Biological roles and potential applications of immune cell-derived extracellular vesicles

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ABSTRACT

Extracellular vesicles (EVs) deliver bioactive macromolecules (i.e. proteins, lipids and nucleic acids) for intercellular communication in multicellular organisms. EVs are secreted by all cell types including immune cells. Immune cell-derived EVs modulate diverse aspects of the immune system to either enhance or suppress immune activities. The extensive effects of immune cell-derived EVs have become the focus of great interest for various nano-biomedical applications, ranging from the medical use of nanoplatform-based diagnostic agents to the development of therapeutic interventions as well as vaccine applications, and thus may be ideal for ‘immune-theranostic’. Here, we review the latest advances concerning the biological roles of immune cell-derived EVs in innate and acquired immunity. The intercellular communication amongst immune cells through their EVs is highlighted, showing that all immune cell-derived EVs have their unique function(s) in immunity through intricate interaction(s). Natural-killer (NK) cell-derived EVs, for example, contain potent cytotoxic proteins and induce apoptosis to targeted cancer cells. On the other hand, cancer cell-derived EVs bearing NK ligands may evade immune surveillance and responses. Finally, we discuss possible medical uses for the immune cell-derived EVs as a tool for immune-theranostic: as diagnostic biomarkers, for use in therapeutic interventions and for vaccination.

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Exosome secretion: molecular mechanisms and roles in immune responses.

Angélique Bobrie, Marina Colombo, Graça Raposo … (2011)

Exosomes are small membrane vesicles, secreted by most cell types from multivesicular endosomes, and thought to play important roles in intercellular communications. Initially described in 1983, as specifically secreted by reticulocytes, exosomes became of interest for immunologists in 1996, when they were proposed to play a role in antigen presentation. More recently, the finding that exosomes carry genetic materials, mRNA and miRNA, has been a major breakthrough in the field, unveiling their capacity to vehicle genetic messages. It is now clear that not only immune cells but probably all cell types are able to secrete exosomes: their range of possible functions expands well beyond immunology to neurobiology, stem cell and tumor biology, and their use in clinical applications as biomarkers or as therapeutic tools is an extensive area of research. Despite intensive efforts to understand their functions, two issues remain to be solved in the future: (i) what are the physiological function(s) of exosomes in vivo and (ii) what are the relative contributions of exosomes and of other secreted membrane vesicles in these proposed functions? Here, we will focus on the current ideas on exosomes and immune responses, but also on their mechanisms of secretion and the use of this knowledge to elucidate the latter issue. © 2011 John Wiley & Sons A/S.

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Malignant effusions and immunogenic tumour-derived exosomes.

Fabrice André, Noel E C Schartz, Mojgan Movassagh … (2002)

Exosomes derived from tumours are small vesicles released in vitro by tumour cell lines in culture supernatants. To assess the role of these exosomes in vivo, we examined malignant effusions for their presence. We also investigated whether these exosomes could induce production of tumour-specific T cells when pulsed with dendritic cells. We isolated exosomes by ultracentrifugation on sucrose and D(2)O gradients of 11 malignant effusions. We characterised exosomes with Western blot analyses, immunoelectron microscopy, and in-vitro stimulations of autologous T lymphocytes. Malignant effusions accumulate high numbers of membrane vesicles that have a mean diameter of 80 nm (SD 30). These vesicles have antigen-presenting molecules (MHC class-I heat-shock proteins), tetraspanins (CD81), and tumour antigens (Her2/Neu, Mart1, TRP, gp100). These criteria, including their morphological characteristics, indicate the similarities between these vesicles and exosomes. Exosomes from patients with melanoma deliver Mart1 tumour antigens to dendritic cells derived from monocytes (MD-DCs) for cross presentation to clones of cytotoxic T lymphocytes specific to Mart1. In seven of nine patients with cancer, lymphocytes specific to the tumour could be efficiently expanded from peripheral blood cells by pulsing autologous MD-DCs with autologous ascitis exosomes. In one patient tested, we successfully expanded a restricted T-cell repertoire, which could not be recovered carcinomatosis nodules. Exosomes derived from tumours accumulate in ascites from patients with cancer. Ascitis exosomes are a natural and new source of tumour-rejection antigens, opening up new avenues for immunisation against cancers.

