High-intensity exercise and mitochondrial biogenesis: current controversies and future research directions

Bishop, David J.; Botella, Javier; Genders, Amanda J.; Lee, Matthew J-C.; Saner, Nicholas J.; Kuang, Jujiao; Yan, Xu; Granata, Cesare

doi:10.1152/physiol.00038.2018

Cited by 180Cardiovascular and exercise physiologyExercise and Physiological ResponsesAdipose Tissue and Metabolism

High-intensity exercise and mitochondrial biogenesis: current controversies and future research directions

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Bishop, David J., Botella, Javier, Genders, Amanda J., Lee, Matthew J-C., Saner, Nicholas J., Kuang, Jujiao, Yan, Xu, Granata, Cesare·2019·Physiology

DOI 10.1152/physiol.00038.2018

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Abstract

It is well established that different types of exercise can provide a powerful stimulus for mitochondrial biogenesis. However, there are conflicting findings in the literature, and a consensus has not been reached regarding the efficacy of high-intensity exercise to promote mitochondrial biogenesis in humans. The purpose of this review is to examine current controversies in the field and to highlight some important methodological issues that need to be addressed to resolve existing conflicts.

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High-intensity interval exercise is a time-efficient format of endurance exercise and a potent stimulus for induction of mitochondrial biogenesis.
“High-intensity interval exercise (HIIE) is a time-efficient format of endurance exercise and also a potent stimulus for the induction of mitochondrial biogenesis [23]”
From Exercise mitigates sleep-loss-induced changes in glucose tolerance, mitochondrial function, sarcoplasmic protein synthesis, and diurnal rhythms (2021) · cites this paper as [23]
Mitochondrial protein synthesis (MitoPS) is the measure that best reflects the process of mitochondrial biogenesis.
“Mitochondrial protein synthesis (MitoPS) is the measure that best reflects the process of mitochondrial biogenesis [23,48].”
From Exercise mitigates sleep-loss-induced changes in glucose tolerance, mitochondrial function, sarcoplasmic protein synthesis, and diurnal rhythms (2021) · cites this paper as [23]
One explanation for the observations may involve processes regulating mitochondrial dynamics/remodeling (fission and fusion), which can alter efficiency and oxidative capacity without necessarily altering mitochondrial content.
“One explanation for our observations may involve the processes regulating mitochondrial dynamics/remodeling (i.e., fission and fusion), which can alter the efficiency and oxidative capacity of the mitochondria, without necessarily altering mitochondrial content [23].”
From Exercise mitigates sleep-loss-induced changes in glucose tolerance, mitochondrial function, sarcoplasmic protein synthesis, and diurnal rhythms (2021) · cites this paper as [23]

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Donato, D. M. D., West, D. W. D., Churchward‐Venne, T. A., Breen, L., Baker, S. K., & Phillips, S. M. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00487.2013 · Cited by 141 · see citing works
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Fibre-Specific Responses to Endurance and Low Volume High Intensity Interval Training: Striking Similarities in Acute and Chronic Adaptation
Scribbans, T. D., Edgett, B. A., Vorobej, K., Mitchell, A. S., Joanisse, S., Matusiak, J. B. L., Parise, G., Quadrilatero, J., & Gurd, B. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0098119 · Cited by 129 · see citing works
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Day-to-Day changes in muscle protein synthesis in recovery from resistance, aerobic, and high-intensity interval exercise in older men
Bell, K. E., Séguin, C., Parise, G., Baker, S. K., & Phillips, S. M. (2015) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/glu313 · Cited by 118 · see citing works
Human muscle fibre type‐specific regulation of AMPK and downstream targets by exercise
Steenberg, D. E., Albers, P. H., Prats, C., Baba, O., Birk, J. B., & Wojtaszewski, J. F. P. (2015) · The Journal of Physiology · doi:10.1113/jphysiol.2014.283267 · Cited by 118 · see citing works
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Coffey, V. G., Pilegaard, H., Garnham, A. P., O'Brien, B. J., & Hawley, J. A. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.91221.2008 · Cited by 116 · see citing works
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Sex differences in mitochondrial respiratory function in human skeletal muscle
Miotto, P. M., McGlory, C., Holloway, T. M., Phillips, S. M., & Holloway, G. P. (2018) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00025.2018 · Cited by 109 · see citing works
Increased FXYD1 and PGC‐1 α mRNA after blood flow‐restricted running is related to fibre type‐specific AMPK signalling and oxidative stress in human muscle
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Montero, D., Madsen, K., Meinild‐Lundby, A., Edin, F., & Lundby, C. (2018) · Experimental Physiology · doi:10.1113/ep087007 · Cited by 105 · see citing works
Sex Differences in Global mRNA Content of Human Skeletal Muscle
Maher, A. C., Fu, M., Isfort, R. J., Varbanov, A. R., Qu, X. A., & Tarnopolsky, M. A. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006335 · Cited by 103 · see citing works
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van der Zwaard, S., de Ruiter, C. J., Noordhof, D. A., Sterrenburg, R., Bloemers, F. W., de Koning, J. J., Jaspers, R. T., & van der Laarse, W. J. (2016) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00355.2016 · Cited by 100 · see citing works
Effect of training status and relative exercise intensity on physiological responses in men
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Coordination of mitochondrial biogenesis by PGC-1α in human skeletal muscle: A re-evaluation
Islam, H., Edgett, B. A., & Gurd, B. J. (2018) · Metabolism · doi:10.1016/j.metabol.2017.11.001 · Cited by 99 · see citing works
Stable isotope tracers and exercise physiology: Past, present and future
Wilkinson, D. J., Brook, M. S., Smith, K., & Atherton, P. J. (2017) · The Journal of Physiology · doi:10.1113/jp272277 · Cited by 97 · see citing works
The relationship between skeletal muscle mitochondrial citrate synthase activity and whole body oxygen uptake adaptations in response to exercise training.
