Clinical relevance of extracellular vesicles in hematological neoplasms: from liquid biopsy to cell biopsy

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Abstract

In the era of precision medicine, liquid biopsy is becoming increasingly important in oncology. It consists in the isolation and analysis of tumor-derived biomarkers, including extracellular vesicles (EVs), in body fluids. EVs are lipid bilayer-enclosed particles, heterogeneous in size and molecular composition, released from both normal and neoplastic cells. In tumor context, EVs are valuable carriers of cancer information; in fact, their amount, phenotype and molecular cargo, including proteins, lipids, metabolites and nucleic acids, mirror nature and origin of parental cells rendering EVs appealing candidates as novel biomarkers. Translation of these new potential diagnostic tools into clinical practice could deeply revolutionize the cancer field mainly for solid tumors but for hematological neoplasms, too.

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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 … (2020)

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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The biology, function, and biomedical applications of exosomes

Raghu Kalluri, Valerie LeBleu (2020)

The study of extracellular vesicles (EVs) has the potential to identify unknown cellular and molecular mechanisms in intercellular communication and in organ homeostasis and disease. Exosomes, with an average diameter of ~100 nanometers, are a subset of EVs. The biogenesis of exosomes involves their origin in endosomes, and subsequent interactions with other intracellular vesicles and organelles generate the final content of the exosomes. Their diverse constituents include nucleic acids, proteins, lipids, amino acids, and metabolites, which can reflect their cell of origin. In various diseases, exosomes offer a window into altered cellular or tissue states, and their detection in biological fluids potentially offers a multicomponent diagnostic readout. The efficient exchange of cellular components through exosomes can inform their applied use in designing exosome-based therapeutics.

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RNA delivery by extracellular vesicles in mammalian cells and its applications

Killian O’Brien, Koen Breyne, Stefano Ughetto … (2020)

The term ‘extracellular vesicles’ refers to a heterogeneous population of vesicular bodies of cellular origin that derive either from the endosomal compartment (exosomes) or as a result of shedding from the plasma membrane (microvesicles, oncosomes and apoptotic bodies). Extracellular vesicles carry a variety of cargo, including RNAs, proteins, lipids and DNA, which can be taken up by other cells, both in the direct vicinity of the source cell and at distant sites in the body via biofluids, and elicit a variety of phenotypic responses. Owing to their unique biology and roles in cell–cell communication, extracellular vesicles have attracted strong interest, which is further enhanced by their potential clinical utility. Because extracellular vesicles derive their cargo from the contents of the cells that produce them, they are attractive sources of biomarkers for a variety of diseases. Furthermore, studies demonstrating phenotypic effects of specific extracellular vesicle-associated cargo on target cells have stoked interest in extracellular vesicles as therapeutic vehicles. There is particularly strong evidence that the RNA cargo of extracellular vesicles can alter recipient cell gene expression and function. During the past decade, extracellular vesicles and their RNA cargo have become better defined, but many aspects of extracellular vesicle biology remain to be elucidated. These include selective cargo loading resulting in substantial differences between the composition of extracellular vesicles and source cells; heterogeneity in extracellular vesicle size and composition; and undefined mechanisms for the uptake of extracellular vesicles into recipient cells and the fates of their cargo. Further progress in unravelling the basic mechanisms of extracellular vesicle biogenesis, transport, and cargo delivery and function is needed for successful clinical implementation. This Review focuses on the current state of knowledge pertaining to packaging, transport and function of RNAs in extracellular vesicles and outlines the progress made thus far towards their clinical applications.

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Author and article information

Contributors

Daniela Lamorte:

ORCID: http://orcid.org/0000-0002-1114-1963

daniela.lamorte@crob.it

Ilaria Laurenzana:

ORCID: http://orcid.org/0000-0001-8289-8325

ilaria.laurenzana@crob.it

Journal

Journal ID (nlm-ta): Leukemia

Journal ID (iso-abbrev): Leukemia

Title: Leukemia

Publisher: Nature Publishing Group UK (London )

ISSN (Print): 0887-6924

ISSN (Electronic): 1476-5551

Publication date (Electronic): 9 December 2020

Publication date PMC-release: 9 December 2020

Publication date (Print): 2021

Volume: 35

Issue: 3

Pages: 661-678

Affiliations

[1 ]GRID grid.418322.e, ISNI 0000 0004 1756 8751, Laboratory of Preclinical and Translational Research, , Centro di Riferimento Oncologico della Basilicata (IRCCS-CROB), ; Rionero in Vulture, PZ Italy

[2 ]GRID grid.418322.e, ISNI 0000 0004 1756 8751, Laboratory of Clinical Research and Advanced Diagnostics, , Centro di Riferimento Oncologico della Basilicata (IRCCS-CROB), ; Rionero in Vulture, PZ Italy

[3 ]GRID grid.418322.e, ISNI 0000 0004 1756 8751, Scientific Direction, , Centro di Riferimento Oncologico della Basilicata (IRCCS-CROB), ; Rionero in Vulture, PZ Italy

Author information

Stefania Trino http://orcid.org/0000-0002-0289-5288

Daniela Lamorte http://orcid.org/0000-0002-1114-1963

Ilaria Laurenzana http://orcid.org/0000-0001-8289-8325

Article

Publisher ID: 1104

DOI: 10.1038/s41375-020-01104-1

PMC ID: 7932927

PubMed ID: 33299143

SO-VID: f236a165-86b0-42e8-8e6d-061ca9123113

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 27 July 2020

Date revision received : 30 October 2020

Date accepted : 18 November 2020

Funding

Funded by: FundRef https://doi.org/10.13039/501100003196, Ministero della Salute (Ministry of Health, Italy);

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ScienceOpen disciplines: Oncology & Radiotherapy

Keywords: cancer,haematological cancer

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ScienceOpen disciplines: Oncology & Radiotherapy

Keywords: cancer, haematological cancer

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Clinical relevance of extracellular vesicles in hematological neoplasms: from liquid biopsy to cell biopsy

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Karger: Oncology

Most cited references 106

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

The biology, function, and biomedical applications of exosomes

RNA delivery by extracellular vesicles in mammalian cells and its applications

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