Synchronous deficits in cumulative muscle protein synthesis and ribosomal biogenesis underlie age‐related anabolic resistance to exercise in humans
Key points Resistance exercise training (RET) is one of the most effective strategies for preventing declines in skeletal muscle mass and strength with age. Hypertrophic responses to RET with age are diminished compared to younger individuals. In response to 6 weeks RET, we found blunted hypertrophi...
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| Veröffentlicht in: | The Journal of physiology 2016-12, Vol.594 (24), p.7399-7417 |
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| creator | Brook, Matthew S. Wilkinson, Daniel J. Mitchell, William K. Lund, Jonathan N. Phillips, Bethan E. Szewczyk, Nathaniel J. Greenhaff, Paul L. Smith, Kenneth Atherton, Philip J. |
| description | Key points
Resistance exercise training (RET) is one of the most effective strategies for preventing declines in skeletal muscle mass and strength with age.
Hypertrophic responses to RET with age are diminished compared to younger individuals.
In response to 6 weeks RET, we found blunted hypertrophic responses with age are underpinned by chronic deficits in long‐term muscle protein synthesis.
We show this is likely to be the result of multifactorial deficits in anabolic hormones and blunted translational efficiency and capacity.
These results provide great insight into age‐related exercise adaptations and provide a platform on which to devise appropriate nutritional and exercise interventions on a longer term basis.
Ageing is associated with impaired hypertrophic responses to resistance exercise training (RET). Here we investigated the aetiology of ‘anabolic resistance’ in older humans. Twenty healthy male individuals, 10 younger (Y; 23 ± 1 years) and 10 older (O; 69 ± 3 years), performed 6 weeks unilateral RET (6 × 8 repetitions, 75% of one repetition maximum (1‐RM), 3 times per week). After baseline bilateral vastus lateralis (VL) muscle biopsies, subjects consumed 150 ml D2O (70 atom%; thereafter 50 ml week−1), further bilateral VL muscle biopsies were taken at 3 and 6 weeks to quantify muscle protein synthesis (MPS) via gas chromatography–pyrolysis–isotope ratio mass spectrometry. After RET, 1‐RM increased in Y (+35 ± 4%) and O (+25 ± 3%; P |
| doi_str_mv | 10.1113/JP272857 |
| format | Article |
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Resistance exercise training (RET) is one of the most effective strategies for preventing declines in skeletal muscle mass and strength with age.
Hypertrophic responses to RET with age are diminished compared to younger individuals.
In response to 6 weeks RET, we found blunted hypertrophic responses with age are underpinned by chronic deficits in long‐term muscle protein synthesis.
We show this is likely to be the result of multifactorial deficits in anabolic hormones and blunted translational efficiency and capacity.
These results provide great insight into age‐related exercise adaptations and provide a platform on which to devise appropriate nutritional and exercise interventions on a longer term basis.
Ageing is associated with impaired hypertrophic responses to resistance exercise training (RET). Here we investigated the aetiology of ‘anabolic resistance’ in older humans. Twenty healthy male individuals, 10 younger (Y; 23 ± 1 years) and 10 older (O; 69 ± 3 years), performed 6 weeks unilateral RET (6 × 8 repetitions, 75% of one repetition maximum (1‐RM), 3 times per week). After baseline bilateral vastus lateralis (VL) muscle biopsies, subjects consumed 150 ml D2O (70 atom%; thereafter 50 ml week−1), further bilateral VL muscle biopsies were taken at 3 and 6 weeks to quantify muscle protein synthesis (MPS) via gas chromatography–pyrolysis–isotope ratio mass spectrometry. After RET, 1‐RM increased in Y (+35 ± 4%) and O (+25 ± 3%; P < 0.01), while MVC increased in Y (+21 ± 5%; P < 0.01) but not O (+6 ± 3%; not significant (NS)). In comparison to Y, O displayed blunted RET‐induced increases in muscle thickness (at 3 and 6 weeks, respectively, Y: +8 ± 1% and +11 ± 2%, P < 0.01; O: +2.6 ± 1% and +3.5 ± 2%, NS). While ‘basal’ longer term MPS was identical between Y and O (∼1.35 ± 0.1% day−1), MPS increased in response to RET only in Y (3 weeks, Y: 1.61 ± 0.1% day−1; O: 1.49 ± 0.1% day−1). Consistent with this, O exhibited inferior ribosomal biogenesis (RNA:DNA ratio and c‐MYC induction: Y: +4 ± 2 fold change; O: +1.9 ± 1 fold change), translational efficiency (S6K1 phosphorylation, Y: +10 ± 4 fold change; O: +4 ± 2 fold change) and anabolic hormone milieu (testosterone, Y: 367 ± 19; O: 274 ± 19 ng dl−1 (all P < 0.05). Anabolic resistance is thus multifactorial.
