Superoxide flashes in mouse skeletal muscle are produced by discrete arrays of active mitochondria operating coherently
Reactive Oxygen Species (ROS) constitute important intracellular signaling molecules. Mitochondria are admitted sources of ROS, especially of superoxide anions through the electron transport chain. Here the mitochondria-targeted ratiometric pericam (RPmt) was used as a superoxide biosensor, by appro...
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description | Reactive Oxygen Species (ROS) constitute important intracellular signaling molecules. Mitochondria are admitted sources of ROS, especially of superoxide anions through the electron transport chain. Here the mitochondria-targeted ratiometric pericam (RPmt) was used as a superoxide biosensor, by appropriate choice of the excitation wavelength. RPmt was transfected in vivo into mouse muscles. Confocal imaging of isolated muscle fibers reveals spontaneous flashes of RPmt fluorescence. Flashes correspond to increases in superoxide production, as shown by simultaneous recordings of the fluorescence from MitoSox, a mitochondrial superoxide probe. Flashes occur in all subcellular populations of mitochondria. Spatial analysis of the flashes pattern over time revealed that arrays of mitochondria work as well-defined superoxide-production-units. Increase of superoxide production at the muscle fiber level involves recruitment of supplemental units with no increase in per-unit production. Altogether, these results demonstrate that superoxide flashes in muscle fibers correspond to physiological signals linked to mitochondrial metabolism. They also suggest that superoxide, or one of its derivatives, modulates its own production at the mitochondrial level. |
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Mitochondria are admitted sources of ROS, especially of superoxide anions through the electron transport chain. Here the mitochondria-targeted ratiometric pericam (RPmt) was used as a superoxide biosensor, by appropriate choice of the excitation wavelength. RPmt was transfected in vivo into mouse muscles. Confocal imaging of isolated muscle fibers reveals spontaneous flashes of RPmt fluorescence. Flashes correspond to increases in superoxide production, as shown by simultaneous recordings of the fluorescence from MitoSox, a mitochondrial superoxide probe. Flashes occur in all subcellular populations of mitochondria. Spatial analysis of the flashes pattern over time revealed that arrays of mitochondria work as well-defined superoxide-production-units. Increase of superoxide production at the muscle fiber level involves recruitment of supplemental units with no increase in per-unit production. Altogether, these results demonstrate that superoxide flashes in muscle fibers correspond to physiological signals linked to mitochondrial metabolism. They also suggest that superoxide, or one of its derivatives, modulates its own production at the mitochondrial level.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0013035</identifier><identifier>PMID: 20927399</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Anions ; Biosensors ; Cardiomyocytes ; Cell Biology/Cell Signaling ; Confocal ; Electron transport ; Electron transport chain ; Fluorescence ; Gene expression ; Intracellular signalling ; Male ; Metabolism ; Mice ; Microscopy, Confocal ; Mitochondria ; Mitochondria, Muscle - chemistry ; Mitochondria, Muscle - metabolism ; Muscle, Skeletal - chemistry ; Muscle, Skeletal - metabolism ; Muscles ; Musculoskeletal system ; Oxygen ; Permeability ; Physiological aspects ; Physiology ; Physiology/Cell Signaling ; Physiology/Muscle and Connective Tissue ; Protein expression ; Proteins ; Reactive oxygen species ; Recruitment ; Skeletal muscle ; Spatial analysis ; Superoxide ; Superoxide anions ; Superoxides ; Superoxides - analysis ; Superoxides - metabolism ; Trends</subject><ispartof>PloS one, 2010-09, Vol.5 (9), p.e13035</ispartof><rights>COPYRIGHT 2010 Public Library of Science</rights><rights>2010 Sandrine Pouvreau. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://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>Sandrine Pouvreau. 2010</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c691t-6c9e9ad96d5d11cf03eadfbf6a59aa64c5f9bcdbf002af2e6eda5a9e0ddd0fea3</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2946926/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2946926/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20927399$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Moran, Maria</contributor><creatorcontrib>Pouvreau, Sandrine</creatorcontrib><title>Superoxide flashes in mouse skeletal muscle are produced by discrete arrays of active mitochondria operating coherently</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Reactive Oxygen Species (ROS) constitute important intracellular signaling molecules. Mitochondria are admitted sources of ROS, especially of superoxide anions through the electron transport chain. Here the mitochondria-targeted ratiometric pericam (RPmt) was used as a superoxide biosensor, by appropriate choice of the excitation wavelength. RPmt was transfected in vivo into mouse muscles. Confocal imaging of isolated muscle fibers reveals spontaneous flashes of RPmt fluorescence. Flashes correspond to increases in superoxide production, as shown by simultaneous recordings of the fluorescence from MitoSox, a mitochondrial superoxide probe. Flashes occur in all subcellular populations of mitochondria. Spatial analysis of the flashes pattern over time revealed that arrays of mitochondria work as well-defined superoxide-production-units. Increase of superoxide production at the muscle fiber level involves recruitment of supplemental units with no increase in per-unit production. Altogether, these results demonstrate that superoxide flashes in muscle fibers correspond to physiological signals linked to mitochondrial metabolism. They also suggest that superoxide, or one of its derivatives, modulates its own production at the mitochondrial level.