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Matrix-associated extracellular vesicles modulate human smooth muscle cell adhesion and directionality by presenting collagen VI. / Kapustin, AN; Tsakali, SS; Whitehead, M; Chennell, G; Wu, MY; Molenaar, C; Kutikhin, A; Chen, YM; Ahmad, S; Bogdanov, L; Sinitsky, M; Rubina, K; Clayton, A; Verweij, FJ; Pegtel, DM; Zingaro, S; Lobov, A; Zainullina, B; Owen, D; Parsons, M; Cheney, RE; Warren, DT; Humphries, MJ; Iskratsch, T; Holt, M; Shanahan, CM.

в: eLife, Том 12, 2025.

Результаты исследований: Научные публикации в периодических изданияхстатьяРецензирование

Harvard

Kapustin, AN, Tsakali, SS, Whitehead, M, Chennell, G, Wu, MY, Molenaar, C, Kutikhin, A, Chen, YM, Ahmad, S, Bogdanov, L, Sinitsky, M, Rubina, K, Clayton, A, Verweij, FJ, Pegtel, DM, Zingaro, S, Lobov, A, Zainullina, B, Owen, D, Parsons, M, Cheney, RE, Warren, DT, Humphries, MJ, Iskratsch, T, Holt, M & Shanahan, CM 2025, 'Matrix-associated extracellular vesicles modulate human smooth muscle cell adhesion and directionality by presenting collagen VI', eLife, Том. 12. https://doi.org/10.7554/eLife.90375

APA

Kapustin, AN., Tsakali, SS., Whitehead, M., Chennell, G., Wu, MY., Molenaar, C., Kutikhin, A., Chen, YM., Ahmad, S., Bogdanov, L., Sinitsky, M., Rubina, K., Clayton, A., Verweij, FJ., Pegtel, DM., Zingaro, S., Lobov, A., Zainullina, B., Owen, D., ... Shanahan, CM. (2025). Matrix-associated extracellular vesicles modulate human smooth muscle cell adhesion and directionality by presenting collagen VI. eLife, 12. https://doi.org/10.7554/eLife.90375

Vancouver

Author

Kapustin, AN ; Tsakali, SS ; Whitehead, M ; Chennell, G ; Wu, MY ; Molenaar, C ; Kutikhin, A ; Chen, YM ; Ahmad, S ; Bogdanov, L ; Sinitsky, M ; Rubina, K ; Clayton, A ; Verweij, FJ ; Pegtel, DM ; Zingaro, S ; Lobov, A ; Zainullina, B ; Owen, D ; Parsons, M ; Cheney, RE ; Warren, DT ; Humphries, MJ ; Iskratsch, T ; Holt, M ; Shanahan, CM. / Matrix-associated extracellular vesicles modulate human smooth muscle cell adhesion and directionality by presenting collagen VI. в: eLife. 2025 ; Том 12.

BibTeX

@article{8a6c2b45e38240f0bbcd9c655073d2bc,
title = "Matrix-associated extracellular vesicles modulate human smooth muscle cell adhesion and directionality by presenting collagen VI",
abstract = "The extracellular matrix (ECM) supports blood vessel architecture and functionality and undergoes active remodelling during vascular repair and atherogenesis. Vascular smooth muscle cells (VSMCs) are essential for vessel repair and, via their secretome, can invade from the vessel media into the intima to mediate ECM remodelling. Accumulation of fibronectin (FN) is a hallmark of early vascular repair and atherosclerosis. Here, we show that FN stimulates human VSMCs to secrete small extracellular vesicles (sEVs) by activating the beta 1 integrin/FAK/Src pathway as well as Arp2/3-dependent branching of the actin cytoskeleton. We found that sEVs are trapped by the ECM in vitro and colocalise with FN in symptomatic atherosclerotic plaques in vivo. Functionally, ECM-trapped sEVs induced the formation of focal adhesions (FA) with enhanced pulling forces at the cellular periphery preventing cellular spreading and adhesion. Proteomic and GO pathway analysis revealed that VSMC-derived sEVs display a cell adhesion signature and are specifically enriched with collagen VI on the sEV surface. In vitro assays identified collagen VI as playing a key role in cell adhesion and invasion directionality. Taken together, our data suggests that the accumulation of FN is a key early event in vessel repair acting to promote secretion of collagen VI enriched sEVs by VSMCs. These sEVs stimulate directional invasion, most likely by triggering peripheral focal adhesion formation and actomyosin contraction to exert sufficient traction force to enable VSMC movement within the complex vascular ECM network.",
keywords = "extracellular matrix, cell migration, cell adhesion, regeneration, BINDING PROTEIN RHO, ACTIN STRESS FIBERS, EXOSOME SECRETION, ATHEROSCLEROTIC PLAQUES, VASCULAR CALCIFICATION, AMEBOID INVASIVENESS, MEMBRANE PROTRUSION, FOCAL ADHESIONS, MYOSIN-X, INTEGRIN",
author = "AN Kapustin and SS Tsakali and M Whitehead and G Chennell and MY Wu and C Molenaar and A Kutikhin and YM Chen and S Ahmad and L Bogdanov and M Sinitsky and K Rubina and A Clayton and FJ Verweij and DM Pegtel and S Zingaro and A Lobov and B Zainullina and D Owen and M Parsons and RE Cheney and DT Warren and MJ Humphries and T Iskratsch and M Holt and CM Shanahan",
note = "Times Cited in Web of Science Core Collection: 1 Total Times Cited: 1 Cited Reference Count: 111",
year = "2025",
doi = "10.7554/eLife.90375",
language = "Английский",
volume = "12",
journal = "eLife",
issn = "2050-084X",
publisher = "eLife Sciences Publications",