Key points
Resistance exercise training (RET) is one of the most effective strategies for preventing declines in skeletal muscle mass and strength with age.
Hypertrophic responses to RET with age are diminished compared to younger individuals.
In response to 6 weeks RET, we found blunted hypertrophic responses with age are underpinned by chronic deficits in long‐term muscle protein synthesis.
We show this is likely to be the result of multifactorial deficits in anabolic hormones and blunted translational efficiency and capacity.
These results provide great insight into age‐related exercise adaptations and provide a platform on which to devise appropriate nutritional and exercise interventions on a longer term basis.</description><identifier>ISSN: 0022-3751</identifier><identifier>EISSN: 1469-7793</identifier><identifier>DOI: 10.1113/JP272857</identifier><identifier>PMID: 27654940</identifier><identifier>CODEN: JPHYA7</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Adult ; Aged ; ageing ; Aging - physiology ; DNA - metabolism ; exercise ; Exercise Physiology ; Humans ; hypertrophy ; Hypertrophy - metabolism ; Male ; Muscle ; Muscle Physiology ; Muscle Proteins - biosynthesis ; Protein Biosynthesis ; protein synthesis ; Quadriceps Muscle - metabolism ; Quadriceps Muscle - pathology ; Research Paper ; Resistance Training ; ribosomal biogenesis ; Ribosomes - metabolism ; RNA - metabolism ; signalling ; stable isotope ; Young Adult</subject><ispartof>The Journal of physiology, 2016-12, Vol.594 (24), p.7399-7417</ispartof><rights>2016 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society</rights><rights>2016 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.</rights><rights>Journal compilation © 2016 The Physiological Society</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5775-1b1ebbe671ae43fd229714ff7d764971f1c9b6fe61f0a2eab2381a180767bd3</citedby><cites>FETCH-LOGICAL-c5775-1b1ebbe671ae43fd229714ff7d764971f1c9b6fe61f0a2eab2381a180767bd3</cites><orcidid>0000-0003-4425-9746</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/PMC5157077/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5157077/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,1411,1427,27901,27902,45550,45551,46384,46808,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27654940$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Brook, Matthew S.</creatorcontrib><creatorcontrib>Wilkinson, Daniel J.</creatorcontrib><creatorcontrib>Mitchell, William K.</creatorcontrib><creatorcontrib>Lund, Jonathan N.</creatorcontrib><creatorcontrib>Phillips, Bethan E.</creatorcontrib><creatorcontrib>Szewczyk, Nathaniel J.</creatorcontrib><creatorcontrib>Greenhaff, Paul L.</creatorcontrib><creatorcontrib>Smith, Kenneth</creatorcontrib><creatorcontrib>Atherton, Philip J.</creatorcontrib><title>Synchronous deficits in cumulative muscle protein synthesis and ribosomal biogenesis underlie age‐related anabolic resistance to exercise in humans</title><title>The Journal of physiology</title><addtitle>J Physiol</addtitle><description>Key points
Resistance exercise training (RET) is one of the most effective strategies for preventing declines in skeletal muscle mass and strength with age.
Hypertrophic responses to RET with age are diminished compared to younger individuals.
In response to 6 weeks RET, we found blunted hypertrophic responses with age are underpinned by chronic deficits in long‐term muscle protein synthesis.
We show this is likely to be the result of multifactorial deficits in anabolic hormones and blunted translational efficiency and capacity.
These results provide great insight into age‐related exercise adaptations and provide a platform on which to devise appropriate nutritional and exercise interventions on a longer term basis.
