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Long-term exercise treatment reduces oxidative stress in the hippocampus of aging rats
Abstract
Exercise can exert beneficial effects on cognitive functions of older subjects and it can also play an important role in the prevention of neurodegenerative diseases. At the same time it is perceivable that limited information is available on the nature of molecular pathways supporting the antioxidant effects of exercise in the brain. In this study 12-month old, middle-aged female Wistar rats were subjected to daily moderate intensity exercise on a rodent treadmill for a period of 15weeks which covered the early aging period unmasking already some aging-related molecular disturbances. The levels of reactive oxygen species (ROS), the amount of protein carbonyls, the levels of antioxidant intracellular enzymes superoxide dismutases (SOD-1, SOD-2) and glutathione peroxidase (GPx) were determined in the hippocampus. In addition, to identify the molecular pathways that may be involved in ROS metabolism and mitochondrial biogenesis, the activation of 5'-AMP-activated protein kinase (AMPK), the protein level of peroxisome proliferator-activated receptor gamma coactivator 1-alpha (PGC-1α), nuclear respiratory factor 1 (NRF-1) and mitochondrial transcription factor A (mtTFA) were measured. Our results revealed a lower level of ROS associated with a reduced amount of protein carbonyls in the hippocampus of physically trained rats compared to sedentary controls. Furthermore, exercise induced an up-regulation of SOD-1 and GPx enzymes, p-AMPK and PGC-1α, that can be related to an improved redox balance in the hippocampus. These results suggest that long-term physical exercise can comprises antioxidant properties and by this way protect neurons against oxidative stress at the early stage of aging.
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“Indeed, just 2 wk of treadmill running has been shown to increase the abundance of antioxidants superoxide dismutase-1 and −2 and glutathione peroxidase and reduce ROS in the hippocampus of 12-month-old rats (26).”
From Exercise Counters the Age-Related Accumulation of Senescent Cells (2022) · cites this paper as [26]
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“In addition, exercise alleviated diet-induced neuroinflammation and oxidative stress in the hippocampus (55), consistent with prior reports (26).”
From Exercise Counters the Age-Related Accumulation of Senescent Cells (2022) · cites this paper as [26]
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Cites
Aging: a theory based on free radical and radiation chemistry
Harman, D. (1956) · Journal of Gerontology · doi:10.1093/geronj/11.3.298 · Cited by 8,567
Neurodegenerative diseases and oxidative stress
Barnham, K. J., Masters, C. L., & Bush, A. I. (2004) · Nature Reviews Drug Discovery · doi:10.1038/nrd1330 · Cited by 3,683 · cited 1×
“Extensive damage to these biomolecules in the brain can cause neuronal dysfunction and trigger apoptosis (Emerit et al., 2004).”
BackgroundAMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1α
Jäger, S., Handschin, C., St.-Pierre, J., & Spiegelman, B. M. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705070104 · Cited by 2,491
St-Pierre, J., Drori, S., Uldry, M., Silvaggi, J. M., Rhee, J., Jäger, S., Handschin, C., Zheng, K., Lin, J., Yang, W., et al. (2006) · Cell · doi:10.1016/j.cell.2006.09.024 · Cited by 2,233
Antioxidant and redox regulation of gene transcription
Sen, C. K., & Packer, L. (1996) · The FASEB Journal · doi:10.1096/fasebj.10.7.8635688 · Cited by 1,972
PGC-1α, SIRT1 and AMPK, an energy sensing network that controls energy expenditure
Cantó, C., & Auwerx, J. (2009) · Current Opinion in Lipidology · doi:10.1097/mol.0b013e328328d0a4 · Cited by 1,624
Hawley, S. A., Pan, D. A., Mustard, K. J., Ross, L., Bain, J., Edelman, A. M., Frenguelli, B. G., & Hardie, D. G. (2005) · Cell Metabolism · doi:10.1016/j.cmet.2005.05.009 · Cited by 1,589
Oxidant signals and oxidative stress
Finkel, T. (2003) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(03)00002-4 · Cited by 1,393
Douglas, R. (1967) · Psychological bulletin · doi:10.1037/h0024599 · Cited by 1,092
Neurodegenerative diseases and oxidative stress
Emerit, J., Edeas, M. A., & Bricaire, F. (2003) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2003.11.004 · Cited by 1,057
Oxygen poisoning and x-irradiation: a mechanism in common
Gerschman, R., Gilbert, D. L., Nye, S. W., Dwyer, P., & Fenn, W. O. (1954) · Science · doi:10.1126/science.119.3097.623 · Cited by 961 · cited 1×
“A number of studies have demonstrated that increased levels of ROS are involved in the aging process (Gerschman et al., 1954; Harman, 1956; Droge, 2003) and contribute to pathological changes in neurodegenerative disorders (Floyd and Hensley, 2002).”
