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Muscle Releases Alpha-Sarcoglycan Positive Extracellular Vesicles Carrying miRNAs in the Bloodstream
In the past few years, skeletal muscle has emerged as an important secretory organ producing soluble factors, called myokines, that exert either autocrine, paracrine or endocrine effects. Moreover, recent studies have shown that muscle releases microRNAs into the bloodstream in response to physical...
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Published in: | PloS one 2015-05, Vol.10 (5), p.e0125094-e0125094 |
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description | In the past few years, skeletal muscle has emerged as an important secretory organ producing soluble factors, called myokines, that exert either autocrine, paracrine or endocrine effects. Moreover, recent studies have shown that muscle releases microRNAs into the bloodstream in response to physical exercise. These microRNAs affect target cells, such as hormones and cytokines. The mechanisms underlying microRNA secretion are poorly characterized at present. Here, we investigated whether muscle tissue releases extracellular vesicles (EVs), which carry microRNAs in the bloodstream under physiological conditions such as physical exercise. Using density gradient separation of plasma from sedentary and physically fit young men we found EVs positive for TSG101 and alpha-sarcoglycan (SGCA), and enriched for miR-206. Cytometric analysis showed that the SGCA+ EVs account for 1-5% of the total and that 60-65% of these EVs were also positive for the exosomal marker CD81. Furthermore, the SGCA-immuno captured sub-population of EVs exhibited higher levels of the miR-206/miR16 ratio compared to total plasma EVs. Finally, a significant positive correlation was found between the aerobic fitness and muscle-specific miRNAs and EV miR-133b and -181a-5p were significantly up-regulated after acute exercise. Thus, our study proposes EVs as a novel means of muscle communication potentially involved in muscle remodeling and homeostasis. |
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Moreover, recent studies have shown that muscle releases microRNAs into the bloodstream in response to physical exercise. These microRNAs affect target cells, such as hormones and cytokines. The mechanisms underlying microRNA secretion are poorly characterized at present. Here, we investigated whether muscle tissue releases extracellular vesicles (EVs), which carry microRNAs in the bloodstream under physiological conditions such as physical exercise. Using density gradient separation of plasma from sedentary and physically fit young men we found EVs positive for TSG101 and alpha-sarcoglycan (SGCA), and enriched for miR-206. Cytometric analysis showed that the SGCA+ EVs account for 1-5% of the total and that 60-65% of these EVs were also positive for the exosomal marker CD81. Furthermore, the SGCA-immuno captured sub-population of EVs exhibited higher levels of the miR-206/miR16 ratio compared to total plasma EVs. Finally, a significant positive correlation was found between the aerobic fitness and muscle-specific miRNAs and EV miR-133b and -181a-5p were significantly up-regulated after acute exercise. Thus, our study proposes EVs as a novel means of muscle communication potentially involved in muscle remodeling and homeostasis.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0125094</identifier><identifier>PMID: 25955720</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adult ; Aerobics ; Analysis ; Autocrine signalling ; Biomarkers ; Cardiorespiratory fitness ; CD81 antigen ; Cell Communication ; Cell cycle ; Centrifugation, Density Gradient ; Communication ; Cytokines ; Density gradients ; Deoxyribonucleic acid ; DNA ; DNA-Binding Proteins - blood ; DNA-Binding Proteins - genetics ; Endosomal Sorting Complexes Required for Transport - blood ; Endosomal Sorting Complexes Required for Transport - genetics ; Exercise ; Exosomes - chemistry ; Exosomes - metabolism ; Extracellular vesicles ; Extracellular Vesicles - chemistry ; Extracellular Vesicles - metabolism ; Gene expression ; Gene Expression