Ageing is associated with impaired hypertrophic responses to resistance exercise training (RET). Here we investigated the aetiology of ‘anabolic resistance’ in older humans. Twenty healthy male individuals, 10 younger (Y; 23 ± 1 years) and 10 older (O; 69 ± 3 years), performed 6 weeks unilateral RET (6 × 8 repetitions, 75% of one repetition maximum (1‐RM), 3 times per week). After baseline bilateral vastus lateralis (VL) muscle biopsies, subjects consumed 150 ml D2O (70 atom%; thereafter 50 ml week−1), further bilateral VL muscle biopsies were taken at 3 and 6 weeks to quantify muscle protein synthesis (MPS) via gas chromatography–pyrolysis–isotope ratio mass spectrometry. After RET, 1‐RM increased in Y (+35 ± 4%) and O (+25 ± 3%; P < 0.01), while MVC increased in Y (+21 ± 5%; P < 0.01) but not O (+6 ± 3%; not significant (NS)). In comparison to Y, O displayed blunted RET‐induced increases in muscle thickness (at 3 and 6 weeks, respectively, Y: +8 ± 1% and +11 ± 2%, P < 0.01; O: +2.6 ± 1% and +3.5 ± 2%, NS). While ‘basal’ longer term MPS was identical between Y and O (∼1.35 ± 0.1% day−1), MPS increased in response to RET only in Y (3 weeks, Y: 1.61 ± 0.1% day−1; O: 1.49 ± 0.1% day−1). Consistent with this, O exhibited inferior ribosomal biogenesis (RNA:DNA ratio and c‐MYC induction: Y: +4 ± 2 fold change; O: +1.9 ± 1 fold change), translational efficiency (S6K1 phosphorylation, Y: +10 ± 4 fold change; O: +4 ± 2 fold change) and anabolic hormone milieu (testosterone, Y: 367 ± 19; O: 274 ± 19 ng dl−1 (all P < 0.05). Anabolic resistance is thus multifactorial.
Key points
Resistance exercise training (RET) is one of the most effective strategies for preventing declines in skeletal muscle mass and strength with age.
Hypertrophic responses to RET with age are diminished compared to younger individuals.
In response to 6 weeks RET, we found blunted hypertrophic responses with age are underpinned by chronic deficits in long‐term muscle protein synthesis.
We show this is likely to be the result of multifactorial deficits in anabolic hormones and blunted translational efficiency and capacity.
These results provide great insight into age‐related exercise adaptations and provide a platform on which to devise appropriate nutritional and exercise interventions on a longer term basis.</description><subject>Adult</subject><subject>Aged</subject><subject>ageing</subject><subject>Aging - physiology</subject><subject>DNA - metabolism</subject><subject>exercise</subject><subject>Exercise Physiology</subject><subject>Humans</subject><subject>hypertrophy</subject><subject>Hypertrophy - metabolism</subject><subject>Male</subject><subject>Muscle</subject><subject>Muscle Physiology</subject><subject>Muscle Proteins - biosynthesis</subject><subject>Protein Biosynthesis</subject><subject>protein synthesis</subject><subject>Quadriceps Muscle - metabolism</subject><subject>Quadriceps Muscle - pathology</subject><subject>Research Paper</subject><subject>Resistance Training</subject><subject>ribosomal biogenesis</subject><subject>Ribosomes - metabolism</subject><subject>RNA - metabolism</subject><subject>signalling</subject><subject>stable isotope</subject><subject>Young Adult</subject><issn>0022-3751</issn><issn>1469-7793</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNqNkttqFTEUhgdR7LYKPoEEvOnNrlnJZDJzI0jxVAoW2vuQZNbsnZJJtslM677rI3jjC_okZtuDBxC8SuD_-JK1-KvqOdBDAOCvjk-ZZK2QD6oF1E23lLLjD6sFpYwtuRSwVz3J-YJS4LTrHld7TDai7mq6qL6dbYNdpxjinEmPg7NuysQFYudx9npyl0jGOVuPZJPihCXJ2zCtMbtMdOhJcibmOGpPjIsrDD-DOfSYvEOiV_j9-mvCYsK-8NpE7yxJO2rSwSKZIsEvmKzLuHt2PY865KfVo0H7jM9uz_3q7N3b86MPy5NP7z8evTlZWiGlWIIBNAYbCRprPvSMdRLqYZC9bOpyHcB2phmwgYFqhtow3oKGlspGmp7vV69vrJvZjNhbDFPSXm2SG3Xaqqid-jMJbq1W8VIJEJJKWQQHt4IUP8-YJzW6bNF7HbDsU0ErBJW8afn_oMBkLTgt6Mu_0Is4p1D2UKi6lSA6yn4JbYo5Jxzu_w1U7Uqh7kpR0Be_z3kP3rWgAIc3wJXzuP2nSJ0fnwKjTPAfraPEww</recordid><startdate>20161215</startdate><enddate>20161215</enddate><creator>Brook, Matthew S.