Single‐extracellular vesicle (EV) analyses validate the use of L1 Cell Adhesion Molecule (L1CAM) as a reliable biomarker of neuron‐derived EVs

Isolation of neuron‐derived extracellular vesicles (NDEVs) with L1 Cell Adhesion Molecule (L1CAM)‐specific antibodies has been widely used to identify blood biomarkers of CNS disorders. However, full methodological validation requires demonstration of L1CAM in individual NDEVs and lower levels or ab...

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Published in:	Journal of extracellular vesicles Vol. 13; no. 6; pp. e12459 - n/a
Main Authors:	Nogueras‐Ortiz, Carlos J, Eren, Erden, Yao, Pamela, Calzada, Elizabeth, Dunn, Christopher, Volpert, Olga, Delgado‐Peraza, Francheska, Mustapic, Maja, Lyashkov, Alexey, Rubio, F Javier, Vreones, Michael, Cheng, Lesley, You, Yang, Hill, Andrew F, Ikezu, Tsuneya, Eitan, Erez, Goetzl, Edward J, Kapogiannis, Dimitrios
Format:	Journal Article
Language:	English
Published:	United States John Wiley & Sons, Inc 01.06.2024 John Wiley and Sons Inc Wiley
Subjects:	Alzheimer's disease Biomarkers Biomarkers - blood Biomarkers - metabolism blood biomarkers Brain diseases Cell adhesion & migration Cell adhesion molecules Cerebrospinal fluid Epitopes Extracellular vesicles Extracellular Vesicles - metabolism Humans L1CAM Ligands Microscopy Molecules Neural Cell Adhesion Molecule L1 - metabolism Neurons Neurons - metabolism neuron‐derived extracellular vesicles Pathology Plasma Proteins Tubulin Tubulin - metabolism Vesicle-Associated Membrane Protein 2 - metabolism blood biomarkers extracellular vesicles neuron‐derived extracellular vesicles L1CAM Alzheimer's disease
ISSN:	2001-3078, 2001-3078
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Abstract	Isolation of neuron‐derived extracellular vesicles (NDEVs) with L1 Cell Adhesion Molecule (L1CAM)‐specific antibodies has been widely used to identify blood biomarkers of CNS disorders. However, full methodological validation requires demonstration of L1CAM in individual NDEVs and lower levels or absence of L1CAM in individual EVs from other cells. Here, we used multiple single‐EV techniques to establish the neuronal origin and determine the abundance of L1CAM‐positive EVs in human blood. L1CAM epitopes of the ectodomain are shown to be co‐expressed on single‐EVs with the neuronal proteins β‐III‐tubulin, GAP43, and VAMP2, the levels of which increase in parallel with the enrichment of L1CAM‐positive EVs. Levels of L1CAM‐positive EVs carrying the neuronal proteins VAMP2 and β‐III‐tubulin range from 30% to 63%, in contrast to 0.8%–3.9% of L1CAM‐negative EVs. Plasma fluid‐phase L1CAM does not bind to single‐EVs. Our findings support the use of L1CAM as a target for isolating plasma NDEVs and leveraging their cargo to identify biomarkers reflecting neuronal function. Previous research suggest that extracellular vesicles (EVs) secreted by brain neurons carry L1CAM and circulate in peripheral blood, coexisting with L1CAM‐positive EVs from peripheral cellular sources and free L1CAM peptides (top left). These other versions of L1CAM in blood challenge the approach of targeting L1CAM for the immunoaffinity isolation of neuronal EVs (top right), a methodology widely adopted to derive blood biomarkers for brain disorders. To further understand L1CAM‐positive EVs, we sought to establish their neuronal origin and determine the abundance of L1CAM‐positive neuronal EVs in human blood using single‐, intact‐EV techniques including flow cytometry, confocal microscopy and a novel Simoa® assay specific for L1CAM in EVs carrying tetraspanins CD9, CD63 and CD81 (bottom left). Results demonstrate that L1CAM ectodomain epitopes are co‐expressed on blood‐derived EVs with the neuronal proteins β‐III‐tubulin, GAP43, and VAMP2, the levels of which increase in parallel with the enrichment of L1CAM‐positive EVs via L1CAM immunocapture (bottom right). Results further validate the use of L1CAM as a target for the immunoaffinity isolation of neuron‐derived EVs from blood.
