Increased mitochondrial surface area and cristae density in the skeletal muscle of strength athletes
Mitochondria are the cellular organelles responsible for resynthesising the majority of ATP. In skeletal muscle, there is an increased ATP turnover during resistance exercise to sustain the energetic demands of muscle contraction. Despite this, little is known regarding the mitochondrial characteris...
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creator | Botella, Javier Schytz, Camilla T. Pehrson, Thomas F. Hokken, Rune Laugesen, Simon Aagaard, Per Suetta, Charlotte Christensen, Britt Ørtenblad, Niels Nielsen, Joachim |
description | Mitochondria are the cellular organelles responsible for resynthesising the majority of ATP. In skeletal muscle, there is an increased ATP turnover during resistance exercise to sustain the energetic demands of muscle contraction. Despite this, little is known regarding the mitochondrial characteristics of chronically strength‐trained individuals and any potential pathways regulating the strength‐specific mitochondrial remodelling. Here, we investigated the mitochondrial structural characteristics in skeletal muscle of strength athletes and age‐matched untrained controls. The mitochondrial pool in strength athletes was characterised by increased mitochondrial cristae density, decreased mitochondrial size, and increased surface‐to‐volume ratio, despite similar mitochondrial volume density. We also provide a fibre‐type and compartment‐specific assessment of mitochondria morphology in human skeletal muscle, which reveals across groups a compartment‐specific influence on mitochondrial morphology that is largely independent of fibre type. Furthermore, we show that resistance exercise leads to signs of mild mitochondrial stress, without an increase in the number of damaged mitochondria. Using publicly available transcriptomic data we show that acute resistance exercise increases the expression of markers of mitochondrial biogenesis, fission and mitochondrial unfolded protein responses (UPRmt). Further, we observed an enrichment of the UPRmt in the basal transcriptome of strength‐trained individuals. Together, these findings show that strength athletes possess a unique mitochondrial remodelling, which minimises the space required for mitochondria. We propose that the concurrent activation of markers of mitochondrial biogenesis and mitochondrial remodelling pathways (fission and UPRmt) with resistance exercise may be partially responsible for the observed mitochondrial phenotype of strength athletes.
Key points
Untrained individuals and strength athletes possess comparable skeletal muscle mitochondrial volume density.
In contrast, strength athletes’ mitochondria are characterised by increased cristae density, decreased size and increased surface‐to‐volume ratio.
Type I fibres have an increased number of mitochondrial profiles with minor differences in the mitochondrial morphological characteristics compared with type II fibres.
The mitochondrial morphology is distinct across the subcellular compartments in both groups, with subsarcolemmal mitochondria being bigger |
doi_str_mv | 10.1113/JP284394 |
format | Article |
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Key points
Untrained individuals and strength athletes possess comparable skeletal muscle mitochondrial volume density.
In contrast, strength athletes’ mitochondria are characterised by increased cristae density, decreased size and increased surface‐to‐volume ratio.
Type I fibres have an increased number of mitochondrial profiles with minor differences in the mitochondrial morphological characteristics compared with type II fibres.
The mitochondrial morphology is distinct across the subcellular compartments in both groups, with subsarcolemmal mitochondria being bigger in size when compared with intermyofibrillar.
Acute resistance exercise leads to signs of mild morphological mitochondrial stress accompanied by increased gene expression of markers of mitochondrial biogenesis, fission and mitochondrial unfolded protein response (UPRmt).
