Mitohormesis in exercise training

Merry, Troy L.; Ristow, Michael

doi:10.1016/j.freeradbiomed.2015.11.032

Cited by 176Exercise and Physiological ResponsesMitochondrial Function and PathologyAdipose Tissue and Metabolism

Mitohormesis in exercise training

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Merry, Troy L., Ristow, Michael·2016·Free Radical Biology and Medicine

DOI 10.1016/j.freeradbiomed.2015.11.032

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Abstract

Hormesis is a process whereby exposure to a low dose of a potentially harmful stressor promotes adaptive changes to the cell that enables it to better tolerate subsequent stress. In recent years this concept has been applied specifically to the mitochondria (mitohormesis), suggesting that in response to a perturbation the mitochondria can initiate and transduce a signal to the nucleus that coordinates a transcriptional response resulting in both mitochondrial and non-mitochondrial adaptations that return and maintain cellular homeostasis. In this review we summarize the evidence that mitohormesis is a significant adaptive-response signaling pathway, and suggest that it plays a role in mediating exercise-induced adaptations. We discuss potential mitochondrial emitters of retrograde signals that may activate known exercise-sensitive transcription factors to modulate transcription responses to exercise, and draw on evidence from mitochondrial dysfunction animal models to support a role for mitohormesis in mitochondrial biogenesis. Studies directly linking mitohormesis to the exercise training response are lacking, however mounting evidence suggests numerous signals are emitted from the mitochondria during exercise and have the potential to induce a nuclear transcription response, with reactive oxygen species (ROS) being the primary candidate.

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Contracting muscle generates ROS and this is accompanied by increased antioxidant defense orchestrated by NFE2L2.
“It is well established that contracting muscle generates ROS and that this is accompanied by increased antioxidant defense orchestrated by NFE2L2 (2, 7, 36).”
From Skeletal muscle NOX4 is required for adaptive responses that prevent insulin resistance (2021) · cites this paper as [36]

