Potential of extracellular vesicles in the pathogenesis, diagnosis and therapy for parasitic diseases

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Abstract

Parasitic diseases have a significant impact on human and animal health, representing a major hazard to the public and causing economic and health damage worldwide. Extracellular vesicles (EVs) have long been recognized as diagnostic and therapeutic tools but are now also known to be implicated in the natural history of parasitic diseases and host immune response modulation. Studies have shown that EVs play a role in parasitic disease development by interacting with parasites and communicating with other types of cells. This review highlights the most recent research on EVs and their role in several aspects of parasite‐host interactions in five key parasitic diseases: Chagas disease, malaria, toxoplasmosis, leishmaniasis and helminthiases. We also discuss the potential use of EVs as diagnostic tools or treatment options for these infectious diseases.

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Most cited references 226

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Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines

Clotilde Théry, Kenneth W Witwer, Elena Aikawa … (2019)

ABSTRACT The last decade has seen a sharp increase in the number of scientific publications describing physiological and pathological functions of extracellular vesicles (EVs), a collective term covering various subtypes of cell-released, membranous structures, called exosomes, microvesicles, microparticles, ectosomes, oncosomes, apoptotic bodies, and many other names. However, specific issues arise when working with these entities, whose size and amount often make them difficult to obtain as relatively pure preparations, and to characterize properly. The International Society for Extracellular Vesicles (ISEV) proposed Minimal Information for Studies of Extracellular Vesicles (“MISEV”) guidelines for the field in 2014. We now update these “MISEV2014” guidelines based on evolution of the collective knowledge in the last four years. An important point to consider is that ascribing a specific function to EVs in general, or to subtypes of EVs, requires reporting of specific information beyond mere description of function in a crude, potentially contaminated, and heterogeneous preparation. For example, claims that exosomes are endowed with exquisite and specific activities remain difficult to support experimentally, given our still limited knowledge of their specific molecular machineries of biogenesis and release, as compared with other biophysically similar EVs. The MISEV2018 guidelines include tables and outlines of suggested protocols and steps to follow to document specific EV-associated functional activities. Finally, a checklist is provided with summaries of key points.

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Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles.

Marina Colombo, Graça Raposo, Clotilde Théry (2014)

In the 1980s, exosomes were described as vesicles of endosomal origin secreted from reticulocytes. Interest increased around these extracellular vesicles, as they appeared to participate in several cellular processes. Exosomes bear proteins, lipids, and RNAs, mediating intercellular communication between different cell types in the body, and thus affecting normal and pathological conditions. Only recently, scientists acknowledged the difficulty of separating exosomes from other types of extracellular vesicles, which precludes a clear attribution of a particular function to the different types of secreted vesicles. To shed light into this complex but expanding field of science, this review focuses on the definition of exosomes and other secreted extracellular vesicles. Their biogenesis, their secretion, and their subsequent fate are discussed, as their functions rely on these important processes.

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Biological properties of extracellular vesicles and their physiological functions

María Yañez-Mó, Pia Siljander, Zoraida Andreu … (2015)

In the past decade, extracellular vesicles (EVs) have been recognized as potent vehicles of intercellular communication, both in prokaryotes and eukaryotes. This is due to their capacity to transfer proteins, lipids and nucleic acids, thereby influencing various physiological and pathological functions of both recipient and parent cells. While intensive investigation has targeted the role of EVs in different pathological processes, for example, in cancer and autoimmune diseases, the EV-mediated maintenance of homeostasis and the regulation of physiological functions have remained less explored. Here, we provide a comprehensive overview of the current understanding of the physiological roles of EVs, which has been written by crowd-sourcing, drawing on the unique EV expertise of academia-based scientists, clinicians and industry based in 27 European countries, the United States and Australia. This review is intended to be of relevance to both researchers already working on EV biology and to newcomers who will encounter this universal cell biological system. Therefore, here we address the molecular contents and functions of EVs in various tissues and body fluids from cell systems to organs. We also review the physiological mechanisms of EVs in bacteria, lower eukaryotes and plants to highlight the functional uniformity of this emerging communication system.