figure legend Mitochondria are the cellular organelles responsible for resynthesising the majority of ATP. The present study aimed to investigate the mitochondrial structural characteristics of strength athletes when compared with age‐matched untrained individuals. Here we show that the mitochondria of strength athletes have an increased mitochondrial cristae density, an increased number of profiles and an increased surface‐to‐volume ratio; despite similar mitochondrial volumetric density. Furthermore, we show that human type I fibres, when compared with type II fibres, are characterised by an increased number of mitochondrial profiles without differences in their morphological characteristics. Finally, we show that acute resistance exercise leads to mild signs of mitochondrial morphological stress and an increased expression of markers of mitochondrial biogenesis, fission and mitochondrial unfolded protein response (UPRmt).</description><identifier>ISSN: 0022-3751</identifier><identifier>ISSN: 1469-7793</identifier><identifier>EISSN: 1469-7793</identifier><identifier>DOI: 10.1113/JP284394</identifier><identifier>PMID: 37042493</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Adenosine Triphosphate - metabolism ; Athletes ; Biosynthesis ; Cristae ; cristae density ; Gene expression ; Humans ; Mitochondria ; Mitochondria - metabolism ; Mitochondria, Muscle - metabolism ; Morphology ; Muscle contraction ; Muscle, Skeletal - metabolism ; Musculoskeletal system ; Olympic weightlifting ; Organelles ; Phenotypes ; Physical characteristics ; Protein folding ; resistance exercise ; Skeletal muscle ; strength ; Transcriptomes ; Transcriptomics ; Unfolded Protein Response</subject><ispartof>The Journal of physiology, 2023-07, Vol.601 (14), p.2899-2915</ispartof><rights>2023 The Authors. published by John Wiley & Sons Ltd on behalf of The Physiological Society.</rights><rights>2023 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.</rights><rights>2023. This article 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.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3844-bb48aec726b96ad8015bf1fc90f0df32e578d754033f7553d3de0a51b74592c13</citedby><cites>FETCH-LOGICAL-c3844-bb48aec726b96ad8015bf1fc90f0df32e578d754033f7553d3de0a51b74592c13</cites><orcidid>0000-0003-1730-3094 ; 0000-0003-1371-4275 ; 0000-0001-9060-4139 ; 0000-0001-9722-8519</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1113%2FJP284394$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1113%2FJP284394$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>314,780,784,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37042493$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Botella, Javier</creatorcontrib><creatorcontrib>Schytz, Camilla T.</creatorcontrib><creatorcontrib>Pehrson, Thomas F.</creatorcontrib><creatorcontrib>Hokken, Rune</creatorcontrib><creatorcontrib>Laugesen, Simon</creatorcontrib><creatorcontrib>Aagaard, Per</creatorcontrib><creatorcontrib>Suetta, Charlotte</creatorcontrib><creatorcontrib>Christensen, Britt</creatorcontrib><creatorcontrib>Ørtenblad, Niels</creatorcontrib><creatorcontrib>Nielsen, Joachim</creatorcontrib><title>Increased mitochondrial surface area and cristae density in the skeletal muscle of strength athletes</title><title>The Journal of physiology</title><addtitle>J Physiol</addtitle><description>Mitochondria are the cellular organelles responsible for resynthesising the majority of ATP. In skeletal muscle, there is an increased ATP turnover during resistance exercise to sustain the energetic demands of muscle contraction. Despite this, little is known regarding the mitochondrial characteristics of chronically strength‐trained individuals and any potential pathways regulating the strength‐specific mitochondrial remodelling. Here, we investigated the mitochondrial structural characteristics in skeletal muscle of strength athletes and age‐matched untrained controls. The mitochondrial pool in strength athletes was characterised by increased mitochondrial cristae density, decreased mitochondrial size, and increased surface‐to‐volume ratio, despite similar mitochondrial volume density. We also provide a fibre‐type and compartment‐specific assessment of mitochondria morphology in human skeletal muscle, which reveals across groups a compartment‐specific influence on mitochondrial morphology that is largely independent of fibre type. Furthermore, we show that resistance exercise leads to signs of mild mitochondrial stress, without an increase in the number of damaged mitochondria. Using publicly available transcriptomic data we show that acute resistance exercise increases the expression of markers of mitochondrial biogenesis, fission and mitochondrial unfolded protein responses (UPRmt). Further, we observed an enrichment of the UPRmt in the basal transcriptome of strength‐trained individuals. Together, these findings show that strength athletes possess a unique mitochondrial remodelling, which minimises the space required for mitochondria. We propose that the concurrent activation of markers of mitochondrial biogenesis and mitochondrial remodelling pathways (fission and UPRmt) with resistance exercise may be partially responsible for the observed mitochondrial phenotype of strength athletes.