</creator><creator>Wilkinson, Daniel J.</creator><creator>Mitchell, William K.</creator><creator>Lund, Jonathan N.</creator><creator>Phillips, Bethan E.</creator><creator>Szewczyk, Nathaniel J.</creator><creator>Greenhaff, Paul L.</creator><creator>Smith, Kenneth</creator><creator>Atherton, Philip J.</creator><general>Wiley Subscription Services, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</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><scope>7TM</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-4425-9746</orcidid></search><sort><creationdate>20161215</creationdate><title>Synchronous deficits in cumulative muscle protein synthesis and ribosomal biogenesis underlie age‐related anabolic resistance to exercise in humans</title><author>Brook, Matthew S. ; Wilkinson, Daniel J. ; Mitchell, William K. ; Lund, Jonathan N. ; Phillips, Bethan E. ; Szewczyk, Nathaniel J. ; Greenhaff, Paul L. ; Smith, Kenneth ; Atherton, Philip J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5775-1b1ebbe671ae43fd229714ff7d764971f1c9b6fe61f0a2eab2381a180767bd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Adult</topic><topic>Aged</topic><topic>ageing</topic><topic>Aging - physiology</topic><topic>DNA - metabolism</topic><topic>exercise</topic><topic>Exercise Physiology</topic><topic>Humans</topic><topic>hypertrophy</topic><topic>Hypertrophy - metabolism</topic><topic>Male</topic><topic>Muscle</topic><topic>Muscle Physiology</topic><topic>Muscle Proteins - biosynthesis</topic><topic>Protein Biosynthesis</topic><topic>protein synthesis</topic><topic>Quadriceps Muscle - metabolism</topic><topic>Quadriceps Muscle - pathology</topic><topic>Research Paper</topic><topic>Resistance Training</topic><topic>ribosomal biogenesis</topic><topic>Ribosomes - metabolism</topic><topic>RNA - metabolism</topic><topic>signalling</topic><topic>stable isotope</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Brook, Matthew S.</creatorcontrib><creatorcontrib>Wilkinson, Daniel J.</creatorcontrib><creatorcontrib>Mitchell, William K.</creatorcontrib><creatorcontrib>Lund, Jonathan N.</creatorcontrib><creatorcontrib>Phillips, Bethan E.</creatorcontrib><creatorcontrib>Szewczyk, Nathaniel J.</creatorcontrib><creatorcontrib>Greenhaff, Paul L.</creatorcontrib><creatorcontrib>Smith, Kenneth</creatorcontrib><creatorcontrib>Atherton, Philip J.</creatorcontrib><collection>Wiley Online Library Open Access</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><collection>Nucleic Acids Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Brook, Matthew S.</au><au>Wilkinson, Daniel J.</au><au>Mitchell, William K.</au><au>Lund, Jonathan N.</au><au>Phillips, Bethan E.</au><au>Szewczyk, Nathaniel J.</au><au>Greenhaff, Paul L.</au><au>Smith, Kenneth</au><au>Atherton, Philip J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Synchronous deficits in cumulative muscle protein synthesis and ribosomal biogenesis underlie age‐related anabolic resistance to exercise in humans</atitle><jtitle>The Journal of physiology</jtitle><addtitle>J Physiol</addtitle><date>2016-12-15</date><risdate>2016</risdate><volume>594</volume><issue>24</issue><spage>7399</spage><epage>7417</epage><pages>7399-7417</pages><issn>0022-3751</issn><eissn>1469-7793</eissn><coden>JPHYA7</coden><abstract>Key points
Resistance exercise training (RET) is one of the most effective strategies for preventing declines in skeletal muscle mass and strength with age.