AbstractList	Isolation of neuron‐derived extracellular vesicles (NDEVs) with L1 Cell Adhesion Molecule (L1CAM)‐specific antibodies has been widely used to identify blood biomarkers of CNS disorders. However, full methodological validation requires demonstration of L1CAM in individual NDEVs and lower levels or absence of L1CAM in individual EVs from other cells. Here, we used multiple single‐EV techniques to establish the neuronal origin and determine the abundance of L1CAM‐positive EVs in human blood. L1CAM epitopes of the ectodomain are shown to be co‐expressed on single‐EVs with the neuronal proteins β‐III‐tubulin, GAP43, and VAMP2, the levels of which increase in parallel with the enrichment of L1CAM‐positive EVs. Levels of L1CAM‐positive EVs carrying the neuronal proteins VAMP2 and β‐III‐tubulin range from 30% to 63%, in contrast to 0.8%–3.9% of L1CAM‐negative EVs. Plasma fluid‐phase L1CAM does not bind to single‐EVs. Our findings support the use of L1CAM as a target for isolating plasma NDEVs and leveraging their cargo to identify biomarkers reflecting neuronal function. Abstract Isolation of neuron‐derived extracellular vesicles (NDEVs) with L1 Cell Adhesion Molecule (L1CAM)‐specific antibodies has been widely used to identify blood biomarkers of CNS disorders. However, full methodological validation requires demonstration of L1CAM in individual NDEVs and lower levels or absence of L1CAM in individual EVs from other cells. Here, we used multiple single‐EV techniques to establish the neuronal origin and determine the abundance of L1CAM‐positive EVs in human blood. L1CAM epitopes of the ectodomain are shown to be co‐expressed on single‐EVs with the neuronal proteins β‐III‐tubulin, GAP43, and VAMP2, the levels of which increase in parallel with the enrichment of L1CAM‐positive EVs. Levels of L1CAM‐positive EVs carrying the neuronal proteins VAMP2 and β‐III‐tubulin range from 30% to 63%, in contrast to 0.8%–3.9% of L1CAM‐negative EVs. Plasma fluid‐phase L1CAM does not bind to single‐EVs. Our findings support the use of L1CAM as a target for isolating plasma NDEVs and leveraging their cargo to identify biomarkers reflecting neuronal function. Isolation of neuron‐derived extracellular vesicles (NDEVs) with L1 Cell Adhesion Molecule (L1CAM)‐specific antibodies has been widely used to identify blood biomarkers of CNS disorders. However, full methodological validation requires demonstration of L1CAM in individual NDEVs and lower levels or absence of L1CAM in individual EVs from other cells. Here, we used multiple single‐EV techniques to establish the neuronal origin and determine the abundance of L1CAM‐positive EVs in human blood. L1CAM epitopes of the ectodomain are shown to be co‐expressed on single‐EVs with the neuronal proteins β‐III‐tubulin, GAP43, and VAMP2, the levels of which increase in parallel with the enrichment of L1CAM‐positive EVs. Levels of L1CAM‐positive EVs carrying the neuronal proteins VAMP2 and β‐III‐tubulin range from 30% to 63%, in contrast to 0.8%–3.9% of L1CAM‐negative EVs. Plasma fluid‐phase L1CAM does not bind to single‐EVs. Our findings support the use of L1CAM as a target for isolating plasma NDEVs and leveraging their cargo to identify biomarkers reflecting neuronal function. Previous research suggest that extracellular vesicles (EVs) secreted by brain neurons carry L1CAM and circulate in peripheral blood, coexisting with L1CAM‐positive EVs from peripheral cellular sources and free L1CAM peptides (top left). These other versions of L1CAM in blood challenge the approach of targeting L1CAM for the immunoaffinity isolation of neuronal EVs (top right), a methodology widely adopted to derive blood biomarkers for brain disorders. To further understand L1CAM‐positive EVs, we sought to establish their neuronal origin and determine the abundance of L1CAM‐positive neuronal EVs in human blood using single‐, intact‐EV techniques including flow cytometry, confocal microscopy and a novel Simoa® assay specific for L1CAM in EVs carrying tetraspanins CD9, CD63 and CD81 (bottom left). Results demonstrate that L1CAM ectodomain epitopes are co‐expressed on blood‐derived EVs with the neuronal proteins β‐III‐tubulin, GAP43, and VAMP2, the levels of which increase in parallel with the enrichment of L1CAM‐positive EVs via L1CAM immunocapture (bottom right). Results further validate the use of L1CAM as a target for the immunoaffinity isolation of neuron‐derived EVs