Key points
Untrained individuals and strength athletes possess comparable skeletal muscle mitochondrial volume density.
In contrast, strength athletes’ mitochondria are characterised by increased cristae density, decreased size and increased surface‐to‐volume ratio.
Type I fibres have an increased number of mitochondrial profiles with minor differences in the mitochondrial morphological characteristics compared with type II fibres.
The mitochondrial morphology is distinct across the subcellular compartments in both groups, with subsarcolemmal mitochondria being bigger in size when compared with intermyofibrillar.
Acute resistance exercise leads to signs of mild morphological mitochondrial stress accompanied by increased gene expression of markers of mitochondrial biogenesis, fission and mitochondrial unfolded protein response (UPRmt).
figure legend Mitochondria are the cellular organelles responsible for resynthesising the majority of ATP. The present study aimed to investigate the mitochondrial structural characteristics of strength athletes when compared with age‐matched untrained individuals. Here we show that the mitochondria of strength athletes have an increased mitochondrial cristae density, an increased number of profiles and an increased surface‐to‐volume ratio; despite similar mitochondrial volumetric density. Furthermore, we show that human type I fibres, when compared with type II fibres, are characterised by an increased number of mitochondrial profiles without differences in their morphological characteristics. Finally, we show that acute resistance exercise leads to mild signs of mitochondrial morphological stress and an increased expression of markers of mitochondrial biogenesis, fission and mitochondrial unfolded protein response (UPRmt).</description><subject>Adenosine Triphosphate - metabolism</subject><subject>Athletes</subject><subject>Biosynthesis</subject><subject>Cristae</subject><subject>cristae density</subject><subject>Gene expression</subject><subject>Humans</subject><subject>Mitochondria</subject><subject>Mitochondria - metabolism</subject><subject>Mitochondria, Muscle - metabolism</subject><subject>Morphology</subject><subject>Muscle contraction</subject><subject>Muscle, Skeletal - metabolism</subject><subject>Musculoskeletal system</subject><subject>Olympic weightlifting</subject><subject>Organelles</subject><subject>Phenotypes</subject><subject>Physical characteristics</subject><subject>Protein folding</subject><subject>resistance exercise</subject><subject>Skeletal muscle</subject><subject>strength</subject><subject>Transcriptomes</subject><subject>Transcriptomics</subject><subject>Unfolded Protein Response</subject><issn>0022-3751</issn><issn>1469-7793</issn><issn>1469-7793</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNp1kMlKBDEQQIMoOi7gF0jAi5fWpCuZdI4irgh60HOTTipOay-apJH5eyOOCoKnOtSrR_EI2efsmHMOJzf3ZSVAizUy42KuC6U0rJMZY2VZgJJ8i2zH-MwYB6b1JtkCxUQpNMyIux5sQBPR0b5No12Mgwut6WicgjcWqclbagZHbWhjMkgdDrFNS9oONC2QxhfsMOWDfoq2Qzp6GlPA4SktqEmLvMO4Sza86SLureYOebw4fzi7Km7vLq_PTm8LC5UQRdOIyqBV5bzRc-MqxmXjubeaeeY8lChV5ZQUDMArKcGBQ2Ykb5SQurQcdsjRl_c1jG8TxlT3bbTYdWbAcYp1WeUEQkmoMnr4B30epzDk7zIFc61AavgV2jDGGNDXr6HtTVjWnNWf5evv8hk9WAmnpkf3A36nzsDxF_Dedrj8V1Q_3NxzKYWAD5GOi2o</recordid><startdate>20230701</startdate><enddate>20230701</enddate><creator>Botella, Javier</creator><creator>Schytz, Camilla T.</creator><creator>Pehrson, Thomas F.