Mass Spectrometry-Based Multiomics Identifies Metabolic Signatures of Sarcopenia in Rhesus Monkey Skeletal Muscle
Sarcopenia is a progressive disorder characterized by age-related loss of skeletal muscle mass and function. Although significant progress has been made over the years to identify the molecular determinants of sarcopenia, the precise mechanisms underlying the age-related loss of contractile function...
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Veröffentlicht in: | Journal of proteome research 2024-08, Vol.23 (8), p.2845-2856 |
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creator | Pergande, Melissa R. Osterbauer, Katie J. Buck, Kevin M. Roberts, David S. Wood, Nina N. Balasubramanian, Priya Mann, Morgan W. Rossler, Kalina J. Diffee, Gary M. Colman, Ricki J. Anderson, Rozalyn M. Ge, Ying |
description | Sarcopenia is a progressive disorder characterized by age-related loss of skeletal muscle mass and function. Although significant progress has been made over the years to identify the molecular determinants of sarcopenia, the precise mechanisms underlying the age-related loss of contractile function remains unclear. Advances in “omics” technologies, including mass spectrometry-based proteomic and metabolomic analyses, offer great opportunities to better understand sarcopenia. Herein, we performed mass spectrometry-based analyses of the vastus lateralis from young, middle-aged, and older rhesus monkeys to identify molecular signatures of sarcopenia. In our proteomic analysis, we identified proteins that change with age, including those involved in adenosine triphosphate and adenosine monophosphate metabolism as well as fatty acid beta oxidation. In our untargeted metabolomic analysis, we identified metabolites that changed with age largely related to energy metabolism including fatty acid beta oxidation. Pathway analysis of age-responsive proteins and metabolites revealed changes in muscle structure and contraction as well as lipid, carbohydrate, and purine metabolism. Together, this study discovers new metabolic signatures and offers new insights into the molecular mechanisms underlying sarcopenia for the evaluation and monitoring of a therapeutic treatment of sarcopenia. |
doi_str_mv | 10.1021/acs.jproteome.3c00474 |
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Although significant progress has been made over the years to identify the molecular determinants of sarcopenia, the precise mechanisms underlying the age-related loss of contractile function remains unclear. Advances in “omics” technologies, including mass spectrometry-based proteomic and metabolomic analyses, offer great opportunities to better understand sarcopenia. Herein, we performed mass spectrometry-based analyses of the vastus lateralis from young, middle-aged, and older rhesus monkeys to identify molecular signatures of sarcopenia. In our proteomic analysis, we identified proteins that change with age, including those involved in adenosine triphosphate and adenosine monophosphate metabolism as well as fatty acid beta oxidation. In our untargeted metabolomic analysis, we identified metabolites that changed with age largely related to energy metabolism including fatty acid beta oxidation. Pathway analysis of age-responsive proteins and metabolites revealed changes in muscle structure and contraction as well as lipid, carbohydrate, and purine metabolism. Together, this study discovers new metabolic signatures and offers new insights into the molecular mechanisms underlying sarcopenia for the evaluation and monitoring of a therapeutic treatment of sarcopenia.