The power of imaging to understand extracellular vesicle biology in vivo

Frederik J. Verweij; Leonora Balaj; Chantal M. Boulanger; David R.F. Carter; Ewoud B. Compeer; Gisela D’Angelo; Samir El Andaloussi; Jacky G. Goetz; Julia Christina Gross; Vincent Hyenne; Eva Maria Krämer-Albers; Charles P. Lai; Xavier Loyer; Alex Marki; Stefan Momma; Esther N.M. Nolte-‘t Hoen; D. Michiel Pegtel; Hector Peinado; Graça Raposo; Kirsi Rilla; Hidetoshi Tahara; Clotilde Théry; Martin E. van Royen; Roosmarijn E. Vandenbroucke; Ann M. Wehman; Kenneth Witwer; Zhiwei Wu; Richard Wubbolts; Guillaume van Niel

doi:10.1038/s41592-021-01206-3

The power of imaging to understand extracellular vesicle biology in vivo

Frederik J. Verweij^*, Leonora Balaj, Chantal M. Boulanger, David R.F. Carter, Ewoud B. Compeer, Gisela D’Angelo, Samir El Andaloussi, Jacky G. Goetz, Julia Christina Gross, Vincent Hyenne, Eva Maria Krämer-Albers, Charles P. Lai, Xavier Loyer, Alex Marki, Stefan Momma, Esther N.M. Nolte-‘t Hoen, D. Michiel Pegtel, Hector Peinado, Graça Raposo, Kirsi RillaHidetoshi Tahara, Clotilde Théry, Martin E. van Royen, Roosmarijn E. Vandenbroucke, Ann M. Wehman, Kenneth Witwer, Zhiwei Wu, Richard Wubbolts, Guillaume van Niel^*

^*Corresponding author for this work

Pathology

Research output: Contribution to journal › Review article › Academic › peer-review

197 Citations (Scopus)

Abstract

Extracellular vesicles (EVs) are nano-sized lipid bilayer vesicles released by virtually every cell type. EVs have diverse biological activities, ranging from roles in development and homeostasis to cancer progression, which has spurred the development of EVs as disease biomarkers and drug nanovehicles. Owing to the small size of EVs, however, most studies have relied on isolation and biochemical analysis of bulk EVs separated from biofluids. Although informative, these approaches do not capture the dynamics of EV release, biodistribution, and other contributions to pathophysiology. Recent advances in live and high-resolution microscopy techniques, combined with innovative EV labeling strategies and reporter systems, provide new tools to study EVs in vivo in their physiological environment and at the single-vesicle level. Here we critically review the latest advances and challenges in EV imaging, and identify urgent, outstanding questions in our quest to unravel EV biology and therapeutic applications.

Original language	English
Pages (from-to)	1013-1026
Number of pages	14
Journal	Nature Methods
Volume	18
Issue number	9
Early online date	26 Aug 2021
DOIs	https://doi.org/10.1038/s41592-021-01206-3
Publication status	Published - Sept 2021

Bibliographical note

Funding Information:
The authors acknowledge financial support from the International Society for Extracellular Vesicles, the French Society of Extracellular vesicles, the Société Française des Microscopies, the ITMO BCDE for their support for the organization of the ISEV workshop ‘EV imaging in vivo’ that provided the basis for this review. We thank the workshop organizing committee members G.D.’A., V.H., E.-M.K.-A., X.L., and K.W. for their help. We thank P. Stahl (Washington University School of Medicine, USA) for stimulating discussions and insight. F.J.V. is supported by INCa 2019-125, E.B.C. thanks M. Dustin for support through ERC AdG 670930. D.R.F.C. is supported by the BBSRC (BB/P006205/1) and Cancer Research UK (A28052). V.H. and J.G.G. are funded by La Ligue contre le Cancer, by INCa (PLBIO19-291), by Plan Cancer (Nanotumor) and through institutional funds from University of Strasbourg and INSERM. K.R. is supported by the UEF Cell and Tissue Imaging Unit, Biocenter Kuopio and Biocenter Finland. We apologize to colleagues for any relevant work that could not be cited due to space restrictions.

Publisher Copyright:
© 2021, Springer Nature America, Inc.