</creator><creator>Hokken, Rune</creator><creator>Laugesen, Simon</creator><creator>Aagaard, Per</creator><creator>Suetta, Charlotte</creator><creator>Christensen, Britt</creator><creator>Ørtenblad, Niels</creator><creator>Nielsen, Joachim</creator><general>Wiley Subscription Services, Inc</general><scope>24P</scope><scope>WIN</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TS</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-1730-3094</orcidid><orcidid>https://orcid.org/0000-0003-1371-4275</orcidid><orcidid>https://orcid.org/0000-0001-9060-4139</orcidid><orcidid>https://orcid.org/0000-0001-9722-8519</orcidid></search><sort><creationdate>20230701</creationdate><title>Increased mitochondrial surface area and cristae density in the skeletal muscle of strength athletes</title><author>Botella, Javier ; Schytz, Camilla T. ; Pehrson, Thomas F. ; Hokken, Rune ; Laugesen, Simon ; Aagaard, Per ; Suetta, Charlotte ; Christensen, Britt ; Ørtenblad, Niels ; Nielsen, Joachim</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3844-bb48aec726b96ad8015bf1fc90f0df32e578d754033f7553d3de0a51b74592c13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Adenosine Triphosphate - metabolism</topic><topic>Athletes</topic><topic>Biosynthesis</topic><topic>Cristae</topic><topic>cristae density</topic><topic>Gene expression</topic><topic>Humans</topic><topic>Mitochondria</topic><topic>Mitochondria - metabolism</topic><topic>Mitochondria, Muscle - metabolism</topic><topic>Morphology</topic><topic>Muscle contraction</topic><topic>Muscle, Skeletal - metabolism</topic><topic>Musculoskeletal system</topic><topic>Olympic weightlifting</topic><topic>Organelles</topic><topic>Phenotypes</topic><topic>Physical characteristics</topic><topic>Protein folding</topic><topic>resistance exercise</topic><topic>Skeletal muscle</topic><topic>strength</topic><topic>Transcriptomes</topic><topic>Transcriptomics</topic><topic>Unfolded Protein Response</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Botella, Javier</creatorcontrib><creatorcontrib>Schytz, Camilla T.</creatorcontrib><creatorcontrib>Pehrson, Thomas F.</creatorcontrib><creatorcontrib>Hokken, Rune</creatorcontrib><creatorcontrib>Laugesen, Simon</creatorcontrib><creatorcontrib>Aagaard, Per</creatorcontrib><creatorcontrib>Suetta, Charlotte</creatorcontrib><creatorcontrib>Christensen, Britt</creatorcontrib><creatorcontrib>Ørtenblad, Niels</creatorcontrib><creatorcontrib>Nielsen, Joachim</creatorcontrib><collection>Wiley Online Library (Open Access Collection)</collection><collection>Wiley Online Library (Open Access Collection)</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Physical Education Index</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The Journal of physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Botella, Javier</au><au>Schytz, Camilla T.</au><au>Pehrson, Thomas F.</au><au>Hokken, Rune</au><au>Laugesen, Simon</au><au>Aagaard, Per</au><au>Suetta, Charlotte</au><au>Christensen, Britt</au><au>Ørtenblad, Niels</au><au>Nielsen, Joachim</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Increased mitochondrial surface area and cristae density in the skeletal muscle of strength athletes</atitle><jtitle>The Journal of physiology</jtitle><addtitle>J Physiol</addtitle><date>2023-07-01</date><risdate>2023</risdate><volume>601</volume><issue>14</issue><spage>2899</spage><epage>2915</epage><pages>2899-2915</pages><issn>0022-3751</issn><issn>1469-7793</issn><eissn>1469-7793</eissn><abstract>Mitochondria are the cellular organelles responsible for resynthesising the majority of ATP. In skeletal muscle, there is an increased ATP turnover during resistance exercise to sustain the energetic demands of muscle contraction. Despite this, little is known regarding the mitochondrial characteristics of chronically strength‐trained individuals and any potential pathways regulating the strength‐specific mitochondrial remodelling. Here, we investigated the mitochondrial structural characteristics in skeletal muscle of strength athletes and age‐matched untrained controls. The mitochondrial pool in strength athletes was characterised by increased mitochondrial cristae density, decreased mitochondrial size, and increased surface‐to‐volume ratio, despite similar mitochondrial volume density. We also provide a fibre‐type