Vigelsø, A., Andersen, N. B., & Dela, F. (2014) · Europe PMC (PubMed Central) · Cited by 96 · see citing works
Exercise and Training in Women, Part I: Influence of Gender on Exercise and Training Responses
Shephard, R. J. (2000) · Canadian Journal of Applied Physiology · doi:10.1139/h00-002 · Cited by 91 · see citing works
Exercise, sex, menstrual cycle phase, and 17β-estradiol influence metabolism-related genes in human skeletal muscle
Fu, M.-H. H., Maher, A. C., Hamadeh, M. J., Ye, C., & Tarnopolsky, M. A. (2009) · Physiological Genomics · doi:10.1152/physiolgenomics.00115.2009 · Cited by 90 · see citing works
Men supplemented with 17β-estradiol have increased β-oxidation capacity in skeletal muscle
Maher, A. C., Akhtar, M., & Tarnopolsky, M. A. (2010) · Physiological Genomics · doi:10.1152/physiolgenomics.00016.2010 · Cited by 87 · see citing works
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Miller, B. F., & Hamilton, K. L. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00578.2011 · Cited by 86 · see citing works
Twenty‐eight days at 3454‐m altitude diminishes respiratory capacity but enhances efficiency in human skeletal muscle mitochondria
Jacobs, R. A., Siebenmann, C., Hug, M., Toigo, M., Meinild, A., & Lundby, C. (2012) · The FASEB Journal · doi:10.1096/fj.12-218206 · Cited by 85 · see citing works
Relative Workload Determines Exercise-Induced Increases in PGC-1α mRNA
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Mitochondrial dismissal in mammals, from protein degradation to mitophagy
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Sprint-interval but not continuous exercise increases PGC-1α protein content and p53 phosphorylation in nuclear fractions of human skeletal muscle
Granata, C., Oliveira, R. S. F., Little, J. P., Renner, K., & Bishop, D. J. (2017) · Scientific Reports · doi:10.1038/srep44227 · Cited by 78 · see citing works
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Relationship between plasma lactate parameters and muscle characteristics in female cyclists
Bishop, D. J., Jenkins, D. G., McEniery, M. T., & Carey, M. (2000) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-200006000-00008 · Cited by 77 · see citing works
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High-intensity exercise acutely decreases the membrane content of MCT1 and MCT4 and buffer capacity in human skeletal muscle
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Bishop, D. J., Jenkins, D. G., & MACKINNON, L. T. (1998) · Journal of science and medicine in sport · doi:10.1016/s1440-2440(98)80012-1 · Cited by 68 · see citing works
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Lindholm, M. E., Giacomello, S., Solnestam, B. W., Fischer, H., Huss, M., Kjellqvist, S., & Sundberg, C. J. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006294 · Cited by 67 · see citing works
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Yan, X., Eynon, N., Papadimitriou, I. D., Kuang, J., Munson, F., Tirosh, O., O’Keefe, L., Griffiths, L. R., Ashton, K. J., Byrne, N. M., et al. (2017) · BMC Genomics · doi:10.1186/s12864-017-4186-4 · Cited by 64 · see citing works
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Effects of endurance training on oxidative capacity and structural composition of human arm and leg muscles
Turner, D. L., Hoppeler, H. H., Claassen, H., Vock, P., Kayser, B., Schena, F. F., & Ferretti, G. (1997) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.1997.00246.x · Cited by 63 · see citing works
Transient transcriptional events in human skeletal muscle at the outset of concentric resistance exercise training
Murton, A. J., Billeter, R., Stephens, F. B., Etages, S. G. D., Graber, F., Hill, R. J. W., Marimuthu, K., & Greenhaff, P. L. (2013) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00426.2013 · Cited by 61 · see citing works
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Sodium bicarbonate ingestion prior to training improves mitochondrial adaptations in rats
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Repeated Sprints Alter Signaling Related to Mitochondrial Biogenesis in Humans
Serpiello, F. R., McKenna, M. J., Bishop, D. J., Aughey, R. J., Caldow, M. K., Cameron‐Smith, D., & Stepto, N. K. (2011) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e318240067e · Cited by 48 · see citing works
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Skeletal muscle fiber-type-specific changes in markers of capillary and mitochondrial content after low-volume interval training in overweight women
Tan, R., Nederveen, J. P., Gillen, J. B., Joanisse, S., Parise, G., Tarnopolsky, M. A., & Gibala, M. J. (2018) · Physiological Reports · doi:10.14814/phy2.13597 · Cited by 48 · see citing works
Effect of p53 on mitochondrial morphology, import, and assembly in skeletal muscle
Saleem, A., Iqbal, S., Zhang, Y., & Hood, D. A. (2014) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00253.2014 · Cited by 39 · see citing works
Effect of sex on the acute skeletal muscle response to sprint interval exercise
Skelly, L. E., Gillen, J. B., MacInnis, M. J., Martin, B. J., Safdar, A., Akhtar, M., MacDonald, M. J., Tarnopolsky, M. A., & Gibala, M. J. (2017) · Experimental Physiology · doi:10.1113/ep086118 · Cited by 39 · see citing works
The effect of continuous and interval exercise on PGC‐1α and PDK4 mRNA in type I and type II fibres of human skeletal muscle
Wang, L., & Sahlin, K. (2011) · Acta Physiologica · doi:10.1111/j.1748-1716.2011.02354.x · Cited by 38 · see citing works
