Platelet extracellular vesicles induce a pro-inflammatory smooth muscle cell phenotype
Extracellular vesicles (EVs) are mediators of cell communication during health and disease, and abundantly released by platelets upon activation or during ageing. Platelet EVs exert modulatory effects on immune and vascular cells. Platelet EVs may modulate the function of vascular smooth muscle cell...
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| Veröffentlicht in: | Journal of extracellular vesicles 2017-12, Vol.6 (1), p.1322454-n/a |
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| creator | Vajen, Tanja Benedikter, Birke J. Heinzmann, Alexandra C. A. Vasina, Elena M. Henskens, Yvonne Parsons, Martin Maguire, Patricia B. Stassen, Frank R. Heemskerk, Johan W. M. Schurgers, Leon J. Koenen, Rory R. |
| description | Extracellular vesicles (EVs) are mediators of cell communication during health and disease, and abundantly released by platelets upon activation or during ageing. Platelet EVs exert modulatory effects on immune and vascular cells. Platelet EVs may modulate the function of vascular smooth muscle cells (SMC). Platelet EVs were isolated from platelet-rich plasma and incubated with SMC in order to assess binding, proliferation, migration and pro-inflammatory phenotype of the cells. Platelet EVs firmly bound to resting SMC through the platelet integrin α
IIb
β
3
, while binding also occurred in a CX3CL1-CX3CR1-dependent manner after cytokine stimulation. Platelet EVs increased SMC migration comparable to platelet derived growth factor or platelet factor 4 and induced SMC proliferation, which relied on CD40- and P-selectin interactions. Flow-resistant monocyte adhesion to platelet EV-treated SMC was increased compared with resting SMC. Again, this adhesion depended on integrin α
IIb
β
3
and P-selectin, and to a lesser extent on CD40 and CX3CR1. Treatment of SMC with platelet EVs induced interleukin 6 secretion. Finally, platelet EVs induced a synthetic SMC morphology and decreased calponin expression. Collectively, these data indicate that platelet EVs exert a strong immunomodulatory activity on SMC. In particular, platelet EVs induce a switch towards a pro-inflammatory phenotype, stimulating vascular remodelling. |
| doi_str_mv | 10.1080/20013078.2017.1322454 |
| format | Article |
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IIb
β
3
, while binding also occurred in a CX3CL1-CX3CR1-dependent manner after cytokine stimulation. Platelet EVs increased SMC migration comparable to platelet derived growth factor or platelet factor 4 and induced SMC proliferation, which relied on CD40- and P-selectin interactions. Flow-resistant monocyte adhesion to platelet EV-treated SMC was increased compared with resting SMC. Again, this adhesion depended on integrin α
IIb
β
3
and P-selectin, and to a lesser extent on CD40 and CX3CR1. Treatment of SMC with platelet EVs induced interleukin 6 secretion. Finally, platelet EVs induced a synthetic SMC morphology and decreased calponin expression. Collectively, these data indicate that platelet EVs exert a strong immunomodulatory activity on SMC. In particular, platelet EVs induce a switch towards a pro-inflammatory phenotype, stimulating vascular remodelling.</description><identifier>ISSN: 2001-3078</identifier><identifier>EISSN: 2001-3078</identifier><identifier>DOI: 10.1080/20013078.2017.1322454</identifier><identifier>PMID: 28717419</identifier><language>eng</language><publisher>Sweden: Taylor & Francis</publisher><subject>Aging ; Angiogenesis ; Atherosclerosis ; Blood platelets ; Calponin ; CD40 antigen ; Cell activation ; Cell growth ; Cell interactions ; Cell proliferation ; Chemokines ; Coronary vessels ; CR1 ; CX3CR1 ; CX3CR1 protein ; cytokine ; Cytokines ; Endothelium ; Extracellular vesicles ; Flow cytometry ; Gene expression ; Genotype & phenotype ; Glioma ; Growth factors ; Immunomodulation ; Inflammation ; Interleukin 6 ; Leukocyte migration ; Leukocytes ; Ligands ; Monocytes ; P-selectin ; pathway analysis ; Penicillin ; Phenotypes ; Plasma ; Platelet factor 4 ; Platelet-derived growth factor ; Platelets ; proteomics ; Recruitment ; Rodents ; Smooth muscle ; synthetic phenotype ; vascular remodeling ; Veins & arteries</subject><ispartof>Journal of extracellular vesicles, 2017-12, Vol.6 (1), p.1322454-n/a</ispartof><rights>2017 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. 