The influence of skeletal muscle mitochondria and sex on critical torque and performance fatiguability in humans.
aerobic fitness
critical intensity
exercise
exercise prescription
fatigue
quadriceps
sex differences
small muscle mass
Journal
The Journal of physiology
ISSN: 1469-7793
Titre abrégé: J Physiol
Pays: England
ID NLM: 0266262
Informations de publication
Date de publication:
Dec 2023
Dec 2023
Historique:
received:
02
05
2023
accepted:
04
10
2023
medline:
4
12
2023
pubmed:
30
10
2023
entrez:
30
10
2023
Statut:
ppublish
Résumé
Critical torque (CT) represents the highest oxidative steady state for intermittent knee extensor exercise, but the extent to which it is influenced by skeletal muscle mitochondria and sex is unclear. Vastus lateralis muscle biopsy samples were collected from 12 females and 12 males -matched for relative maximal oxygen uptake normalized to fat-free mass (FFM) (F: 57.3 (7.5) ml (kg FFM)
Substances chimiques
Protein Isoforms
0
Mitochondrial Proteins
0
Oxygen
S88TT14065
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
5295-5316Subventions
Organisme : Natural Sciences and Engineering Research Council of Canada
ID : RGPIN-2018-06424
Organisme : University of Calgary
Informations de copyright
© 2023 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.
Références
Aboodarda, S. J., Zhang, C. X. Y., Sharara, R., Cline, M., & Millet, G. Y. (2019). Exercise-induced fatigue in one leg does not impair the neuromuscular performance in the contralateral leg but improves the excitability of the ipsilateral corticospinal pathway. Brain Sciences, 9(10), 250.
Allen, D. G., Lamb, G. D., & Westerblad, H. (2008). Skeletal muscle fatigue: Cellular mechanisms. Physiological Reviews, 88(1), 287-332.
Andersen, P., & Saltin, B. (1985). Maximal perfusion of skeletal muscle in man. The Journal of Physiology, 366(1), 233-249.
Ansdell, P., Brownstein, C. G., Škarabot, J., Hicks, K. M., Howatson, G., Thomas, K., Hunter, S. K., & Goodall, S. (2019a). Sex differences in fatigability and recovery relative to the intensity-duration relationship. The Journal of Physiology, 597(23), 5577-5595.
Ansdell, P., Brownstein, C. G., Škarabot, J., Hicks, K. M., Howatson, G., Thomas, K., Hunter, S. K., & Goodall, S. (2019b). Methodological issues influence determination of critical force during intermittent exercise: Authors’ reply. The Journal of Physiology, 597(24), 5987-5989.
Ansdell, P., Brownstein, C. G., Škarabot, J., Hicks, K. M., Simoes, D. C. M., Thomas, K., Howatson, G., Hunter, S. K., & Goodall, S. (2019). Menstrual cycle-associated modulations in neuromuscular function and fatigability of the knee extensors in eumenorrheic women. Journal of Applied Physiology (1985), 126(6), 1701-1712.
Ansdell, P., Škarabot, J., Atkinson, E., Corden, S., Tygart, A., Hicks, K. M., Thomas, K., Hunter, S. K., Howatson, G., & Goodall, S. (2020). Sex differences in fatigability following exercise normalised to the power-duration relationship. The Journal of Physiology, 598(24), 5717-5737.
Ansdell, P., Thomas, K., Hicks, K. M., Hunter, S. K., Howatson, G., & Goodall, S. (2020). Physiological sex differences affect the integrative response to exercise: Acute and chronic implications. Experimental Physiology, 105(12), 2007-2021.
Ansdell, P., Thomas, K., Howatson, G., Hunter, S., & Goodall, S. (2017). Contraction intensity and sex differences in knee-extensor fatigability. Journal of Electromyography and Kinesiology, 37, 68-74.
Azevedo, R. D.e A., Forot, J., Iannetta, D., Macinnis, M. J., Millet, G. Y., & Murias, J. M. (2021). Slight power output manipulations around the maximal lactate steady state have a similar impact on fatigue in females and males. Journal of Applied Physiology, 130(6), 1879-1892.
Bassett, D. R. (2000). Limiting factors for maximum oxygen uptake and determinants of endurance performance. Medicine and Science in Sports and Exercise, 32(1), 70-84.
Batterson, P. M., Norton, M. R., Hetz, S. E., Rohilla, S., Lindsay, K. G., Subudhi, A. W., & Jacobs, R. A. (2020). Improving biologic predictors of cycling endurance performance with near-infrared spectroscopy derived measures of skeletal muscle respiration: E pluribus unum. Physiological Reports, 8(2), e14342.
Beever, A. T., Tripp, T. R., Zhang, J., & Macinnis, M. J. (2020). NIRS-derived skeletal muscle oxidative capacity is correlated with aerobic fitness and independent of sex. Journal of Applied Physiology, 129(3), 558-568.
Beneke, R., & Von Duvillard, S. P. (1996). Determination of maximal lactate steady state response in selected sports events. Medicine and Science in Sports and Exercise, 28(2), 241-246.
Billat, V. R. L., Sirvent, P., Py, G., Koralsztein, J.-P., & Mercier, J. (2003). The concept of maximal lactate steady state: A bridge between biochemistry, physiology and sport science. Sports Medicine, 33(6), 407-426.
Birch, K., & Reilly, T. (2002). The diurnal rhythm in isometric muscular performance differs with eumenorrheic menstrual cycle phase. Chronobiology International, 19(4), 731-742.