BackgroundTranscriptional control of mitochondrial biogenesis: the central role of PGC-1
Ventura-Clapier, R., Garnier, A., & Veksler, V. (2008) · Cardiovascular Research · doi:10.1093/cvr/cvn098 · Cited by 932
Cantó, C., Jiang, L. Q., Deshmukh, A. S., Mataki, C., Coste, A., Lagouge, M., Zierath, J. R., & Auwerx, J. (2010) · Cell Metabolism · doi:10.1016/j.cmet.2010.02.006 · Cited by 921
Oxidative stress in brain agingImplications for therapeutics of neurodegenerative diseases
Floyd, R. A., & Hensley, K. (2002) · Neurobiology of Aging · doi:10.1016/s0197-4580(02)00019-2 · Cited by 837
Protein Oxidation in Aging and Age‐Related Diseases
Stadtman, E. R. (2001) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2001.tb05632.x · Cited by 660
PGC-1α regulates the mitochondrial antioxidant defense system in vascular endothelial cells
VALLE, I., ALVAREZBARRIENTOS, A., ARZA, E., LAMAS, S., & MONSALVE, M. (2005) · Cardiovascular Research · doi:10.1016/j.cardiores.2005.01.026 · Cited by 556 · cited 1×
“Peroxisome proliferator-activated receptor gamma coactivator 1-alpha (PGC-1a) may play an important role in the control of ROS metabolism, since it regulates the expression of ROS-detoxifying enzymes (Valle et al., 2005).”
BackgroundProtein oxidation in the brain in Alzheimer's disease
Aksenov, M. Y., Aksenova, M. V., Butterfield, D. A., Geddes, J. W., & Markesbery, W. R. (2001) · Neuroscience · doi:10.1016/s0306-4522(00)00580-7 · Cited by 505
Diet and exercise signals regulate SIRT3 and activate AMPK and PGC-1α in skeletal muscle
Palacios, O. M., Carmona, J. J., Michan, S., Chen, K. Y., Manabe, Y., III, J. L. W., Goodyear, L. J., & Tong, Q. (2009) · Aging · doi:10.18632/aging.100075 · Cited by 487
Oxidative modification of proteins during aging
Levine, R. L., & Stadtman, E. R. (2001) · Experimental Gerontology · doi:10.1016/s0531-5565(01)00135-8 · Cited by 466
Reactive oxygen species and synaptic plasticity in the aging hippocampus
Serrano, F., & Klann, E. (2004) · Ageing Research Reviews · doi:10.1016/j.arr.2004.05.002 · Cited by 426
Dröge, W. (2003) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-8997-0_14 · Cited by 415
O'Neill, H. M., Maarbjerg, S. J., Crane, J. D., Jeppesen, J., Jørgensen, S. B., Schertzer, J. D., Shyroka, O., Kiens, B., van Denderen, B. J., Tarnopolsky, M. A., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1105062108 · Cited by 406
Morris, R. G. M. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04888.x · Cited by 398
Mungai, P. T., Waypa, G. B., Jairaman, A., Prakriya, M., Dokic, D., Ball, M. K., & Schumacker, P. T. (2011) · Molecular and Cellular Biology · doi:10.1128/mcb.05124-11 · Cited by 385
Egan, B., Carson, B. P., Garcia-Roves, P. M., Chibalin, A. V., Sarsfield, F. M., Barron, N., McCaffrey, N., Moyna, N. M., Zierath, J. R., & O’Gorman, D. J. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2010.188011 · Cited by 373
Exercise training increases mitochondrial biogenesis in the brain
Steiner, J. L., Murphy, E. A., McClellan, J. L., Carmichael, M. D., & Davis, J. M. (2011) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00343.2011 · Cited by 368
Mitochondrial biogenesis and healthy aging
López-Lluch, G., Irusta, P. M., Navas, P., & de Cabo, R. (2008) · Experimental Gerontology · doi:10.1016/j.exger.2008.06.014 · Cited by 364
Estrogenic control of mitochondrial function and biogenesis
Klinge, C. M. (2008) · Journal of Cellular Biochemistry · doi:10.1002/jcb.21936 · Cited by 320
Adaptation to exercise-induced oxidative stress: from muscle to brain.