}

RIS

TY - JOUR

T1 - Matrix-associated extracellular vesicles modulate human smooth muscle cell adhesion and directionality by presenting collagen VI

AU - Kapustin, AN

AU - Tsakali, SS

AU - Whitehead, M

AU - Chennell, G

AU - Wu, MY

AU - Molenaar, C

AU - Kutikhin, A

AU - Chen, YM

AU - Ahmad, S

AU - Bogdanov, L

AU - Sinitsky, M

AU - Rubina, K

AU - Clayton, A

AU - Verweij, FJ

AU - Pegtel, DM

AU - Zingaro, S

AU - Lobov, A

AU - Zainullina, B

AU - Owen, D

AU - Parsons, M

AU - Cheney, RE

AU - Warren, DT

AU - Humphries, MJ

AU - Iskratsch, T

AU - Holt, M

AU - Shanahan, CM

N1 - Times Cited in Web of Science Core Collection: 1 Total Times Cited: 1 Cited Reference Count: 111

PY - 2025

Y1 - 2025

N2 - The extracellular matrix (ECM) supports blood vessel architecture and functionality and undergoes active remodelling during vascular repair and atherogenesis. Vascular smooth muscle cells (VSMCs) are essential for vessel repair and, via their secretome, can invade from the vessel media into the intima to mediate ECM remodelling. Accumulation of fibronectin (FN) is a hallmark of early vascular repair and atherosclerosis. Here, we show that FN stimulates human VSMCs to secrete small extracellular vesicles (sEVs) by activating the beta 1 integrin/FAK/Src pathway as well as Arp2/3-dependent branching of the actin cytoskeleton. We found that sEVs are trapped by the ECM in vitro and colocalise with FN in symptomatic atherosclerotic plaques in vivo. Functionally, ECM-trapped sEVs induced the formation of focal adhesions (FA) with enhanced pulling forces at the cellular periphery preventing cellular spreading and adhesion. Proteomic and GO pathway analysis revealed that VSMC-derived sEVs display a cell adhesion signature and are specifically enriched with collagen VI on the sEV surface. In vitro assays identified collagen VI as playing a key role in cell adhesion and invasion directionality. Taken together, our data suggests that the accumulation of FN is a key early event in vessel repair acting to promote secretion of collagen VI enriched sEVs by VSMCs. These sEVs stimulate directional invasion, most likely by triggering peripheral focal adhesion formation and actomyosin contraction to exert sufficient traction force to enable VSMC movement within the complex vascular ECM network.

AB - The extracellular matrix (ECM) supports blood vessel architecture and functionality and undergoes active remodelling during vascular repair and atherogenesis. Vascular smooth muscle cells (VSMCs) are essential for vessel repair and, via their secretome, can invade from the vessel media into the intima to mediate ECM remodelling. Accumulation of fibronectin (FN) is a hallmark of early vascular repair and atherosclerosis. Here, we show that FN stimulates human VSMCs to secrete small extracellular vesicles (sEVs) by activating the beta 1 integrin/FAK/Src pathway as well as Arp2/3-dependent branching of the actin cytoskeleton. We found that sEVs are trapped by the ECM in vitro and colocalise with FN in symptomatic atherosclerotic plaques in vivo. Functionally, ECM-trapped sEVs induced the formation of focal adhesions (FA) with enhanced pulling forces at the cellular periphery preventing cellular spreading and adhesion. Proteomic and GO pathway analysis revealed that VSMC-derived sEVs display a cell adhesion signature and are specifically enriched with collagen VI on the sEV surface. In vitro assays identified collagen VI as playing a key role in cell adhesion and invasion directionality. Taken together, our data suggests that the accumulation of FN is a key early event in vessel repair acting to promote secretion of collagen VI enriched sEVs by VSMCs. These sEVs stimulate directional invasion, most likely by triggering peripheral focal adhesion formation and actomyosin contraction to exert sufficient traction force to enable VSMC movement within the complex vascular ECM network.

KW - extracellular matrix

KW - cell migration

KW - cell adhesion

KW - regeneration

KW - BINDING PROTEIN RHO

KW - ACTIN STRESS FIBERS

KW - EXOSOME SECRETION

KW - ATHEROSCLEROTIC PLAQUES

KW - VASCULAR CALCIFICATION

KW - AMEBOID INVASIVENESS

KW - MEMBRANE PROTRUSION

KW - FOCAL ADHESIONS

KW - MYOSIN-X

KW - INTEGRIN

U2 - 10.7554/eLife.90375

DO - 10.7554/eLife.90375

M3 - статья

VL - 12

JO - eLife

JF - eLife

SN - 2050-084X

ER -

ID: 147948735