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Verweij, F. J., Balaj, L., Boulanger, C. M., Carter, D. R. F., Compeer, E. B., D’Angelo, G., El Andaloussi, S., Goetz, J. G., Gross, J. C., Hyenne, V., Krämer-Albers, E. M., Lai, C. P., Loyer, X., Marki, A., Momma, S., Nolte-‘t Hoen, E. N. M., Pegtel, D. M., Peinado, H., Raposo, G., ... van Niel, G. (2021). The power of imaging to understand extracellular vesicle biology in vivo. Nature Methods, 18(9), 1013-1026. https://doi.org/10.1038/s41592-021-01206-3

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title = "The power of imaging to understand extracellular vesicle biology in vivo",

abstract = "Extracellular vesicles (EVs) are nano-sized lipid bilayer vesicles released by virtually every cell type. EVs have diverse biological activities, ranging from roles in development and homeostasis to cancer progression, which has spurred the development of EVs as disease biomarkers and drug nanovehicles. Owing to the small size of EVs, however, most studies have relied on isolation and biochemical analysis of bulk EVs separated from biofluids. Although informative, these approaches do not capture the dynamics of EV release, biodistribution, and other contributions to pathophysiology. Recent advances in live and high-resolution microscopy techniques, combined with innovative EV labeling strategies and reporter systems, provide new tools to study EVs in vivo in their physiological environment and at the single-vesicle level. Here we critically review the latest advances and challenges in EV imaging, and identify urgent, outstanding questions in our quest to unravel EV biology and therapeutic applications.",

author = "Verweij, {Frederik J.} and Leonora Balaj and Boulanger, {Chantal M.} and Carter, {David R.F.} and Compeer, {Ewoud B.} and Gisela D{\textquoteright}Angelo and {El Andaloussi}, Samir and Goetz, {Jacky G.} and Gross, {Julia Christina} and Vincent Hyenne and Kr{\"a}mer-Albers, {Eva Maria} and Lai, {Charles P.} and Xavier Loyer and Alex Marki and Stefan Momma and {Nolte-{\textquoteleft}t Hoen}, {Esther N.M.} and Pegtel, {D. Michiel} and Hector Peinado and Gra{\c c}a Raposo and Kirsi Rilla and Hidetoshi Tahara and Clotilde Th{\'e}ry and {van Royen}, {Martin E.} and Vandenbroucke, {Roosmarijn E.} and Wehman, {Ann M.} and Kenneth Witwer and Zhiwei Wu and Richard Wubbolts and {van Niel}, Guillaume",

note = "Funding Information: The authors acknowledge financial support from the International Society for Extracellular Vesicles, the French Society of Extracellular vesicles, the Soci{\'e}t{\'e} Fran{\c c}aise des Microscopies, the ITMO BCDE for their support for the organization of the ISEV workshop {\textquoteleft}EV imaging in vivo{\textquoteright} that provided the basis for this review. We thank the workshop organizing committee members G.D.{\textquoteright}A., V.H., E.-M.K.-A., X.L., and K.W. for their help. We thank P. Stahl (Washington University School of Medicine, USA) for stimulating discussions and insight. F.J.V. is supported by INCa 2019-125, E.B.C. thanks M. Dustin for support through ERC AdG 670930. D.R.F.C. is supported by the BBSRC (BB/P006205/1) and Cancer Research UK (A28052). V.H. and J.G.G. are funded by La Ligue contre le Cancer, by INCa (PLBIO19-291), by Plan Cancer (Nanotumor) and through institutional funds from University of Strasbourg and INSERM. K.R. is supported by the UEF Cell and Tissue Imaging Unit, Biocenter Kuopio and Biocenter Finland. We apologize to colleagues for any relevant work that could not be cited due to space restrictions. Publisher Copyright: {\textcopyright} 2021, Springer Nature America, Inc.",

year = "2021",

month = sep,

doi = "10.1038/s41592-021-01206-3",

language = "English",

volume = "18",

pages = "1013--1026",

journal = "Nature Methods",

issn = "1548-7091",

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Verweij, FJ, Balaj, L, Boulanger, CM, Carter, DRF, Compeer, EB, D’Angelo, G, El Andaloussi, S, Goetz, JG, Gross, JC, Hyenne, V, Krämer-Albers, EM, Lai, CP, Loyer, X, Marki, A, Momma, S, Nolte-‘t Hoen, ENM, Pegtel, DM, Peinado, H, Raposo, G, Rilla, K, Tahara, H, Théry, C, van Royen, ME, Vandenbroucke, RE, Wehman, AM, Witwer, K, Wu, Z, Wubbolts, R & van Niel, G 2021, 'The power of imaging to understand extracellular vesicle biology in vivo', Nature Methods, vol. 18, no. 9, pp. 1013-1026. https://doi.org/10.1038/s41592-021-01206-3

TY - JOUR

T1 - The power of imaging to understand extracellular vesicle biology in vivo

AU - Verweij, Frederik J.