4 retracted

RETRACTED: Endurance exercise rescues progeroid aging and induces systemic mitochondrial rejuvenation in mtDNA mutator mice
Safdar, A., Bourgeois, J. M., Ogborn, D. I., Little, J. P., Hettinga, B. P., Akhtar, M., Thompson, J. E., Melov, S., Mocellin, N. J., Kujoth, G. C., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019581108 · Cited by 358 · see citing works
Retracted
RETRACTED: Activation of the PPAR/PGC-1α Pathway Prevents a Bioenergetic Deficit and Effectively Improves a Mitochondrial Myopathy Phenotype
Wenz, T., Diaz, F., Spiegelman, B. M., & Moraes, C. T. (2008) · Cell Metabolism · doi:10.1016/j.cmet.2008.07.006 · Cited by 297 · see citing works
Retracted
Hepatitis C Virus NS5A and Subgenomic Replicon Activate NF-κB via Tyrosine Phosphorylation of IκBα and Its Degradation by Calpain Protease
Waris, G., Livolsi, A., Imbert, V., Peyron, J., & Siddiqui, A. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m303248200 · Cited by 117 · see citing works
Retracted
Endurance exercise is protective for mice with mitochondrial myopathy
Wenz, T., Diaz, F., Hernandez, D., & Moraes, C. T. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.91571.2008 · Cited by 78 · see citing works
Retracted
Sequence and organization of the human mitochondrial genome
Anderson, S., Bankier, A. T., Barrell, B. G., de Bruijn, M. H. L., Coulson, A. R., Drouin, J., Eperon, I. C., Nierlich, D. P., Roe, B. A., Sanger, F., et al. (1981) · Nature · doi:10.1038/290457a0 · Cited by 9,640 · see citing works
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 · see citing works
Health benefits of physical activity: the evidence
Warburton, D. E. R. (2006) · Canadian Medical Association Journal · doi:10.1503/cmaj.051351 · Cited by 8,007 · see citing works
A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis
Boström, P., Wu, J., Jedrychowski, M. P., Korde, A., Ye, L., Lo, J. C., Rasbach, K. A., Boström, E. A., Choi, J. H., Long, J. Z., et al. (2012) · Nature · doi:10.1038/nature10777 · Cited by 4,810 · see citing works
A Syndrome produced by Diverse Nocuous Agents
Selye, H. (1936) · Nature · doi:10.1038/138032a0 · Cited by 3,967 · see citing works
Effects of a combination of beta carotene and vitamin A on lung cancer and cardiovascular disease
Omenn, G. S., Goodman, G. E., Thornquist, M. D., Balmes, J., Cullen, M. R., Glass, A., Keogh, J. P., Meyskens, F. L., Valanis, B., Williams, J. H., et al. (1996) · New England Journal of Medicine · doi:10.1056/nejm199605023341802 · Cited by 3,638 · see citing works
Oxidative Stress and Neurodegenerative Diseases: A Review of Upstream and Downstream Antioxidant Therapeutic Options
Uttara, B., Singh, A., Zamboni, P., & Mahajan, R. (2009) · Current Neuropharmacology · doi:10.2174/157015909787602823 · Cited by 3,378 · see citing works
Reactive oxygen species in cell signaling
Thannickal, V. J., & Fanburg, B. L. (2000) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.2000.279.6.l1005 · Cited by 2,936 · see citing works
Physiological Roles of Mitochondrial Reactive Oxygen Species
Sena, L. A., & Chandel, N. S. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.09.025 · Cited by 2,632 · see citing works
Reactive oxygen species have a causal role in multiple forms of insulin resistance
Houstis, N., Rosen, E. D., & Lander, E. S. (2006) · Nature · doi:10.1038/nature04634 · Cited by 2,525 · see citing works
Exercise-Induced Oxidative Stress: Cellular Mechanisms and Impact on Muscle Force Production
Powers, S. K., & Jackson, M. J. (2008) · Physiological Reviews · doi:10.1152/physrev.00031.2007 · Cited by 2,459 · see citing works
Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer
WISEMAN, H., & HALLIWELL, B. (1996) · Biochemical Journal · doi:10.1042/bj3130017 · Cited by 2,345 · see citing works
Mortality in Randomized Trials of Antioxidant Supplements for Primary and Secondary Prevention: Systematic Review and Meta-analysis
Bjelakovic, G., Nikolova, D., Gluud, L. L., Simonetti, R. G., & Gluud, C. (2007) · JAMA · doi:10.1001/jama.297.8.842 · Cited by 2,275 · see citing works
Exercise Metabolism and the Molecular Regulation of Skeletal Muscle Adaptation
Egan, B., & Zierath, J. R. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2012.12.012 · Cited by 2,084 · see citing works
Adaptations of skeletal muscle to endurance exercise and their metabolic consequences
Holloszy, J. O., & Coyle, E. F. (1984) · Journal of Applied Physiology · doi:10.1152/jappl.1984.56.4.831 · Cited by 1,985 · see citing works
SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function
Price, N. L., Gomes, A. P., Ling, A. J. Y., Duarte, F. V., Martin-Montalvo, A., North, B. J., Agarwal, B., Ye, L., Ramadori, G., Teodoro, J. S., et al. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.04.003 · Cited by 1,602 · see citing works
Antioxidants prevent health-promoting effects of physical exercise in humans
Ristow, M., Zarse, K., Oberbach, A., Klöting, N., Birringer, M., Kiehntopf, M., Stumvoll, M., Kahn, C. R., & Blüher, M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0903485106 · Cited by 1,582 · see citing works
Self-citation
Extension of Life-Span by Overexpression of Superoxide Dismutase and Catalase in Drosophila melanogaster
Orr, W. C., & Sohal, R. S. (1994) · Science · doi:10.1126/science.8108730 · Cited by 1,461 · see citing works
Invited Review: Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance
Kregel, K. C. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01267.2001 · Cited by 1,450 · see citing works
Exercise, GLUT4, and skeletal muscle glucose uptake
Richter, E. A., & Hargreaves, M. (2013) · Physiological Reviews · doi:10.1152/physrev.00038.2012 · Cited by 1,407 · see citing works
Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL
Jin, S. M., Lazarou, M., Wang, C., Kane, L. A., Narendra, D. P., & Youle, R. J. (2010) · Journal of Cell Biology · doi:10.1083/jcb.201008084 · Cited by 1,375 · see citing works
Effects of Long-term Vitamin E Supplementation on Cardiovascular Events and Cancer: A Randomized Controlled Trial
(2005) · JAMA · doi:10.1001/jama.293.11.1338 · Cited by 1,209 · see citing works
Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress
Schulz, T. J., Zarse, K., Voigt, A., Urban, N., Birringer, M., & Ristow, M. (2007) · Cell Metabolism · doi:10.1016/j.cmet.2007.08.011 · Cited by 1,209 · see citing works
Self-citation
Integrative Biology of Exercise
Hawley, J. A., Hargreaves, M., Joyner, M. J., & Zierath, J. R. (2014) · Cell · doi:10.1016/j.cell.2014.10.029 · Cited by 1,152 · see citing works
The role of exercise and PGC1α in inflammation and chronic disease
Handschin, C., & Spiegelman, B. M. (2008) · Nature · doi:10.1038/nature07206 · Cited by 1,083 · see citing works
Use of antioxidant vitamins for the prevention of cardiovascular disease: meta-analysis of randomised trials
Vivekananthan, D. P., Penn, M. S., Sapp, S. K., Hsu, A., & Topol, E. J. (2003) · The Lancet · doi:10.1016/s0140-6736(03)13637-9 · Cited by 1,083 · see citing works
The Cell Non-Autonomous Nature of Electron Transport Chain-Mediated Longevity
Durieux, J., Wolff, S., & Dillin, A. (2011) · Cell · doi:10.1016/j.cell.2010.12.016 · Cited by 1,059 · see citing works
Mitochondrial Import Efficiency of ATFS-1 Regulates Mitochondrial UPR Activation
Nargund, A. M., Pellegrino, M., Fiorese, C. J., Baker, B. M., & Haynes, C. M. (2012) · Science · doi:10.1126/science.1223560 · Cited by 1,027 · see citing works
Extension of Life-Span with Superoxide Dismutase/Catalase Mimetics
Melov, S., Ravenscroft, J., Malik, S., Gill, M. S., Walker, D. W., Clayton, P., Wallace, D. C., Malfroy, B., Doctrow, S. R., & Lithgow, G. J. (2000) · Science · doi:10.1126/science.289.5484.1567 · Cited by 913 · see citing works
