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      Exosomes: a promising avenue for cancer diagnosis beyond treatment

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          Abstract

          Exosomes, extracellular vesicles secreted by cells, have garnered significant attention in recent years for their remarkable therapeutic potential. These nanoscale carriers can be harnessed for the targeted delivery of therapeutic agents, such as pharmaceuticals, proteins, and nucleic acids, across biological barriers. This versatile attribute of exosomes is a promising modality for precision medicine applications, notably in the realm of cancer therapy. However, despite their substantial therapeutic potential, exosomes still confront challenges tied to standardization and scalability that impede their practice in clinical applications. Moreover, heterogeneity in isolation methodologies and limited cargo loading mechanisms pose obstacles to ensuring consistent outcomes, thereby constraining their therapeutic utility. In contrast, exosomes exhibit a distinct advantage in cancer diagnosis, as they harbor specific signatures reflective of the tumor’s genetic and proteomic profile. This characteristic endows them with the potential to serve as valuable liquid biopsies for non-invasive and real-time monitoring, making possible early cancer detection for the development of personalized treatment strategies. In this review, we provide an extensive evaluation of the advancements in exosome research, critically examining their advantages and limitations in the context of cancer therapy and early diagnosis. Furthermore, we present a curated overview of the most recent technological innovations utilizing exosomes, with a focus on enhancing the efficacy of early cancer detection.

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          The biology, function, and biomedical applications of exosomes

          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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            Specificities of secretion and uptake of exosomes and other extracellular vesicles for cell-to-cell communication

            The ability of exosomes to transfer cargo from donor to acceptor cells, thereby triggering phenotypic changes in the latter, has generated substantial interest in the scientific community. However, the extent to which exosomes differ from other extracellular vesicles in terms of their biogenesis and functions remains ill-defined. Here, we discuss the current knowledge on the specificities of exosomes and other types of extracellular vesicles, and their roles as important agents of cell-to-cell communication.
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              Tumour exosome integrins determine organotropic metastasis

              Ever since Stephen Paget’s 1889 hypothesis, metastatic organotropism has remained one of cancer’s greatest mysteries. Here we demonstrate that exosomes from mouse and human lung-, liver- and brain-tropic tumour cells fuse preferentially with resident cells at their predicted destination, namely lung fibroblasts and epithelial cells, liver Kupffer cells and brain endothelial cells. We show that tumour-derived exosomes uptaken by organ-specific cells prepare the pre-metastatic niche. Treatment with exosomes from lung-tropic models redirected the metastasis of bone-tropic tumour cells. Exosome proteomics revealed distinct integrin expression patterns, in which the exosomal integrins α6β4 and α6β1 were associated with lung metastasis, while exosomal integrin αvβ5 was linked to liver metastasis. Targeting the integrins α6β4 and αvβ5 decreased exosome uptake, as well as lung and liver metastasis, respectively. We demonstrate that exosome integrin uptake by resident cells activates Src phosphorylation and pro-inflammatory S100 gene expression. Finally, our clinical data indicate that exosomal integrins could be used to predict organ-specific metastasis.
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                Author and article information

                Contributors
                URI : https://loop.frontiersin.org/people/1903173/overviewRole:
                Role: Role:
                Role:
                URI : https://loop.frontiersin.org/people/1241413/overviewRole: Role: Role: Role: Role:
                Journal
                Front Cell Dev Biol
                Front Cell Dev Biol
                Front. Cell Dev. Biol.
                Frontiers in Cell and Developmental Biology
                Frontiers Media S.A.
                2296-634X
                13 February 2024
                2024
                : 12
                : 1344705
                Affiliations
                [1] 1 Breast Center, West China Hospital, Sichuan University , Chengdu, China
                [2] 2 Department of General Surgery, West China Hospital, Sichuan University , Chengdu, China
                [3] 3 Institute for Breast Health Medicine, West China Hospital, Sichuan University , Chengdu, China
                [4] 4 Department of Oncology, The First Affiliated Hospital of Zhengzhou University , Zhengzhou, China
                [5] 5 School of Basic Medicine, Dali University , Dali, Yunnan, China
                Author notes

                Edited by: Li Yan, University of Maryland, College Park, United States

                Reviewed by: Dwijendra K. Gupta, Allahabad University, India

                Jianwei Wang, Chongqing Medical University, China

                *Correspondence: Jie Chen, chenjiewestchina@ 123456163.com
                Article
                1344705
                10.3389/fcell.2024.1344705
                10900531
                38419843
                dd5560a9-b949-4192-b1c2-2660398ed989
                Copyright © 2024 Wang, Wang, Qin and Chen.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 26 November 2023
                : 31 January 2024
                Funding
                The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work is supported by the National Natural Science Foundation of China (No. 8197211).
                Categories
                Cell and Developmental Biology
                Review
                Custom metadata
                Stem Cell Research

                exosome,cancer,diagnosis,therapy,translational research
                exosome, cancer, diagnosis, therapy, translational research

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