AU - Balaj, Leonora

AU - Boulanger, Chantal M.

AU - Carter, David R.F.

AU - Compeer, Ewoud B.

AU - D’Angelo, Gisela

AU - El Andaloussi, Samir

AU - Goetz, Jacky G.

AU - Gross, Julia Christina

AU - Hyenne, Vincent

AU - Krämer-Albers, Eva Maria

AU - Lai, Charles P.

AU - Loyer, Xavier

AU - Marki, Alex

AU - Momma, Stefan

AU - Nolte-‘t Hoen, Esther N.M.

AU - Pegtel, D. Michiel

AU - Peinado, Hector

AU - Raposo, Graça

AU - Rilla, Kirsi

AU - Tahara, Hidetoshi

AU - Théry, Clotilde

AU - van Royen, Martin E.

AU - Vandenbroucke, Roosmarijn E.

AU - Wehman, Ann M.

AU - Witwer, Kenneth

AU - Wu, Zhiwei

AU - Wubbolts, Richard

AU - van Niel, Guillaume

N1 - Funding Information: The authors acknowledge financial support from the International Society for Extracellular Vesicles, the French Society of Extracellular vesicles, the Société Française des Microscopies, the ITMO BCDE for their support for the organization of the ISEV workshop ‘EV imaging in vivo’ that provided the basis for this review. We thank the workshop organizing committee members G.D.’A., V.H., E.-M.K.-A., X.L., and K.W. for their help. We thank P. Stahl (Washington University School of Medicine, USA) for stimulating discussions and insight. F.J.V. is supported by INCa 2019-125, E.B.C. thanks M. Dustin for support through ERC AdG 670930. D.R.F.C. is supported by the BBSRC (BB/P006205/1) and Cancer Research UK (A28052). V.H. and J.G.G. are funded by La Ligue contre le Cancer, by INCa (PLBIO19-291), by Plan Cancer (Nanotumor) and through institutional funds from University of Strasbourg and INSERM. K.R. is supported by the UEF Cell and Tissue Imaging Unit, Biocenter Kuopio and Biocenter Finland. We apologize to colleagues for any relevant work that could not be cited due to space restrictions. Publisher Copyright: © 2021, Springer Nature America, Inc.

PY - 2021/9

Y1 - 2021/9

N2 - Extracellular vesicles (EVs) are nano-sized lipid bilayer vesicles released by virtually every cell type. EVs have diverse biological activities, ranging from roles in development and homeostasis to cancer progression, which has spurred the development of EVs as disease biomarkers and drug nanovehicles. Owing to the small size of EVs, however, most studies have relied on isolation and biochemical analysis of bulk EVs separated from biofluids. Although informative, these approaches do not capture the dynamics of EV release, biodistribution, and other contributions to pathophysiology. Recent advances in live and high-resolution microscopy techniques, combined with innovative EV labeling strategies and reporter systems, provide new tools to study EVs in vivo in their physiological environment and at the single-vesicle level. Here we critically review the latest advances and challenges in EV imaging, and identify urgent, outstanding questions in our quest to unravel EV biology and therapeutic applications.

AB - Extracellular vesicles (EVs) are nano-sized lipid bilayer vesicles released by virtually every cell type. EVs have diverse biological activities, ranging from roles in development and homeostasis to cancer progression, which has spurred the development of EVs as disease biomarkers and drug nanovehicles. Owing to the small size of EVs, however, most studies have relied on isolation and biochemical analysis of bulk EVs separated from biofluids. Although informative, these approaches do not capture the dynamics of EV release, biodistribution, and other contributions to pathophysiology. Recent advances in live and high-resolution microscopy techniques, combined with innovative EV labeling strategies and reporter systems, provide new tools to study EVs in vivo in their physiological environment and at the single-vesicle level. Here we critically review the latest advances and challenges in EV imaging, and identify urgent, outstanding questions in our quest to unravel EV biology and therapeutic applications.

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DO - 10.1038/s41592-021-01206-3

M3 - Review article

C2 - 34446922

AN - SCOPUS:85111844476

SN - 1548-7091

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SP - 1013

EP - 1026

JO - Nature Methods

JF - Nature Methods

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ER -

The power of imaging to understand extracellular vesicle biology in vivo

Abstract

Bibliographical note

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