Filopodium-derived vesicles produced by MIM enhance the migration of recipient cells

Nishimura, Taiichi; Oyama, Takuya; Hu, Hooi Ting; Fujioka, Toshifumi; Hanawa-Suetsugu, Kyoko; Ikeda, Kazutaka; Yamada, Sohei; Kawana, Hiroki; Saigusa, Daisuke; Ikeda, Hiroki; Kurata, Rie; Oono-Yakura, Kayoko; Kitamata, Manabu; Kida, Kazuki; Hikita, Tomoya; Mizutani, Kiyohito; Yasuhara, Kazuma; Mimori-Kiyosue, Yuko; Oneyama, Chitose; Kurimoto, Kazuki; Hosokawa, Yoichiroh; Aoki, Junken; Takai, Yoshimi; Arita, Makoto; Suetsugu, Shiro

doi:10.1016/j.devcel.2021.02.029

Cited by 36 publications

(29 citation statements)

References 99 publications

(123 reference statements)

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“…It was suggested that N‐BAR protein endophilin can create points of friction at sites of inwards membrane tubulation via a so‐called friction‐driven scission model (Simunovic et al., 2017 ). Furthermore, a recent study suggests that external forces promote scission of filopodia with the assistance of I‐BAR proteins to generate filopodia‐derived vesicles (Nishimura et al., 2021 ). This is an interesting finding to show the role of friction in EV release and to open novel research lines for protrusion‐derived EVs.…”

Section: Role Of Actin and Other Proteins Regulating The Cytoskeleton And Membranes In Ev Shedding Processmentioning

confidence: 99%

“…A recent study by Nishimura et al. describes the specific proteins (IRS4 and Rac1) carried by filopodia‐derived EVs and their enhanced effect on the migration of target cells (Nishimura et al., 2021 ). These findings are promising for more specific identification and determination of the proportion of the EVs originated from plasma membrane protrusions.…”

Section: Final Conclusionmentioning

confidence: 99%

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Diverse plasma membrane protrusions act as platforms for extracellular vesicle shedding

Rilla

2021

J of Extracellular Vesicle

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Plasma membrane curvature is an important factor in the regulation of cellular phenotype and is critical for various cellular activities including the shedding of extracellular vesicles (EV). One of the most striking morphological features of cells is different plasma membrane‐covered extensions supported by actin core such as filopodia and microvilli. Despite the various functions of these extensions are partially unexplained, they are known to facilitate many crucial cellular functions such as migration, adhesion, absorption, and secretion. Due to the rapid increase in the research activity of EVs, there is raising evidence that one of the general features of cellular plasma membrane protrusions is to act as specialized platforms for the budding of EVs. This review will focus on early observations and recent findings supporting this hypothesis, discuss the putative budding and shedding mechanisms of protrusion‐derived EVs and their biological significance.

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Section: Role Of Actin and Other Proteins Regulating The Cytoskeleton And Membranes In Ev Shedding Processmentioning

confidence: 99%

Section: Final Conclusionmentioning

confidence: 99%

Diverse plasma membrane protrusions act as platforms for extracellular vesicle shedding

Rilla

2021

J of Extracellular Vesicle

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“…Ectosomes, also known as microvesicles ( Figure 1 A), are generated through outward budding of the cell plasma membrane, producing vesicles ranging from 50–1000 nm in diameter [ 3 ]. Inherent cellular protrusions such as microvilli, as well as other types of protrusions observed during cell division and migration such as filopodia and retraction fibers, are also linked to ectosome biogenesis and act as a source of EVs [ 21 , 22 ].…”

Section: Biogenesis Of Evsmentioning

confidence: 99%

Extracellular Vesicles: Interplay with the Extracellular Matrix and Modulated Cell Responses

