Can Organoid Model Reveal a Key Role of Extracellular Vesicles in Tumors? A Comprehensive Review of the Literature

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Abstract

Extracellular vesicles (EVs) are small membrane-bound vesicles that are released by cells into the extracellular environment. The role of EVs in tumors has been extensively studied, and they have been shown to play a crucial role in tumor growth, progression, and metastasis. Past research has mainly used 2D-cultured cell line models to investigate the role of EVs in tumors, which poorly simulate the tumor microenvironment. Organoid technology has gradually matured in recent years. Organoids are similar in composition and behavior to physiological cells and have the potential to recapitulate the architecture and function of the original tissue. It has been widely used in organogenesis, drug screening, gene editing, precision medicine and other fields. The integration of EVs and organoids has the potential to revolutionize the field of cancer research and represents a promising avenue for advancing our understanding of cancer biology and the development of novel therapeutic strategies. Here, we aimed to present a comprehensive overview of studies using organoids to study EVs in tumors.

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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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Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors.

Kazutoshi Takahashi, Shinya Yamanaka (2006)

Differentiated cells can be reprogrammed to an embryonic-like state by transfer of nuclear contents into oocytes or by fusion with embryonic stem (ES) cells. Little is known about factors that induce this reprogramming. Here, we demonstrate induction of pluripotent stem cells from mouse embryonic or adult fibroblasts by introducing four factors, Oct3/4, Sox2, c-Myc, and Klf4, under ES cell culture conditions. Unexpectedly, Nanog was dispensable. These cells, which we designated iPS (induced pluripotent stem) cells, exhibit the morphology and growth properties of ES cells and express ES cell marker genes. Subcutaneous transplantation of iPS cells into nude mice resulted in tumors containing a variety of tissues from all three germ layers. Following injection into blastocysts, iPS cells contributed to mouse embryonic development. These data demonstrate that pluripotent stem cells can be directly generated from fibroblast cultures by the addition of only a few defined factors.

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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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Author and article information

Journal

Journal ID (nlm-ta): Int J Nanomedicine

Journal ID (iso-abbrev): Int J Nanomedicine

Journal ID (publisher-id): ijn

Title: International Journal of Nanomedicine

Publisher: Dove

ISSN (Print): 1176-9114

ISSN (Electronic): 1178-2013

Publication date (Electronic): 27 September 2023

Publication date Collection: 2023

Volume: 18

Pages: 5511-5527

Affiliations

[1 ]Colorectal Cancer Center, West China Hospital, Sichuan University , Chengdu, 610041, People’s Republic of China

[2 ]Department of General Surgery, West China Hospital, Sichuan University , Chengdu, 610041, People’s Republic of China

[3 ]Department of Central Transportation, West China Hospital, Sichuan University , Chengdu, 610041, People’s Republic of China

[4 ]West China School of Nursing, Sichuan University , Chengdu, 610041, People’s Republic of China

[5 ]Research Laboratory of Tumor Epigenetics and Genomics, Department of General Surgery, Frontiers Science Center for Disease-Related Molecular Network and National Clinical Research Center for Geriatrics, State Key Laboratory of Biotherapy and Cancer Center, West China Hospital, Sichuan University , Chengdu, 610041, People’s Republic of China

Author notes

Correspondence: Ziqiang Wang; Xuyang Yang, Colorectal Cancer Center, West China Hospital, Sichuan University , Chengdu, 610041, People’s Republic of China, Email wangziqiang@scu.edu.cn; yangxuyang@wchscu.cn

[*]

These authors contributed equally to this work

Author information

Yang Zhang http://orcid.org/0000-0003-0138-0028

Ziqiang Wang http://orcid.org/0000-0002-2874-1535

Article

Publisher ID: 424737

DOI: 10.2147/IJN.S424737

PMC ID: 10544113

PubMed ID: 37791321

SO-VID: a8e3692f-eabf-45ed-9eba-8d141a94c30b

License:

This work is published and licensed by Dove Medical Press Limited. The full terms of this license are available at https://www.dovepress.com/terms.php and incorporate the Creative Commons Attribution – Non Commercial (unported, v3.0) License ( http://creativecommons.org/licenses/by-nc/3.0/). By accessing the work you hereby accept the Terms. Non-commercial uses of the work are permitted without any further permission from Dove Medical Press Limited, provided the work is properly attributed. For permission for commercial use of this work, please see paragraphs 4.2 and 5 of our Terms ( https://www.dovepress.com/terms.php).

History

Date received : 07 June 2023

Date accepted : 19 September 2023

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Figures: 4, Tables: 3, References: 121, Pages: 17

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Can Organoid Model Reveal a Key Role of Extracellular Vesicles in Tumors? A Comprehensive Review of the Literature

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Most cited references 121

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

Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors.

Shedding light on the cell biology of extracellular vesicles

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