</description><identifier>ISSN: 1535-3893</identifier><identifier>ISSN: 1535-3907</identifier><identifier>EISSN: 1535-3907</identifier><identifier>DOI: 10.1021/acs.jproteome.3c00474</identifier><identifier>PMID: 37991985</identifier><language>eng</language><publisher>United States: American Chemical Society</publisher><subject>adenosine monophosphate ; adenosine triphosphate ; Aging - metabolism ; Animals ; beta oxidation ; carbohydrates ; Energy Metabolism ; fatty acids ; Fatty Acids - metabolism ; Macaca mulatta ; Male ; mass spectrometry ; Mass Spectrometry - methods ; metabolites ; Metabolome ; metabolomics ; Metabolomics - methods ; multiomics ; Multiomics - methods ; Muscle Proteins - metabolism ; Muscle, Skeletal - metabolism ; muscles ; proteome ; proteomics ; Proteomics - methods ; sarcopenia ; Sarcopenia - metabolism ; Sarcopenia - pathology ; skeletal muscle ; therapeutics</subject><ispartof>Journal of proteome research, 2024-08, Vol.23 (8), p.2845-2856</ispartof><rights>2023 American Chemical Society</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-a332t-c9785cc7348e42d6b89cc3d0cdaf7aea3a7cadb1df73dde211c6de410fc5cc893</cites><orcidid>0000-0001-5211-6812 ; 0000-0001-6623-9522 ; 0000-0002-0478-4987 ; 0000-0003-1197-4057 ; 0009-0000-5632-8628 ; 0000-0003-0353-1774</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://pubs.acs.org/doi/pdf/10.1021/acs.jproteome.3c00474$$EPDF$$P50$$Gacs$$H</linktopdf><linktohtml>$$Uhttps://pubs.acs.org/doi/10.1021/acs.jproteome.3c00474$$EHTML$$P50$$Gacs$$H</linktohtml><link.rule.ids>314,776,780,2752,27053,27901,27902,56713,56763</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37991985$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Pergande, Melissa R.</creatorcontrib><creatorcontrib>Osterbauer, Katie J.</creatorcontrib><creatorcontrib>Buck, Kevin M.</creatorcontrib><creatorcontrib>Roberts, David S.</creatorcontrib><creatorcontrib>Wood, Nina N.</creatorcontrib><creatorcontrib>Balasubramanian, Priya</creatorcontrib><creatorcontrib>Mann, Morgan W.</creatorcontrib><creatorcontrib>Rossler, Kalina J.</creatorcontrib><creatorcontrib>Diffee, Gary M.</creatorcontrib><creatorcontrib>Colman, Ricki J.</creatorcontrib><creatorcontrib>Anderson, Rozalyn M.</creatorcontrib><creatorcontrib>Ge, Ying</creatorcontrib><title>Mass Spectrometry-Based Multiomics Identifies Metabolic Signatures of Sarcopenia in Rhesus Monkey Skeletal Muscle</title><title>Journal of proteome research</title><addtitle>J. Proteome Res</addtitle><description>Sarcopenia is a progressive disorder characterized by age-related loss of skeletal muscle mass and function. Although significant progress has been made over the years to identify the molecular determinants of sarcopenia, the precise mechanisms underlying the age-related loss of contractile function remains unclear. Advances in “omics” technologies, including mass spectrometry-based proteomic and metabolomic analyses, offer great opportunities to better understand sarcopenia. Herein, we performed mass spectrometry-based analyses of the vastus lateralis from young, middle-aged, and older rhesus monkeys to identify molecular signatures of sarcopenia. In our proteomic analysis, we identified proteins that change with age, including those involved in adenosine triphosphate and adenosine monophosphate metabolism as well as fatty acid beta oxidation. In our untargeted metabolomic analysis, we identified metabolites that changed with age largely related to energy metabolism including fatty acid beta oxidation. Pathway analysis of age-responsive proteins and metabolites revealed changes in muscle structure and contraction as well as lipid, carbohydrate, and purine metabolism. Together, this study discovers new metabolic signatures and offers new insights into the molecular mechanisms underlying sarcopenia for the evaluation and monitoring of a therapeutic treatment of sarcopenia.