"Sr stress" in mixed hindlimb muscles of aging Male rats
Abstract
Impaired sarcoplasmic reticulum (SR) function has been associated with reduced muscle force generation and locomotor function in aging animals. This study was conducted to determine the extent to which aging increased SR stress markers in male rats, and the extent to which volitional exercise affected them. We harvested medial gastrocnemius muscles from F344/BN rats that were adult (8 months; n = 8), aging (24 months; n = 8) and that aged with wheel access for 16 months (24 months; n = 4). SR calcium handling assays and immunoblotting (Caspase 12, dysferlin and LC3) were performed on crude homogenates and SR-enriched microsomal fractions. Aging was associated with increased Caspase 12 and SR dysferlin, as well as a reduced LC3II/I ratio and impaired calcium release. Despite further increases in Caspase 12, voluntary wheel running partially restored SR calcium release and dysferlin toward younger levels. Of note, the LC3II/I was also partially restored in the voluntary wheel running group, suggesting increased autophagy. These results suggest that impaired SR function with aging is associated with age-related increases in SR stress, possibly related to reduced autophagy. Long-term volitional exercise improved SR function and markers of autophagy, despite increased Caspase 12, suggesting that running contributed a beneficial stress that differed from the "distress" of sedentary aging.
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Impaired mitochondrial autophagy (mitophagy) machinery is another primary cause of mitochondrial dysfunction in aging muscle.
“Another primary cause of mitochondrial dysfunction in aging muscle is the impaired mitochondrial autophagy (mitophagy) machinery.”
From From mitochondria to sarcopenia: role of 17β-estradiol and testosterone (2023) · cites this paper as [92]
Aging provokes alterations of several key mitophagy regulators, leading to mitophagy deficiency and subsequent accumulation of dysfunctional mitochondria in skeletal muscle.
“Studies indicate that aging provokes certain alternations of several key mitophagy regulators, leading to mitophagy deficiency and subsequent accumulation of dysfunctional mitochondria in skeletal muscle (91, 92).”
From From mitochondria to sarcopenia: role of 17β-estradiol and testosterone (2023) · cites this paper as [92]
Cites
A new generation of Ca2+ indicators with greatly improved fluorescence properties.
Grynkiewicz, G., Poenie, M., & Tsien, R. Y. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)83641-4 · Cited by 21,722 · see citing works
Newman, A. B., Kupelian, V., Visser, M., Simonsick, E. M., Goodpaster, B. H., Kritchevsky, S. B., Tylavsky, F. A., Rubin, S. M., Harris, T. B., & on Behalf of the Health, A. A. B. C. S. I. (2006) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/61.1.72 · Cited by 1,692 · see citing works
Attenuation of skeletal muscle and strength in the elderly: the Health ABC Study
Goodpaster, B. H., Carlson, C. L., Visser, M., Kelley, D. E., Scherzinger, A., Harris, T. B., Stamm, E., & Newman, A. B. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.90.6.2157 · Cited by 1,226 · see citing works
Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis
He, C., Bassik, M. C., Moresi, V., Sun, K., Wei, Y., Zou, Z., An, Z., Loh, J., Fisher, J., Sun, Q., et al. (2012) · Nature · doi:10.1038/nature10758 · Cited by 1,136 · see citing works
Defective membrane repair in dysferlin-deficient muscular dystrophy
Bansal, D., Miyake, K., Vogel, S. S., Groh, S., Chen, C.-C., Williamson, R., McNeil, P. L., & Campbell, K. P. (2003) · Nature · doi:10.1038/nature01573 · Cited by 1,022 · see citing works
Skeletal Muscle Strength as a Predictor of All-Cause Mortality in Healthy Men
Metter, E. J., Talbot, L. A., Schrager, M., & CONWIT, R. A. (2002) · The Journals of Gerontology Series A · doi:10.1093/gerona/57.10.b359 · Cited by 843 · see citing works
Effects of Aging on Muscle Fibre Type and Size
Deschenes, M. R. (2004) · Sports Medicine · doi:10.2165/00007256-200434120-00002 · Cited by 671 · see citing works
Growth Curves and Survival Characteristics of the Animals Used in the Biomarkers of Aging Program
Turturro, A., Witt, W. W., Lewis, S. M., Hass, B. S., Lipman, R. D., & Hart, R. W. (1999) · The Journals of Gerontology Series A · doi:10.1093/gerona/54.11.b492 · Cited by 668 · see citing works
Balagopal, P., Rooyackers, O., Adey, D., Ades, P. A., & Nair, K. S. (1997) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1997.273.4.e790 · Cited by 541 · see citing works