from blood. Isolation of neuron-derived extracellular vesicles (NDEVs) with L1 Cell Adhesion Molecule (L1CAM)-specific antibodies has been widely used to identify blood biomarkers of CNS disorders. However, full methodological validation requires demonstration of L1CAM in individual NDEVs and lower levels or absence of L1CAM in individual EVs from other cells. Here, we used multiple single-EV techniques to establish the neuronal origin and determine the abundance of L1CAM-positive EVs in human blood. L1CAM epitopes of the ectodomain are shown to be co-expressed on single-EVs with the neuronal proteins β-III-tubulin, GAP43, and VAMP2, the levels of which increase in parallel with the enrichment of L1CAM-positive EVs. Levels of L1CAM-positive EVs carrying the neuronal proteins VAMP2 and β-III-tubulin range from 30% to 63%, in contrast to 0.8%-3.9% of L1CAM-negative EVs. Plasma fluid-phase L1CAM does not bind to single-EVs. Our findings support the use of L1CAM as a target for isolating plasma NDEVs and leveraging their cargo to identify biomarkers reflecting neuronal function.Isolation of neuron-derived extracellular vesicles (NDEVs) with L1 Cell Adhesion Molecule (L1CAM)-specific antibodies has been widely used to identify blood biomarkers of CNS disorders. However, full methodological validation requires demonstration of L1CAM in individual NDEVs and lower levels or absence of L1CAM in individual EVs from other cells. Here, we used multiple single-EV techniques to establish the neuronal origin and determine the abundance of L1CAM-positive EVs in human blood. L1CAM epitopes of the ectodomain are shown to be co-expressed on single-EVs with the neuronal proteins β-III-tubulin, GAP43, and VAMP2, the levels of which increase in parallel with the enrichment of L1CAM-positive EVs. Levels of L1CAM-positive EVs carrying the neuronal proteins VAMP2 and β-III-tubulin range from 30% to 63%, in contrast to 0.8%-3.9% of L1CAM-negative EVs. Plasma fluid-phase L1CAM does not bind to single-EVs. Our findings support the use of L1CAM as a target for isolating plasma NDEVs and leveraging their cargo to identify biomarkers reflecting neuronal function. Isolation of neuron‐derived extracellular vesicles (NDEVs) with L1 Cell Adhesion Molecule (L1CAM)‐specific antibodies has been widely used to identify blood biomarkers of CNS disorders. However, full methodological validation requires demonstration of L1CAM in individual NDEVs and lower levels or absence of L1CAM in individual EVs from other cells. Here, we used multiple single‐EV techniques to establish the neuronal origin and determine the abundance of L1CAM‐positive EVs in human blood. L1CAM epitopes of the ectodomain are shown to be co‐expressed on single‐EVs with the neuronal proteins β‐III‐tubulin, GAP43, and VAMP2, the levels of which increase in parallel with the enrichment of L1CAM‐positive EVs. Levels of L1CAM‐positive EVs carrying the neuronal proteins VAMP2 and β‐III‐tubulin range from 30% to 63%, in contrast to 0.8%–3.9% of L1CAM‐negative EVs. Plasma fluid‐phase L1CAM does not bind to single‐EVs. Our findings support the use of L1CAM as a target for isolating plasma NDEVs and leveraging their cargo to identify biomarkers reflecting neuronal function. Previous research suggest that extracellular vesicles (EVs) secreted by brain neurons carry L1CAM and circulate in peripheral blood, coexisting with L1CAM‐positive EVs from peripheral cellular sources and free L1CAM peptides (top left). These other versions of L1CAM in blood challenge the approach of targeting L1CAM for the immunoaffinity isolation of neuronal EVs (top right), a methodology widely adopted to derive blood biomarkers for brain disorders. To further understand L1CAM‐positive EVs, we sought to establish their neuronal origin and determine the abundance of L1CAM‐positive neuronal EVs in human blood using single‐, intact‐EV techniques including flow cytometry, confocal microscopy and a novel Simoa® assay specific for L1CAM in EVs carrying tetraspanins CD9, CD63 and CD81 (bottom left). Results demonstrate that L1CAM ectodomain epitopes are co‐expressed on blood‐derived EVs with the neuronal proteins β‐III‐tubulin, GAP43, and VAMP2, the levels of which increase in parallel with the enrichment of L1CAM‐positive EVs via L1CAM immunocapture (bottom right). Results further validate the use of L1CAM as a target for the immunoaffinity isolation of neuron‐derived EVs from blood.
Author	Kapogiannis, Dimitrios Rubio, F Javier Hill, Andrew F Calzada, Elizabeth Goetzl, Edward J Nogueras‐Ortiz, Carlos J Delgado‐Peraza, Francheska Volpert, Olga Cheng, Lesley Eitan, Erez Vreones, Michael Yao, Pamela Mustapic, Maja Lyashkov, Alexey You, Yang Eren, Erden Dunn, Christopher Ikezu, Tsuneya
AuthorAffiliation	3 NeuroDex Inc. Natick Maryland USA 7 Department of Pharmacology and Experimental Therapeutics Boston University School of Medicine Boston Massachusetts USA 1 Laboratory of Clinical Investigation, Intramural Research Program National Institute on Aging, National Institutes of Health (NIA/NIH) Baltimore Maryland USA 4 Neuronal Ensembles in Addiction Section, Behavioral Neuroscience Research Branch Intramural Research Program/National Institute on Drug Abuse/National Institutes of Health Baltimore Maryland USA 8 Institute for Health and Sport Victoria University Melbourne Victoria Australia 10 San Francisco Campus for Jewish Living San Francisco California USA 11 Department of Neurology Johns Hopkins School of Medicine Baltimore Maryland USA 2 Flow Cytometry Unit, Intramural Research Program National Institute on Aging, National Institutes of Health (NIA/NIH) Baltimore Maryland USA 5 La Trobe Institute for Molecular Science La Trobe University Bundoora Victoria Australia 9 Department of Medicine
AuthorAffiliation_xml	– name: 6 Department of Neuroscience Mayo Clinic Jacksonville Florida USA – name: 10 San Francisco Campus for Jewish Living San Francisco California USA – name: 1 Laboratory of Clinical Investigation, Intramural Research Program National Institute on Aging, National Institutes of Health (NIA/NIH) Baltimore Maryland USA – name: 11 Department of Neurology Johns Hopkins School of Medicine Baltimore Maryland USA – name: 3 NeuroDex Inc. Natick Maryland USA – name: 4 Neuronal Ensembles in Addiction Section, Behavioral Neuroscience Research Branch Intramural Research Program/National Institute on Drug Abuse/National Institutes of Health Baltimore Maryland USA – name: 9 Department of Medicine University of California San Francisco California USA – name: 5 La Trobe Institute for Molecular Science La Trobe University Bundoora Victoria Australia – name: 2 Flow Cytometry Unit, Intramural Research Program National Institute on Aging, National Institutes of Health (NIA/NIH) Baltimore Maryland USA – name: 7 Department of Pharmacology and Experimental Therapeutics Boston University School of Medicine Boston Massachusetts USA – name: 8 Institute for Health and Sport Victoria University Melbourne Victoria Australia
Author_xml	– sequence: 1 givenname: Carlos J orcidid: 0000-0003-2503-965X surname: Nogueras‐Ortiz fullname: Nogueras‐Ortiz, Carlos J email: carlos.nogueras-ortiz@nih.gov organization: National Institute on Aging, National Institutes of Health (NIA/NIH) – sequence: 2 givenname: Erden orcidid: 0000-0002-5190-9500 surname: Eren fullname: Eren, Erden organization: National Institute on Aging, National Institutes of Health (NIA/NIH) – sequence: 3 givenname: Pamela surname: Yao fullname: Yao, Pamela organization: National Institute on Aging, National Institutes of Health (NIA/NIH) – sequence: 4 givenname: Elizabeth surname: Calzada fullname: Calzada, Elizabeth organization: National Institute on Aging, National Institutes of Health (NIA/NIH) – sequence: 5 givenname: Christopher surname: Dunn fullname: Dunn, Christopher organization: National Institute on Aging, National Institutes of Health (NIA/NIH) – sequence: 6 givenname: Olga orcidid: 0000-0003-1381-5543 surname: Volpert fullname: Volpert, Olga organization: NeuroDex Inc – sequence: 7 givenname: Francheska surname: Delgado‐Peraza fullname: Delgado‐Peraza, Francheska organization: National Institute on Aging, National Institutes of Health (NIA/NIH) – sequence: 8 givenname: Maja surname: Mustapic fullname: Mustapic, Maja organization: National Institute on Aging, National Institutes of Health (NIA/NIH) – sequence: 9 givenname: Alexey surname: Lyashkov fullname: Lyashkov, Alexey organization: National Institute on Aging, National Institutes of Health (NIA/NIH) – sequence: 10 givenname: F Javier surname: Rubio fullname: Rubio, F Javier organization: Intramural Research Program/National Institute on Drug Abuse/National Institutes of Health – sequence: 11 givenname: Michael orcidid: 0009-0003-1719-8156 surname: Vreones fullname: Vreones, Michael organization: National Institute on Aging, National Institutes of Health (NIA/NIH) – sequence: 12 givenname: Lesley surname: Cheng fullname: Cheng, Lesley organization: La Trobe University – sequence: 13 givenname: Yang surname: You fullname: You, Yang organization: Boston University School of Medicine – sequence: 14 givenname: Andrew F orcidid: 0000-0001-5581-2354 surname: Hill fullname: Hill, Andrew F organization: Victoria University – sequence: 15 givenname: Tsuneya orcidid: 0000-0002-3979-8596 surname: Ikezu fullname: Ikezu, Tsuneya organization: Boston University School of Medicine – sequence: 16 givenname: Erez surname: Eitan fullname: Eitan, Erez organization: NeuroDex Inc – sequence: 17 givenname: Edward J surname: Goetzl fullname: Goetzl, Edward J organization: San Francisco Campus for Jewish Living – sequence: 18 givenname: Dimitrios surname: Kapogiannis fullname: Kapogiannis, Dimitrios email: kapogiannisd@mail.nih.gov organization: Johns Hopkins School of Medicine
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/38868956$$D View this record in MEDLINE/PubMed
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Copyright	2024 Neurodex Inc. and The Author(s). published by Wiley Periodicals LLC on behalf of International Society for Extracellular Vesicles. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA. 2024 The Author(s). Journal of Extracellular Vesicles published by Wiley Periodicals, LLC on behalf of the International Society for Extracellular Vesicles. 2024. This work is published under http://creativecommons.org/licenses/by-nc/4.0/ (the "License"). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2024 The Author(s). published by Wiley Periodicals, LLC on behalf of the International Society for Extracellular Vesicles.
Copyright_xml	– notice: 2024 Neurodex Inc. and The Author(s). published by Wiley Periodicals LLC on behalf of International Society for Extracellular Vesicles. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA. – notice: 2024 The Author(s). Journal of Extracellular Vesicles published by Wiley Periodicals, LLC on behalf of the International Society for Extracellular Vesicles. – notice: 2024. This work is published under http://creativecommons.org/licenses/by-nc/4.0/ (the "License"). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: 2024 The Author(s). published by Wiley Periodicals, LLC on behalf of the International Society for Extracellular Vesicles.
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Keywords	blood biomarkers extracellular vesicles neuron‐derived extracellular vesicles L1CAM Alzheimer's disease
Language	English
License	Attribution-NonCommercial http://creativecommons.org/licenses/by-nc/4.0 2024 The Author(s). Journal of Extracellular Vesicles published by Wiley Periodicals, LLC on behalf of the International Society for Extracellular Vesicles. This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
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Snippet	Isolation of neuron‐derived extracellular vesicles (NDEVs) with L1 Cell Adhesion Molecule (L1CAM)‐specific antibodies has been widely used to identify blood... Isolation of neuron-derived extracellular vesicles (NDEVs) with L1 Cell Adhesion Molecule (L1CAM)-specific antibodies has been widely used to identify blood... Abstract Isolation of neuron‐derived extracellular vesicles (NDEVs) with L1 Cell Adhesion Molecule (L1CAM)‐specific antibodies has been widely used to identify...
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StartPage	e12459
SubjectTerms	Alzheimer's disease Biomarkers Biomarkers - blood Biomarkers - metabolism blood biomarkers Brain diseases Cell adhesion & migration Cell adhesion molecules Cerebrospinal fluid Epitopes Extracellular vesicles Extracellular Vesicles - metabolism Humans L1CAM Ligands Microscopy Molecules Neural Cell Adhesion Molecule L1 - metabolism Neurons Neurons - metabolism neuron‐derived extracellular vesicles Pathology Plasma Proteins Tubulin Tubulin - metabolism Vesicle-Associated Membrane Protein 2 - metabolism
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Title	Single‐extracellular vesicle (EV) analyses validate the use of L1 Cell Adhesion Molecule (L1CAM) as a reliable biomarker of neuron‐derived EVs
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