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      Migrasomes, a new mode of intercellular communication

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          Abstract

          Migrasomes are newly discovered extracellular vesicles (EVs) that are formed in migrating cells and mediate intercellular communication. However, their size, biological generation, cargo packaging, transport, and effects on recipient cells by migrasomes are different from those of other EVs. In addition to mediating organ morphogenesis during zebrafish gastrulation, discarding damaged mitochondria, and lateral transport of mRNA and proteins, growing evidence has demonstrated that migrasomes mediate a variety of pathological processes. In this review, we summarize the discovery, mechanisms of formation, isolation, identification, and mediation of cellular communication in migrasomes. We discuss migrasome-mediated disease processes, such as osteoclast differentiation, proliferative vitreoretinopathy, tumor cell metastasis by PD-L1 transport, immune cell chemotaxis to the site of infection by chemokines, angiogenesis promotion via angiogenic factors by immune cells, and leukemic cells chemotaxis to the site of mesenchymal stromal cells. Moreover, as new EVs, we propose the potential of migrasomes for disease diagnosis and treatment.

          Supplementary Information

          The online version contains supplementary material available at 10.1186/s12964-023-01121-4.

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          Multilineage potential of adult human mesenchymal stem cells.

          M. Pittenger, A M Mackay, S C Beck … (1999)
          Human mesenchymal stem cells are thought to be multipotent cells, which are present in adult marrow, that can replicate as undifferentiated cells and that have the potential to differentiate to lineages of mesenchymal tissues, including bone, cartilage, fat, tendon, muscle, and marrow stroma. Cells that have the characteristics of human mesenchymal stem cells were isolated from marrow aspirates of volunteer donors. These cells displayed a stable phenotype and remained as a monolayer in vitro. These adult stem cells could be induced to differentiate exclusively into the adipocytic, chondrocytic, or osteocytic lineages. Individual stem cells were identified that, when expanded to colonies, retained their multilineage potential.
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            Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET.

            Héctor Peinado, Masa Aleckovic, Simon Lavotshkin … (2012)
            Tumor-derived exosomes are emerging mediators of tumorigenesis. We explored the function of melanoma-derived exosomes in the formation of primary tumors and metastases in mice and human subjects. Exosomes from highly metastatic melanomas increased the metastatic behavior of primary tumors by permanently 'educating' bone marrow progenitors through the receptor tyrosine kinase MET. Melanoma-derived exosomes also induced vascular leakiness at pre-metastatic sites and reprogrammed bone marrow progenitors toward a pro-vasculogenic phenotype that was positive for c-Kit, the receptor tyrosine kinase Tie2 and Met. Reducing Met expression in exosomes diminished the pro-metastatic behavior of bone marrow cells. Notably, MET expression was elevated in circulating CD45(-)C-KIT(low/+)TIE2(+) bone marrow progenitors from individuals with metastatic melanoma. RAB1A, RAB5B, RAB7 and RAB27A, regulators of membrane trafficking and exosome formation, were highly expressed in melanoma cells. Rab27A RNA interference decreased exosome production, preventing bone marrow education and reducing, tumor growth and metastasis. In addition, we identified an exosome-specific melanoma signature with prognostic and therapeutic potential comprised of TYRP2, VLA-4, HSP70, an HSP90 isoform and the MET oncoprotein. Our data show that exosome production, transfer and education of bone marrow cells supports tumor growth and metastasis, has prognostic value and offers promise for new therapeutic directions in the metastatic process.
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              Osteoclast differentiation and activation.

              William J. Boyle, W. Simonet, David L. Lacey (2003)
              Osteoclasts are specialized cells derived from the monocyte/macrophage haematopoietic lineage that develop and adhere to bone matrix, then secrete acid and lytic enzymes that degrade it in a specialized, extracellular compartment. Discovery of the RANK signalling pathway in the osteoclast has provided insight into the mechanisms of osteoclastogenesis and activation of bone resorption, and how hormonal signals impact bone structure and mass. Further study of this pathway is providing the molecular basis for developing therapeutics to treat osteoporosis and other diseases of bone loss.
              Article 0 comments Cited 742 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Yongbin Ma: mayongbin2009@163.com
                Xuefeng Wang:
                ORCID: http://orcid.org/0000-0002-5980-6530
                xuefengwang@ujs.edu.cn
                Journal
                Journal ID (nlm-ta): Cell Commun Signal
                Journal ID (iso-abbrev): Cell Commun Signal
                Title: Cell Communication and Signaling : CCS
                Publisher: BioMed Central (London )
                ISSN (Electronic): 1478-811X
                Publication date (Electronic): 8 May 2023
                Publication date PMC-release: 8 May 2023
                Publication date Collection: 2023
                Volume: 21
                Electronic Location Identifier: 105
                Affiliations
                [1 ]GRID grid.452247.2, Department of Central Laboratory, , The Affiliated Hospital of Jiangsu University, ; Zhenjiang, 212001 China
                [2 ]GRID grid.440785.a, ISNI 0000 0001 0743 511X, Department of Central Laboratory, , Jintan Hospital, Jiangsu University, ; 500 Avenue Jintan, Jintan, 213200 People’s Republic of China
                [3 ]GRID grid.452247.2, Department of Nuclear Medicine and Institute of Digestive Diseases, , The Affiliated Hospital of Jiangsu University, ; Zhenjiang, 212001 China
                Author information
                http://orcid.org/0000-0002-5980-6530
                Article
                Publisher ID: 1121
                DOI: 10.1186/s12964-023-01121-4
                PMC ID: 10165304
                PubMed ID: 37158915
                SO-VID: 9cca0633-4c3f-47e6-84bf-07f08939202f
                Copyright © © The Author(s) 2023
                License:

                Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                Date received : 2 March 2023
                Date accepted : 30 March 2023
                Categories
                Subject: Review
                Custom metadata
                issue-copyright-statement © BioMed Central Ltd., part of Springer Nature 2023

                ScienceOpen disciplines: Cell biology
                Keywords: migrasomes,extracellular vesicles,new mode,intercellular communication
                Data availability:
                ScienceOpen disciplines: Cell biology
                Keywords: migrasomes, extracellular vesicles, new mode, intercellular communication

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