Mitochondrial function and apoptotic susceptibility in aging skeletal muscle
Chabi, B., Ljubicic, V., Menzies, K. J., Huang, J. H., Saleem, A., & Hood, D. A. (2008) · Aging Cell · doi:10.1111/j.1474-9726.2007.00347.x · Cited by 437 · see citing works
Skeletal muscle fiber quality in older men and women
Frontera, W. R., Suh, D., Krivickas, L. S., HUGHES, V. A., Goldstein, R., & Roubenoff, R. (2000) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2000.279.3.c611 · Cited by 424 · see citing works
Ryanodine receptor oxidation causes intracellular calcium leak and muscle weakness in aging
Andersson, D. C., Betzenhauser, M. J., Reiken, S., Meli, A. C., Umanskaya, A., Xie, W., Shiomi, T., Zalk, R., Lacampagne, A., & Marks, A. R. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.05.014 · Cited by 424 · see citing works
Wohlgemuth, S. E., Seo, A. Y., Marzetti, E., Lees, H. A., & Leeuwenburgh, C. (2010) · Experimental Gerontology · doi:10.1016/j.exger.2009.11.002 · Cited by 397 · see citing works
The Influence of Estrogen on Skeletal Muscle: Sex Matters
Enns, D. L., & Tiidus, P. M. (2010) · Sports Medicine · doi:10.2165/11319760-000000000-00000 · Cited by 374 · see citing works
Oxidative Stress, Accumulation of Biological 'Garbage', and Aging
Terman, A., & Brunk, U. T. (2006) · Antioxidants and Redox Signaling · doi:10.1089/ars.2006.8.197 · Cited by 363 · see citing works
Bellinger, A. M., Reiken, S. R., Důra, M., Murphy, P. W., Deng, S., Landry, D. W., Nieman, D. C., Lehnart, S. E., Samaru, M., Lacampagne, A., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711074105 · Cited by 353 · see citing works
ER and aging—Protein folding and the ER stress response
Naidoo, N. N. (2009) · Ageing Research Reviews · doi:10.1016/j.arr.2009.03.001 · Cited by 280 · see citing works
Dysferlin and muscle membrane repair
Han, R., & Campbell, K. P. (2007) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2007.07.001 · Cited by 275 · see citing works
E-C coupling failure in mouse EDL muscle after in vivo eccentric contractions
Ingalls, C. P., Warren, G. L., Williams, J. H., Ward, C. W., & Armstrong, R. B. (1998) · Journal of Applied Physiology · doi:10.1152/jappl.1998.85.1.58 · Cited by 262 · see citing works
Effect of voluntary exercise on longevity of rats
Holloszy, J. O., Smith, E. K., Vining, M., & Adams, S. (1985) · Journal of Applied Physiology · doi:10.1152/jappl.1985.59.3.826 · Cited by 231 · see citing works
Excitation-calcium release uncoupling in aged single human skeletal muscle fibers
Delbono, O., O’Rourke, K. S., & Ettinger, W. H. (1995) · The Journal of Membrane Biology · doi:10.1007/bf00235039 · Cited by 221 · see citing works
Dirks, A. J., & Leeuwenburgh, C. (2004) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2003.10.003 · Cited by 190 · see citing works
Change in Muscle Mass and Muscle Strength After a Hip Fracture: Relationship to Mobility Recovery
Visser, M., Harris, T. B., Fox, K. M., Hawkes, W., Hebel, J. R., YuYahiro, J., Michael, R., Zimmerman, S. I., & Magaziner, J. (2000) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/55.8.m434 · Cited by 157 · see citing works
Evolving concepts on the age-related changes in “muscle quality”
Russ, D., Gregg-Cornell, K., Conaway, M. J., & Clark, B. (2012) · Journal of Cachexia, Sarcopenia and Muscle · doi:10.1007/s13539-011-0054-2 · Cited by 142 · see citing works
Self-citationWeisleder, N. L., Brotto, M. A. P., Komazaki, S., Pan, Z., Zhao, X., Nosek, T. M., Parness, J., Takeshima, H., & Ma, J. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200604166 · Cited by 121 · see citing works
González, E., Messi, M. L., & Delbono, O. (2000) · Journal of Membrane Biology · doi:10.1007/s002320010025 · Cited by 115 · see citing works
ER stress and hormetic regulation of the aging process
Salminen, A., & Kaarniranta, K. (2010) · Ageing Research Reviews · doi:10.1016/j.arr.2010.04.003 · Cited by 115 · see citing works
Takahira, M., & Hughes, B. A. (1997) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1997.273.3.c790 · Cited by 115 · see citing works
Cardioprotection by Endoplasmic Reticulum Stress–Induced Autophagy
Petrovski, G., Das, S., Juhász, B., Kertesz, A., Tósaki, Á., & Das, D. K. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3486 · Cited by 112 · see citing works
Volpe, P., Villa, A., Podini, P., et al. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.13.6142 · Cited by 89 · see citing works
Selective autophagy in the maintenance of cellular homeostasis in aging organisms