Vitamins E and C in the Prevention of Cardiovascular Disease in Men: The Physicians' Health Study II Randomized Controlled Trial
Sesso, H. D. (2008) · JAMA · doi:10.1001/jama.2008.600 · Cited by 913 · see citing works
The Human Mitochondrial Transcriptome
Mercer, T. R., Neph, S., Dinger, M. E., Crawford, J., Smith, M. A., Shearwood, A.-M. J., Haugen, E., Bracken, C. P., Rackham, O., Stamatoyannopoulos, J. A., et al. (2011) · Cell · doi:10.1016/j.cell.2011.06.051 · Cited by 905 · see citing works
-Tocopherol and beta-Carotene Supplements and Lung Cancer Incidence in the Alpha-Tocopherol, Beta-Carotene Cancer Prevention Study: Effects of Base-line Characteristics and Study Compliance
Albanes, D., Heinonen, O. P., Taylor, P. R., Virtamo, J., Edwards, B. K., Rautalahti, M. T., Hartman, A. M., Palmgren, J., Freedman, L. S., Haapakoski, J., et al. (1996) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/88.21.1560 · Cited by 902 · see citing works
Mitochondrial Signaling
Butow, R. A., & Avadhani, N. G. (2004) · Molecular Cell · doi:10.1016/s1097-2765(04)00179-0 · Cited by 882 · see citing works
Oral administration of vitamin C decreases muscle mitochondrial biogenesis and hampers training-induced adaptations in endurance performance
Gomez-Cabrera, M.-C., Domenech, E., Romagnoli, M., Arduini, A., Borras, C., Pallardo, F. V., Sastre, J., & Viña, J. (2008) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/87.1.142 · Cited by 844 · see citing works
How increased oxidative stress promotes longevity and metabolic health: The concept of mitochondrial hormesis (mitohormesis)
Ristow, M., & Zarse, K. (2010) · Experimental Gerontology · doi:10.1016/j.exger.2010.03.014 · Cited by 789 · see citing works
Self-citation
Interactions between NO and reactive oxygen species: pathophysiological importance in atherosclerosis, hypertension, diabetes and heart failure
Kojda, G. (1999) · Cardiovascular Research · doi:10.1016/s0008-6363(99)00169-8 · Cited by 769 · see citing works
A Clinical Trial of Antioxidant Vitamins to Prevent Colorectal Adenoma
Greenberg, E. R., Baron, J. A., Tosteson, T. D., Freeman, D. H., Beck, G. J., Bond, J. H., Colacchio, T. A., Coller, J. A., Frankl, H. D., Haile, R. W., et al. (1994) · New England Journal of Medicine · doi:10.1056/nejm199407213310301 · Cited by 761 · see citing works
The Mitochondrial-Derived Peptide MOTS-c Promotes Metabolic Homeostasis and Reduces Obesity and Insulin Resistance
Lee, C., Zeng, J., Drew, B. G., Sallam, T., Martin-Montalvo, A., Wan, J., Kim, S.-J., Mehta, H., Hevener, A. L., de Cabo, R., et al. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.02.009 · Cited by 715 · see citing works
Regulation of mitochondrial biogenesis in skeletal muscle by CaMK
Wu, H., Kanatous, S. B., Thurmond, F. A., Gallardo, T., Isotani, E., Bassel-Duby, R., & Williams, R. S. (2002) · Science · doi:10.1126/science.1071163 · Cited by 684 · see citing works
Mitochondrial retrograde signaling
Liu, Z., & Butow, R. A. (2006) · Annual Review of Genetics · doi:10.1146/annurev.genet.40.110405.090613 · Cited by 680 · see citing works
Methionine sulfoxide reductase (MsrA) is a regulator of antioxidant defense and lifespan in mammals
Moskovitz, J., Barnoy, S., Williams, W. M., Requena, J. R., Berlett, B. S., & Stadtman, E. R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.231472998 · Cited by 677 · see citing works
Compartment-specific perturbation of protein handling activates genes encoding mitochondrial chaperones
Yoneda, T., Benedetti, C., Urano, F., Clark, S. G., Harding, H. P., & Ron, D. (2004) · Journal of Cell Science · doi:10.1242/jcs.01275 · Cited by 636 · see citing works
Mitohormesis
Yun, J., & Finkel, T. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.01.011 · Cited by 626 · see citing works
Humanin peptide suppresses apoptosis by interfering with Bax activation
Guo, B., Zhai, D., Cabezas, E., Welsh, K., Nouraini, S., Satterthwait, A. C., & Reed, J. C. (2003) · Nature · doi:10.1038/nature01627 · Cited by 619 · see citing works
The mitochondrial p53 pathway
Vaseva, A. V., & Moll, U. M. (2008) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2008.10.005 · Cited by 618 · see citing works
The mitochondrial UPR – protecting organelle protein homeostasis
Haynes, C. M., & Ron, D. (2010) · Journal of Cell Science · doi:10.1242/jcs.075119 · Cited by 490 · see citing works
Exercise-induced mitochondrial biogenesis begins before the increase in muscle PGC-1α expression.
Wright, D. C., Han, D.-H., Garcia-Roves, P. M., Geiger, P. C., Jones, T. E., & Holloszy, J. O. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m606116200 · Cited by 488 · see citing works
Mitochondrial calcium transport
Nicholls, D. G., & Åkerman, K. E. O. (1982) · Biochimica et Biophysica Acta (BBA) - Reviews on Bioenergetics · doi:10.1016/0304-4173(82)90013-1 · Cited by 486 · see citing works
AMPK and the biochemistry of exercise: implications for human health and disease
Richter, E. A., & Ruderman, N. B. (2009) · Biochemical Journal · doi:10.1042/bj20082055 · Cited by 481 · see citing works
Decreasing xanthine oxidase‐mediated oxidative stress prevents useful cellular adaptations to exercise in rats
Gómez‐Cabrera, M. C., Borrás, C., Pallardó, F. V., Sastre, J., Ji, L. L., & Viña, J. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2004.080564 · Cited by 477 · see citing works
Vitamin and mineral supplements in the primary prevention of cardiovascular disease and cancer: an updated systematic evidence review for the U.S. Preventive Services Task Force
Fortmann, S. P., Burda, B. U., Senger, C. A., Lin, J. S., & Whitlock, E. P. (2013) · Annals of Internal Medicine · doi:10.7326/0003-4819-159-12-201312170-00729 · Cited by 442 · see citing works
Reactive Oxygen Species Are Signalling Molecules for Skeletal Muscle Adaptation
Powers, S. K., Duarte, J., Kavazis, A. N., & Talbert, E. E. (2010) · Experimental Physiology · doi:10.1113/expphysiol.2009.050526 · Cited by 440 · see citing works
Biological and physiological role of reactive oxygen species - the good, the bad and the ugly
Zuo, L., Zhou, T., Pannell, B. K., Ziegler, A. C., & Best, T. M. (2015) · Acta Physiologica · doi:10.1111/apha.12515 · Cited by 430 · see citing works
Impaired insulin/IGF1 signaling extends life span by promoting mitochondrial L-proline catabolism to induce a transient ROS signal
Zarse, K., Schmeisser, S., Groth, M., Priebe, S., Beuster, G., Kuhlow, D., Guthke, R., Platzer, M., Kahn, C. R., & Ristow, M. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.02.013 · Cited by 430 · see citing works
Self-citation
RTG1 and RTG2: two yeast genes required for a novel path of communication from mitochondria to the nucleus
Liao, X., & Butow, R. A. (1993) · Cell · doi:10.1016/0092-8674(93)90050-z · Cited by 419 · see citing works
Analysis of global mRNA expression in human skeletal muscle during recovery from endurance exercise
Mahoney, D. J., Parise, G., Melov, S., Safdar, A., & Tarnopolsky, M. A. (2005) · The FASEB Journal · doi:10.1096/fj.04-3149fje · Cited by 418 · see citing works
Unraveling the Truth About Antioxidants: Mitohormesis explains ROS-induced health benefits
Ristow, M. (2014) · Nature Medicine · doi:10.1038/nm.3624 · Cited by 417 · see citing works
Self-citation
Mutations in the clk-1 gene of Caenorhabditis elegans affect developmental and behavioral timing
Wong, A., Boutis, P., & Hekimi, S. (1995) · Genetics · doi:10.1093/genetics/139.3.1247 · Cited by 416 · see citing works
Muscle Mitohormesis Promotes Longevity via Systemic Repression of Insulin Signaling
