Migrasome biogenesis and functions

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Abstract

The migrasome is a newly discovered organelle produced by migrating cells. As cells migrate, long and thin retraction fibers are left in their wake. On these fibers, we discovered the production of a pomegranate‐like structure, which we named migrasomes. The production of migrasomes is highly correlated with the migration of cells. Currently, it has been demonstrated the migrasomes exhibit three modes of action: release of signaling molecules through rupturing or leaking, carriers of damaged mitochondria, and lateral transfer of mRNA or proteins. In this review, we would like to discuss, in detail, the functions, mechanisms, and potential applications of this newly discovered cell organelle.

Abstract

Migrasomes are newly found organelles produced by migrating cells and grow on retraction fibers trailing behind the cells. Migrasomes are produced as a result of tetraspanin‐enriched macrodomain accumulation and could be released into the extracellular matrix or engulfed by other cells. Migrasomes could act as carriers of mRNA, protein, or damaged mitochondria, or as chemoattractive sources.

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Discovery of the migrasome, an organelle mediating release of cytoplasmic contents during cell migration

Liang Ma, Ying Li, Junya Peng … (2014)

Cells communicate with each other through secreting and releasing proteins and vesicles. Many cells can migrate. In this study, we report the discovery of migracytosis, a cell migration-dependent mechanism for releasing cellular contents, and migrasomes, the vesicular structures that mediate migracytosis. As migrating cells move, they leave long tubular strands, called retraction fibers, behind them. Large vesicles, which contain numerous smaller vesicles, grow on the tips and intersections of retraction fibers. These fibers, which connect the vesicles with the main cell body, eventually break, and the vesicles are released into the extracellular space or directly taken up by surrounding cells. Since the formation of these vesicles is migration-dependent, we named them “migrasomes”. We also found that cytosolic contents can be transported into migrasomes and released from the cell through migrasomes. We named this migration-dependent release mechanism “migracytosis”.

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Definition of a consensus integrin adhesome and its dynamics during adhesion complex assembly and disassembly

Edward R. Horton, Adam Byron, Janet Askari … (2015)

Integrin receptor activation initiates the formation of integrin adhesion complexes (IACs) at the cell membrane that transduce adhesion-dependent signals to control a multitude of cellular functions. Proteomic analyses of isolated IACs have revealed an unanticipated molecular complexity; however, a global view of the consensus composition and dynamics of IACs is currently lacking. Here, we have integrated several IAC proteomes and generated a 2,412-protein integrin adhesome. Analysis of this dataset reveals the functional diversity of proteins in IACs and establishes a consensus adhesome of 60 proteins. The consensus adhesome likely represents a core cell adhesion machinery, centred around four axes comprising ILK-PINCH-kindlin, FAK-paxillin, talin-vinculin and α-actinin-zyxin-VASP, and includes underappreciated IAC components such as Rsu-1 and caldesmon. Proteomic quantification of IAC assembly and disassembly detailed the compositional dynamics of the core cell adhesion machinery. The definition of this consensus view of integrin adhesome components provides a resource for the research community.

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Mitocytosis, a migrasome-mediated mitochondrial quality-control process

Haifeng Jiao, Dong Liang Jiang, Xiaoyu Hu … (2021)

Damaged mitochondria need to be cleared to maintain the quality of the mitochondrial pool. Here, we report mitocytosis, a migrasome-mediated mitochondrial quality-control process. We found that, upon exposure to mild mitochondrial stresses, damaged mitochondria are transported into migrasomes and subsequently disposed of from migrating cells. Mechanistically, mitocytosis requires positioning of damaged mitochondria at the cell periphery, which occurs because damaged mitochondria avoid binding to inward motor proteins. Functionally, mitocytosis plays an important role in maintaining mitochondrial quality. Enhanced mitocytosis protects cells from mitochondrial stressor-induced loss of mitochondrial membrane potential (MMP) and mitochondrial respiration; conversely, blocking mitocytosis causes loss of MMP and mitochondrial respiration under normal conditions. Physiologically, we demonstrate that mitocytosis is required for maintaining MMP and viability in neutrophils in vivo. We propose that mitocytosis is an important mitochondrial quality-control process in migrating cells, which couples mitochondrial homeostasis with cell migration.

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Author and article information

Contributors

Li Yu:

ORCID: https://orcid.org/0000-0001-7783-2321

liyulab@mail.tsinghua.edu.cn

Journal

Journal ID (nlm-ta): FEBS J

Journal ID (iso-abbrev): FEBS J

Journal ID (doi): 10.1111/(ISSN)1742-4658

Journal ID (publisher-id): FEBS

Title: The Febs Journal

Publisher: John Wiley and Sons Inc. (Hoboken )

ISSN (Print): 1742-464X

ISSN (Electronic): 1742-4658

Publication date (Electronic): 26 September 2021

Publication date (Print): November 2022

Volume: 289

Issue: 22 , Organelle Homeostasis ( doiID: 10.1111/febs.v289.22 )

Pages: 7246-7254

Affiliations

[ ¹ ] State Key Laboratory of Membrane Biology Beijing Frontier Research Center for Biological Structure School of Life Science Tsinghua University‐Peking University Joint Center for Life Sciences Tsinghua University Beijing China

Author notes

[*] [* ] Correspondence

L. Yu, State Key Laboratory of Membrane Biology, Tsinghua University‐Peking University Joint Center for Life Sciences, Beijing Frontier Research Center for Biological Structure, School of Life Science, Tsinghua University, Beijing 100084, China

Tel: +86 010 62794552

E‐mail: liyulab@ 123456mail.tsinghua.edu.cn

Author information

Li Yu https://orcid.org/0000-0001-7783-2321

Article

Publisher ID: FEBS16183

DOI: 10.1111/febs.16183

PMC ID: 9786993

PubMed ID: 34492154

SO-VID: 9bb58a6e-5aa4-47b9-9ff6-569c240d8e55

License:

This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

History

Date revision received : 22 July 2021

Date received : 05 May 2021

Date accepted : 06 September 2021

Page count

Figures: 4, Tables: 1, Pages: 7254, Words: 6011

Funding

Funded by: Ministry of Science and Technology of the People's Republic of China , doi 10.13039/501100002855;

Award ID: 2016YFA0500202

Award ID: 2017YFA0503404

Funded by: National Natural Science Foundation of China , doi 10.13039/501100001809;

Award ID: 31430053

Award ID: 31621063

Funded by: Ministry of Science and Technology of the People's Republic of China , doi 10.13039/501100002855;

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source-schema-version-number 2.0

cover-date November 2022

details-of-publishers-convertor Converter:WILEY_ML3GV2_TO_JATSPMC version:6.2.3 mode:remove_FC converted:23.12.2022

ScienceOpen disciplines: Molecular biology

Keywords: cell migration,confocal microscopy,migrasomes,tetraspanin,transmission electron microscopy

Data availability:

ScienceOpen disciplines: Molecular biology

Keywords: cell migration, confocal microscopy, migrasomes, tetraspanin, transmission electron microscopy

Migrasome biogenesis and functions

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Most cited references 18

Discovery of the migrasome, an organelle mediating release of cytoplasmic contents during cell migration

Definition of a consensus integrin adhesome and its dynamics during adhesion complex assembly and disassembly

Mitocytosis, a migrasome-mediated mitochondrial quality-control process

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