Hubbard, V. M., Valdor, R., Macián, F., & Cuervo, A. M. (2011) · Biogerontology · doi:10.1007/s10522-011-9331-x · Cited by 89 · see citing works
Myosin and actin expression and oxidation in aging muscle
Thompson, L. V., Durand, D., Fugere, N. A., & Ferrington, D. A. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00426.2006 · Cited by 83 · see citing works
Force generation, but not myosin ATPase activity, declines with age in rat muscle fibers
Lowe, D. A., Thomas, D. D., & Thompson, L. V. (2002) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00008.2002 · Cited by 83 · see citing works
Schwendner, K. I., Mikesky, A. E., Holt, W. S., Peacock, M., & Burr, D. B. (1997) · The Journals of Gerontology Series A · doi:10.1093/gerona/52a.3.m155 · Cited by 77 · see citing works
Grandy, S. A., & Howlett, S. E. (2006) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00070.2006 · Cited by 77 · see citing works
Sarcoplasmic Reticulum Ca2+ Release Declines in Muscle Fibers from Aging Mice
Jiménez-Moreno, R., Wang, Z.-M., Gerring, R., & Delbono, O. (2008) · Biophysical Journal · doi:10.1529/biophysj.107.118786 · Cited by 66 · see citing works
Impaired recovery of dysferlin-null skeletal muscle after contraction-induced injury in vivo
Roche, J. A., Lovering, R., & Bloch, R. (2008) · NeuroReport · doi:10.1097/wnr.0b013e328311ca35 · Cited by 64 · see citing works
Russ, D. W., Grandy, J. S., Toma, K., & Ward, C. W. (2011) · Acta Physiologica · doi:10.1111/j.1748-1716.2010.02191.x · Cited by 61 · see citing works
Self-citationEndoplasmic Reticulum Stress in Skeletal Muscle
Deldicque, L., Hespel, P., & Francaux, M. (2011) · Exercise and Sport Sciences Reviews · doi:10.1097/jes.0b013e3182355e8c · Cited by 61 · see citing works
Sarcopenia: current theories and the potential beneficial effect of creatine application strategies
Candow, D. G. (2011) · Biogerontology · doi:10.1007/s10522-011-9327-6 · Cited by 53 · see citing works
Donati, A., Recchia, G., Cavallini, G., & Bergamini, E. (2008) · The Journals of Gerontology Series A · doi:10.1093/gerona/63.6.550 · Cited by 50 · see citing works
Sarcoplasmic reticulum in aged skeletal muscle
Margreth, Damiani, & Bortoloso (1999) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.1999.00624.x · Cited by 46 · see citing works
Lees, S. J., & Williams, J. H. (2004) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00188.2003 · Cited by 45 · see citing works
Differential cell death regulation between adult-unloaded and aged rat soleus muscle
Ogata, T., Machida, S., Oishi, Y., Higuchi, M., & Muraoka, I. (2009) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2009.02.001 · Cited by 44 · see citing works
Age-related abnormalities in regulation of the ryanodine receptor in rat fast-twitch muscle
Damiani, E., Larsson, L., & Margreth, A. (1996) · Cell Calcium · doi:10.1016/s0143-4160(96)90010-x · Cited by 43 · see citing works
Kayalı, R., Çakatay, U., Uzun, H., & Genç, H. (2007) · Biogerontology · doi:10.1007/s10522-007-9107-5 · Cited by 39 · see citing works
Masseter inhibitory reflex in humans: attempted modulation by various experimental parameters
Mäntyvaara, Sjöholm, & Pertovaara (1999) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.1999.600aa.x · Cited by 34 · see citing works
Muscle atrophy is not always sarcopenia
Hepple, R. T. (2012) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00304.2012 · Cited by 34 · see citing works
Thomas, M. M., Vigna, C., Betik, A. C., Tupling, A. R., & Hepple, R. T. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00663.2009 · Cited by 28 · see citing works
Effects of early-stage aging on locomotor dynamics and hindlimb muscle force production in the rat
Horner, A. M., Russ, D. W., & Biknevicius, A. R. (2011) · Journal of Experimental Biology · doi:10.1242/jeb.055087 · Cited by 26 · see citing works
Self-citationRenganathan, M., & Delbono, O. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)01009-6 · Cited by 25 · see citing works
Increased CaVβ1a expression with aging contributes to skeletal muscle weakness
Taylor, J. R., Zheng, Z., Wang, Z., Payne, A. M., Messi, M. L., & Delbono, O. (2009) · Aging Cell · doi:10.1111/j.1474-9726.2009.00507.x · Cited by 25 · see citing works
Purification of catalytically active caspase-12 and its biochemical characterization
Lee, H., Lee, S. H., Park, S., et al. (2010) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2010.07.013 · Cited by 6 · see citing works
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Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition).