</description><subject>Animals</subject><subject>Anions</subject><subject>Biosensors</subject><subject>Cardiomyocytes</subject><subject>Cell Biology/Cell Signaling</subject><subject>Confocal</subject><subject>Electron transport</subject><subject>Electron transport chain</subject><subject>Fluorescence</subject><subject>Gene expression</subject><subject>Intracellular signalling</subject><subject>Male</subject><subject>Metabolism</subject><subject>Mice</subject><subject>Microscopy, Confocal</subject><subject>Mitochondria</subject><subject>Mitochondria, Muscle - chemistry</subject><subject>Mitochondria, Muscle - metabolism</subject><subject>Muscle, Skeletal - chemistry</subject><subject>Muscle, Skeletal - metabolism</subject><subject>Muscles</subject><subject>Musculoskeletal system</subject><subject>Oxygen</subject><subject>Permeability</subject><subject>Physiological aspects</subject><subject>Physiology</subject><subject>Physiology/Cell Signaling</subject><subject>Physiology/Muscle and Connective Tissue</subject><subject>Protein expression</subject><subject>Proteins</subject><subject>Reactive oxygen species</subject><subject>Recruitment</subject><subject>Skeletal muscle</subject><subject>Spatial analysis</subject><subject>Superoxide</subject><subject>Superoxide anions</subject><subject>Superoxides</subject><subject>Superoxides - 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chemistry</topic><topic>Mitochondria, Muscle - metabolism</topic><topic>Muscle, Skeletal - chemistry</topic><topic>Muscle, Skeletal - metabolism</topic><topic>Muscles</topic><topic>Musculoskeletal system</topic><topic>Oxygen</topic><topic>Permeability</topic><topic>Physiological aspects</topic><topic>Physiology</topic><topic>Physiology/Cell Signaling</topic><topic>Physiology/Muscle and Connective Tissue</topic><topic>Protein expression</topic><topic>Proteins</topic><topic>Reactive oxygen species</topic><topic>Recruitment</topic><topic>Skeletal muscle</topic><topic>Spatial analysis</topic><topic>Superoxide</topic><topic>Superoxide anions</topic><topic>Superoxides</topic><topic>Superoxides - analysis</topic><topic>Superoxides - metabolism</topic><topic>Trends</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Pouvreau, Sandrine</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Mitochondria are admitted sources of ROS, especially of superoxide anions through the electron transport chain. Here the mitochondria-targeted ratiometric pericam (RPmt) was used as a superoxide biosensor, by appropriate choice of the excitation wavelength. RPmt was transfected in vivo into mouse muscles. Confocal imaging of isolated muscle fibers reveals spontaneous flashes of RPmt fluorescence. Flashes correspond to increases in superoxide production, as shown by simultaneous recordings of the fluorescence from MitoSox, a mitochondrial superoxide probe. Flashes occur in all subcellular populations of mitochondria. Spatial analysis of the flashes pattern over time revealed that arrays of mitochondria work as well-defined superoxide-production-units. Increase of superoxide production at the muscle fiber level involves recruitment of supplemental units with no increase in per-unit production. Altogether, these results demonstrate that superoxide flashes in muscle fibers correspond to physiological signals linked to mitochondrial metabolism. They also suggest that superoxide, or one of its derivatives, modulates its own production at the mitochondrial level.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>20927399</pmid><doi>10.1371/journal.pone.0013035</doi><tpages>e13035</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Anions Biosensors Cardiomyocytes Cell Biology/Cell Signaling Confocal Electron transport Electron transport chain Fluorescence Gene expression Intracellular signalling Male Metabolism Mice Microscopy, Confocal Mitochondria Mitochondria, Muscle - chemistry Mitochondria, Muscle - metabolism Muscle, Skeletal - chemistry Muscle, Skeletal - metabolism Muscles Musculoskeletal system Oxygen Permeability Physiological aspects Physiology Physiology/Cell Signaling Physiology/Muscle and Connective Tissue Protein expression Proteins Reactive oxygen species Recruitment Skeletal muscle Spatial analysis Superoxide Superoxide anions Superoxides Superoxides - analysis Superoxides - metabolism Trends |
title | Superoxide flashes in mouse skeletal muscle are produced by discrete arrays of active mitochondria operating coherently |
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