2017</rights><rights>2017 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.</rights><rights>Copyright Taylor & Francis Ltd. 2017</rights><rights>Copyright John Wiley & Sons, Inc. 2017</rights><rights>2017 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. 2017 The Author(s)</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c6452-74e101119c7026da98d3e9926b00c5193d85ca42210a71cb2bd81e5125c1dc983</citedby><cites>FETCH-LOGICAL-c6452-74e101119c7026da98d3e9926b00c5193d85ca42210a71cb2bd81e5125c1dc983</cites><orcidid>0000-0002-9955-9730 ; 0000-0001-8450-9506 ; 0000-0002-1103-2484</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5505004/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5505004/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,1411,2096,11541,27479,27901,27902,45550,45551,46027,46451,53766,53768,59116,59117</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28717419$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Vajen, Tanja</creatorcontrib><creatorcontrib>Benedikter, Birke J.</creatorcontrib><creatorcontrib>Heinzmann, Alexandra C. A.</creatorcontrib><creatorcontrib>Vasina, Elena M.</creatorcontrib><creatorcontrib>Henskens, Yvonne</creatorcontrib><creatorcontrib>Parsons, Martin</creatorcontrib><creatorcontrib>Maguire, Patricia B.</creatorcontrib><creatorcontrib>Stassen, Frank R.</creatorcontrib><creatorcontrib>Heemskerk, Johan W. M.</creatorcontrib><creatorcontrib>Schurgers, Leon J.</creatorcontrib><creatorcontrib>Koenen, Rory R.</creatorcontrib><title>Platelet extracellular vesicles induce a pro-inflammatory smooth muscle cell phenotype</title><title>Journal of extracellular vesicles</title><addtitle>J Extracell Vesicles</addtitle><description>Extracellular vesicles (EVs) are mediators of cell communication during health and disease, and abundantly released by platelets upon activation or during ageing. Platelet EVs exert modulatory effects on immune and vascular cells. Platelet EVs may modulate the function of vascular smooth muscle cells (SMC). Platelet EVs were isolated from platelet-rich plasma and incubated with SMC in order to assess binding, proliferation, migration and pro-inflammatory phenotype of the cells. Platelet EVs firmly bound to resting SMC through the platelet integrin α
IIb
β
3
, while binding also occurred in a CX3CL1-CX3CR1-dependent manner after cytokine stimulation. Platelet EVs increased SMC migration comparable to platelet derived growth factor or platelet factor 4 and induced SMC proliferation, which relied on CD40- and P-selectin interactions. Flow-resistant monocyte adhesion to platelet EV-treated SMC was increased compared with resting SMC. Again, this adhesion depended on integrin α
IIb
β
3
and P-selectin, and to a lesser extent on CD40 and CX3CR1. Treatment of SMC with platelet EVs induced interleukin 6 secretion. Finally, platelet EVs induced a synthetic SMC morphology and decreased calponin expression. Collectively, these data indicate that platelet EVs exert a strong immunomodulatory activity on SMC. In particular, platelet EVs induce a switch towards a pro-inflammatory phenotype, stimulating vascular remodelling.</description><subject>Aging</subject><subject>Angiogenesis</subject><subject>Atherosclerosis</subject><subject>Blood platelets</subject><subject>Calponin</subject><subject>CD40 antigen</subject><subject>Cell activation</subject><subject>Cell growth</subject><subject>Cell interactions</subject><subject>Cell proliferation</subject><subject>Chemokines</subject><subject>Coronary vessels</subject><subject>CR1</subject><subject>CX3CR1</subject><subject>CX3CR1 protein</subject><subject>cytokine</subject><subject>Cytokines</subject><subject>Endothelium</subject><subject>Extracellular vesicles</subject><subject>Flow cytometry</subject><subject>Gene expression</subject><subject>Genotype & phenotype</subject><subject>Glioma</subject><subject>Growth factors</subject><subject>Immunomodulation</subject><subject>Inflammation</subject><subject>Interleukin 6</subject><subject>Leukocyte migration</subject><subject>Leukocytes</subject><subject>Ligands</subject><subject>Monocytes</subject><subject>P-selectin</subject><subject>pathway