Submaximal ADP‐stimulated respiration is impaired in ZDF rats and recovered by resveratrol
Smith, B. K., Perry, C. G. R., Herbst, E. A. F., Ritchie, I. R. W., Beaudoin, M., Smith, J. C., Neufer, P. D., Wright, D. C., & Holloway, G. P. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2013.259226 · Cited by 37 · see citing works
Skeletal muscle signaling response to sprint exercise in men and women
Fuentes, T., Guerra, B., Ponce-González, J. G., Morales-Alamo, D., Guadalupe-Grau, A., Olmedillas, H., Rodríguez-García, L., Feijoo, D., De Pablos-Velasco, P., Fernández-Pérez, L., et al. (2012) · European Journal of Applied Physiology · doi:10.1007/s00421-011-2164-0 · Cited by 36 · see citing works
Exercise and Regulation of Protein Metabolism
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Regulation of oxidative enzyme activity and eukaryotic elongation factor 2 in human skeletal muscle: influence of gender and exercise
Roepstorff, C., Schjerling, P., Vistisen, B., Madsen, M., Steffensen, C. H., Rider, M. H., & Kiens, B. (2005) · Acta Physiologica Scandinavica · doi:10.1111/j.1365-201x.2005.01442.x · Cited by 33 · see citing works
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Cold-water immersion following sprint interval training does not alter endurance signaling pathways or training adaptations in human skeletal muscle
Broatch, J. R., Petersen, A. C., & Bishop, D. J. (2017) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00434.2016 · Cited by 31 · see citing works
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Distinct protein and mRNA kinetics of skeletal muscle proton transporters following exercise can influence interpretation of adaptations to training
McGinley, C., & Bishop, D. J. (2016) · Experimental Physiology · doi:10.1113/ep085921 · Cited by 30 · see citing works
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Reliability of maximal mitochondrial oxidative phosphorylation in permeabilized fibers from thevastus lateralisemploying high-resolution respirometry
Cardinale, D. A., Gejl, K. D., Ørtenblad, N., Ekblom, B. T., Blomstrand, E., & Larsen, F. J. (2018) · Physiological Reports · doi:10.14814/phy2.13611 · Cited by 30 · see citing works
Recent developments in deuterium oxide tracer approaches to measure rates of substrate turnover
Brook, M. S., Wilkinson, D. J., Atherton, P. J., & Smith, K. (2017) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0000000000000392 · Cited by 27 · see citing works
Effects of a Supplementation during Exercise and Recovery
Thomas, C., Perrey, S., Saad, H. B., Delage, M., Dupuy, A., Cristol, J., & Mercier, J. G. (2007) · International Journal of Sports Medicine · doi:10.1055/s-2007-965021 · Cited by 17 · see citing works
Effects of cycle strategy and fibre composition on muscle glycogen depletion pattern and subsequent running economy
Suriano, R., Edge, J., & Bishop, D. J. (2008) · British Journal of Sports Medicine · doi:10.1136/bjsm.2007.046029 · Cited by 16 · see citing works
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Assessing the regulation of skeletal muscle plasticity in response to protein ingestion and resistance exercise
McGlory, C., & Phillips, S. M. (2014) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0000000000000083 · Cited by 15 · see citing works
Measuring mitochondrial protein synthesis to assess biogenesis
Short, K. R. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00117.2012 · Cited by 9 · see citing works
Tissue specificity of mitochondrial adaptations in rats after 4 weeks of normobaric hypoxia
Ferri, A., Panariti, A., Miserocchi, G., Rocchetti, M., Comani, G. B., Rivolta, I., & Bishop, D. J. (2018) · European Journal of Applied Physiology · doi:10.1007/s00421-018-3897-9 · Cited by 9 · see citing works
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Commentaries on Viewpoint: The rigorous study of exercise adaptations: Why mRNA might not be enough
Hornberger, T. A., Carter, H. N., Hood, D. A., Figueiredo, V. C., Dupont‐Versteegden, E. E., Peterson, C. A., McCarthy, J. J., CAMERA, D. M., Hawley, J. A., Chaillou, T., et al. (2016) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00509.2016 · Cited by 7 · see citing works
Exercise As An Intervention To Mitigate Mitochondrial Dysfunction And Impaired Glucose Tolerance Induced By Sleep- loss
Saner, N. J., Bishop, D. J., & Bartlett, J. D. (2018) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000535577.72598.04 · Cited by 1 · see citing works
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Mitochondrial dysfunction in cell senescence and aging
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CrossTalk opposing view: Exercise training volume is more important than training intensity to promote increases in mitochondrial content
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Metabolic responsiveness to training depends on insulin sensitivity and protein content of exosomes in insulin-resistant males
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Soman, S. K., Swain, M., & Dagda, R. K. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-04357-4 · Cited by 54 · see citing works
Exercise twice‐a‐day potentiates markers of mitochondrial biogenesis in men
Andrade‐Souza, V. A., Ghiarone, T., Sansonio, A., Silva, K. A. S., Tomazini, F., Arcoverde, L., Fyfe, J. J., Perri, E., Saner, N. J., Kuang, J., et al. (2019) · The FASEB Journal · doi:10.1096/fj.201901207rr · Cited by 52 · see citing works
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Are Alterations in Skeletal Muscle Mitochondria a Cause or Consequence of Insulin Resistance?