Owusu-Ansah, E., Song, W., & Perrimon, N. (2013) · Cell · doi:10.1016/j.cell.2013.09.021 · Cited by 395 · see citing works
Null mutation of copper/zinc superoxide dismutase in Drosophila confers hypersensitivity to paraquat and reduced longevity.
Phillips, J. P., Campbell, S. D., Michaud, D., Charbonneau, M., & Hilliker, A. J. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.8.2761 · Cited by 389 · see citing works
Genome-wide responses to mitochondrial dysfunction
Epstein, C. B., Waddle, J. A., Hale, W., Davé, V., Thornton, J., Macatee, T. L., Garner, H. R., & Butow, R. A. (2001) · Molecular Biology of the Cell · doi:10.1091/mbc.12.2.297 · Cited by 389 · see citing works
Effects of extract of western red-cedar heartwood on certain wood-decaying fungi in culture
Southam, C. M., & Ehrlich, J. (1943) · Phytopathology · Cited by 370 · see citing works
Retrograde Ca2+ signaling in C2C12 skeletal myocytes in response to mitochondrial genetic and metabolic stress: a novel mode of inter-organelle crosstalk
Biswas, G., Adebanjo, O. A., Freedman, B. D., Anandatheerthavarada, H. K., Vijayasarathy, C., Zaidi, M., Kotlikoff, M., & Avadhani, N. G. (1999) · The EMBO Journal · doi:10.1093/emboj/18.3.522 · Cited by 369 · see citing works
Evolutionary conservation of the <i>clk-1</i> -dependent mechanism of longevity: loss of <i>mclk1</i> increases cellular fitness and lifespan in mice
Liu, X., Jiang, N., Hughes, B., Bigras, E., Shoubridge, E., & Hekimi, S. (2005) · Genes & Development · doi:10.1101/gad.1352905 · Cited by 345 · see citing works
Celastrol Protects against Obesity and Metabolic Dysfunction through Activation of a HSF1-PGC1α Transcriptional Axis
Ma, X., Xu, L., Alberobello, A. T., Gavrilova, O., Bagattin, A., Skarulis, M. C., Liu, J., Finkel, T., & Mueller, E. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.08.005 · Cited by 337 · see citing works
Vitamin C and E supplementation hampers cellular adaptation to endurance training in humans: a double‐blind, randomised, controlled trial
Paulsen, G., Cumming, K. T., Holden, G., Hallén, J., Rønnestad, B. R., Sveen, O., Skaug, A., Paur, I., Bastani, N. E., Østgaard, H. N., et al. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2013.267419 · Cited by 333 · see citing works
The Mitochondrial Genotype Can Influence Nuclear Gene Expression in Yeast
Parikh, V. S., Morgan, M. M., Scott, R., Clements, L. S., & Butow, R. A. (1987) · Science · doi:10.1126/science.3027892 · Cited by 324 · see citing works
Activation of calcium signaling through Trpv1 by nNOS and peroxynitrite as a key trigger of skeletal muscle hypertrophy
Ito, N., Rüegg, U. T., Kudō, A., Miyagoe‐Suzuki, Y., & Takeda, S. (2012) · Nature Medicine · doi:10.1038/nm.3019 · Cited by 315 · see citing works
Calcium Induces Increases in Peroxisome Proliferator-activated Receptor γ Coactivator-1α and Mitochondrial Biogenesis by a Pathway Leading to p38 Mitogen-activated Protein Kinase Activation
Wright, D. C., Geiger, P. C., Han, D.-H., Jones, T. E., & Holloszy, J. O. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m611252200 · Cited by 309 · see citing works
Modulation of skeletal muscle antioxidant defense by exercise: Role of redox signaling
Ji, L. L. (2007) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.02.031 · Cited by 291 · see citing works
Humanin: a harbinger of mitochondrial-derived peptides
Lee, C., Yen, K., & Cohen, P. (2013) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2013.01.005 · Cited by 284 · see citing works
Reactive oxygen species and insulin resistance: the good, the bad and the ugly
Tiganis, T. (2011) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2010.11.006 · Cited by 256 · see citing works
Pharmacological Inhibition of poly(ADP-ribose) polymerases improves fitness and mitochondrial function in skeletal muscle
Pirinen, E., Cantó, C., Jo, Y. S., Morato, L., Zhang, H., Menzies, K. J., Williams, E. G., Mouchiroud, L., Moullan, N., Hagberg, C., et al. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.04.002 · Cited by 254 · see citing works
Humanin: A Novel Central Regulator of Peripheral Insulin Action
Muzumdar, R. H., Huffman, D. M., Atzmon, G., Buettner, C., Cobb, L. J., Fishman, S., Budagov, T., Cui, L., Einstein, F. H., Poduval, A., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006334 · Cited by 248 · see citing works
Sublethal mitochondrial stress with an attendant stoichiometric augmentation of reactive oxygen species may precipitate many of the beneficial alterations in cellular physiology produced by caloric restriction, intermittent fasting, exercise and dietary phytonutrients: “Mitohormesis” for health and vitality
Tapia, P. C. (2005) · Medical Hypotheses · doi:10.1016/j.mehy.2005.09.009 · Cited by 239 · see citing works
Role of sirtuins in lifespan regulation is linked to methylation of nicotinamide
Schmeisser, K., Mansfeld, J., Kuhlow, D., Weimer, S., Priebe, S., Heiland, I., Birringer, M., Groth, M., Segref, A., Kanfi, Y., et al. (2013) · Nature Chemical Biology · doi:10.1038/nchembio.1352 · Cited by 236 · see citing works
Self-citation
Independent and Combined Effects of Exercise Training and Metformin on Insulin Sensitivity in Individuals With Prediabetes
Malin, S. K., Gerber, R., Chipkin, S. R., & Braun, B. (2011) · Diabetes Care · doi:10.2337/dc11-0925 · Cited by 236 · see citing works
PGC-1α is not mandatory for exercise- and training-induced adaptive gene responses in mouse skeletal muscle
Leick, L., Wojtaszewski, J. F. P., Johansen, S. T., Kiilerich, K., Comes, G., Hellsten, Y., Hidalgo, J., & Pilegaard, H. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00666.2007 · Cited by 236 · see citing works
Antioxidant supplements and mortality
Bjelakovic, G., Nikolova, D., & Gluud, C. (2013) · Current Opinion in Clinical Nutrition and Metabolic Care · doi:10.1097/mco.0000000000000009 · Cited by 234 · see citing works
Frataxin activates mitochondrial energy conversion and oxidative phosphorylation
Ristow, M., Pfister, M. F., Yee, A. J., Schubert, M., Michael, L., Zhang, C., Ueki, K., Michael, M. D., Lowell, B. B., & Kahn, C. R. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.220403797 · Cited by 221 · see citing works
Self-citation
A Basic Helix-Loop-Helix–Leucine Zipper Transcription Complex in Yeast Functions in a Signaling Pathway from Mitochondria to the Nucleus
Jia, Y., Rothermel, B., Thornton, J., & Butow, R. A. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.3.1110 · Cited by 219 · see citing works
Intramitochondrial functions regulate nonmitochondrial citrate synthase (CIT2) expression in Saccharomyces cerevisiae.
Liao, X. S., Small, W. C., Srere, P. A., & Butow, R. A. (1991) · Molecular and Cellular Biology · doi:10.1128/mcb.11.1.38 · Cited by 218 · see citing works
Selective delivery of doxorubicin to patients with breast carcinoma metastases by stealth liposomes
Symon, Z., PEYSER, A. B., Tzemach, D., Lyass, O., Sucher, E., Shezen, E., & Gabizón, A. (1999) · Cancer · doi:10.1002/(sici)1097-0142(19990701)86:1 · Cited by 214 · see citing works
Loss of Skeletal Muscle HIF-1α Results in Altered Exercise Endurance
Mason, S. D., Howlett, R. A., Kim, M. J., Olfert, I. M., Hogan, M. C., McNulty, W., Hickey, R. P., Wagner, P. D., Kahn, C. R., Giordano, F. J., et al. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020288 · Cited by 210 · see citing works
Metformin increases the PGC-1α protein and oxidative enzyme activities possibly via AMPK phosphorylation in skeletal muscle in vivo
Suwa, M., Egashira, T., Nakano, H., Sasaki, H., & Kumagai, S. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00255.2006 · Cited by 210 · see citing works
Early Mitochondrial Dysfunction in Long-lived Mclk1+/- Mice