Radak, Z. O., Taylor, A. W., Ohno, H., & Goto, S. (2001) · PubMed · Cited by 292
Self-citationRadak, Z. O., Kaneko, T., Tahara, S., Nakamoto, H., Ohno, H., Sasvári, M., Nyakas, C. J., & Goto, S. (1999) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(99)00038-6 · Cited by 273
Self-citationVenkateshappa, C., Harish, G., Mahadevan, A., Srinivas Bharath, M. M., & Shankar, S. K. (2012) · Neurochemical Research · doi:10.1007/s11064-012-0755-8 · Cited by 232
Um, H.-S., Kang, E., Koo, J., Kim, H.-T., Jin-Lee, Kim, E.-J., Yang, C., An, G.-Y., Cho, I., & Cho, J. (2010) · Neuroscience Research · doi:10.1016/j.neures.2010.10.004 · Cited by 212
The effect of age on cyclooxygenase-2 gene expression
Kim, H., Kim, K., Yu, B., & Chung, H. (2000) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(99)00274-9 · Cited by 199
Hydrogen Peroxide Production by Rat Brain In Vivo
Sinet, P. M., Heikkila, R. E., & Cohen, G. (1980) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1980.tb11222.x · Cited by 197
Physical activity and the elderly
Hollmann, W., Strüder, H. K., Tagarakis, C. V. M., & King, G. (2007) · European Journal of Cardiovascular Prevention & Rehabilitation · doi:10.1097/hjr.0b013e32828622f9 · Cited by 159
The influences of diet and exercise on mental health through hormesis
Gómez‐Pinilla, F. (2007) · Ageing Research Reviews · doi:10.1016/j.arr.2007.04.003 · Cited by 158
Devi, S. A., & Kiran, T. R. (2003) · Neurobiology of Aging · doi:10.1016/s0197-4580(03)00112-x · Cited by 154
Koltai, E., Hart, N., Taylor, A. W., Goto, S., Ngo, J. K., Davies, K. J. A., & Radak, Z. (2012) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00337.2011 · Cited by 152
Self-citationOgonovszky, H., Berkes, I., Kumagai, S., Kaneko, T., Tahara, S., Goto, S., & Radak, Z. O. (2005) · Neurochemistry International · doi:10.1016/j.neuint.2005.02.009 · Cited by 149
Self-citationLee-Young, R. S., Griffee, S. R., Lynes, S. E., Bracy, D. P., Ayala, J. E., McGuinness, O. P., & Wasserman, D. H. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.021048 · Cited by 145
SUBCELLULAR DISTRIBUTION OF d ‐AMINO ACID OXIDASE AND CATALASE IN RAT BRAIN
Gaunt, G. L., & Duve, C. D. (1976) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1976.tb04447.x-i1 · Cited by 144
Radak, Z. O., Pucsok, J. M., Mecseki, S., Csont, T., & Ferdinandy, P. (1999) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(98)00309-8 · Cited by 135
Self-citationREDUCTION OF γ‐AMINOBUTYRIC ACID LEVEL IN THE CAT CEREBRAL CORTEX BY AFFERENT ELECTRICAL STIMULATION
Lichtshtcin, D., & Dobkin, J. (1976) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1976.tb04448.x · Cited by 113
Redox Control of Signal Transduction, Gene Expression and Cellular Senescence
Esposito, F., Ammendola, R., Faraonio, R., Russo, T., & Cimino, F. (2004) · Neurochemical Research · doi:10.1023/b:nere.0000014832.78725.1a · Cited by 113
Long-term treadmill exercise induces neuroprotective molecular changes in rat brain
Bayod, S., del Valle, J., Canudas, A. M., Lalanza, J. F., Sanchez‐Roige, S., Camins, A., Escorihuela, R. M., & Pallàs, M. (2011) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00425.2011 · Cited by 107
The effect of exercise and nettle supplementation on oxidative stress markers in the rat brain
Toldy, A., Stadler, K., Sasvári, M., Jakus, J., Jung, K. J., Chung, H. Y., Berkes, I., Nyakas, C. J., & Radak, Z. O. (2005) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2005.02.028 · Cited by 106
Self-citationNakamoto, H., Kaneko, T., Tahara, S., Hayashi, E., Naıto, H., Radak, Z. O., & Goto, S. (2007) · Experimental Gerontology · doi:10.1016/j.exger.2006.11.006 · Cited by 105