Genders, A. J., Holloway, G. P., & Bishop, D. J. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21186948 · Cited by 51 · see citing works
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Physiological basis of interval training for performance enhancement
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The importance of mitochondrial quality control for maintaining skeletal muscle function across health span
Sligar, J., Debruin, D. A., Saner, N. J., Philp, A. M., & Philp, A. (2022) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00388.2021 · Cited by 49 · see citing works
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Exercise-Regulated Mitochondrial and Nuclear Signalling Networks in Skeletal Muscle
Reisman, E. G., Hawley, J. A., & Hoffman, N. J. (2024) · Sports Medicine · doi:10.1007/s40279-024-02007-2 · Cited by 50 · see citing works
Exercise-specific adaptations in human skeletal muscle: Molecular mechanisms of making muscles fit and mighty
Thomas, A. C. Q., Stead, C. A., Burniston, J. G., & Phillips, S. M. (2024) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2024.08.010 · Cited by 52 · see citing works
Interpretation of exercise-induced changes in human skeletal muscle mRNA expression depends on the timing of the post-exercise biopsies
Kuang, J., McGinley, C., Lee, M. J.-C., Saner, N. J., Garnham, A., & Bishop, D. J. (2022) · PeerJ · doi:10.7717/peerj.12856 · Cited by 45 · see citing works
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Exercise as Mitochondrial Medicine: How Does the Exercise Prescription Affect Mitochondrial Adaptations to Training?
Bishop, D. J., Lee, M. J.-C., & Picard, M. A. (2024) · Annual Review of Physiology · doi:10.1146/annurev-physiol-022724-104836 · Cited by 42 · see citing works
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Forty high-intensity interval training sessions blunt exercise-induced changes in the nuclear protein content of PGC-1α and p53 in human skeletal muscle
Granata, C., Oliveira, R. S. F., Little, J. P., & Bishop, D. J. (2019) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00233.2019 · Cited by 38 · see citing works
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Increased mitochondrial surface area and cristae density in the skeletal muscle of strength athletes
Botella, J., Schytz, C. T., Pehrson, T. F., Hokken, R., Laugesen, S., Aagaard, P., Suetta, C., Christensen, B., Ørtenblad, N., & Nielsen, J. (2023) · The Journal of Physiology · doi:10.1113/jp284394 · Cited by 38 · see citing works
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Human skeletal muscle fiber type-specific responses to sprint interval and moderate-intensity continuous exercise: acute and training-induced changes
Skelly, L. E., Gillen, J. B., Frankish, B. P., MacInnis, M. J., Godkin, F. E., Tarnopolsky, M. A., Murphy, R. M., & Gibala, M. J. (2021) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00862.2020 · Cited by 38 · see citing works
A “human knockout” model to investigate the influence of the α-actinin-3 protein on exercise-induced mitochondrial adaptations
Papadimitriou, I. D., Eynon, N., Yan, X., Munson, F., Jacques, M., Kuang, J., Voisin, S. A. C., North, K. N., & Bishop, D. J. (2019) · Scientific Reports · doi:10.1038/s41598-019-49042-y · Cited by 36 · see citing works
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Muscle Ionic Shifts During Exercise: Implications for Fatigue and Exercise Performance
Hostrup, M., Cairns, S. P., & Bangsbo, J. (2021) · Comprehensive physiology · doi:10.1002/cphy.c190024 · Cited by 47 · see citing works
The impact of exercise on mitochondrial biogenesis in skeletal muscle: A systematic review and meta-analysis of randomized trials
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Effects of 3-month high-intensity interval training vs. moderate endurance training and 4-month follow-up on fat metabolism, cardiorespiratory function and mitochondrial respiration in obese adults
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Physical Exercise Potentially Targets Epicardial Adipose Tissue to Reduce Cardiovascular Disease Risk in Patients with Metabolic Diseases: Oxidative Stress and Inflammation Emerge as Major Therapeutic Targets
Nyawo, T. A., Pheiffer, C., Mazibuko-Mbeje, S. E., Mthembu, S. X. H., Nyambuya, T. M., Nkambule, B. B., Gijsen, H. S., Strijdom, H., Tiano, L., & Dludla, P. V. (2021) · Antioxidants · doi:10.3390/antiox10111758 · Cited by 33 · see citing works
Diet and exercise in frailty and sarcopenia. Molecular aspects