Lapointe, J., & Hekimi, S. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m803287200 · Cited by 207 · see citing works
CREB activation induced by mitochondrial dysfunction is a new signaling pathway that impairs cell proliferation
Arnould, T., Vankoningsloo, S., Renard, P., Houbion, A., Ninane, N., Demazy, C., Remacle, J., & Raes, M. (2002) · The EMBO Journal · doi:10.1093/emboj/21.1.53 · Cited by 201 · see citing works
p53 Improves Aerobic Exercise Capacity and Augments Skeletal Muscle Mitochondrial DNA Content
Park, J., Wang, P., Matsumoto, T., Sung, H. J., Ma, W., Choi, J. W., Anderson, S. A., Leary, S. C., Balaban, R. S., Kang, J., et al. (2009) · Circulation Research · doi:10.1161/circresaha.109.205310 · Cited by 200 · see citing works
NAD+/NADH and skeletal muscle mitochondrial adaptations to exercise
White, A. T., & Schenk, S. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00054.2012 · Cited by 193 · see citing works
Surveillance-Activated Defenses Block the ROS–Induced Mitochondrial Unfolded Protein Response
Runkel, E. D., Liu, S., Baumeister, R., & Schulze, E. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003346 · Cited by 192 · see citing works
Antioxidant Supplementation Reduces Skeletal Muscle Mitochondrial Biogenesis
Strobel, N., Peake, J. M., Matsumoto, A., Marsh, S. A., Coombes, J. S., & Wadley, G. D. (2010) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e318203afa3 · Cited by 187 · see citing works
Sirtuin 1 (SIRT1) Deacetylase Activity Is Not Required for Mitochondrial Biogenesis or Peroxisome Proliferator-activated Receptor-γ Coactivator-1α (PGC-1α) Deacetylation following Endurance Exercise
Philp, A., Chen, A., Lan, D., Meyer, G. A., Murphy, A. N., Knapp, A. E., Olfert, I. M., McCurdy, C. E., Marcotte, G. R., Hogan, M. C., et al. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.261685 · Cited by 184 · see citing works
A Systems Approach for Decoding Mitochondrial Retrograde Signaling Pathways
Chae, S., Ahn, B. Y., Byun, K., Cho, Y. M., Yu, M., Lee, B., Hwang, D., & Park, K. S. (2013) · Science Signaling · doi:10.1126/scisignal.2003266 · Cited by 184 · see citing works
Antioxidant Supplementation Does Not Alter Endurance Training Adaptation
Yfanti, C., Akerstrom, T. C. A., Nielsen, S. J., Nielsen, A. R., Mounier, R., Mortensen, O. H., Lykkesfeldt, J., Rose, A. J., Fischer, C. P., & Pedersen, B. K. (2010) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3181cd76be · Cited by 182 · see citing works
Epidermal Sensing of Oxygen Is Essential for Systemic Hypoxic Response
Boutin, A. T., Weidemann, A., Fu, Z., Mesropian, L., Gradin, K., Jamora, C., Wiesener, M. S., Eckardt, K., Koch, C. J., Ellies, L. G., et al. (2008) · Cell · doi:10.1016/j.cell.2008.02.038 · Cited by 177 · see citing works
Role of AMPKα2 in basal, training-, and AICAR-induced GLUT4, hexokinase II, and mitochondrial protein expression in mouse muscle
Jørgensen, S. B., Treebak, J. T., Viollet, B., Schjerling, P., Vaulont, S., Wojtaszewski, J. F. P., & Richter, E. A. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00243.2006 · Cited by 176 · see citing works
Redox modulation of mitochondriogenesis in exercise. Does antioxidant supplementation blunt the benefits of exercise training?
Gomez-Cabrera, M. C., Salvador-Pascual, A., Cabo, H., Ferrando, B., & Viña, J. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.04.006 · Cited by 172 · see citing works
Sirtuin 1-mediated Effects of Exercise and Resveratrol on Mitochondrial Biogenesis
Menzies, K. J., Singh, K., Saleem, A., & Hood, D. A. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.431155 · Cited by 167 · see citing works
Antioxidant supplementation does not affect fasting plasma glucose in the Supplementation with Antioxidant Vitamins and Minerals (SU.VI.MAX) study in France: association with dietary intake and plasma concentrations 1–3
Czernichow, S., Couthouis, A., Bertrais, S., Vergnaud, A., Dauchet, L., Galan, P., & Herçberg, S. (2006) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/84.1.394 · Cited by 150 · see citing works
Coupling mitochondrial dysfunction to endoplasmic reticulum stress response: A molecular mechanism leading to hepatic insulin resistance
LIM, J., Lee, H., HOJUNG, M., & Song, J. (2008) · Cellular Signalling · doi:10.1016/j.cellsig.2008.10.004 · Cited by 149 · see citing works
Vitamin C and E supplementation alters protein signalling after a strength training session, but not muscle growth during 10 weeks of training
Paulsen, G., Hamarsland, H., Cumming, K. T., Johansen, R. E., Hulmi, J. J., Børsheim, E., Wiig, H., Garthe, I., & Raastad, T. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.279950 · Cited by 148 · see citing works
Normal adaptations to exercise despite protection against oxidative stress
Higashida, K., Kim, S. H., Higuchi, M., Holloszy, J. O., & Han, D.-H. (2011) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00655.2010 · Cited by 148 · see citing works
Neuronal ROS signaling rather than AMPK/sirtuin-mediated energy sensing links dietary restriction to lifespan extension
Schmeisser, S., Priebe, S., Groth, M., Monajembashi, S., Hemmerich, P. H., Guthke, R., Platzer, M., & Ristow, M. (2013) · Molecular Metabolism · doi:10.1016/j.molmet.2013.02.002 · Cited by 145 · see citing works
Self-citation
Effects of Long-Term Daily Low-Dose Supplementation With Antioxidant Vitamins and Minerals on Structure and Function of Large Arteries
Zureik, M., Galan, P., Bertrais, S., Mennen, L. I., Czernichow, S., Blacher, J., Ducimetière, P., & Herçberg, S. (2004) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000136648.62973.c8 · Cited by 144 · see citing works
Mitochondrial gene expression and increased oxidative metabolism: Role in increased lifespan of fat-specific insulin receptor knock-out mice
Katic, M., Kennedy, A. R., Leykin, I., Norris, A., McGettrick, A., Gesta, S., Russell, S. J., Bluher, M., Maratos‐Flier, E., & Kahn, C. R. (2007) · Aging Cell · doi:10.1111/j.1474-9726.2007.00346.x · Cited by 141 · see citing works
Compromised mitochondrial function leads to increased cytosolic calcium and to activation of MAP kinases
Luo, Y., Bond, J. D., & Ingram, V. M. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.18.9705 · Cited by 141 · see citing works
The mitochondrial unfolded protein response–synchronizing genomes
Jovaisaite, V., & Auwerx, J. (2015) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2014.12.003 · Cited by 131 · see citing works
The Physiology of Exercise Under Heat Stress
Wyndham, C. H. (1973) · Annual Review of Physiology · doi:10.1146/annurev.ph.35.030173.001205 · Cited by 130 · see citing works
Mitochondrial SSBP1 protects cells from proteotoxic stresses by potentiating stress-induced HSF1 transcriptional activity
Tan, K., Fujimoto, M., Takii, R., Takaki, E., Hayashida, N., & Nakai, A. (2015) · Nature Communications · doi:10.1038/ncomms7580 · Cited by 119 · see citing works
RTG‐dependent mitochondria to nucleus signaling is negatively regulated by the seven WD‐repeat protein Lst8p
Liu, Z., Sekito, T., Epstein, C. B., & Butow, R. A. (2001) · The EMBO Journal · doi:10.1093/emboj/20.24.7209 · Cited by 112 · see citing works
Zur Lehre von der Arzneiwirkung
Schulz, H. (1887) · Archiv für Pathologische Anatomie und Physiologie und für Klinische Medicin · doi:10.1007/bf02281473 · Cited by 105 · see citing works
Increased mitochondrial biogenesis in muscle improves aging phenotypes in the mtDNA mutator mouse
Dillon, L. M., Williams, S. L., Hida, A., Peacock, J. D., Prolla, T. A., Lincoln, J., & Moraes, C. T. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds049 · Cited by 98 · see citing works
