Massage as a mechanotherapy promotes skeletal muscle protein and ribosomal turnover but does not mitigate muscle atrophy during disuse in adult rats

Aim Interventions that decrease atrophy during disuse are desperately needed to maintain muscle mass. We recently found that massage as a mechanotherapy can improve muscle regrowth following disuse atrophy. Therefore, we aimed to determine if massage has similar anabolic effects when applied during...

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Veröffentlicht in:ACTA PHYSIOLOGICA 2020-07, Vol.229 (3), p.e13460-n/a, Article 13460
Hauptverfasser: Lawrence, Marcus M., Van Pelt, Douglas W., Confides, Amy L., Hunt, Emily R., Hettinger, Zachary R., Laurin, Jaime L., Reid, Justin J., Peelor, Frederick F., Butterfield, Timothy A., Dupont‐Versteegden, Esther E., Miller, Benjamin F.
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container_issue 3
container_start_page e13460
container_title ACTA PHYSIOLOGICA
container_volume 229
creator Lawrence, Marcus M.
Van Pelt, Douglas W.
Confides, Amy L.
Hunt, Emily R.
Hettinger, Zachary R.
Laurin, Jaime L.
Reid, Justin J.
Peelor, Frederick F.
Butterfield, Timothy A.
Dupont‐Versteegden, Esther E.
Miller, Benjamin F.
description Aim Interventions that decrease atrophy during disuse are desperately needed to maintain muscle mass. We recently found that massage as a mechanotherapy can improve muscle regrowth following disuse atrophy. Therefore, we aimed to determine if massage has similar anabolic effects when applied during normal weight bearing conditions (WB) or during atrophy induced by hindlimb suspension (HS) in adult rats. Methods Adult (10 months) male Fischer344‐Brown Norway rats underwent either hindlimb suspension (HS, n = 8) or normal WB (WB, n = 8) for 7 days. Massage was applied using cyclic compressive loading (CCL) in WB (WBM, n = 9) or HS rats (HSM, n = 9) and included four 30‐minute bouts of CCL applied to gastrocnemius muscle every other day. Results Massage had no effect on any anabolic parameter measured under WB conditions (WBM). In contrast, massage during HS (HSM) stimulated protein turnover, but did not mitigate muscle atrophy. Atrophy from HS was caused by both lowered protein synthesis and higher degradation. HS and HSM had lowered total RNA compared with WB and this was the result of significantly higher ribosome degradation in HS that was attenuated in HSM, without differences in ribosomal biogenesis. Also, massage increased protein turnover in the non‐massaged contralateral limb during HS. Finally, we determined that total RNA degradation primarily dictates loss of muscle ribosomal content during disuse atrophy. Conclusion We conclude that massage is an effective mechanotherapy to impact protein turnover during muscle disuse in both the massaged and non‐massaged contralateral muscle, but it does not attenuate the loss of muscle mass.
doi_str_mv 10.1111/apha.13460
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We recently found that massage as a mechanotherapy can improve muscle regrowth following disuse atrophy. Therefore, we aimed to determine if massage has similar anabolic effects when applied during normal weight bearing conditions (WB) or during atrophy induced by hindlimb suspension (HS) in adult rats. Methods Adult (10 months) male Fischer344‐Brown Norway rats underwent either hindlimb suspension (HS, n = 8) or normal WB (WB, n = 8) for 7 days. Massage was applied using cyclic compressive loading (CCL) in WB (WBM, n = 9) or HS rats (HSM, n = 9) and included four 30‐minute bouts of CCL applied to gastrocnemius muscle every other day. Results Massage had no effect on any anabolic parameter measured under WB conditions (WBM). In contrast, massage during HS (HSM) stimulated protein turnover, but did not mitigate muscle atrophy. Atrophy from HS was caused by both lowered protein synthesis and higher degradation. HS and HSM had lowered total RNA compared with WB and this was the result of significantly higher ribosome degradation in HS that was attenuated in HSM, without differences in ribosomal biogenesis. Also, massage increased protein turnover in the non‐massaged contralateral limb during HS. Finally, we determined that total RNA degradation primarily dictates loss of muscle ribosomal content during disuse atrophy. Conclusion We conclude that massage is an effective mechanotherapy to impact protein turnover during muscle disuse in both the massaged and non‐massaged contralateral muscle, but it does not attenuate the loss of muscle mass.