Halawani

Mithieux

Yeo

et al. 2022

IJMS

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The discovery that cells secrete extracellular vesicles (EVs), which carry a variety of regulatory proteins, nucleic acids, and lipids, has shed light on the sophisticated manner by which cells can communicate and accordingly function. The bioactivity of EVs is not only defined by their internal content, but also through their surface associated molecules, and the linked downstream signaling effects they elicit in target cells. The extracellular matrix (ECM) contains signaling and structural molecules that are central to tissue maintenance and repair. Recently, a subset of EVs residing within the extracellular matrix has been identified. Although some roles have been proposed for matrix-bound vesicles, their role as signaling molecules within the ECM is yet to be explored. Given the close association of EVs and the ECM, it is not surprising that EVs partly mediate repair and regeneration by modulating matrix deposition and degradation through their cellular targets. This review addresses unique EV features that allow them to interact with and navigate through the ECM, describes how their release and content is influenced by the ECM, and emphasizes the emerging role of stem-cell derived EVs in tissue repair and regeneration through their matrix-modulating properties.

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“…In order to generate CD30 + EVs for subsequent experiments, we cultivated the CD30 + L540 cell line for 1 h under serum-free conditions and harvested the cell supernatant. The l-EVs sediment at lower gravity than the s-EVs (Nishimura et al, 2021). In order to determine, which EV type preferentially contains CD30, we compared EVs that sediment at different gravity.…”

Section: Production Of Cd30 + Evsmentioning

confidence: 99%

“…They originate from the outward budding of multivesicular endosomes or budding from the plasma membrane. Endosomederived EVs are referred to as small EVs (s-EVs, exosomes) and are generally smaller than plasma membrane-derived large EVs (l-EVs or microvesicles) (Thery et al, 2009;Nishimura et al, 2021). Both EV types are membraneenclosed particles and harbor typical traits of the donor cells, including nucleic acids, lipids, and soluble and membraneassociated proteins.…”

Section: Introductionmentioning

confidence: 99%

CD30-Positive Extracellular Vesicles Enable the Targeting of CD30-Negative DLBCL Cells by the CD30 Antibody-Drug Conjugate Brentuximab Vedotin

Lobastova

Lettau

Babatz

et al. 2021

Front. Cell Dev. Biol.

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CD30, a member of the TNF receptor superfamily, is selectively expressed on a subset of activated lymphocytes and on malignant cells of certain lymphomas, such as classical Hodgkin Lymphoma (cHL), where it activates critical bystander cells in the tumor microenvironment. Therefore, it is not surprising that the CD30 antibody-drug conjugate Brentuximab Vedotin (BV) represents a powerful, FDA-approved treatment option for CD30+ hematological malignancies. However, BV also exerts a strong anti-cancer efficacy in many cases of diffuse large B cell lymphoma (DLBCL) with poor CD30 expression, even when lacking detectable CD30+ tumor cells. The mechanism remains enigmatic. Because CD30 is released on extracellular vesicles (EVs) from both, malignant and activated lymphocytes, we studied whether EV-associated CD30 might end up in CD30– tumor cells to provide binding sites for BV. Notably, CD30+ EVs bind to various DLBCL cell lines as well as to the FITC-labeled variant of the antibody-drug conjugate BV, thus potentially conferring the BV binding also to CD30– cells. Confocal microscopy and imaging cytometry studies revealed that BV binding and uptake depend on CD30+ EVs. Since BV is only toxic toward CD30– DLBCL cells when CD30+ EVs support its uptake, we conclude that EVs not only communicate within the tumor microenvironment but also influence cancer treatment. Ultimately, the CD30-based BV not only targets CD30+ tumor cell but also CD30– DLBCL cells in the presence of CD30+ EVs. Our study thus provides a feasible explanation for the clinical impact of BV in CD30– DLBCL and warrants confirming studies in animal models.

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Filopodium-derived vesicles produced by MIM enhance the migration of recipient cells

Cited by 36 publications

References 99 publications

Diverse plasma membrane protrusions act as platforms for extracellular vesicle shedding

Diverse plasma membrane protrusions act as platforms for extracellular vesicle shedding

Extracellular Vesicles: Interplay with the Extracellular Matrix and Modulated Cell Responses

CD30-Positive Extracellular Vesicles Enable the Targeting of CD30-Negative DLBCL Cells by the CD30 Antibody-Drug Conjugate Brentuximab Vedotin

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