtained from supernatant of B16BL6 cells after transfection with a plasmid DNA encoding gLuc-LA. Labelling was stable when the exosomes were incubated in serum. By using B16BL6 exosomes labelled with PKH26, a lipophilic fluorescent dye, it was demonstrated that PKH26-labelled B16BL6 exosomes were taken up by macrophages in the liver and spleen but not in the lung, while PKH26-labelled exosomes were taken up by the endothelial cells in the lung. Subsequently, gLuc-LA-labelled B16BL6 exosomes were injected into macrophage-depleted mice prepared by injection with clodronate-containing liposomes. The clearance of the intravenously injected B16BL6 exosomes from the blood circulation was much slower in macrophage-depleted mice than that in untreated mice. These results indicate that macrophages play important roles in the clearance of intravenously injected B16BL6 exosomes from the systemic circulation.

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Author and article information

Contributors

Naveed Akbar: Naveed.akbar@cardiov.ox.ac.uk

Myriam Aouadi: Myriam.aouadi@ki.se

Journal

Journal ID (nlm-ta): Diabetologia

Journal ID (iso-abbrev): Diabetologia

Title: Diabetologia

Publisher: Springer Berlin Heidelberg (Berlin/Heidelberg )

ISSN (Print): 0012-186X

ISSN (Electronic): 1432-0428

Publication date (Electronic): 5 November 2019

Publication date PMC-release: 5 November 2019

Publication date (Print): 2019

Volume: 62

Issue: 12

Pages: 2179-2187

Affiliations

[1 ]GRID grid.4991.5, ISNI 0000 0004 1936 8948, Division of Cardiovascular Medicine, Radcliffe Department of Medicine, , University of Oxford, ; Level 6, West Wing, John Radcliffe Hospital, Oxford, OX3 9DU UK

[2 ]GRID grid.4714.6, ISNI 0000 0004 1937 0626, Integrated Cardio Metabolic Centre, Department of Medicine, , Karolinska Institutet, NOVUM, ; Blickagången 6, 141 57 Huddinge, Sweden

Article

Publisher ID: 5014

DOI: 10.1007/s00125-019-05014-5

PMC ID: 6861353

PubMed ID: 31690986

SO-VID: 834a683f-4ba0-44f1-b63e-f45802c52c65

License:

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

History

Date received : 7 May 2019

Date accepted : 6 August 2019

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100004359, Vetenskapsrådet;

Award ID: 2015-0358

Funded by: FundRef http://dx.doi.org/10.13039/100004325, AstraZeneca;

Award ID: Start-up grant

Funded by: British Heart Foundation

Award ID: RE/13/1/30181

Funded by: Novonordisk foundation

Award ID: Tripartite Immunometabolism Consortium/NNF15CC0018

Funded by: strategic research program in diabetes at Karolinska Institute

Custom metadata

ScienceOpen disciplines: Endocrinology & Diabetes

Keywords: adipocytes,diabetes,diagnostic,endothelial cells,exosomes,extracellular vesicle,immune cells,macrophages,metabolic dysfunction,platelets,review,therapeutic

Data availability:

ScienceOpen disciplines: Endocrinology & Diabetes

Keywords: adipocytes, diabetes, diagnostic, endothelial cells, exosomes, extracellular vesicle, immune cells, macrophages, metabolic dysfunction, platelets, review, therapeutic

Extracellular vesicles in metabolic disease

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Bacterial extracellular vesicles

Most cited references 43

Plant-Derived Exosomal MicroRNAs Shape the Gut Microbiota

Local proliferation of macrophages contributes to obesity-associated adipose tissue inflammation.

Macrophage-dependent clearance of systemically administered B16BL6-derived exosomes from the blood circulation in mice

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