A novel multiplexed immunoassay for surface‐exposed proteins in plasma extracellular vesicles

Abstract Small membranous extracellular vesicles (EV) incorporate proteins and nucleic acids from the parent cell. Proteins exposed on EV surface are dictated by cellular origin and biogenesis pathway. To better understand the EV origin and function, it is important to develop methods that reveal su...

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Main Authors: Emma Tordoff, Jillian Allen, Katya Elgart, Ahmed Elsherbini, Vrinda Kalia, Haotian Wu, Erden Eren, Dimitrios Kapogiannis, Olesia Gololobova, Kenneth Witwer, Olga Volpert, Erez Eitan
Format: Article
Language:English
Published: Wiley 2024-11-01
Series:Journal of Extracellular Vesicles
Subjects:
Online Access:https://doi.org/10.1002/jev2.70007
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author Emma Tordoff
Jillian Allen
Katya Elgart
Ahmed Elsherbini
Vrinda Kalia
Haotian Wu
Erden Eren
Dimitrios Kapogiannis
Olesia Gololobova
Kenneth Witwer
Olga Volpert
Erez Eitan
author_facet Emma Tordoff
Jillian Allen
Katya Elgart
Ahmed Elsherbini
Vrinda Kalia
Haotian Wu
Erden Eren
Dimitrios Kapogiannis
Olesia Gololobova
Kenneth Witwer
Olga Volpert
Erez Eitan
author_sort Emma Tordoff
collection DOAJ
description Abstract Small membranous extracellular vesicles (EV) incorporate proteins and nucleic acids from the parent cell. Proteins exposed on EV surface are dictated by cellular origin and biogenesis pathway. To better understand the EV origin and function, it is important to develop methods that reveal surface protein composition of heterogeneous EV populations in culture supernatants and in biofluids. Tetraspanins CD9, CD63, and CD81 are common and abundant EV markers. However, their relative enrichment (profile) on EVs of specific cellular origins is not fully elucidated. We introduce LuminEV, a novel version of the Luminex assay for the multiplexed analysis of EV surface proteins. Optimized LuminEV reagents enable direct, specific, and sensitive measurements of EV markers in biofluids and in culture supernatants, bypassing EV isolation step. LuminEV assay for CD9, CD63, and CD81 was validated by comparing simplex and multiplex measurements, establishing linearity, spike‐in recovery, inter‐ and intra‐assay precision, and reproducibility between operators. LuminEV measurements of CD9, CD63, and CD81 in conditioned media from 15 cell lines revealed strong variations between cell types and showed high sensitivity, which enabled EV detection without prior concentration. Using tetraspanin levels as a readout, we noted suppression and induction of EV release from the cultured cells by GW6869 and monensin. Measurement of EV CD9, CD63, and CD81 in blood plasma from 70 disease‐free donors showed respective abundance of 72, 16, and 12%. CD63 displayed weak, albeit significant, negative correlation with age and was slightly lower in female samples. The assay was then used to detect cell type‐specific EV surface markers, including CD235a (erythrocytes), GAP43 (neurons), and CD68 (macrophages), and to detect differences in tetraspanin profiles between healthy and diseased donors. In summary, LuminEV offers robust and sensitive approach for multiplexed assessment of EV surface proteins, to facilitate the research into EV biology, biomarker, and therapeutic applications.