Self-citationMoorthy, K., Sharma, D., Basir, S. F., & Baquer, N. Z. (2005) · Experimental Gerontology · doi:10.1016/j.exger.2005.01.004 · Cited by 96
Functional foods and physical activities in health promotion of aging people
Ferrari, C. K. B. (2007) · Maturitas · doi:10.1016/j.maturitas.2007.09.011 · Cited by 77
Yu, L., & Yang, S. J. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.04.063 · Cited by 76
Aging Brain: Prevention of Oxidative Stress by Vitamin E and Exercise
Devi, S. A. (2009) · The Scientific World JOURNAL · doi:10.1100/tsw.2009.46 · Cited by 42
Hippocampal functional hyperemia mediated by NMDA receptor/NO signaling in rats during mild exercise
Nishijima, T., Okamoto, M., Matsui, T., Kita, I., & Soya, H. (2011) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00763.2011 · Cited by 38
Offen, D., Hochman, A., Gorodin, S., Ziv, I., Shirvan, A., Barzilai, A., & Melamed, E. (1999) · PubMed · Cited by 38
Hescham, S., Grace, L. K., Kellaway, L. A., Bugarith, K., & Russell, V. A. (2009) · Metabolic Brain Disease · doi:10.1007/s11011-009-9165-2 · Cited by 30
Moorthy, K., Yadav, U. C. S., Siddiqui, M. R., Mantha, A. K., Basir, S. F., Sharma, D., Cowsik, S. M., & Baquer, N. Z. (2005) · Biogerontology · doi:10.1007/s10522-005-4810-6 · Cited by 28
LaPolt, P. S., Yu, S. M., & Lu, J. K. H. (1988) · Biology of Reproduction · doi:10.1095/biolreprod38.5.987 · Cited by 25
Ww, M. (1967) · PubMed · Cited by 24
Aydın, C., SONAT, F. A., Şahin, Ş., Cangül, İ. T., & Özkaya, G. (2009) · PubMed · Cited by 22
Effects of an Exercise Program on Frontal Lobe Cognitive Function in Elders
Shin, M. (2009) · Journal of Korean Academy of Nursing · doi:10.4040/jkan.2009.39.1.107 · Cited by 20
Bergersen, L. H., & Storm‐Mathisen, J. (2006) · PubMed · Cited by 3
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- Bradford, 1976, New, rapid, sensitive method for protein determination, Fed Proc, 35, 274
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Booth, F. W., Roberts, C. K., Thyfault, J. P., Ruegsegger, G. N., & Toedebusch, R. G. (2017) · Physiological Reviews · doi:10.1152/physrev.00019.2016 · Cited by 696
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Metadata
- Authors
- Marosi, K., Bori, Z., Hart, N., Sárga, L., Koltai, E., Radák, Z., & Nyakas, C.
- Affiliations
- Semmelweis University (HU)
- Corresponding author
- Nyakas, C.
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2012-12
- Volume
- 226
- Pages
- 21-28
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W2130449421
- Cited by
- 186
- References
- 60
- Citations by year
- 2026: 9 · 2025: 14 · 2024: 11 · 2023: 9 · 2022: 14 · 2021: 17 · 2020: 7 · 2019: 16 · 2018: 17 · 2017: 14 · 2016: 19 · 2015: 14 · 2014: 12 · 2013: 12 · 2012: 1
- FWCI
- 13.20
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Repository of the Academy's Library (Library of the Hungarian Academy of Sciences) (acceptedVersion)
- Topics
- Health Sciences › Medicine › Physiology (medical) › Exercise and Physiological Responses
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- physical activity, oxidative stress, hippocampus, aging, reactive oxygen species, protein carbonyls, superoxide dismutase, glutathione peroxidase, AMPK, PGC-1α, mitochondrial biogenesis, neuroprotection, antioxidant enzymes, redox homeostasis
- MeSH terms
- Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha, Aging, Animals, Antioxidants, Female, Glutathione Peroxidase, Hippocampus, Physical Conditioning, Animal, Superoxide Dismutase, Transcription Factors, Blotting, Western, RNA-Binding Proteins, Rats, Wistar, Reactive Oxygen Species, Cyclic AMP-Dependent Protein Kinases, Oxidative Stress, Protein Carbonylation, Rats
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