</description><identifier>ISSN: 1748-1708</identifier><identifier>ISSN: 1748-1716</identifier><identifier>EISSN: 1748-1716</identifier><identifier>DOI: 10.1111/apha.13460</identifier><identifier>PMID: 32125770</identifier><language>eng</language><publisher>HOBOKEN: Wiley</publisher><subject>Animals ; Atrophy ; cross‐over effect ; Degradation ; disuse atrophy ; Gastrocnemius muscle ; Hindlimb Suspension ; Life Sciences &amp; Biomedicine ; Male ; Massage ; Muscle Proteins - biosynthesis ; Muscle, Skeletal - pathology ; Muscular Atrophy - pathology ; Muscular Atrophy - prevention &amp; control ; Physiology ; Protein biosynthesis ; Protein turnover ; Proteins ; Rats ; Rats, Inbred BN ; Rats, Inbred F344 ; Ribonucleic acid ; ribosome biogenesis ; ribosome turnover ; Ribosomes - metabolism ; RNA ; Rodents ; Science &amp; Technology ; Skeletal muscle</subject><ispartof>ACTA PHYSIOLOGICA, 2020-07, Vol.229 (3), p.e13460-n/a, Article 13460</ispartof><rights>2020 Scandinavian Physiological Society. 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We recently found that massage as a mechanotherapy can improve muscle regrowth following disuse atrophy. Therefore, we aimed to determine if massage has similar anabolic effects when applied during normal weight bearing conditions (WB) or during atrophy induced by hindlimb suspension (HS) in adult rats. Methods Adult (10 months) male Fischer344‐Brown Norway rats underwent either hindlimb suspension (HS, n = 8) or normal WB (WB, n = 8) for 7 days. Massage was applied using cyclic compressive loading (CCL) in WB (WBM, n = 9) or HS rats (HSM, n = 9) and included four 30‐minute bouts of CCL applied to gastrocnemius muscle every other day. Results Massage had no effect on any anabolic parameter measured under WB conditions (WBM). In contrast, massage during HS (HSM) stimulated protein turnover, but did not mitigate muscle atrophy. Atrophy from HS was caused by both lowered protein synthesis and higher degradation. HS and HSM had lowered total RNA compared with WB and this was the result of significantly higher ribosome degradation in HS that was attenuated in HSM, without differences in ribosomal biogenesis. Also, massage increased protein turnover in the non‐massaged contralateral limb during HS. Finally, we determined that total RNA degradation primarily dictates loss of muscle ribosomal content during disuse atrophy. Conclusion We conclude that massage is an effective mechanotherapy to impact protein turnover during muscle disuse in both the massaged and non‐massaged contralateral muscle, but it does not attenuate the loss of muscle mass.</description><subject>Animals</subject><subject>Atrophy</subject><subject>cross‐over effect</subject><subject>Degradation</subject><subject>disuse atrophy</subject><subject>Gastrocnemius muscle</subject><subject>Hindlimb Suspension</subject><subject>Life Sciences &amp; Biomedicine</subject><subject>Male</subject><subject>Massage</subject><subject>Muscle Proteins - biosynthesis</subject><subject>Muscle, Skeletal - pathology</subject><subject>Muscular Atrophy - pathology</subject><subject>Muscular Atrophy - prevention &amp; control</subject><subject>Physiology</subject><subject>Protein biosynthesis</subject><subject>Protein turnover</subject><subject>Proteins</subject><subject>Rats</subject><subject>Rats, Inbred BN</subject><subject>Rats, Inbred F344</subject><subject>Ribonucleic acid</subject><subject>ribosome biogenesis</subject><subject>ribosome turnover</subject><subject>Ribosomes - metabolism</subject><subject>RNA</subject><subject>Rodents</subject><subject>Science &amp; 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Van Pelt, Douglas W. ; Confides, Amy L. ; Hunt, Emily R. ; Hettinger, Zachary R. ; Laurin, Jaime L. ; Reid, Justin J. ; Peelor, Frederick F. ; Butterfield, Timothy A. ; Dupont‐Versteegden, Esther E. ; Miller, Benjamin F.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4480-37c44b49fd2683c5db7fd971e6da64a7faa4b997713d133433cdf6fbc6c6a1253</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Animals</topic><topic>Atrophy</topic><topic>cross‐over effect</topic><topic>Degradation</topic><topic>disuse atrophy</topic><topic>Gastrocnemius muscle</topic><topic>Hindlimb Suspension</topic><topic>Life Sciences &amp; Biomedicine</topic><topic>Male</topic><topic>Massage</topic><topic>Muscle Proteins - biosynthesis</topic><topic>Muscle, Skeletal - pathology</topic><topic>Muscular Atrophy - pathology</topic><topic>Muscular Atrophy - prevention &amp; control</topic><topic>Physiology</topic><topic>Protein biosynthesis</topic><topic>Protein turnover</topic><topic>Proteins</topic><topic>Rats</topic><topic>Rats, Inbred BN</topic><topic>Rats, Inbred F344</topic><topic>Ribonucleic acid</topic><topic>ribosome biogenesis</topic><topic>ribosome turnover</topic><topic>Ribosomes - metabolism</topic><topic>RNA</topic><topic>Rodents</topic><topic>Science &amp; Technology</topic><topic>Skeletal muscle</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lawrence, Marcus M.