Muscle-derived interleukin 6 increases exercise capacity by signaling in osteoblasts
Given the numerous health benefits of exercise, understanding how exercise capacity is regulated is a question of paramount importance. Circulating interleukin 6 (IL-6) levels surge during exercise and IL-6 favors exercise capacity. However, neither the cellular origin of circulating IL-6 during exe...
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| Veröffentlicht in: | The Journal of clinical investigation 2020-06, Vol.130 (6), p.2888-2902 |
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| creator | Chowdhury, Subrata Schulz, Logan Palmisano, Biagio Singh, Parminder Berger, Julian M Yadav, Vijay K Mera, Paula Ellingsgaard, Helga Hidalgo, Juan Brüning, Jens Karsenty, Gerard |
| description | Given the numerous health benefits of exercise, understanding how exercise capacity is regulated is a question of paramount importance. Circulating interleukin 6 (IL-6) levels surge during exercise and IL-6 favors exercise capacity. However, neither the cellular origin of circulating IL-6 during exercise nor the means by which this cytokine enhances exercise capacity has been formally established yet. Here we show through genetic means that the majority of circulating IL-6 detectable during exercise originates from muscle and that to increase exercise capacity, IL-6 must signal in osteoblasts to favor osteoclast differentiation and the release of bioactive osteocalcin in the general circulation. This explains why mice lacking the IL-6 receptor only in osteoblasts exhibit a deficit in exercise capacity of similar severity to the one seen in mice lacking muscle-derived IL-6 (mIL-6), and why this deficit is correctable by osteocalcin but not by IL-6. Furthermore, in agreement with the notion that IL-6 acts through osteocalcin, we demonstrate that mIL-6 promotes nutrient uptake and catabolism into myofibers during exercise in an osteocalcin-dependent manner. Finally, we show that the crosstalk between osteocalcin and IL-6 is conserved between rodents and humans. This study provides evidence that a muscle-bone-muscle endocrine axis is necessary to increase muscle function during exercise in rodents and humans. |
| doi_str_mv | 10.1172/JCI133572 |
| format | Article |
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Circulating interleukin 6 (IL-6) levels surge during exercise and IL-6 favors exercise capacity. However, neither the cellular origin of circulating IL-6 during exercise nor the means by which this cytokine enhances exercise capacity has been formally established yet. Here we show through genetic means that the majority of circulating IL-6 detectable during exercise originates from muscle and that to increase exercise capacity, IL-6 must signal in osteoblasts to favor osteoclast differentiation and the release of bioactive osteocalcin in the general circulation. This explains why mice lacking the IL-6 receptor only in osteoblasts exhibit a deficit in exercise capacity of similar severity to the one seen in mice lacking muscle-derived IL-6 (mIL-6), and why this deficit is correctable by osteocalcin but not by IL-6. Furthermore, in agreement with the notion that IL-6 acts through osteocalcin, we demonstrate that mIL-6 promotes nutrient uptake and catabolism into myofibers during exercise in an osteocalcin-dependent manner. Finally, we show that the crosstalk between osteocalcin and IL-6 is conserved between rodents and humans. This study provides evidence that a muscle-bone-muscle endocrine axis is necessary to increase muscle function during exercise in rodents and humans.</description><identifier>ISSN: 0021-9738</identifier><identifier>EISSN: 1558-8238</identifier><identifier>DOI: 10.1172/JCI133572</identifier><identifier>PMID: 32078586</identifier><language>eng</language><publisher>United States: American Society for Clinical Investigation</publisher><subject>Animals ; Antibodies ; Biomedical research ; Capacity ; Cytokines ; Exercise ; Experiments ; Female ; Fitness equipment ; Health insurance ; Interleukin 6 ; Interleukin 6 receptors ; Interleukin-6 - genetics ; Interleukin-6 - immunology ; Interleukins ; Macaca mulatta ; Mice ; Mice, Knockout ; Muscle function ; Muscle, Skeletal - immunology ; Nutrient uptake ; Osteoblastogenesis ; Osteoblasts ; Osteoblasts - immunology ; Osteocalcin ; Osteoclastogenesis ; Physiology ; Running ; Scientific equipment industry ; Signal Transduction - genetics ; Signal Transduction - immunology</subject><ispartof>The Journal of clinical investigation, 2020-06, Vol.130 (6), p.2888-2902</ispartof><rights>COPYRIGHT 2020 American Society for Clinical Investigation</rights><rights>Copyright American Society for Clinical Investigation Jun 2020</rights><rights>2020 American Society for Clinical Investigation 2020 American Society for Clinical Investigation</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c647t-f41961e307a93472962c9710f6cc92b3db7f242c7b06574c7dae50b2ca1de94a3</citedby><cites>FETCH-LOGICAL-c647t-f41961e307a93472962c9710f6cc92b3db7f242c7b06574c7dae50b2ca1de94a3</cites><orcidid>0000-0003-0921-1122 ; 0000-0002-1287-5256 ; 0000-0001-8941-4637 ; 0000-0002-2851-6805 ; 0000-0002-9253-7627</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/PMC7260002/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7260002/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32078586$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chowdhury, Subrata</creatorcontrib><creatorcontrib>Schulz, Logan</creatorcontrib><creatorcontrib>Palmisano, Biagio</creatorcontrib><creatorcontrib>Singh, Parminder</creatorcontrib><creatorcontrib>Berger, Julian M</creatorcontrib><creatorcontrib>Yadav, Vijay K</creatorcontrib><creatorcontrib>Mera, Paula</creatorcontrib><creatorcontrib>Ellingsgaard, Helga</creatorcontrib><creatorcontrib>Hidalgo, Juan</creatorcontrib><creatorcontrib>Brüning, Jens</creatorcontrib><creatorcontrib>Karsenty, Gerard</creatorcontrib><title>Muscle-derived interleukin 6 increases exercise capacity by signaling in osteoblasts</title><title>The Journal of clinical investigation</title><addtitle>J Clin Invest</addtitle><description>Given the numerous health benefits of exercise, understanding how exercise capacity is regulated is a question of paramount importance. Circulating interleukin 6 (IL-6) levels surge during exercise and IL-6 favors exercise capacity. However, neither the cellular origin of circulating IL-6 during exercise nor the means by which this cytokine enhances exercise capacity has been formally established yet. Here we show through genetic means that the majority of circulating IL-6 detectable during exercise originates from muscle and that to increase exercise capacity, IL-6 must signal in osteoblasts to favor osteoclast differentiation and the release of bioactive osteocalcin in the general circulation. This explains why mice lacking the IL-6 receptor only in osteoblasts exhibit a deficit in exercise capacity of similar severity to the one seen in mice lacking muscle-derived IL-6 (mIL-6), and why this deficit is correctable by osteocalcin but not by IL-6. Furthermore, in agreement with the notion that IL-6 acts through osteocalcin, we demonstrate that mIL-6 promotes nutrient uptake and catabolism into myofibers during exercise in an osteocalcin-dependent manner. Finally, we show that the crosstalk between osteocalcin and IL-6 is conserved between rodents and humans. This study provides evidence that a muscle-bone-muscle endocrine axis is necessary to increase muscle function during exercise in rodents and humans.</description><subject>Animals</subject><subject>Antibodies</subject><subject>Biomedical research</subject><subject>Capacity</subject><subject>Cytokines</subject><subject>Exercise</subject><subject>Experiments</subject><subject>Female</subject><subject>Fitness equipment</subject><subject>Health insurance</subject><subject>Interleukin 6</subject><subject>Interleukin 6 receptors</subject><subject>Interleukin-6 - genetics</subject><subject>Interleukin-6 - immunology</subject><subject>Interleukins</subject><subject>Macaca mulatta</subject><subject>Mice</subject><subject>Mice, Knockout</subject><subject>Muscle function</subject><subject>Muscle, Skeletal - immunology</subject><subject>Nutrient uptake</subject><subject>Osteoblastogenesis</subject><subject>Osteoblasts</subject><subject>Osteoblasts - immunology</subject><subject>Osteocalcin</subject><subject>Osteoclastogenesis</subject><subject>Physiology</subject><subject>Running</subject><subject>Scientific equipment industry</subject><subject>Signal Transduction - 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genetics</topic><topic>Interleukin-6 - immunology</topic><topic>Interleukins</topic><topic>Macaca mulatta</topic><topic>Mice</topic><topic>Mice, Knockout</topic><topic>Muscle function</topic><topic>Muscle, Skeletal - immunology</topic><topic>Nutrient uptake</topic><topic>Osteoblastogenesis</topic><topic>Osteoblasts</topic><topic>Osteoblasts - immunology</topic><topic>Osteocalcin</topic><topic>Osteoclastogenesis</topic><topic>Physiology</topic><topic>Running</topic><topic>Scientific equipment industry</topic><topic>Signal