Hypertrophic responses to RET with age are diminished compared to younger individuals.
In response to 6 weeks RET, we found blunted hypertrophic responses with age are underpinned by chronic deficits in long‐term muscle protein synthesis.
We show this is likely to be the result of multifactorial deficits in anabolic hormones and blunted translational efficiency and capacity.
These results provide great insight into age‐related exercise adaptations and provide a platform on which to devise appropriate nutritional and exercise interventions on a longer term basis.
Ageing is associated with impaired hypertrophic responses to resistance exercise training (RET). Here we investigated the aetiology of ‘anabolic resistance’ in older humans. Twenty healthy male individuals, 10 younger (Y; 23 ± 1 years) and 10 older (O; 69 ± 3 years), performed 6 weeks unilateral RET (6 × 8 repetitions, 75% of one repetition maximum (1‐RM), 3 times per week). After baseline bilateral vastus lateralis (VL) muscle biopsies, subjects consumed 150 ml D2O (70 atom%; thereafter 50 ml week−1), further bilateral VL muscle biopsies were taken at 3 and 6 weeks to quantify muscle protein synthesis (MPS) via gas chromatography–pyrolysis–isotope ratio mass spectrometry. After RET, 1‐RM increased in Y (+35 ± 4%) and O (+25 ± 3%; P < 0.01), while MVC increased in Y (+21 ± 5%; P < 0.01) but not O (+6 ± 3%; not significant (NS)). In comparison to Y, O displayed blunted RET‐induced increases in muscle thickness (at 3 and 6 weeks, respectively, Y: +8 ± 1% and +11 ± 2%, P < 0.01; O: +2.6 ± 1% and +3.5 ± 2%, NS). While ‘basal’ longer term MPS was identical between Y and O (∼1.35 ± 0.1% day−1), MPS increased in response to RET only in Y (3 weeks, Y: 1.61 ± 0.1% day−1; O: 1.49 ± 0.1% day−1). Consistent with this, O exhibited inferior ribosomal biogenesis (RNA:DNA ratio and c‐MYC induction: Y: +4 ± 2 fold change; O: +1.9 ± 1 fold change), translational efficiency (S6K1 phosphorylation, Y: +10 ± 4 fold change; O: +4 ± 2 fold change) and anabolic hormone milieu (testosterone, Y: 367 ± 19; O: 274 ± 19 ng dl−1 (all P < 0.05). Anabolic resistance is thus multifactorial.
Key points
Resistance exercise training (RET) is one of the most effective strategies for preventing declines in skeletal muscle mass and strength with age.
Hypertrophic responses to RET with age are diminished compared to younger individuals.
In response to 6 weeks RET, we found blunted hypertrophic responses with age are underpinned by chronic deficits in long‐term muscle protein synthesis.
We show this is likely to be the result of multifactorial deficits in anabolic hormones and blunted translational efficiency and capacity.
These results provide great insight into age‐related exercise adaptations and provide a platform on which to devise appropriate nutritional and exercise interventions on a longer term basis.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>27654940</pmid><doi>10.1113/JP272857</doi><tpages>19</tpages><orcidid>https://orcid.org/0000-0003-4425-9746</orcidid><oa>free_for_read</oa></addata></record> |
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| source | Wiley Free Content; MEDLINE; Wiley Online Library Journals Frontfile Complete; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central |
| subjects | Adult Aged ageing Aging - physiology DNA - metabolism exercise Exercise Physiology Humans hypertrophy Hypertrophy - metabolism Male Muscle Muscle Physiology Muscle Proteins - biosynthesis Protein Biosynthesis protein synthesis Quadriceps Muscle - metabolism Quadriceps Muscle - pathology Research Paper Resistance Training ribosomal biogenesis Ribosomes - metabolism RNA - metabolism signalling stable isotope Young Adult |
| title | Synchronous deficits in cumulative muscle protein synthesis and ribosomal biogenesis underlie age‐related anabolic resistance to exercise in humans |
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