analysis</subject><subject>Penicillin</subject><subject>Phenotypes</subject><subject>Plasma</subject><subject>Platelet factor 4</subject><subject>Platelet-derived growth factor</subject><subject>Platelets</subject><subject>proteomics</subject><subject>Recruitment</subject><subject>Rodents</subject><subject>Smooth muscle</subject><subject>synthetic phenotype</subject><subject>vascular remodeling</subject><subject>Veins & arteries</subject><issn>2001-3078</issn><issn>2001-3078</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>0YH</sourceid><sourceid>24P</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNkkFv1DAQhSMEolXpTwBF4sJll5mxvbEvCKhaKKoEB-jVchxvNysnXuykZf89DrstLYeKudjyvPnkeXpF8RJhjiDhLQEgg0rOCbCaIyPigj8pDqf32dR4eu9-UByntIZciqOQ6nlxQLLCiqM6LC6_eTM474bS_Rqisc770ZtYXrvUWu9S2fbNaF1pyk0Ms7ZfetN1ZghxW6YuhGFVdmPKwnKaLDcr14dhu3EvimdL45M73p9HxY-z0-8nn2cXXz-dn3y4mNkFFzSruENARGUroEVjlGyYU4oWNYAVqFgjhTWcCMFUaGuqG4lOIAmLjVWSHRXnO24TzFpvYtuZuNXBtPrPQ4hX2sRh2kTbWgqSS5VhnEuojTVIlcvc2pB1JrPe7Vibse5cY12fDfEPoA87fbvSV-FaCwECgGfAmz0ghp-jS4Pu2jT5YnoXxqRRESKrECfp63-k6zDGPlulGShiPBd7TEUgCVjFFGSV2KlsDClFt7z7MoKe4qJv46KnuOh9XPLcq_v73k3dhuOvITetd9v_o-ovp5f08SzbQZQB73eAnJsQO3MTom_0YLY-xGU0vW3zuo9_8jcANN7e</recordid><startdate>201712</startdate><enddate>201712</enddate><creator>Vajen, Tanja</creator><creator>Benedikter, Birke J.</creator><creator>Heinzmann, Alexandra C. A.</creator><creator>Vasina, Elena M.</creator><creator>Henskens, Yvonne</creator><creator>Parsons, Martin</creator><creator>Maguire, Patricia B.</creator><creator>Stassen, Frank R.</creator><creator>Heemskerk, Johan W. M.</creator><creator>Schurgers, Leon J.</creator><creator>Koenen, Rory R.</creator><general>Taylor & Francis</general><general>John Wiley & Sons, Inc</general><general>Wiley</general><scope>0YH</scope><scope>24P</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QP</scope><scope>8FE</scope><scope>8FH</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M7P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-9955-9730</orcidid><orcidid>https://orcid.org/0000-0001-8450-9506</orcidid><orcidid>https://orcid.org/0000-0002-1103-2484</orcidid></search><sort><creationdate>201712</creationdate><title>Platelet extracellular vesicles induce a pro-inflammatory smooth muscle cell phenotype</title><author>Vajen, Tanja ; Benedikter, Birke J. ; Heinzmann, Alexandra C. A. ; Vasina, Elena M. ; Henskens, Yvonne ; Parsons, Martin ; Maguire, Patricia B. ; Stassen, Frank R. ; Heemskerk, Johan W. M. ; Schurgers, Leon J. ; Koenen, Rory R.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c6452-74e101119c7026da98d3e9926b00c5193d85ca42210a71cb2bd81e5125c1dc983</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Aging</topic><topic>Angiogenesis</topic><topic>Atherosclerosis</topic><topic>Blood platelets</topic><topic>Calponin</topic><topic>CD40 antigen</topic><topic>Cell activation</topic><topic>Cell growth</topic><topic>Cell interactions</topic><topic>Cell proliferation</topic><topic>Chemokines</topic><topic>Coronary vessels</topic><topic>CR1</topic><topic>CX3CR1</topic><topic>CX3CR1 protein</topic><topic>cytokine</topic><topic>Cytokines</topic><topic>Endothelium</topic><topic>Extracellular vesicles</topic><topic>Flow cytometry</topic><topic>Gene expression</topic><topic>Genotype & phenotype</topic><topic>Glioma</topic><topic>Growth factors</topic><topic>Immunomodulation</topic><topic>Inflammation</topic><topic>Interleukin 6</topic><topic>Leukocyte migration</topic><topic>Leukocytes</topic><topic>Ligands</topic><topic>Monocytes</topic><topic>P-selectin</topic><topic>pathway analysis</topic><topic>Penicillin</topic><topic>Phenotypes</topic><topic>Plasma</topic><topic>Platelet factor 4</topic><topic>Platelet-derived growth factor</topic><topic>Platelets</topic><topic>proteomics</topic><topic>Recruitment</topic><topic>Rodents</topic><topic>Smooth muscle</topic><topic>synthetic phenotype</topic><topic>vascular remodeling</topic><topic>Veins & arteries</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Vajen, Tanja</creatorcontrib><creatorcontrib>Benedikter, Birke J.</creatorcontrib><creatorcontrib>Heinzmann, Alexandra C. A.</creatorcontrib><creatorcontrib>Vasina, Elena M.