Transduction - genetics</topic><topic>Signal Transduction - immunology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chowdhury, Subrata</creatorcontrib><creatorcontrib>Schulz, Logan</creatorcontrib><creatorcontrib>Palmisano, Biagio</creatorcontrib><creatorcontrib>Singh, Parminder</creatorcontrib><creatorcontrib>Berger, Julian M</creatorcontrib><creatorcontrib>Yadav, Vijay K</creatorcontrib><creatorcontrib>Mera, Paula</creatorcontrib><creatorcontrib>Ellingsgaard, Helga</creatorcontrib><creatorcontrib>Hidalgo, Juan</creatorcontrib><creatorcontrib>Brüning, Jens</creatorcontrib><creatorcontrib>Karsenty, Gerard</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>ProQuest Nursing and Allied Health Journals</collection><collection>ProQuest_Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>ProQuest SciTech 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>ProQuest Central (Alumni)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>eLibrary</collection><collection>ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>ProQuest Biological Science Journals</collection><collection>Nursing & Allied Health Premium</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>SIRS Editorial</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of clinical investigation</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chowdhury, Subrata</au><au>Schulz, Logan</au><au>Palmisano, Biagio</au><au>Singh, Parminder</au><au>Berger, Julian M</au><au>Yadav, Vijay K</au><au>Mera, Paula</au><au>Ellingsgaard, Helga</au><au>Hidalgo, Juan</au><au>Brüning, Jens</au><au>Karsenty, Gerard</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Muscle-derived interleukin 6 increases exercise capacity by signaling in osteoblasts</atitle><jtitle>The Journal of clinical investigation</jtitle><addtitle>J Clin Invest</addtitle><date>2020-06-01</date><risdate>2020</risdate><volume>130</volume><issue>6</issue><spage>2888</spage><epage>2902</epage><pages>2888-2902</pages><issn>0021-9738</issn><eissn>1558-8238</eissn><abstract>Given the numerous health benefits of exercise, understanding how exercise capacity is regulated is a question of paramount importance. Circulating interleukin 6 (IL-6) levels surge during exercise and IL-6 favors exercise capacity. However, neither the cellular origin of circulating IL-6 during exercise nor the means by which this cytokine enhances exercise capacity has been formally established yet. Here we show through genetic means that the majority of circulating IL-6 detectable during exercise originates from muscle and that to increase exercise capacity, IL-6 must signal in osteoblasts to favor osteoclast differentiation and the release of bioactive osteocalcin in the general circulation. This explains why mice lacking the IL-6 receptor only in osteoblasts exhibit a deficit in exercise capacity of similar severity to the one seen in mice lacking muscle-derived IL-6 (mIL-6), and why this deficit is correctable by osteocalcin but not by IL-6. Furthermore, in agreement with the notion that IL-6 acts through osteocalcin, we demonstrate that mIL-6 promotes nutrient uptake and catabolism into myofibers during exercise in an osteocalcin-dependent manner. Finally, we show that the crosstalk between osteocalcin and IL-6 is conserved between rodents and humans. This study provides evidence that a muscle-bone-muscle endocrine axis is necessary to increase muscle function during exercise in rodents and humans.</abstract><cop>United States</cop><pub>American Society for Clinical Investigation</pub><pmid>32078586</pmid><doi>10.1172/JCI133572</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0003-0921-1122</orcidid><orcidid>https://orcid.org/0000-0002-1287-5256</orcidid><orcidid>https://orcid.org/0000-0001-8941-4637</orcidid><orcidid>https://orcid.org/0000-0002-2851-6805</orcidid><orcidid>https://orcid.org/0000-0002-9253-7627</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Antibodies Biomedical research Capacity Cytokines Exercise Experiments Female Fitness equipment Health insurance Interleukin 6 Interleukin 6 receptors Interleukin-6 - genetics Interleukin-6 - immunology Interleukins Macaca mulatta Mice Mice, Knockout Muscle function Muscle, Skeletal - immunology Nutrient uptake Osteoblastogenesis Osteoblasts Osteoblasts - immunology Osteocalcin Osteoclastogenesis Physiology Running Scientific equipment industry Signal Transduction - genetics Signal Transduction - immunology |
| title | Muscle-derived interleukin 6 increases exercise capacity by signaling in osteoblasts |
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