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Structural functionality of skeletal muscle mitochondria and its correlation with metabolic diseases
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Discordant skeletal muscle gene and protein responses to exercise
Bishop, D. J., Hoffman, N. J., Taylor, D. F., Saner, N. J., Lee, M. J.-C., & Hawley, J. A. (2023) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2023.08.005 · Cited by 32 · see citing works
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Secreted Protein Acidic and Rich in Cysteine (Sparc) KO Leads to an Accelerated Ageing Phenotype Which Is Improved by Exercise Whereas SPARC Overexpression Mimics Exercise Effects in Mice
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Mitochondrial-based therapies for neurodegenerative diseases: a review of the current literature
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Assessing mitochondrial respiration in permeabilized fibres and biomarkers for mitochondrial content in human skeletal muscle
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Skeletal muscle mechanisms contributing to improved glycemic control following intense interval exercise and training
Islam, H., & Gillen, J. B. (2023) · Sports Medicine and Health Science · doi:10.1016/j.smhs.2023.01.002 · Cited by 30 · see citing works
Energy, Entropy and Quantum Tunneling of Protons and Electrons in Brain Mitochondria: Relation to Mitochondrial Impairment in Aging-Related Human Brain Diseases and Therapeutic Measures
Bennett, J. P., & Onyango, I. G. (2021) · Biomedicines · doi:10.3390/biomedicines9020225 · Cited by 28 · see citing works
Programming Interval Training to Optimize Time-Trial Performance: A Systematic Review and Meta-Analysis
Rosenblat, M. A., Lin, E. B., da Costa, B. R., & Thomas, S. G. (2021) · Sports Medicine · doi:10.1007/s40279-021-01457-2 · Cited by 29 · see citing works
Nitric Oxide Deficiency in Mitochondrial Disorders: The Utility of Arginine and Citrulline
Almannai, M., & El‐Hattab, A. W. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.682780 · Cited by 28 · see citing works
Conserved and convergent mechanisms underlying performance–life-history trade-offs
Husak, J. F., & Lailvaux, S. P. (2022) · Journal of Experimental Biology · doi:10.1242/jeb.243351 · Cited by 28 · see citing works
Moderate intensity continuous versus high intensity interval training: Metabolic responses of slow and fast skeletal muscles in rat
Pengam, M., Goanvec, C., Cann-Moisan, C., Simon, B. M., Albacète, G., Féray, A., Guernec, A., & Amérand, A. (2023) · PLoS ONE · doi:10.1371/journal.pone.0292225 · Cited by 29 · see citing works
Impact of Physical Activity on Cellular Metabolism Across Both Neurodegenerative and General Neurological Conditions: A Narrative Review
Clemente‐Suárez, V. J., Rubio-Zarapuz, A., Belinchón-deMiguel, P., Beltrán-Velasco, A. I., Martín-Rodríguez, A., & Tornero-Aguilera, J. F. (2024) · Cells · doi:10.3390/cells13231940 · Cited by 30 · see citing works
Exercise, Mitohormesis, and Mitochondrial ORF of the 12S rRNA Type-C (MOTS-c)
Yoon, T. K., Lee, C. H., Kwon, O., & Kim, M. (2022) · Diabetes & Metabolism Journal · doi:10.4093/dmj.2022.0092 · Cited by 27 · see citing works
Emerging Multi-omic Approaches to the Molecular Diagnosis of Mitochondrial Disease and Available Strategies for Treatment and Prevention
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Running to save sight: The effects of exercise on retinal health and function
Chu‐Tan, J. A., Kirkby, M., & Natoli, R. (2021) · Clinical and Experimental Ophthalmology · doi:10.1111/ceo.14023 · Cited by 27 · see citing works
Fibre-specific mitochondrial protein abundance is linked to resting and post-training mitochondrial content in the muscle of men
Reisman, E. G., Botella, J., Huang, C., Schittenhelm, R. B., Stroud, D. A., Granata, C., Chandrasiri, O. S., Ramm, G., Oorschot, V. M. J., Caruana, N. J., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-50632-2 · Cited by 27 · see citing works
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Customizing intense interval exercise training prescription using the “frequency, intensity, time, and type of exercise” (FITT) principle
Stavrinou, P. S., Astorino, T. A., Giannaki, C. D., Aphamis, G., & Bogdanis, G. C. (2025) · Frontiers in Physiology · doi:10.3389/fphys.2025.1553846 · Cited by 27 · see citing works
Advances in Cardiotoxicity Induced by Altered Mitochondrial Dynamics and Mitophagy
Yin, Y., & Shen, H. (2021) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2021.739095 · Cited by 21 · see citing works