A nuclear role for the respiratory enzyme CLK-1 in regulating mitochondrial stress responses and longevity
Monaghan, R. M., Barnes, R. G., Fisher, K., Andreou, T., Rooney, N., Poulin, G. B., & Whitmarsh, A. J. (2015) · Nature Cell Biology · doi:10.1038/ncb3170 · Cited by 90 · see citing works
Overtraining and glycogen depletion hypothesis
Snyder, A. C. (1998) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-199807000-00020 · Cited by 90 · see citing works
Mitochondrial Calcium Uptake Regulates Rapid Calcium Transients in Skeletal Muscle during Excitation-Contraction (E-C) Coupling
Yi, J., Ma, C., Li, Y., Weisleder, N. L., Rı́os, E., Ma, J., & Zhou, J. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.217711 · Cited by 87 · see citing works
Effects of supplemental alpha-tocopherol and beta-carotene on urinary tract cancer: incidence and mortality in a controlled trial (Finland)
Virtamo, J. R. K., Edwards, B. K., Virtanen, M., et al. (2000) · Cancer Causes & Control · doi:10.1023/a:1026546803917 · Cited by 85 · see citing works
Effect of antioxidant supplementation on insulin sensitivity in response to endurance exercise training
Yfanti, C., Nielsen, A. R., Åkerström, T., Nielsen, S., Rose, A. J., Richter, E. A., Lykkesfeldt, J., Fischer, C. P., & Pedersen, B. K. (2011) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00207.2010 · Cited by 85 · see citing works
The effects of supplementation with alpha-tocopherol and beta-carotene on the incidence and mortality of carcinoma of the pancreas in a randomized, controlled trial.
Rautalahti, M. T., Virtamo, J. R. K., Taylor, P. R., et al. (1999) · PubMed · Cited by 81 · see citing works
Effect of supplementation with antioxidants upon long-term risk of hypertension in the SU.VI.MAX study: association with plasma antioxidant levels
Czernichow, S., Bertrais, S., Blacher, J., et al. (2005) · Journal of Hypertension · doi:10.1097/01.hjh.0000187259.94448.8a · Cited by 81 · see citing works
Enhanced insulin-stimulated glycogen synthesis in response to insulin, metformin or rosiglitazone is associated with increased mRNA expression of GLUT4 and peroxisomal proliferator activator receptor gamma co-activator 1
Al-Khalili, L., Forsgren, M., Kannisto, K., Zierath, J. R., Lönnqvist, F., & Krook, A. (2005) · Diabetologia · doi:10.1007/s00125-005-1741-3 · Cited by 78 · see citing works
Morphofunctional and Biochemical Approaches for Studying Mitochondrial Changes during Myoblasts Differentiation
Barbieri, E., Battistelli, M., Casadei, L., Vallorani, L., Piccoli, G., Guescini, M., Gioacchini, A. M., Polidori, E., Zeppa, S. D., Ceccaroli, P., et al. (2011) · Journal of Aging Research · doi:10.4061/2011/845379 · Cited by 78 · see citing works
Haploinsufficiency of Akt1 Prolongs the Lifespan of Mice
Nojima, A., Yamashita, M., Yoshida, Y., Shimizu, I., Ichimiya, H., Kamimura, N., Kobayashi, Y., Ohta, S., Ishii, N., & Minamino, T. (2013) · PLoS ONE · doi:10.1371/journal.pone.0069178 · Cited by 76 · see citing works
Ramping up the signal: promoting endurance training adaptation in skeletal muscle by nutritional manipulation
Hawley, J. A., & Morton, J. P. (2014) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/1440-1681.12246 · Cited by 70 · see citing works
Xanthine oxidase inhibition attenuates skeletal muscle signaling following acute exercise but does not impair mitochondrial adaptations to endurance training
Wadley, G. D., Nicolas, M. A., Hiam, D., & McConell, G. K. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00568.2012 · Cited by 63 · see citing works
Adaptive reactions to stress.
Selye, H., & Fortier, C. (1949) · PubMed · Cited by 63 · see citing works
AMP kinase is not required for the GLUT4 response to exercise and denervation in skeletal muscle
Holmes, B. F., Lang, D. B., Birnbaum, M. J., Mu, J., & Dohm, G. L. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00080.2004 · Cited by 61 · see citing works
Exercise and CaMK activation both increase the binding of MEF2A to theGlut4promoter in skeletal muscle in vivo
Smith, J. A. H., Collins, M., Grobler, L., Magee, C. J., & Ojuka, E. O. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00142.2006 · Cited by 60 · see citing works
Vitamin C Administration Attenuates Overload-Induced Skeletal Muscle Hypertrophy in Rats
Makanae, Y., Kawada, S., Sasaki, K., Nakazato, K., & Ishii, N. (2013) · Acta Physiologica · doi:10.1111/apha.12042 · Cited by 59 · see citing works
Comparative approaches to facilitate the discovery of prolongevity interventions: Effects of tocopherols on lifespan of three invertebrate species
ZOU, S., Sinclair, J. W., WILSON, M., Carey, J. R., Liedo, P., Oropeza, A., KALRA, A., de Cabo, R., INGRAM, D., & Longo, D. L. (2006) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2006.11.026 · Cited by 55 · see citing works
Expression of oxidative phosphorylation components in mitochondria of long-living Ames dwarf mice
Brown-Borg, H. M., Johnson, W. T., & Rakoczy, S. G. (2012) · AGE · doi:10.1007/s11357-011-9212-x · Cited by 52 · see citing works
High-dose antioxidant vitamin C supplementation does not prevent acute exercise-induced increases in markers of skeletal muscle mitochondrial biogenesis in rats
Wadley, G. D., & McConell, G. K. (2010) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00127.2010 · Cited by 49 · see citing works
Hydrogen Peroxide
Faraci, F. M. (2006) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000238355.56172.b3 · Cited by 45 · see citing works
Mitochondria in Skeletal Muscle
Adhihetty, P. J., O′Leary, M. F. N., & Hood, D. A. (2008) · Exercise and Sport Sciences Reviews · doi:10.1097/jes.0b013e31817be7b7 · Cited by 41 · see citing works
Impaired mitochondrial respiration and decreased fatigue resistance followed by severe muscle weakness in skeletal muscle of mitochondrial DNA mutator mice
Yamada, T., Ivarsson, N., Hernández, A., Fahlström, A., Cheng, A. J., Zhang, S., Bruton, J. D., Ulfhake, B., & Westerblad, H. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.240077 · Cited by 41 · see citing works
The AMPK activator R419 improves exercise capacity and skeletal muscle insulin sensitivity in obese mice
Marcinko, K., Bujak, A. L., Lally, J., Ford, R. J., Wong, T. H., Smith, B. K., Kemp, B. E., Jenkins, Y., Li, W., Kinsella, T. M., et al. (2015) · Molecular Metabolism · doi:10.1016/j.molmet.2015.06.002 · Cited by 35 · see citing works
Nicotinamide N-methyltransferase increases complex I activity in SH-SY5Y cells via sirtuin 3
Liu, K. Y., Mistry, R. J., Aguirre, C., Fasouli, E. S., Thomas, M. G., Klamt, F., Ramsden, D. B., & Parsons, R. B. (2015) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2015.10.023 · Cited by 34 · see citing works
Mitohormesis in muscle cells: a morphological, molecular, and proteomic approach
Berberi, E., Sestili, P., Vallorani, L., Guescini, M., Calcabrini, C., Gioacchini, A. M., Annibalini, G., Lucertini, F., Piccoli, G., & Stocchi, V. (2019) · Muscles Ligaments and Tendons Journal · doi:10.32098/mltj.04.2013.05 · Cited by 31 · see citing works
Calcium Content and Respiratory Control Index of Isolated Skeletal Muscle Mitochondria: Effects of Different Isolation Media
Madsen, K., Ertbjerg, P., & Pedersen, P. K. (1996) · Analytical Biochemistry · doi:10.1006/abio.1996.0197 · Cited by 22 · see citing works
XXII. Zur Lehre von der Arzneiwirkung.
Schulz, H. (1887) · De Gruyter eBooks · doi:10.1515/9783112369043-025 · Cited by 6 · see citing works
Compensatory elevation of voluntary activity in mouse mutants with impaired mitochondrial energy metabolism
Lapointe, J., Hughes, B. G., Bigras, E., & Hekimi, S. (2014) · Physiological Reports · doi:10.14814/phy2.12214 · Cited by 3 · see citing works