and compartment‐specific assessment of mitochondria morphology in human skeletal muscle, which reveals across groups a compartment‐specific influence on mitochondrial morphology that is largely independent of fibre type. Furthermore, we show that resistance exercise leads to signs of mild mitochondrial stress, without an increase in the number of damaged mitochondria. Using publicly available transcriptomic data we show that acute resistance exercise increases the expression of markers of mitochondrial biogenesis, fission and mitochondrial unfolded protein responses (UPRmt). Further, we observed an enrichment of the UPRmt in the basal transcriptome of strength‐trained individuals. Together, these findings show that strength athletes possess a unique mitochondrial remodelling, which minimises the space required for mitochondria. We propose that the concurrent activation of markers of mitochondrial biogenesis and mitochondrial remodelling pathways (fission and UPRmt) with resistance exercise may be partially responsible for the observed mitochondrial phenotype of strength athletes.
Key points
Untrained individuals and strength athletes possess comparable skeletal muscle mitochondrial volume density.
In contrast, strength athletes’ mitochondria are characterised by increased cristae density, decreased size and increased surface‐to‐volume ratio.
Type I fibres have an increased number of mitochondrial profiles with minor differences in the mitochondrial morphological characteristics compared with type II fibres.
The mitochondrial morphology is distinct across the subcellular compartments in both groups, with subsarcolemmal mitochondria being bigger in size when compared with intermyofibrillar.
Acute resistance exercise leads to signs of mild morphological mitochondrial stress accompanied by increased gene expression of markers of mitochondrial biogenesis, fission and mitochondrial unfolded protein response (UPRmt).
figure legend Mitochondria are the cellular organelles responsible for resynthesising the majority of ATP. The present study aimed to investigate the mitochondrial structural characteristics of strength athletes when compared with age‐matched untrained individuals. Here we show that the mitochondria of strength athletes have an increased mitochondrial cristae density, an increased number of profiles and an increased surface‐to‐volume ratio; despite similar mitochondrial volumetric density. Furthermore, we show that human type I fibres, when compared with type II fibres, are characterised by an increased number of mitochondrial profiles without differences in their morphological characteristics. Finally, we show that acute resistance exercise leads to mild signs of mitochondrial morphological stress and an increased expression of markers of mitochondrial biogenesis, fission and mitochondrial unfolded protein response (UPRmt).</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>37042493</pmid><doi>10.1113/JP284394</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0003-1730-3094</orcidid><orcidid>https://orcid.org/0000-0003-1371-4275</orcidid><orcidid>https://orcid.org/0000-0001-9060-4139</orcidid><orcidid>https://orcid.org/0000-0001-9722-8519</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adenosine Triphosphate - metabolism Athletes Biosynthesis Cristae cristae density Gene expression Humans Mitochondria Mitochondria - metabolism Mitochondria, Muscle - metabolism Morphology Muscle contraction Muscle, Skeletal - metabolism Musculoskeletal system Olympic weightlifting Organelles Phenotypes Physical characteristics Protein folding resistance exercise Skeletal muscle strength Transcriptomes Transcriptomics Unfolded Protein Response |
title | Increased mitochondrial surface area and cristae density in the skeletal muscle of strength athletes |
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