Klionsky, D. J., Abdelmohsen, K., Abe, A., Abedin, M. J., Abeliovich, H., Acevedo Arozena, A., Adachi, H., Adams, C. M., Adams, P. D., Adeli, K., et al. (2016) · Autophagy · doi:10.1080/15548627.2015.1100356 · Cited by 5,894 · see citing works
Self-citationKlionsky, D. J., Abdel-Aziz, A. K., Abdelfatah, S., Abdellatif, M., Abdoli, A., Abel, S., Abeliovich, H., Abildgaard, M. H., Abudu, Y. P., Acevedo-Arozena, A., et al. (2021) · Autophagy · doi:10.1080/15548627.2020.1797280 · Cited by 2,622 · see citing works
Mitochondrial dysfunction and sarcopenia of aging: from signaling pathways to clinical trials
Marzetti, E., Calvani, R., Cesari, M., Buford, T. W., Lorenzi, M., Behnke, B. J., & Leeuwenburgh, C. (2013) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2013.06.024 · Cited by 627 · see citing works
Mitochondrial quality control and muscle mass maintenance.
Romanello, V., & Sandri, M. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2015.00422 · Cited by 434 · see citing works
Picca, A., Lezza, A. M. S., Leeuwenburgh, C., Pesce, V., Calvani, R., Bossola, M., Manes-Gravina, E., Landi, F., Bernabei, R., & Marzetti, E. (2018) · Rejuvenation Research · doi:10.1089/rej.2017.1989 · Cited by 144 · see citing works
Update on mitochondria and muscle aging: All wrong roads lead to sarcopenia
Picca, A., Calvani, R., Bossola, M., Allocca, E., Menghi, A., Pesce, V., Lezza, A. M. S., Bernabei, R., Landi, F., & Marzetti, E. (2018) · Biological Chemistry · doi:10.1515/hsz-2017-0331 · Cited by 116 · see citing works
Dethlefsen, M. M., Halling, J. F., Møller, H. D., Plomgaard, P., Regenberg, B., Ringholm, S., & Pilegaard, H. (2018) · Experimental Gerontology · doi:10.1016/j.exger.2018.07.011 · Cited by 54 · see citing works
From mitochondria to sarcopenia: role of 17β-estradiol and testosterone
Tian, X., Lou, S., & Shi, R. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1156583 · Cited by 54 · see citing works
“Studies indicate that aging provokes certain alternations of several key mitophagy regulators, leading to mitophagy deficiency and subsequent accumulation of dysfunctional mitochondria in skeletal muscle (91, 92).”
BackgroundRegulatory role of exercise-induced autophagy for sarcopenia
Liang, J., Zeng, Z., Zhang, Y., & Chen, N. (2020) · Experimental Gerontology · doi:10.1016/j.exger.2019.110789 · Cited by 33 · see citing works
- Authors
- Russ, D. W., Krause, J., Wills, A., & Arreguin, R.
- Affiliations
- Ohio University (US)
- Corresponding author
- Russ, David W.
- Venue
- Biogerontology
- Published
- 2012-09-06
- Volume
- 13
- Issue
- 5
- Pages
- 547-555
- ISSN
- 1389-5729 (ISSN-L)
- 1573-6768
- OpenAlex
- W2072581177
- Cited by
- 32
- References
- 53
- Citations by year
- 2026: 1 · 2024: 1 · 2023: 2 · 2021: 4 · 2020: 2 · 2019: 2 · 2018: 3 · 2017: 4 · 2016: 4 · 2015: 6 · 2014: 1 · 2013: 2
- FWCI
- 1.16
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Biogerontology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- sarcoplasmic reticulum calcium handling, muscle aging, voluntary wheel running, autophagy, caspase-12, dysferlin, LC3, medial gastrocnemius, hindlimb muscles, sarcoplasmic reticulum calcium release, exercise and aging
- MeSH terms
- Aging, Animals, Calcium, Electrophoresis, Polyacrylamide Gel, Hindlimb, Male, Sarcoplasmic Reticulum, Stress, Physiological, Blotting, Western, Muscle, Skeletal, Rats
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