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Interleukins (from IL-1 to IL-38), interferons, transforming growth factor β, and TNF-α: Receptors, functions, and roles in diseases

Alar Aab, Can Altunbulakli, Kursat Azkur … (2016)

There have been extensive developments on cellular and molecular mechanisms of immune regulation in allergy, asthma, autoimmune diseases, tumor development, organ transplantation, and chronic infections during the last few years. Better understanding the functions, reciprocal regulation, and counterbalance of subsets of immune and inflammatory cells that interact through interleukins, interferons, TNF-α, and TGF-β offer opportunities for immune interventions and novel treatment modalities in the era of development of biological immune response modifiers particularly targeting these molecules or their receptors. More than 60 cytokines have been designated as interleukins since the initial discoveries of monocyte and lymphocyte interleukins (called IL-1 and IL-2, respectively). Studies of transgenic or gene-deficient mice with altered expression of these cytokines or their receptors and analyses of mutations and polymorphisms in human genes that encode these products have provided essential information about their functions. Here we review recent developments on IL-1 to IL-38, TNF-α, TGF-β, and interferons. We highlight recent advances during the last few years in this area and extensively discuss their cellular sources, targets, receptors, signaling pathways, and roles in immune regulation in patients with allergy and asthma and other inflammatory diseases.

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Author and article information

Journal

Journal ID (nlm-ta): J Extracell Vesicles

Journal ID (iso-abbrev): J Extracell Vesicles

Journal ID (archive): ZJEV

Journal ID (publisher-id): zjev20

Title: Journal of Extracellular Vesicles

Publisher: Taylor & Francis

ISSN (Electronic): 2001-3078

Publication date Collection: 2017

Publication date (Electronic): 22 November 2017

Volume: 6

Issue: 1

Electronic Location Identifier: 1400370

Affiliations

[ ^a ] Department of Pediatrics, Children’s Center for Cancer and Blood Diseases and Divisions of Hematology, Oncology, Blood and Marrow Transplantation

[ ^b ] Division of Hematology, Children’s Medical Center, The Second Xiangya Hospital, Central South University/Institute of Pediatrics, Central South University , Changsha, Hunan, PR China

[ ^c ] Department of Pathology, The Saban Research Institute, Children’s Hospital Los Angeles, USC-Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California , Los Angeles, CA, USA

Author notes

CONTACT Ambrose Y. Jong ajong@ 123456chla.usc.edu Division of Hematology, Oncology and Blood & Marrow Transplantation , Mailstop 57, 4650 Sunset Blvd., Los Angeles, CA 90027, USA

Article

Publisher ID: 1400370

DOI: 10.1080/20013078.2017.1400370

PMC ID: 5706476

PubMed ID: 29209467

SO-VID: 07215e45-79c0-4dae-a0f6-2816155eee4f

License:

This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

History

Date received : 06 July 2017

Date accepted : 22 October 2017

Page count

Figures: 3, Tables: 1, References: 182, Pages: 20

Funding

Funded by: National Cancer Institute 10.13039/100000054

Award ID: P30CA014089

Funded by: the Team Connor Foundation

Award ID: n/a

Funded by: Alex’s Lemonade Stand Foundation for Childhood Cancer (US)

Award ID: n/a

This work was supported by the National Cancer Institute [P30CA014089]; the Whittier Foundation; the William Lawrence and Blanche Hughes Foundation; Alex’s Lemonade Stand Foundation for Childhood Cancer (US); the Team Connor Foundation (US).

Biological roles and potential applications of immune cell-derived extracellular vesicles

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ABSTRACT

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Most cited references 123

Exosome secretion: molecular mechanisms and roles in immune responses.

Malignant effusions and immunogenic tumour-derived exosomes.

Interleukins (from IL-1 to IL-38), interferons, transforming growth factor β, and TNF-α: Receptors, functions, and roles in diseases

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