Diverse plasma membrane protrusions act as platforms for extracellular vesicle shedding

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Abstract

Plasma membrane curvature is an important factor in the regulation of cellular phenotype and is critical for various cellular activities including the shedding of extracellular vesicles (EV). One of the most striking morphological features of cells is different plasma membrane‐covered extensions supported by actin core such as filopodia and microvilli. Despite the various functions of these extensions are partially unexplained, they are known to facilitate many crucial cellular functions such as migration, adhesion, absorption, and secretion. Due to the rapid increase in the research activity of EVs, there is raising evidence that one of the general features of cellular plasma membrane protrusions is to act as specialized platforms for the budding of EVs. This review will focus on early observations and recent findings supporting this hypothesis, discuss the putative budding and shedding mechanisms of protrusion‐derived EVs and their biological significance.

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Most cited references 88

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Shedding light on the cell biology of extracellular vesicles

Guillaume van Niel, Gisela D'Angelo, Graça Raposo (2018)

Extracellular vesicles are a heterogeneous group of cell-derived membranous structures comprising exosomes and microvesicles, which originate from the endosomal system or which are shed from the plasma membrane, respectively. They are present in biological fluids and are involved in multiple physiological and pathological processes. Extracellular vesicles are now considered as an additional mechanism for intercellular communication, allowing cells to exchange proteins, lipids and genetic material. Knowledge of the cellular processes that govern extracellular vesicle biology is essential to shed light on the physiological and pathological functions of these vesicles as well as on clinical applications involving their use and/or analysis. However, in this expanding field, much remains unknown regarding the origin, biogenesis, secretion, targeting and fate of these vesicles.

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Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells.

Hadi Valadi, Karin Ekström, Apostolos Bossios … (2007)

Exosomes are vesicles of endocytic origin released by many cells. These vesicles can mediate communication between cells, facilitating processes such as antigen presentation. Here, we show that exosomes from a mouse and a human mast cell line (MC/9 and HMC-1, respectively), as well as primary bone marrow-derived mouse mast cells, contain RNA. Microarray assessments revealed the presence of mRNA from approximately 1300 genes, many of which are not present in the cytoplasm of the donor cell. In vitro translation proved that the exosome mRNAs were functional. Quality control RNA analysis of total RNA derived from exosomes also revealed presence of small RNAs, including microRNAs. The RNA from mast cell exosomes is transferable to other mouse and human mast cells. After transfer of mouse exosomal RNA to human mast cells, new mouse proteins were found in the recipient cells, indicating that transferred exosomal mRNA can be translated after entering another cell. In summary, we show that exosomes contain both mRNA and microRNA, which can be delivered to another cell, and can be functional in this new location. We propose that this RNA is called "exosomal shuttle RNA" (esRNA).

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Extracellular vesicles: Exosomes, microvesicles, and friends

Graça Raposo, Willem Stoorvogel (2013)

Cells release into the extracellular environment diverse types of membrane vesicles of endosomal and plasma membrane origin called exosomes and microvesicles, respectively. These extracellular vesicles (EVs) represent an important mode of intercellular communication by serving as vehicles for transfer between cells of membrane and cytosolic proteins, lipids, and RNA. Deficiencies in our knowledge of the molecular mechanisms for EV formation and lack of methods to interfere with the packaging of cargo or with vesicle release, however, still hamper identification of their physiological relevance in vivo. In this review, we focus on the characterization of EVs and on currently proposed mechanisms for their formation, targeting, and function.

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Author and article information

Contributors

Kirsi Rilla:

ORCID: https://orcid.org/0000-0002-7862-5727

kirsi.rilla@uef.fi

Journal

Journal ID (nlm-ta): J Extracell Vesicles

Journal ID (iso-abbrev): J Extracell Vesicles

Journal ID (doi): 10.1002/(ISSN)2001-3078

Journal ID (publisher-id): JEV2

Title: Journal of Extracellular Vesicles

Publisher: John Wiley and Sons Inc. (Hoboken )

ISSN (Electronic): 2001-3078

Publication date (Electronic): 17 September 2021

Publication date (Print): September 2021

Volume: 10

Issue: 11 ( doiID: 10.1002/jev2.v10.11 )

Electronic Location Identifier: e12148

Affiliations

[ ¹ ] Institute of Biomedicine University of Eastern Finland Kuopio Finland

Author notes

[*] [* ] Correspondence

Kirsi Rilla, Institute of Biomedicine, University of Eastern Finland, Kuopio, Finland.

Email: kirsi.rilla@ 123456uef.fi

Author information

Kirsi Rilla https://orcid.org/0000-0002-7862-5727

Article

Publisher ID: JEV212148

DOI: 10.1002/jev2.12148

PMC ID: 8448080

PubMed ID: 34533887

SO-VID: 4b556405-b7c9-46d9-a491-41bd20756e3c

License:

This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

History

Date revision received : 24 August 2021

Date received : 02 June 2021

Date accepted : 07 September 2021

Page count

Figures: 7, Tables: 1, Pages: 13, Words: 8842

Funding

Funded by: Academy of Finland GeneCellNano Flagship

Award ID: 337120

Funded by: Jane and Aatos Erkko Foundation , doi 10.13039/501100004012;

Funded by: Mizutani Foundation , doi 10.13039/100009578;

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source-schema-version-number 2.0

cover-date September 2021

details-of-publishers-convertor Converter:WILEY_ML3GV2_TO_JATSPMC version:6.0.7 mode:remove_FC converted:17.09.2021

Diverse plasma membrane protrusions act as platforms for extracellular vesicle shedding

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Journal of Circulating Biomarkers

Most cited references 88

Shedding light on the cell biology of extracellular vesicles

Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells.

Extracellular vesicles: Exosomes, microvesicles, and friends

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