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Newsholme, P., Cruzat, V. F., Keane, K. N., Carlessi, R., & de Bittencourt, P. I. H. (2016) · Biochemical Journal · doi:10.1042/bcj20160503c · Cited by 878 · see citing works
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López-Otín, C., & Kroemer, G. (2021) · Cell · doi:10.1016/j.cell.2020.11.034 · Cited by 499 · see citing works
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Qiu, Y., Fernández-García, B., Lehmann, H. I., Li, G., Kroemer, G., López-Otín, C., & Xiao, J. (2023) · Journal of Sport and Health Science · doi:10.1016/j.jshs.2022.10.003 · Cited by 270 · see citing works
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Lee, C., Kim, K. H., & Cohen, P. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.05.015 · Cited by 178 · see citing works
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Merry, T. L., Chan, A., Woodhead, J. S. T., Reynolds, J. C., Kumagai, H., Kim, S.-J., & Lee, C. (2020) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00249.2020 · Cited by 141 · see citing works
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Zhou, H., Yuan, D., Gao, W., Tian, J., Sun, H., Yu, S., Wang, J., & Sun, L. (2020) · IUBMB Life · doi:10.1002/iub.2289 · Cited by 22 · see citing works

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Calabrese, E. J., Bachmann, K. A., Bailer, A. J., Bolger, P. M., Borak, J. B., Cai, L., Nina Cedergreen, G., Cherian, M. G., Chiueh, C. C., Clarkson, T. W., et al. (2007) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2007.02.015 · Cited by 751 · see citing works
Adaptive response to hydrogen peroxide in yeast: Induction, time course, and relationship to dose–response models
Hoffmann, G. R., Moczula, A. V., Laterza, A. M., MacNeil, L. K., & Tartaglione, J. P. (2013) · Environmental and Molecular Mutagenesis · doi:10.1002/em.21785 · Cited by 11 · see citing works
Converging concepts: Adaptive response, preconditioning, and the Yerkes–Dodson Law are manifestations of hormesis
Calabrese, E. J. (2008) · Ageing Research Reviews · doi:10.1016/j.arr.2007.07.001 · Cited by 180 · see citing works
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Zhang, Q., Pi, J., Woods, C. G., Jarabek, A. M., M.A., H. J. C. I., & Andersen, M. E. (2008) · Dose-Response · doi:10.2203/dose-response.07-028.zhang · Cited by 62 · see citing works

