Aging in Rats Differentially Affects Markers of Transcriptional and Translational Capacity in Soleus and Plantaris Muscle

Alterations in transcriptional and translational mechanisms occur during skeletal muscle aging and such changes may contribute to age-related atrophy. Herein, we examined markers related to global transcriptional output (i.e., myonuclear number, total mRNA and RNA pol II levels), translational effic...

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Main Authors: Christopher B. Mobley, Petey W. Mumford, Wesley C. Kephart, Cody T. Haun, Angelia M. Holland, Darren T. Beck, Jeffrey S. Martin, Kaelin C. Young, Richard G. Anderson, Romil K. Patel, Gillis L. Langston, Ryan P. Lowery, Jacob M. Wilson, Michael D. Roberts
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-07-01
Series:Frontiers in Physiology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fphys.2017.00518/full
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author Christopher B. Mobley
Petey W. Mumford
Wesley C. Kephart
Cody T. Haun
Angelia M. Holland
Darren T. Beck
Darren T. Beck
Jeffrey S. Martin
Jeffrey S. Martin
Kaelin C. Young
Kaelin C. Young
Richard G. Anderson
Romil K. Patel
Gillis L. Langston
Ryan P. Lowery
Ryan P. Lowery
Jacob M. Wilson
Michael D. Roberts
Michael D. Roberts
author_facet Christopher B. Mobley
Petey W. Mumford
Wesley C. Kephart
Cody T. Haun
Angelia M. Holland
Darren T. Beck
Darren T. Beck
Jeffrey S. Martin
Jeffrey S. Martin
Kaelin C. Young
Kaelin C. Young
Richard G. Anderson
Romil K. Patel
Gillis L. Langston
Ryan P. Lowery
Ryan P. Lowery
Jacob M. Wilson
Michael D. Roberts
Michael D. Roberts
author_sort Christopher B. Mobley
collection DOAJ
description Alterations in transcriptional and translational mechanisms occur during skeletal muscle aging and such changes may contribute to age-related atrophy. Herein, we examined markers related to global transcriptional output (i.e., myonuclear number, total mRNA and RNA pol II levels), translational efficiency [i.e., eukaryotic initiation and elongation factor levels and muscle protein synthesis (MPS) levels] and translational capacity (ribosome density) in the slow-twitch soleus and fast-twitch plantaris muscles of male Fischer 344 rats aged 3, 6, 12, 18, and 24 months (n = 9–10 per group). We also examined alterations in markers of proteolysis and oxidative stress in these muscles (i.e., 20S proteasome activity, poly-ubiquinated protein levels and 4-HNE levels). Notable plantaris muscle observations included: (a) fiber cross sectional area (CSA) was 59% (p < 0.05) and 48% (p < 0.05) greater in 12 month vs. 3 month and 24 month rats, respectively, suggesting a peak lifetime value near 12 months and age-related atrophy by 24 months, (b) MPS levels were greatest in 18 month rats (p < 0.05) despite the onset of atrophy, (c) while regulators of ribosome biogenesis [c-Myc and upstream binding factor (UBF) protein levels] generally increased with age, ribosome density linearly decreased from 3 months of age and RNA polymerase (Pol) I protein levels were lowest in 24 month rats, and d) 20S proteasome activity was robustly up-regulated in 6 and 24 month rats (p < 0.05). Notable soleus muscle observations included: (a) fiber CSA was greatest in 6 month rats and was maintained in older age groups, and (b) 20S proteasome activity was modestly but significantly greater in 24 month vs. 3/12/18 month rats (p < 0.05), and (c) total mRNA levels (suggestive of transcriptional output) trended downward in older rats despite non-significant between-group differences in myonuclear number and/or RNA Pol II protein levels. Collectively, these findings suggest that plantaris, not soleus, atrophy occurs following 12 months of age in male Fisher rats and this may be due to translational deficits (i.e., changes in MPS and ribosome density) and/or increases in proteolysis rather than increased oxidative stress and/or alterations in global transcriptional mechanisms.