Reactive oxygen and nitrogen species: multifaceted regulators of ovarian activity
Bezdíček, J., Sekaninová, J., Janků, M., Makarevič, A., Luhová, L., Dujíčková, L., & Petřivalský, M. (2025) · Biology of Reproduction · doi:10.1093/biolre/ioaf032 · Cited by 22 · see citing works
Physiological Responses to Low-Volume Interval Training in Women
Skelly, L. E., Bailleul, C., & Gillen, J. B. (2021) · Sports Medicine - Open · doi:10.1186/s40798-021-00390-y · Cited by 18 · see citing works
It’s about the long game, not epic workouts: unpacking HIIT for endurance athletes
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High-intensity interval training with or without chlorella vulgaris supplementation in obese and overweight women: effects on mitochondrial biogenesis, performance and body composition
Sanayei, M., Hajizadeh‐Sharafabad, F., Amirsasan, R., & Barzegar, A. (2021) · British Journal Of Nutrition · doi:10.1017/s0007114521003287 · Cited by 18 · see citing works
The acute and chronic influence of exercise on mitochondrial dynamics in skeletal muscle
Ritenis, E. J., Padilha, C. S., Cooke, M. B., Stathis, C. G., Philp, A., & CAMERA, D. M. (2024) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00311.2024 · Cited by 17 · see citing works
Physiological adaptations to interval training to promote endurance
Gibala, M. J., Bostad, W., & McCarthy, D. G. (2019) · Current Opinion in Physiology · doi:10.1016/j.cophys.2019.05.013 · Cited by 20 · see citing works
Delineating the contribution of ageing and physical activity to changes in mitochondrial characteristics across the lifespan
Lee, M. J.-C., Saner, N. J., Ferri, A., García-Domínguez, E., Broatch, J. R., & Bishop, D. J. (2024) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2024.101272 · Cited by 16 · see citing works
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Exercise Is Medicine…and the Dose Matters
Langan, S. P., & Grosicki, G. J. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.660818 · Cited by 16 · see citing works
Mechanical, Cardiorespiratory, and Muscular Oxygenation Responses to Sprint Interval Exercises Under Different Hypoxic Conditions in Healthy Moderately Trained Men
Solsona, R., Berthelot, H., Borrani, F., & Sanchez, A. M. J. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.773950 · Cited by 17 · see citing works
The Effect of High-Intensity Interval Training on Mitochondrial-Associated Indices in Overweight and Obese Adults: A Systematic Review and Meta-Analysis
Hadjispyrou, S., Dinas, P. C., Delitheos, S. M., Koumprentziotis, I., Chryssanthopοulos, C., & Philippou, Α. (2023) · Frontiers in Bioscience-Landmark · doi:10.31083/j.fbl2811281 · Cited by 16 · see citing works
PGC-1α Methylation, miR-23a, and miR-30e Expression as Biomarkers for Exercise- and Diet-Induced Mitochondrial Biogenesis in Capillary Blood from Healthy Individuals: A Single-Arm Intervention
Krammer, U. D. B., Sommer, A., Tschida, S., Mayer, A., Lilja, S., Switzeny, O. J., Hippe, B., Rust, P., & Haslberger, A. G. (2022) · Sports · doi:10.3390/sports10050073 · Cited by 14 · see citing works
High-Intensity Interval Training vs. Medium-Intensity Continuous Training in Cardiac Rehabilitation Programs: A Narrative Review
Costache, A. D., Maștaleru, A., Leon, M. M., Roca, M., Gavril, R. S., Cosău, D. E., Rotundu, A., Amagdalinei, A. I., Mitu, O., Enache, I. I. C., et al. (2024) · Medicina · doi:10.3390/medicina60111875 · Cited by 14 · see citing works
Optimal exercise dose on Body Mass Index (BMI) in children and adolescents with overweight and obesity: a systematic review and bayesian model-based network meta-analysis
Huang, Z., Sun, G., Li, J., Zhang, B., Lai, G., Jing, H., & Zhou, Y. (2025) · BMC Public Health · doi:10.1186/s12889-025-21405-3 · Cited by 14 · see citing works
Investigating the influence of mtDNA and nuclear encoded mitochondrial variants on high intensity interval training outcomes
Harvey, N. R., Voisin, S. A. C., Lea, R. A., Yan, X., Benton, M. C., Papadimitriou, I. D., Jacques, M., Haupt, L. M., Ashton, K. J., Eynon, N., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-67870-1 · Cited by 14 · see citing works
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Operational Modal Analysis of Near-Infrared Spectroscopy Measure of 2-Month Exercise Intervention Effects in Sedentary Older Adults with Diabetes and Cognitive Impairment
Zhao, F., Tomita, M., & Dutta, A. (2023) · Brain Sciences · doi:10.3390/brainsci13071099 · Cited by 14 · see citing works
Small peptides: Could they have a big role in metabolism and the response to exercise?