</description><subject>adenosine monophosphate</subject><subject>adenosine triphosphate</subject><subject>Aging - metabolism</subject><subject>Animals</subject><subject>beta oxidation</subject><subject>carbohydrates</subject><subject>Energy Metabolism</subject><subject>fatty acids</subject><subject>Fatty Acids - metabolism</subject><subject>Macaca mulatta</subject><subject>Male</subject><subject>mass spectrometry</subject><subject>Mass Spectrometry - methods</subject><subject>metabolites</subject><subject>Metabolome</subject><subject>metabolomics</subject><subject>Metabolomics - methods</subject><subject>multiomics</subject><subject>Multiomics - methods</subject><subject>Muscle Proteins - metabolism</subject><subject>Muscle, Skeletal - metabolism</subject><subject>muscles</subject><subject>proteome</subject><subject>proteomics</subject><subject>Proteomics - methods</subject><subject>sarcopenia</subject><subject>Sarcopenia - metabolism</subject><subject>Sarcopenia - pathology</subject><subject>skeletal muscle</subject><subject>therapeutics</subject><issn>1535-3893</issn><issn>1535-3907</issn><issn>1535-3907</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkUtPwzAQhC0Eorx-AshHLil2nNTxERCPSq2QKJwjd70BlyQutnPov8fQwpWTV9Y3s9oZQs45G3OW8ysNYbxaexfRdTgWwFghiz1yxEtRZkIxuf87V0qMyHEIK8Z4KZk4JCMhleKqKo_I51yHQBdrhOiTUfSb7EYHNHQ-tNG6zkKgU4N9tI3FQOcY9dK1FujCvvU6Dj59uoYutAe3xt5qanv6_I5hSLDrP3BDFx_YJlmbLAO0eEoOGt0GPNu9J-T1_u7l9jGbPT1Mb69nmRYijxkoWZUAUhQVFrmZLCsFIAwDoxupUQstQZslN40UxmDOOUwMFpw1kGTp5hNyufVNIX0OGGLd2QDYtrpHN4RapHQkK_mk_BfNK5WrQqoJT2i5RcG7EDw29drbTvtNzVn9XUydiqn_iql3xSTdxW7FsOzQ_Kl-m0gA3wI_ejf4PoXzj-kXaLShfg</recordid><startdate>20240802</startdate><enddate>20240802</enddate><creator>Pergande, Melissa R.</creator><creator>Osterbauer, Katie J.</creator><creator>Buck, Kevin M.</creator><creator>Roberts, David S.</creator><creator>Wood, Nina N.</creator><creator>Balasubramanian, Priya</creator><creator>Mann, Morgan W.</creator><creator>Rossler, Kalina J.</creator><creator>Diffee, Gary M.</creator><creator>Colman, Ricki J.</creator><creator>Anderson, Rozalyn M.</creator><creator>Ge, Ying</creator><general>American Chemical Society</general><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>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0001-5211-6812</orcidid><orcidid>https://orcid.org/0000-0001-6623-9522</orcidid><orcidid>https://orcid.org/0000-0002-0478-4987</orcidid><orcidid>https://orcid.org/0000-0003-1197-4057</orcidid><orcidid>https://orcid.org/0009-0000-5632-8628</orcidid><orcidid>https://orcid.org/0000-0003-0353-1774</orcidid></search><sort><creationdate>20240802</creationdate><title>Mass Spectrometry-Based Multiomics Identifies Metabolic Signatures of Sarcopenia in Rhesus Monkey Skeletal Muscle</title><author>Pergande, Melissa R. ; Osterbauer, Katie J. ; Buck, Kevin M. ; Roberts, David S. ; Wood, Nina N. ; Balasubramanian, Priya ; Mann, Morgan W. ; Rossler, Kalina J. ; Diffee, Gary M. ; Colman, Ricki J. ; Anderson, Rozalyn M. ; Ge, Ying</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a332t-c9785cc7348e42d6b89cc3d0cdaf7aea3a7cadb1df73dde211c6de410fc5cc893</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>adenosine monophosphate</topic><topic>adenosine triphosphate</topic><topic>Aging - metabolism</topic><topic>Animals</topic><topic>beta oxidation</topic><topic>carbohydrates</topic><topic>Energy Metabolism</topic><topic>fatty acids</topic><topic>Fatty Acids - metabolism</topic><topic>Macaca mulatta</topic><topic>Male</topic><topic>mass spectrometry</topic><topic>Mass Spectrometry - methods</topic><topic>metabolites</topic><topic>Metabolome</topic><topic>metabolomics</topic><topic>Metabolomics - methods</topic><topic>multiomics</topic><topic>Multiomics - methods</topic><topic>Muscle Proteins - metabolism</topic><topic>Muscle, Skeletal - metabolism</topic><topic>muscles</topic><topic>proteome</topic><topic>proteomics</topic><topic>Proteomics - methods</topic><topic>sarcopenia</topic><topic>Sarcopenia - metabolism</topic><topic>Sarcopenia - pathology</topic><topic>skeletal muscle</topic><topic>therapeutics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Pergande, Melissa R.</creatorcontrib><creatorcontrib>Osterbauer, Katie J.</creatorcontrib><creatorcontrib>Buck, Kevin M.</creatorcontrib><creatorcontrib>Roberts, David S.