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spelling doaj.art-b442423b262f4d67832d915c86211cde2022-12-22T03:23:37ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2017-07-01810.3389/fphys.2017.00518268081Aging in Rats Differentially Affects Markers of Transcriptional and Translational Capacity in Soleus and Plantaris MuscleChristopher B. Mobley0Petey W. Mumford1Wesley C. Kephart2Cody T. Haun3Angelia M. Holland4Darren T. Beck5Darren T. Beck6Jeffrey S. Martin7Jeffrey S. Martin8Kaelin C. Young9Kaelin C. Young10Richard G. Anderson11Romil K. Patel12Gillis L. Langston13Ryan P. Lowery14Ryan P. Lowery15Jacob M. Wilson16Michael D. Roberts17Michael D. Roberts18School of Kinesiology, Auburn UniversityAuburn, AL, United StatesSchool of Kinesiology, Auburn UniversityAuburn, AL, United StatesSchool of Kinesiology, Auburn UniversityAuburn, AL, United StatesSchool of Kinesiology, Auburn UniversityAuburn, AL, United StatesSchool of Kinesiology, Auburn UniversityAuburn, AL, United StatesSchool of Kinesiology, Auburn UniversityAuburn, AL, United StatesEdward via College of Osteopathic MedicineAuburn, AL, United StatesSchool of Kinesiology, Auburn UniversityAuburn, AL, United StatesEdward via College of Osteopathic MedicineAuburn, AL, United StatesSchool of Kinesiology, Auburn UniversityAuburn, AL, United StatesEdward via College of Osteopathic MedicineAuburn, AL, United StatesSchool of Kinesiology, Auburn UniversityAuburn, AL, United StatesSchool of Kinesiology, Auburn UniversityAuburn, AL, United StatesSchool of Kinesiology, Auburn UniversityAuburn, AL, United StatesApplied Science and Performance InstituteTampa, FL, United StatesDepartment of Health and Human Performance, Concordia University ChicagoRiver Forest, IL, United StatesApplied Science and Performance InstituteTampa, FL, United StatesSchool of Kinesiology, Auburn UniversityAuburn, AL, United StatesEdward via College of Osteopathic MedicineAuburn, AL, United StatesAlterations in transcriptional and translational mechanisms occur during skeletal muscle aging and such changes may contribute to age-related atrophy. Herein, we examined markers related to global transcriptional output (i.e., myonuclear number, total mRNA and RNA pol II levels), translational efficiency [i.e., eukaryotic initiation and elongation factor levels and muscle protein synthesis (MPS) levels] and translational capacity (ribosome density) in the slow-twitch soleus and fast-twitch plantaris muscles of male Fischer 344 rats aged 3, 6, 12, 18, and 24 months (n = 9–10 per group). We also examined alterations in markers of proteolysis and oxidative stress in these muscles (i.e., 20S proteasome activity, poly-ubiquinated protein levels and 4-HNE levels). Notable plantaris muscle observations included: (a) fiber cross sectional area (CSA) was 59% (p < 0.05) and 48% (p < 0.05) greater in 12 month vs. 3 month and 24 month rats, respectively, suggesting a peak lifetime value near 12 months and age-related atrophy by 24 months, (b) MPS levels were greatest in 18 month rats (p < 0.05) despite the onset of atrophy, (c) while regulators of ribosome biogenesis [c-Myc and upstream binding factor (UBF) protein levels] generally increased with age, ribosome density linearly decreased from 3 months of age and RNA polymerase (Pol) I protein levels were lowest in 24 month rats, and d) 20S proteasome activity was robustly up-regulated in 6 and 24 month rats (p < 0.05). Notable soleus muscle observations included: (a) fiber CSA was greatest in 6 month rats and was maintained in older age groups, and (b) 20S proteasome activity was modestly but significantly greater in 24 month vs. 3/12/18 month rats (p < 0.05), and (c) total mRNA levels (suggestive of transcriptional output) trended downward in older rats despite non-significant between-group differences in myonuclear number and/or RNA Pol II protein levels. Collectively, these findings suggest that plantaris, not soleus, atrophy occurs following 12 months of age in male Fisher rats and this may be due to translational deficits (i.e., changes in MPS and ribosome density) and/or increases in proteolysis rather than increased oxidative stress and/or alterations in global transcriptional mechanisms.http://journal.frontiersin.org/article/10.3389/fphys.2017.00518/fullfast-twitch muscleagingatrophymuscle protein synthesismRNAribosome
spellingShingle Christopher B. Mobley
Petey W. Mumford
Wesley C. Kephart
Cody T. Haun
Angelia M. Holland
Darren T. Beck
Darren T. Beck
Jeffrey S. Martin
Jeffrey S. Martin
Kaelin C. Young
Kaelin C. Young
Richard G. Anderson
Romil K. Patel
Gillis L. Langston
Ryan P. Lowery
Ryan P. Lowery
Jacob M. Wilson
Michael D. Roberts
Michael D. Roberts
Aging in Rats Differentially Affects Markers of Transcriptional and Translational Capacity in Soleus and Plantaris Muscle
Frontiers in Physiology
fast-twitch muscle
aging
atrophy
muscle protein synthesis
mRNA
ribosome
title Aging in Rats Differentially Affects Markers of Transcriptional and Translational Capacity in Soleus and Plantaris Muscle
title_full Aging in Rats Differentially Affects Markers of Transcriptional and Translational Capacity in Soleus and Plantaris Muscle
title_fullStr Aging in Rats Differentially Affects Markers of Transcriptional and Translational Capacity in Soleus and Plantaris Muscle
title_full_unstemmed Aging in Rats Differentially Affects Markers of Transcriptional and Translational Capacity in Soleus and Plantaris Muscle
title_short Aging in Rats Differentially Affects Markers of Transcriptional and Translational Capacity in Soleus and Plantaris Muscle
title_sort aging in rats differentially affects markers of transcriptional and translational capacity in soleus and plantaris muscle
topic fast-twitch muscle
aging
atrophy
muscle protein synthesis
mRNA
ribosome
url http://journal.frontiersin.org/article/10.3389/fphys.2017.00518/full
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