Regulation ; Homeostasis ; Hormones ; Humans ; Lipids ; Lung cancer ; Male ; MicroRNA ; MicroRNAs ; MicroRNAs - blood ; MicroRNAs - genetics ; miRNA ; Muscle contraction ; Muscle, Skeletal - cytology ; Muscle, Skeletal - metabolism ; Muscles ; Musculoskeletal system ; Paracrine signalling ; Physical exercise ; Physical fitness ; Plasma ; Proteins ; Researchers ; Ribonucleic acid ; RNA ; Sarcoglycans - blood ; Sarcoglycans - genetics ; Science ; Sedentary Lifestyle ; Signal Transduction ; Skeletal muscle ; Studies ; Tetraspanin 28 - genetics ; Tetraspanin 28 - metabolism ; Transcription Factors - blood ; Transcription Factors - genetics ; Vesicles</subject><ispartof>PloS one, 2015-05, Vol.10 (5), p.e0125094-e0125094</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Guescini et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2015 Guescini et al 2015 Guescini et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c758t-760ae1219fa0535b14c4168646177da11b701589297c50bda2068a653bbb46043</citedby><cites>FETCH-LOGICAL-c758t-760ae1219fa0535b14c4168646177da11b701589297c50bda2068a653bbb46043</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1982584088/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1982584088?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25955720$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Martelli, Fabio</contributor><creatorcontrib>Guescini, Michele</creatorcontrib><creatorcontrib>Canonico, Barbara</creatorcontrib><creatorcontrib>Lucertini, Francesco</creatorcontrib><creatorcontrib>Maggio, Serena</creatorcontrib><creatorcontrib>Annibalini, Giosué</creatorcontrib><creatorcontrib>Barbieri, Elena</creatorcontrib><creatorcontrib>Luchetti, Francesca</creatorcontrib><creatorcontrib>Papa, Stefano</creatorcontrib><creatorcontrib>Stocchi, Vilberto</creatorcontrib><title>Muscle Releases Alpha-Sarcoglycan Positive Extracellular Vesicles Carrying miRNAs in the Bloodstream</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>In the past few years, skeletal muscle has emerged as an important secretory organ producing soluble factors, called myokines, that exert either autocrine, paracrine or endocrine effects. Moreover, recent studies have shown that muscle releases microRNAs into the bloodstream in response to physical exercise. These microRNAs affect target cells, such as hormones and cytokines. The mechanisms underlying microRNA secretion are poorly characterized at present. Here, we investigated whether muscle tissue releases extracellular vesicles (EVs), which carry microRNAs in the bloodstream under physiological conditions such as physical exercise. Using density gradient separation of plasma from sedentary and physically fit young men we found EVs positive for TSG101 and alpha-sarcoglycan (SGCA), and enriched for miR-206. Cytometric analysis showed that the SGCA+ EVs account for 1-5% of the total and that 60-65% of these EVs were also positive for the exosomal marker CD81. Furthermore, the SGCA-immuno captured sub-population of EVs exhibited higher levels of the miR-206/miR16 ratio compared to total plasma EVs. Finally, a significant positive correlation was found between the aerobic fitness and muscle-specific miRNAs and EV miR-133b and -181a-5p were significantly up-regulated after acute exercise. Thus, our study proposes EVs as a novel means of muscle communication potentially involved in muscle remodeling and homeostasis.</description><subject>Adult</subject><subject>Aerobics</subject><subject>Analysis</subject><subject>Autocrine signalling</subject><subject>Biomarkers</subject><subject>Cardiorespiratory fitness</subject><subject>CD81 antigen</subject><subject>Cell Communication</subject><subject>Cell cycle</subject><subject>Centrifugation, Density Gradient</subject><subject>Communication</subject><subject>Cytokines</subject><subject>Density gradients</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA-Binding Proteins - blood</subject><subject>DNA-Binding Proteins - genetics</subject><subject>Endosomal Sorting Complexes Required for Transport - blood</subject><subject>Endosomal Sorting Complexes Required for Transport - genetics</subject><subject>Exercise</subject><subject>Exosomes - chemistry</subject><subject>Exosomes - metabolism</subject><subject>Extracellular vesicles</subject><subject>Extracellular Vesicles - chemistry</subject><subject>Extracellular Vesicles - metabolism</subject><subject>Gene expression</subject><subject>Gene Expression Regulation</subject><subject>Homeostasis</subject><subject>Hormones</subject><subject>Humans</subject><subject>Lipids</subject><subject>Lung cancer</subject><subject>Male</subject><subject>MicroRNA</subject><subject>MicroRNAs</subject><subject>MicroRNAs - blood</subject><subject>MicroRNAs - genetics</subject><subject>miRNA</subject><subject>Muscle contraction</subject><subject>Muscle, Skeletal - cytology</subject><subject>Muscle, Skeletal - metabolism</subject><subject>Muscles</subject><subject>Musculoskeletal system</subject><subject>Paracrine signalling</subject><subject>Physical exercise</subject><subject>Physical fitness</subject><subject>Plasma</subject><subject>Proteins</subject><subject>Researchers</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Sarcoglycans - blood</subject><subject>Sarcoglycans - genetics</subject><subject>Science</subject><subject>Sedentary Lifestyle</subject><subject>Signal Transduction</subject><subject>Skeletal muscle</subject><subject>Studies</subject><subject>Tetraspanin 28 - 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Moreover, recent studies have shown that muscle releases microRNAs into the bloodstream in response to physical exercise. These microRNAs affect target cells, such as hormones and cytokines. The mechanisms underlying microRNA secretion are poorly characterized at present. Here, we investigated whether muscle tissue releases extracellular vesicles (EVs), which carry microRNAs in the bloodstream under physiological conditions such as physical exercise. Using density gradient separation of plasma from sedentary and physically fit young men we found EVs positive for TSG101 and alpha-sarcoglycan (SGCA), and enriched for miR-206. Cytometric analysis showed that the SGCA+ EVs account for 1-5% of the total and that 60-65% of these EVs were also positive for the exosomal marker CD81. Furthermore, the SGCA-immuno captured sub-population of EVs exhibited higher levels of the miR-206/miR16 ratio compared to total plasma EVs. Finally, a significant positive correlation was found between the aerobic fitness and muscle-specific miRNAs and EV miR-133b and -181a-5p were significantly up-regulated after acute exercise. Thus, our study proposes EVs as a novel means of muscle communication potentially involved in muscle remodeling and homeostasis.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25955720</pmid><doi>10.1371/journal.pone.0125094</doi><oa>free_for_read</oa></addata></record> |
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subjects | Adult Aerobics Analysis Autocrine signalling Biomarkers Cardiorespiratory fitness CD81 antigen Cell Communication Cell cycle Centrifugation, Density Gradient Communication Cytokines Density gradients Deoxyribonucleic acid DNA DNA-Binding Proteins - blood DNA-Binding Proteins - genetics Endosomal Sorting Complexes Required for Transport - blood Endosomal Sorting Complexes Required for Transport - genetics Exercise Exosomes - chemistry Exosomes - metabolism Extracellular vesicles Extracellular Vesicles - chemistry Extracellular Vesicles - metabolism Gene expression Gene Expression Regulation Homeostasis Hormones Humans Lipids Lung cancer Male MicroRNA MicroRNAs MicroRNAs - blood MicroRNAs - genetics miRNA Muscle contraction Muscle, Skeletal - cytology Muscle, Skeletal - metabolism Muscles Musculoskeletal system Paracrine signalling Physical exercise Physical fitness Plasma Proteins Researchers Ribonucleic acid RNA Sarcoglycans - blood Sarcoglycans - genetics Science Sedentary Lifestyle Signal Transduction Skeletal muscle Studies Tetraspanin 28 - genetics Tetraspanin 28 - metabolism Transcription Factors - blood Transcription Factors - genetics Vesicles |
title | Muscle Releases Alpha-Sarcoglycan Positive Extracellular Vesicles Carrying miRNAs in the Bloodstream |
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