</creatorcontrib><creatorcontrib>Henskens, Yvonne</creatorcontrib><creatorcontrib>Parsons, Martin</creatorcontrib><creatorcontrib>Maguire, Patricia B.</creatorcontrib><creatorcontrib>Stassen, Frank R.</creatorcontrib><creatorcontrib>Heemskerk, Johan W. M.</creatorcontrib><creatorcontrib>Schurgers, Leon J.</creatorcontrib><creatorcontrib>Koenen, Rory R.</creatorcontrib><collection>Taylor & Francis Open Access</collection><collection>Wiley Online Library Open Access</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Biological Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Journal of extracellular vesicles</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Vajen, Tanja</au><au>Benedikter, Birke J.</au><au>Heinzmann, Alexandra C. A.</au><au>Vasina, Elena M.</au><au>Henskens, Yvonne</au><au>Parsons, Martin</au><au>Maguire, Patricia B.</au><au>Stassen, Frank R.</au><au>Heemskerk, Johan W. M.</au><au>Schurgers, Leon J.</au><au>Koenen, Rory R.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Platelet extracellular vesicles induce a pro-inflammatory smooth muscle cell phenotype</atitle><jtitle>Journal of extracellular vesicles</jtitle><addtitle>J Extracell Vesicles</addtitle><date>2017-12</date><risdate>2017</risdate><volume>6</volume><issue>1</issue><spage>1322454</spage><epage>n/a</epage><pages>1322454-n/a</pages><issn>2001-3078</issn><eissn>2001-3078</eissn><abstract>Extracellular vesicles (EVs) are mediators of cell communication during health and disease, and abundantly released by platelets upon activation or during ageing. Platelet EVs exert modulatory effects on immune and vascular cells. Platelet EVs may modulate the function of vascular smooth muscle cells (SMC). Platelet EVs were isolated from platelet-rich plasma and incubated with SMC in order to assess binding, proliferation, migration and pro-inflammatory phenotype of the cells. Platelet EVs firmly bound to resting SMC through the platelet integrin α
IIb
β
3
, while binding also occurred in a CX3CL1-CX3CR1-dependent manner after cytokine stimulation. Platelet EVs increased SMC migration comparable to platelet derived growth factor or platelet factor 4 and induced SMC proliferation, which relied on CD40- and P-selectin interactions. Flow-resistant monocyte adhesion to platelet EV-treated SMC was increased compared with resting SMC. Again, this adhesion depended on integrin α
IIb
β
3
and P-selectin, and to a lesser extent on CD40 and CX3CR1. Treatment of SMC with platelet EVs induced interleukin 6 secretion. Finally, platelet EVs induced a synthetic SMC morphology and decreased calponin expression. Collectively, these data indicate that platelet EVs exert a strong immunomodulatory activity on SMC. In particular, platelet EVs induce a switch towards a pro-inflammatory phenotype, stimulating vascular remodelling.</abstract><cop>Sweden</cop><pub>Taylor & Francis</pub><pmid>28717419</pmid><doi>10.1080/20013078.2017.1322454</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-9955-9730</orcidid><orcidid>https://orcid.org/0000-0001-8450-9506</orcidid><orcidid>https://orcid.org/0000-0002-1103-2484</orcidid><oa>free_for_read</oa></addata></record> |
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| source | Taylor & Francis Open Access; Wiley Online Library Open Access; DOAJ Directory of Open Access Journals; Wiley Online Library Journals Frontfile Complete; Co-Action Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central |
| subjects | Aging Angiogenesis Atherosclerosis Blood platelets Calponin CD40 antigen Cell activation Cell growth Cell interactions Cell proliferation Chemokines Coronary vessels CR1 CX3CR1 CX3CR1 protein cytokine Cytokines Endothelium Extracellular vesicles Flow cytometry Gene expression Genotype & phenotype Glioma Growth factors Immunomodulation Inflammation Interleukin 6 Leukocyte migration Leukocytes Ligands Monocytes P-selectin pathway analysis Penicillin Phenotypes Plasma Platelet factor 4 Platelet-derived growth factor Platelets proteomics Recruitment Rodents Smooth muscle synthetic phenotype vascular remodeling Veins & arteries |
| title | Platelet extracellular vesicles induce a pro-inflammatory smooth muscle cell phenotype |
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