</creatorcontrib><creatorcontrib>Van Pelt, Douglas W.</creatorcontrib><creatorcontrib>Confides, Amy L.</creatorcontrib><creatorcontrib>Hunt, Emily R.</creatorcontrib><creatorcontrib>Hettinger, Zachary R.</creatorcontrib><creatorcontrib>Laurin, Jaime L.</creatorcontrib><creatorcontrib>Reid, Justin J.</creatorcontrib><creatorcontrib>Peelor, Frederick F.</creatorcontrib><creatorcontrib>Butterfield, Timothy A.</creatorcontrib><creatorcontrib>Dupont‐Versteegden, Esther E.</creatorcontrib><creatorcontrib>Miller, Benjamin F.</creatorcontrib><collection>Web of Science - Science Citation Index Expanded - 2020</collection><collection>Web of Science Core Collection</collection><collection>Science Citation Index Expanded</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>Physical Education Index</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>ACTA PHYSIOLOGICA</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lawrence, Marcus M.</au><au>Van Pelt, Douglas W.</au><au>Confides, Amy L.</au><au>Hunt, Emily R.</au><au>Hettinger, Zachary R.</au><au>Laurin, Jaime L.</au><au>Reid, Justin J.</au><au>Peelor, Frederick F.</au><au>Butterfield, Timothy A.</au><au>Dupont‐Versteegden, Esther E.</au><au>Miller, Benjamin F.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Massage as a mechanotherapy promotes skeletal muscle protein and ribosomal turnover but does not mitigate muscle atrophy during disuse in adult rats</atitle><jtitle>ACTA PHYSIOLOGICA</jtitle><stitle>ACTA PHYSIOL</stitle><addtitle>Acta Physiol (Oxf)</addtitle><date>2020-07</date><risdate>2020</risdate><volume>229</volume><issue>3</issue><spage>e13460</spage><epage>n/a</epage><pages>e13460-n/a</pages><artnum>13460</artnum><issn>1748-1708</issn><issn>1748-1716</issn><eissn>1748-1716</eissn><abstract>Aim Interventions that decrease atrophy during disuse are desperately needed to maintain muscle mass. We recently found that massage as a mechanotherapy can improve muscle regrowth following disuse atrophy. Therefore, we aimed to determine if massage has similar anabolic effects when applied during normal weight bearing conditions (WB) or during atrophy induced by hindlimb suspension (HS) in adult rats. Methods Adult (10 months) male Fischer344‐Brown Norway rats underwent either hindlimb suspension (HS, n = 8) or normal WB (WB, n = 8) for 7 days. Massage was applied using cyclic compressive loading (CCL) in WB (WBM, n = 9) or HS rats (HSM, n = 9) and included four 30‐minute bouts of CCL applied to gastrocnemius muscle every other day. Results Massage had no effect on any anabolic parameter measured under WB conditions (WBM). In contrast, massage during HS (HSM) stimulated protein turnover, but did not mitigate muscle atrophy. Atrophy from HS was caused by both lowered protein synthesis and higher degradation. HS and HSM had lowered total RNA compared with WB and this was the result of significantly higher ribosome degradation in HS that was attenuated in HSM, without differences in ribosomal biogenesis. Also, massage increased protein turnover in the non‐massaged contralateral limb during HS. Finally, we determined that total RNA degradation primarily dictates loss of muscle ribosomal content during disuse atrophy. Conclusion We conclude that massage is an effective mechanotherapy to impact protein turnover during muscle disuse in both the massaged and non‐massaged contralateral muscle, but it does not attenuate the loss of muscle mass.</abstract><cop>HOBOKEN</cop><pub>Wiley</pub><pmid>32125770</pmid><doi>10.1111/apha.13460</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0001-7106-574X</orcidid><orcidid>https://orcid.org/0000-0003-3283-0685</orcidid><oa>free_for_read</oa></addata></record>
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subjects Animals
Atrophy
cross‐over effect
Degradation
disuse atrophy
Gastrocnemius muscle
Hindlimb Suspension
Life Sciences & Biomedicine
Male
Massage
Muscle Proteins - biosynthesis
Muscle, Skeletal - pathology
Muscular Atrophy - pathology
Muscular Atrophy - prevention & control
Physiology
Protein biosynthesis
Protein turnover
Proteins
Rats
Rats, Inbred BN
Rats, Inbred F344
Ribonucleic acid
ribosome biogenesis
ribosome turnover
Ribosomes - metabolism
RNA
Rodents
Science & Technology
Skeletal muscle
title Massage as a mechanotherapy promotes skeletal muscle protein and ribosomal turnover but does not mitigate muscle atrophy during disuse in adult rats
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