Atakan, M. M., Türkel, İ., Özerkliğ, B., Koşar, Ş. N., Taylor, D. F., Yan, X., & Bishop, D. J. (2024) · The Journal of Physiology · doi:10.1113/jp283214 · Cited by 13 · see citing works
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Effects of Lactate Administration on Mitochondrial Respiratory Function in Mouse Skeletal Muscle
Takahashi, K., Tamura, Y., Kitaoka, Y., Matsunaga, Y., & Hatta, H. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.920034 · Cited by 13 · see citing works
Keeping the beat against time: Mitochondrial fitness in the aging heart
Mendoza, A., & Karch, J. M. (2022) · Frontiers in Aging · doi:10.3389/fragi.2022.951417 · Cited by 13 · see citing works
Factors associated with high-level endurance performance: An expert consensus derived via the Delphi technique
Konopka, M. J., Zeegers, M. P., Solberg, P. A., Delhaije, L., MEEUSEN, R. R., Ruigrok, G., Rietjens, G. J., & Sperlich, B. (2022) · PLoS ONE · doi:10.1371/journal.pone.0279492 · Cited by 15 · see citing works
Attenuated Metabolic and Cardiorespiratory Responses to Isoenergetic High-Intensity Interval Exercise of Short Versus Long Bouts
Bogdanis, G. C., Stavrinou, P. S., TSIRIGKAKIS, S., MOUGIOS, V., ASTORINO, T. A., & MASTORAKOS, G. (2022) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000002905 · Cited by 13 · see citing works
Muscle Ionic Shifts During Exercise: Implications for Fatigue and Exercise Performance
Hostrup, M., Cairns, S. P., & Bangsbo, J. (2021) · Comprehensive physiology · doi:10.1002/j.2040-4603.2021.tb00169.x · Cited by 12 · see citing works
The Effect of Sleep Restriction, With or Without Exercise, on Skeletal Muscle Transcriptomic Profiles in Healthy Young Males
Lin, W., Saner, N. J., Weng, X., Caruana, N. J., Botella, J., Kuang, J., Lee, M. J.-C., Jamnick, N. A., Pitchford, N. W., GARNHAM, A. P., et al. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.863224 · Cited by 14 · see citing works
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Novel insights into exhaustive exercise-induced myocardial injury: Focusing on mitochondrial quality control
Shi, M., Dong, Z., Zhao, K., He, X., Sun, Y., Ren, J. T., & Ge, W. (2022) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.1015639 · Cited by 11 · see citing works
The Maximal Lactate Steady State Workload Determines Individual Swimming Performance
Hering, G. O., & Stepan, J. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.668123 · Cited by 10 · see citing works
Effects of Two In-Season Short High-Intensity Interval Training Formats on Aerobic and Neuromuscular Performance in Young Soccer Players
Thomakos, P., Tsekos, P., Tselios, Z., Spyrou, K., Katsikas, C., Τσούκος, Α., & Bogdanis, G. C. (2024) · Journal of Sports Science and Medicine · doi:10.52082/jssm.2024.812 · Cited by 10 · see citing works
Effects of Polarized Training vs. Other Training Intensity Distribution Models on Physiological Variables and Endurance Performance in Different-Level Endurance Athletes: A Scoping Review
Rivera-Köfler, T., Varela-Sanz, A., Padrón-Cabo, A., García, M. A. G., & Muñoz‐Pérez, I. (2024) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0000000000005033 · Cited by 11 · see citing works
Effects of exercise training on skeletal muscle mitochondrial outcomes in type 2 diabetes: a systematic review and meta-analysis
Zhu, W., Zhou, Z., Sun, J., & Si, J. (2025) · Frontiers in Physiology · doi:10.3389/fphys.2025.1671926 · Cited by 11 · see citing works
Methods to match high-intensity interval exercise intensity in hypoxia and normoxia – A pilot study
Li, Y., Li, J., ATAKAN, M. M., Wang, Z., Hu, Y., Nazif, M., Zarekookandeh, N., Ye, H. Z., Kuang, J., Ferri, A., et al. (2021) · Journal of Exercise Science & Fitness · doi:10.1016/j.jesf.2021.12.003 · Cited by 10 · see citing works
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Effects of the Combined Supplementation of Caffeine and Rhodiola Rosea with Resistance Training on Lower Limb Explosive Power in Male Volleyball Players
Wang, Z., Du, H., Li, H., Zhao, K., Zhao, B., Ma, Y., Zhang, J., Wu, K., Jiang, W., & Liu, C. (2025) · Nutrients · doi:10.3390/nu17040681 · Cited by 9 · see citing works
Exercise-mediated regulation of mitochondrial dynamics in aging muscle: implications for mitochondrial diseases
Zhang, C., Zheng, X., Xiang, L., & Su, Z. (2025) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-025-05441-6 · Cited by 9 · see citing works
Resistance‐only and concurrent exercise induce similar myofibrillar protein synthesis rates and associated molecular responses in moderately active men before and after training
Lee, M. J.-C., Caruana, N. J., Saner, N. J., Kuang, J., Stokes, T., Mcleod, J. C., Oikawa, S. Y., Bishop, D. J., Bartlett, J. D., & Phillips, S. M. (2023) · The FASEB Journal · doi:10.1096/fj.202302024r · Cited by 10 · see citing works
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PoWeR elicits intracellular signaling, mitochondrial adaptations, and hypertrophy in multiple muscles consistent with endurance and resistance exercise training
Elliehausen, C. J., Olszewski, S. S., Minton, D. M., Spiegelhoff, A., Shult, C. G., Zhu, W. G., Hornberger, T. A., & Konopka, A. R. (2025) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00872.2024 · Cited by 8 · see citing works
Effects of 10 weeks of walking-based exercise training on resting substrate oxidation in postmenopausal women with obesity
Güzel, Y., ATAKAN, M. M., Turnagöl, H. H., & Koşar, Ş. N. (2024) · European Journal of Clinical Nutrition · doi:10.1038/s41430-024-01546-1 · Cited by 7 · see citing works
Much Ado About Zone 2: A Narrative Review Assessing the Efficacy of Zone 2 Training for Improving Mitochondrial Capacity and Cardiorespiratory Fitness in the General Population