Authors: Merry, T. L., & Ristow, M.
Affiliations: ETH Zurich (CH)
Corresponding author: Merry, Troy L.
ORCID: Merry, Troy L.
Ristow, Michael
Venue: Free Radical Biology and Medicine
Publisher: Elsevier BV
Published: 2016-09
Volume: 98
Pages: 123-130
ISSN: 0891-5849 (ISSN-L)
DOI: 10.1016/j.freeradbiomed.2015.11.032
OpenAlex: W2182825530
Cited by: 176
References: 144
Citations by year: 2026: 19 · 2025: 14 · 2024: 21 · 2023: 11 · 2022: 22 · 2021: 19 · 2020: 24 · 2019: 14 · 2018: 11 · 2017: 13 · 2016: 8
FWCI: 10.77
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (am, 337 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Free Radical Biology and Medicine (acceptedVersion)
PubMed (publishedVersion)
ResearchSpace (University of Auckland) (submittedVersion)
Funders: German Ministry for Education and Research (Bundesministerium für Bildung und Forschung (BMBF 0315581)
German Research Association (Deutsche Forschungsgemeinschaft, DFG)
Swiss National Science Foundation (Schweizerischer Nationalfonds (SNF 31003A_156031)
Novartis Foundation for Medical-Biological Research (14C149)
European Foundation for the Study of Diabetes
Topics: Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
Keywords: mitohormesis, hormesis, exercise training, mitochondrial biogenesis, retrograde signaling, mitochondrial stress response, exercise-induced adaptations, transcription factors, reactive oxygen species, mitochondrial dysfunction, cellular homeostasis
MeSH terms: Animals, Humans, Mitochondria, Peptides, Physical Conditioning, Animal, Signal Transduction, Exercise, Reactive Oxygen Species, Hormesis

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Mitohormesis in exercise training

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