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spelling doaj-art-fbe12b47bc20462b80379b836781f1c12024-11-29T11:34:28ZengWileyJournal of Extracellular Vesicles2001-30782024-11-011311n/an/a10.1002/jev2.70007A novel multiplexed immunoassay for surface‐exposed proteins in plasma extracellular vesiclesEmma Tordoff0Jillian Allen1Katya Elgart2Ahmed Elsherbini3Vrinda Kalia4Haotian Wu5Erden Eren6Dimitrios Kapogiannis7Olesia Gololobova8Kenneth Witwer9Olga Volpert10Erez Eitan11NeuroDex, Inc. Natick Massachusetts USANeuroDex, Inc. Natick Massachusetts USANeuroDex, Inc. Natick Massachusetts USANeuroDex, Inc. Natick Massachusetts USADepartment of Environmental Health Sciences, Mailman School of Public Health Columbia University New York New York USADepartment of Environmental Health Sciences, Mailman School of Public Health Columbia University New York New York USALaboratory of Neurosciences, Intramural Research Program National Institute on Aging/National Institutes of Health (NIA/NIH) Baltimore Maryland USALaboratory of Neurosciences, Intramural Research Program National Institute on Aging/National Institutes of Health (NIA/NIH) Baltimore Maryland USADepartment of Molecular and Comparative Pathobiology Johns Hopkins University Baltimore Maryland USADepartment of Molecular and Comparative Pathobiology Johns Hopkins University Baltimore Maryland USANeuroDex, Inc. Natick Massachusetts USANeuroDex, Inc. Natick Massachusetts USAAbstract Small membranous extracellular vesicles (EV) incorporate proteins and nucleic acids from the parent cell. Proteins exposed on EV surface are dictated by cellular origin and biogenesis pathway. To better understand the EV origin and function, it is important to develop methods that reveal surface protein composition of heterogeneous EV populations in culture supernatants and in biofluids. Tetraspanins CD9, CD63, and CD81 are common and abundant EV markers. However, their relative enrichment (profile) on EVs of specific cellular origins is not fully elucidated. We introduce LuminEV, a novel version of the Luminex assay for the multiplexed analysis of EV surface proteins. Optimized LuminEV reagents enable direct, specific, and sensitive measurements of EV markers in biofluids and in culture supernatants, bypassing EV isolation step. LuminEV assay for CD9, CD63, and CD81 was validated by comparing simplex and multiplex measurements, establishing linearity, spike‐in recovery, inter‐ and intra‐assay precision, and reproducibility between operators. LuminEV measurements of CD9, CD63, and CD81 in conditioned media from 15 cell lines revealed strong variations between cell types and showed high sensitivity, which enabled EV detection without prior concentration. Using tetraspanin levels as a readout, we noted suppression and induction of EV release from the cultured cells by GW6869 and monensin. Measurement of EV CD9, CD63, and CD81 in blood plasma from 70 disease‐free donors showed respective abundance of 72, 16, and 12%. CD63 displayed weak, albeit significant, negative correlation with age and was slightly lower in female samples. The assay was then used to detect cell type‐specific EV surface markers, including CD235a (erythrocytes), GAP43 (neurons), and CD68 (macrophages), and to detect differences in tetraspanin profiles between healthy and diseased donors. In summary, LuminEV offers robust and sensitive approach for multiplexed assessment of EV surface proteins, to facilitate the research into EV biology, biomarker, and therapeutic applications.https://doi.org/10.1002/jev2.70007assay validationextracellular vesiclessurface marker analysistetraspanin composition
spellingShingle Emma Tordoff
Jillian Allen
Katya Elgart
Ahmed Elsherbini
Vrinda Kalia
Haotian Wu
Erden Eren
Dimitrios Kapogiannis
Olesia Gololobova
Kenneth Witwer
Olga Volpert
Erez Eitan
A novel multiplexed immunoassay for surface‐exposed proteins in plasma extracellular vesicles
Journal of Extracellular Vesicles
assay validation
extracellular vesicles
surface marker analysis
tetraspanin composition
title A novel multiplexed immunoassay for surface‐exposed proteins in plasma extracellular vesicles
title_full A novel multiplexed immunoassay for surface‐exposed proteins in plasma extracellular vesicles
title_fullStr A novel multiplexed immunoassay for surface‐exposed proteins in plasma extracellular vesicles
title_full_unstemmed A novel multiplexed immunoassay for surface‐exposed proteins in plasma extracellular vesicles
title_short A novel multiplexed immunoassay for surface‐exposed proteins in plasma extracellular vesicles
title_sort novel multiplexed immunoassay for surface exposed proteins in plasma extracellular vesicles
topic assay validation
extracellular vesicles
surface marker analysis
tetraspanin composition
url https://doi.org/10.1002/jev2.70007
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