Storoschuk, K. L., Moran-MacDonald, A., Gibala, M. J., & Gurd, B. J. (2025) · Sports Medicine · doi:10.1007/s40279-025-02261-y · Cited by 7 · see citing works
Isolated and combined impact of dietary olive oil and exercise on markers of health and energy metabolism in female mice
Heden, T. D., Chen, C., Leland, G., Mashek, M. T., Najt, C. P., Shang, L., Chow, L. S., & Mashek, D. G. (2022) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2022.109040 · Cited by 6 · see citing works
The effect of sleep restriction, with or without high‐intensity interval exercise, on behavioural alertness and mood state in young healthy males
Saner, N. J., Lee, M. J.-C., Pitchford, N. W., Broatch, J. R., Roach, G. D., Bishop, D. J., & Bartlett, J. D. (2023) · Journal of Sleep Research · doi:10.1111/jsr.13987 · Cited by 8 · see citing works
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Bridging the gap: Integrating exercise mimicry into chronic disease management through suppressing chronic inflammation
Nasb, M., Li, F., Dayoub, L., Wu, T., Wei, M., & Chen, N. (2024) · Journal of Advanced Research · doi:10.1016/j.jare.2024.04.034 · Cited by 7 · see citing works
Sportizumab – Multimodal progressive exercise over 10 weeks decreases Th17 frequency and CD49d expression on CD8+ T cells in relapsing-remitting multiple sclerosis: A randomized controlled trial
Proschinger, S., Belen, S., Adammek, F., Schlagheck, M. L., Rademacher, A., Schenk, A., Warnke, C., Bloch, W., & Zimmer, P. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.12.017 · Cited by 6 · see citing works
Human skeletal muscle mitochondrial responses to single‐leg intermittent or continuous cycle exercise training matched for absolute intensity and total work
Skelly, L. E., MacInnis, M. J., Bostad, W., McCarthy, D. G., Jenkins, E. M., Archila, L. R., Tarnopolsky, M. A., & Gibala, M. J. (2023) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/sms.14332 · Cited by 8 · see citing works
The Effect of Moderate-Intensity Physical Exercise on Some Serum Inflammation Markers and the Immune System in Rats Fed Intermittent Fasting with a High-Fat Diet
GÜNBATAR, N., Bulduk, B., Bezgin, S., Oto, G., Bayıroğlu, F., & Bulduk, M. (2023) · Medicina · doi:10.3390/medicina59091687 · Cited by 6 · see citing works
Training-induced bioenergetic improvement in human skeletal muscle is associated with non-stoichiometric changes in the mitochondrial proteome without reorganization of respiratory chain contentPreprint
Granata, C., Caruana, N. J., Botella, J., Jamnick, N. A., Huynh, K., Kuang, J., Janssen, H. A., Reljić, B., Mellett, N. A., Laskowski, A., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.02.19.431993 · Cited by 6 · see citing works
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Markers of clinical and mitochondrial adaptation in response to moderate intensity continuous training: A systematic review and meta-analysis
Vabishchevich, V., Smith, R. T., & Bittel, A. J. (2026) · PLoS ONE · doi:10.1371/journal.pone.0339902 · Cited by 5 · see citing works

Mitochondria Biogenesis and Exercise
김태우 (2007)
Molecular basis of exercise-induced skeletal muscle mitochondrial biogenesis: historical advances, current knowledge, and future challenges
Perry, C. G. R., & Hawley, J. A. (2018) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a029686 · Cited by 130 · see citing works
Mitochondrial Biogenesis in Continuous vs High-intensity Interval Swimming
Heiat, F., Ghanbarzadeh, M., Ranjbar, R., & Shojaeifard, M. B. (2022) · Annals of Military and Health Sciences Research · doi:10.5812/amh-119122
Metabolic stress‐dependent regulation of the mitochondrial biogenic molecular response to high‐intensity exercise in human skeletal muscle
Fiorenza, M., Gunnarsson, T. P., Hostrup, M., Iaia, F. M., Schena, F. F., Pilegaard, H., & Bangsbo, J. (2018) · The Journal of Physiology · doi:10.1113/jp275972 · Cited by 132 · see citing works
The effects of different types of exercise on mitochondrial adaptations
Daussin, F. (2023) · HAL

Authors: Bishop, D. J., Botella, J., Genders, A. J., Lee, M. J.-C., Saner, N. J., Kuang, J., Yan, X., & Granata, C.
Affiliations: Edith Cowan University (AU)
Victoria University (AU)
Monash University (AU)
Corresponding author: Bishop, David J.
ORCID: Bishop, David J.
Botella, Javier
Genders, Amanda J.
Lee, Matthew J-C.
Saner, Nicholas J.
Kuang, Jujiao
Yan, Xu
Granata, Cesare
Venue: Physiology
Publisher: American Physiological Society
Published: 2019-01-01
Volume: 34
Issue: 1
Pages: 56-70
ISSN: 0886-1714 (ISSN-L)
1548-9213
1548-9221
DOI: 10.1152/physiol.00038.2018
OpenAlex: W2903667549
Cited by: 180
References: 138
Citations by year: 2026: 17 · 2025: 25 · 2024: 33 · 2023: 19 · 2022: 31 · 2021: 29 · 2020: 16 · 2019: 9 · 2018: 1
FWCI: 3.23
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Physiology (publishedVersion)
PubMed (publishedVersion)
Victoria University Research Repository (Victoria University) (submittedVersion)
Australasian Journal of Paramedicine (submittedVersion)
Own your potential (DEAKIN) (submittedVersion)
Figshare (submittedVersion, cc-by)
Funders: Monash University
Topics: Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
Keywords: high-intensity exercise, mitochondrial biogenesis, exercise training, skeletal muscle mitochondria, methodological issues
MeSH terms: Animals, Organelle Biogenesis, Humans, Mitochondria, Physical Conditioning, Animal, Research, Exercise

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High-intensity exercise and mitochondrial biogenesis: current controversies and future research directions

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