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Author and article information

Contributors

Patricia R. M. Rocco:

ORCID: https://orcid.org/0000-0003-1412-7136

prmrocco@gmail.com

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): 08 August 2024

Publication date (Print): August 2024

Volume: 13

Issue: 8 ( doiID: 10.1002/jev2.v13.8 )

Electronic Location Identifier: e12496

Affiliations

[ ¹ ] Instituto de Biofísica Carlos Chagas Filho Universidade Federal do Rio de Janeiro (UFRJ) Rio de Janeiro Brazil

[ ² ] Rio de Janeiro Innovation Network in Nanosystems for Health‐NanoSAÚDE/Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) Rio de Janeiro Brazil

[ ³ ] Departamento de Ciências Farmacêuticas Diadema Campus, Instituto de Ciências Ambientais, Químicas e Farmacêuticas Universidade Federal de São Paulo (UNIFESP) Diadema São Paulo Brazil

[ ⁴ ] Center for Biotechnology and Cell Therapy São Rafael Hospital Salvador Brazil

[ ⁵ ] D'Or Institute for Research and Education (IDOR) Salvador Brazil

[ ⁶ ] Instituto de Microbiologia Paulo de Goés (IMPG) Universidade Federal do Rio de Janeiro (UFRJ) Rio de Janeiro Brazil

[ ⁷ ] Fundação Oswaldo Cruz (FIOCRUZ) Instituto Oswaldo Cruz (IOC) Rio de Janeiro Brazil

[ ⁸ ] Deparment of Pediatrics Center for Cystic Fibrosis and Airway Disease Research Emory University School of Medicine Atlanta Georgia USA

[ ⁹ ] National Institute of Science and Technology for Regenerative Medicine INCT‐REGENERA Rio de Janeiro Brazil

Author notes

[*] [* ] Correspondence

Patricia R. M. Rocco, Laboratory of Pulmonary Investigation, Carlos Chagas Filho Institute of Biophysics, Federal University of Rio de Janeiro, Rio de Janeiro, 21941‐902, Brazil. Email: prmrocco@ 123456gmail.com

Author information

Ana Acacia Sá Pinheiro https://orcid.org/0000-0002-3894-1645

Ana Claudia Torrecilhas https://orcid.org/0000-0001-5724-2199

Bruno Solano de Freitas Souza https://orcid.org/0000-0003-3771-0439

Fernanda Ferreira Cruz https://orcid.org/0000-0001-9443-3648

Herbert Leonel de Matos Guedes https://orcid.org/0000-0002-3819-3069

Tadeu Diniz Ramos https://orcid.org/0000-0002-8523-4361

Miqueias Lopes‐Pacheco https://orcid.org/0000-0002-7444-9359

Celso Caruso‐Neves https://orcid.org/0000-0002-2415-7753

Patricia R. M. Rocco https://orcid.org/0000-0003-1412-7136

Article

Publisher ID: JEV212496

DOI: 10.1002/jev2.12496

PMC ID: 11306921

PubMed ID: 39113589

SO-VID: 99c59a48-47be-4f70-8591-82154f231ddc

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 received : 22 February 2024

Date accepted : 11 July 2024

Page count

Figures: 1, Tables: 3, Pages: 24, Words: 19241

Funding

Funded by: Brazilian Council for Scientific and Technological Development (CNPq), Brazil

Award ID: 408124/2021‐0

Funded by: Rio de Janeiro State Research Foundation

Award ID: E‐26/210.181/2020 [PRMR]

Custom metadata

source-schema-version-number 2.0

cover-date August 2024

details-of-publishers-convertor Converter:WILEY_ML3GV2_TO_JATSPMC version:6.4.6 mode:remove_FC converted:08.08.2024

Keywords: chagas disease,extracellular vesicles,helminthiasis,leishmaniasis,malaria,toxoplasmosis

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Keywords: chagas disease, extracellular vesicles, helminthiasis, leishmaniasis, malaria, toxoplasmosis

Potential of extracellular vesicles in the pathogenesis, diagnosis and therapy for parasitic diseases

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Abstract

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Bacterial extracellular vesicles

Most cited references 226

Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines

Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles.

Biological properties of extracellular vesicles and their physiological functions

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