</creatorcontrib><creatorcontrib>Wood, Nina N.</creatorcontrib><creatorcontrib>Balasubramanian, Priya</creatorcontrib><creatorcontrib>Mann, Morgan W.</creatorcontrib><creatorcontrib>Rossler, Kalina J.</creatorcontrib><creatorcontrib>Diffee, Gary M.</creatorcontrib><creatorcontrib>Colman, Ricki J.</creatorcontrib><creatorcontrib>Anderson, Rozalyn M.</creatorcontrib><creatorcontrib>Ge, Ying</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Journal of proteome research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Pergande, Melissa R.</au><au>Osterbauer, Katie J.</au><au>Buck, Kevin M.</au><au>Roberts, David S.</au><au>Wood, Nina N.</au><au>Balasubramanian, Priya</au><au>Mann, Morgan W.</au><au>Rossler, Kalina J.</au><au>Diffee, Gary M.</au><au>Colman, Ricki J.</au><au>Anderson, Rozalyn M.</au><au>Ge, Ying</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Mass Spectrometry-Based Multiomics Identifies Metabolic Signatures of Sarcopenia in Rhesus Monkey Skeletal Muscle</atitle><jtitle>Journal of proteome research</jtitle><addtitle>J. Proteome Res</addtitle><date>2024-08-02</date><risdate>2024</risdate><volume>23</volume><issue>8</issue><spage>2845</spage><epage>2856</epage><pages>2845-2856</pages><issn>1535-3893</issn><issn>1535-3907</issn><eissn>1535-3907</eissn><abstract>Sarcopenia is a progressive disorder characterized by age-related loss of skeletal muscle mass and function. Although significant progress has been made over the years to identify the molecular determinants of sarcopenia, the precise mechanisms underlying the age-related loss of contractile function remains unclear. Advances in “omics” technologies, including mass spectrometry-based proteomic and metabolomic analyses, offer great opportunities to better understand sarcopenia. Herein, we performed mass spectrometry-based analyses of the vastus lateralis from young, middle-aged, and older rhesus monkeys to identify molecular signatures of sarcopenia. In our proteomic analysis, we identified proteins that change with age, including those involved in adenosine triphosphate and adenosine monophosphate metabolism as well as fatty acid beta oxidation. In our untargeted metabolomic analysis, we identified metabolites that changed with age largely related to energy metabolism including fatty acid beta oxidation. Pathway analysis of age-responsive proteins and metabolites revealed changes in muscle structure and contraction as well as lipid, carbohydrate, and purine metabolism. Together, this study discovers new metabolic signatures and offers new insights into the molecular mechanisms underlying sarcopenia for the evaluation and monitoring of a therapeutic treatment of sarcopenia.</abstract><cop>United States</cop><pub>American Chemical Society</pub><pmid>37991985</pmid><doi>10.1021/acs.jproteome.3c00474</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0001-5211-6812</orcidid><orcidid>https://orcid.org/0000-0001-6623-9522</orcidid><orcidid>https://orcid.org/0000-0002-0478-4987</orcidid><orcidid>https://orcid.org/0000-0003-1197-4057</orcidid><orcidid>https://orcid.org/0009-0000-5632-8628</orcidid><orcidid>https://orcid.org/0000-0003-0353-1774</orcidid></addata></record> |
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subjects | adenosine monophosphate adenosine triphosphate Aging - metabolism Animals beta oxidation carbohydrates Energy Metabolism fatty acids Fatty Acids - metabolism Macaca mulatta Male mass spectrometry Mass Spectrometry - methods metabolites Metabolome metabolomics Metabolomics - methods multiomics Multiomics - methods Muscle Proteins - metabolism Muscle, Skeletal - metabolism muscles proteome proteomics Proteomics - methods sarcopenia Sarcopenia - metabolism Sarcopenia - pathology skeletal muscle therapeutics |
title | Mass Spectrometry-Based Multiomics Identifies Metabolic Signatures of Sarcopenia in Rhesus Monkey Skeletal Muscle |
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