Black, M. I., Jones, A. M., Blackwell, J. R., Bailey, S. J., Wylie, L. J., Mcdonagh, S. T. J., Thompson, C., Kelly, J., Sumners, P., Mileva, K. N., Bowtell, J. L., & Vanhatalo, A. (2017). Muscle metabolic and neuromuscular determinants of fatigue during cycling in different exercise intensity domains. Journal of Applied Physiology, 122(3), 446-459.
Bonafiglia, J. T., Islam, H., Preobrazenski, N., Drouin, P., Ma, A., Gerhart, A., Quadrilatero, J., Tschakovsky, M. E., Tripp, D. A., Perry, C. G. R., Simpson, C. A., & Gurd, B. J. (2020). A comparison of pain responses, hemodynamic reactivity and fibre type composition between Bergström and microbiopsy skeletal muscle biopsies. Current Research in Physiology, 3, 1-10.
Borg, G. A. V. (1982). Psychophysical bases of perceived exertion. Medicine and Science in Sports and Exercise, 14(5), 377-381.
Burnley, M. (2009). Estimation of critical torque using intermittent isometric maximal voluntary contractions of the quadriceps in humans. Journal of Applied Physiology, 106(3), 975-983.
Burnley, M., & Jones, A. M. (2018). Power-duration relationship: Physiology, fatigue, and the limits of human performance. European Journal of Sport Science, 18(1), 1-12.
Burnley, M., Vanhatalo, A., & Jones, A. M. (2012). Distinct profiles of neuromuscular fatigue during muscle contractions below and above the critical torque in humans. Journal of Applied Physiology, 113(2), 215-223.
Cardinale, D. A., Larsen, F. J., Schiffer, T. A., Morales-Alamo, D., Ekblom, B., Calbet, J. A. L., Holmberg, H.-C., & Boushel, R. (2018). Superior intrinsic mitochondrial respiration in women than in men. Frontiers in Physiology, 9, 1133.
Carroll, T. J., Taylor, J. L., & Gandevia, S. C. (2017). Recovery of central and peripheral neuromuscular fatigue after exercise. Journal of Applied Physiology, 122(5), 1068-1076.
Carter, S. L., Rennie, C. D., Hamilton, S. J., & Tarnopolsky, M. A. (2001). Changes in skeletal muscle in males and females following endurance training. Canadian Journal of Physiology and Pharmacology, 79(5), 386-392.
Christiansen, D., Macinnis, M. J., Zacharewicz, E., Xu, H., Frankish, B. P., & Murphy, R. M. (2019). A fast, reliable and sample-sparing method to identify fibre types of single muscle fibres. Scientific Reports, 9(1), 6473.
Cureton, K. J. (1981). Matching of male and female subjects using VO2 max. Research Quarterly for Exercise and Sport, 52(2), 264-268.
Degens, H., & Veerkamp, J. H. (1994). Changes in oxidative capacity and fatigue resistance in skeletal muscle. International Journal of Biochemistry, 26(7), 871-878.
Denadai, B. S., & Greco, C. C. (2019). Methodological issues influence determination of critical force during intermittent exercise: Time to task failure vs. contraction time. The Journal of Physiology, 597(24), 5985-5986.
Duke, A. M., & Steele, D. S. (2000). Characteristics of phosphate-induced Ca2+ efflux from the SR in mechanically skinned rat skeletal muscle fibers. American Journal of Physiology. Cell Physiology, 278(1), C126-C135.
Elias, L. J., Bryden, M. P., & Bulman-Fleming, M. B. (1998). Footedness is a better predictor than is handedness of emotional lateralization. Neuropsychologia, 36(1), 37-43.
Enoka, R. M., & Duchateau, J. (2008). Muscle fatigue: What, why and how it influences muscle function. The Journal of Physiology, 586(1), 11-23.
Esbjörnsson, M., Sylvén, C., Holm, I., & Jansson, E. (1993). Fast twitch fibres may predict anaerobic performance in both females and males. International Journal of Sports Medicine, 14(05), 257-263.
Formosa, L. E., Muellner-Wong, L., Reljic, B., Sharpe, A. J., Jackson, T. D., Beilharz, T. H., Stojanovski, D., Lazarou, M., Stroud, D. A., & Ryan, M. T. (2020). Dissecting the roles of mitochondrial complex I intermediate assembly complex factors in the biogenesis of complex I. Cell Reports, 31(3), 107541.
Foster, C., Florhaug, J. A., Franklin, J., Gottschall, L., Hrovatin, L. A., Parker, S., Doleshal, P., & Dodge, C. (2001). A new approach to monitoring exercise training. Journal of Strength and Conditioning Research, 15(1), 109-115.
Frankish, B. P., Najdovska, P., Xu, H., Wette, S. G., & Murphy, R. M. (2021). Effects of voluntary wheel running on mitochondrial content and dynamics in rat skeletal muscle. Journal of Muscle Research and Cell Motility, 42(1), 67-76.
Fuku, N., Kumagai, H., & Ahmetov, I. I. (2019). Genetics of muscle fiber composition. In Sports, exercise, and nutritional genomics: Current status and future directions, (pp. 295-314).
Gandevia, S. C. (2001). Spinal and supraspinal factors in human muscle fatigue. Physiological Reviews, 81(4), 1725-1789.
Gifford, J. R., Garten, R. S., Nelson, A. D., Trinity, J. D., Layec, G., Witman, M. A. H., Weavil, J. C., Mangum, T., Hart, C., Etheredge, C., Jessop, J., Bledsoe, A., Morgan, D. E., