Bulk serum extracellular vesicles from stressed mice show a distinct proteome and induce behavioral and molecular changes in naive mice
Chronic stress can trigger several pathologies including mood disorders for which no clear diagnostic molecular markers have been established yet. Attractive biomarker sources are extracellular vesicles (EVs). Evs are released by cells in health and disease and contain genetic material, proteins and...
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| creator | Monteleone, Melisa C Billi, Silvia C Abarzúa-Catalán, Lorena Henzi, Roberto Fernández, Eliana M Kaehne, Thilo Wyneken, Ursula Brocco, Marcela A |
| description | Chronic stress can trigger several pathologies including mood disorders for which no clear diagnostic molecular markers have been established yet. Attractive biomarker sources are extracellular vesicles (EVs). Evs are released by cells in health and disease and contain genetic material, proteins and lipids characteristic of the cell state. Here we show that Evs recovered from the blood of animals exposed to a repeated interrupted stress protocol (RIS) have a different protein profile compared to those obtained from control animals. Proteomic analysis indicated that proteins differentially present in bulk serum Evs from stressed animals were implicated in metabolic and inflammatory pathways and several of them were previously related to psychiatric disorders. Interestingly, these serum Evs carry brain-enriched proteins including the stress-responsive neuronal protein M6a. Then, we used an in-utero electroporation strategy to selectively overexpress M6a-GFP in brain neurons and found that M6a-GFP could also be detected in bulk serum Evs suggesting a neuronal origin. Finally, to determine if these Evs could have functional consequences, we administered Evs from control and RIS animals intranasally to naïve mice. Animals receiving stress EVs showed changes in behavior and brain M6a levels similar to those observed in physically stressed animals. Such changes could therefore be attributed, or at least in part, to EV protein transfer. Altogether these findings show that EVs may participate in stress signaling and propose proteins carried by EVs as a valuable source of biomarkers for stress-induced diseases. |
| doi_str_mv | 10.1371/journal.pone.0308976 |
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Attractive biomarker sources are extracellular vesicles (EVs). Evs are released by cells in health and disease and contain genetic material, proteins and lipids characteristic of the cell state. Here we show that Evs recovered from the blood of animals exposed to a repeated interrupted stress protocol (RIS) have a different protein profile compared to those obtained from control animals. Proteomic analysis indicated that proteins differentially present in bulk serum Evs from stressed animals were implicated in metabolic and inflammatory pathways and several of them were previously related to psychiatric disorders. Interestingly, these serum Evs carry brain-enriched proteins including the stress-responsive neuronal protein M6a. Then, we used an in-utero electroporation strategy to selectively overexpress M6a-GFP in brain neurons and found that M6a-GFP could also be detected in bulk serum Evs suggesting a neuronal origin. Finally, to determine if these Evs could have functional consequences, we administered Evs from control and RIS animals intranasally to naïve mice. Animals receiving stress EVs showed changes in behavior and brain M6a levels similar to those observed in physically stressed animals. Such changes could therefore be attributed, or at least in part, to EV protein transfer. Altogether these findings show that EVs may participate in stress signaling and propose proteins carried by EVs as a valuable source of biomarkers for stress-induced diseases.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0308976</identifier><identifier>PMID: 39146369</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Antibodies ; Behavior, Animal ; Biology and Life Sciences ; Biomarkers ; Brain ; Brain - metabolism ; Disease ; Disorders ; Electroporation ; Emotional disorders ; Ethylenediaminetetraacetic acid ; Experiments ; Extracellular vesicles ; Extracellular Vesicles - metabolism ; Glycoproteins ; Laboratory animals ; Lipid metabolism ; Lipids ; Male ; Medicine and Health Sciences ; Membranes ; Mental disorders ; Mental illness ; Methyltransferases ; Mice ; Mice, Inbred C57BL ; Molecular weight ; Mood disorders ; Neurons ; Neurons - metabolism ; Protein sources ; Proteins ; Proteome - metabolism ; Proteomes ; Proteomics ; Proteomics - methods ; Research and Analysis Methods ; Social Sciences ; Standard deviation ; Stress ; Stress (Psychology) ; Stress, Psychological - blood ; Stress, Psychological - metabolism ; Vesicles</subject><ispartof>PloS one, 2024-08, Vol.19 (8), p.e0308976</ispartof><rights>Copyright: © 2024 Monteleone et al. 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Finally, to determine if these Evs could have functional consequences, we administered Evs from control and RIS animals intranasally to naïve mice. Animals receiving stress EVs showed changes in behavior and brain M6a levels similar to those observed in physically stressed animals. Such changes could therefore be attributed, or at least in part, to EV protein transfer. Altogether these findings show that EVs may participate in stress signaling and propose proteins carried by EVs as a valuable source of biomarkers for stress-induced diseases.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>39146369</pmid><doi>10.1371/journal.pone.0308976</doi><tpages>e0308976</tpages><orcidid>https://orcid.org/0000-0002-6282-4019</orcidid><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; Public Library of Science (PLoS) Journals Open Access; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Animals Antibodies Behavior, Animal Biology and Life Sciences Biomarkers Brain Brain - metabolism Disease Disorders Electroporation Emotional disorders Ethylenediaminetetraacetic acid Experiments Extracellular vesicles Extracellular Vesicles - metabolism Glycoproteins Laboratory animals Lipid metabolism Lipids Male Medicine and Health Sciences Membranes Mental disorders Mental illness Methyltransferases Mice Mice, Inbred C57BL Molecular weight Mood disorders Neurons Neurons - metabolism Protein sources Proteins Proteome - metabolism Proteomes Proteomics Proteomics - methods Research and Analysis Methods Social Sciences Standard deviation Stress Stress (Psychology) Stress, Psychological - blood Stress, Psychological - metabolism Vesicles |
| title | Bulk serum extracellular vesicles from stressed mice show a distinct proteome and induce behavioral and molecular changes in naive mice |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-07T07%3A42%3A07IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Bulk%20serum%20extracellular%20vesicles%20from%20stressed%20mice%20show%20a%20distinct%20proteome%20and%20induce%20behavioral%20and%20molecular%20changes%20in%20naive%20mice&rft.jtitle=PloS%20one&rft.au=Monteleone,%20Melisa%20C&rft.date=2024-08-15&rft.volume=19&rft.issue=8&rft.spage=e0308976&rft.pages=e0308976-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0308976&rft_dat=%3Cgale_plos_%3EA804938670%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=3093519987&rft_id=info:pmid/39146369&rft_galeid=A804938670&rft_doaj_id=oai_doaj_org_article_f08e958881164548b68ccdcb9bfb87d8&rfr_iscdi=true |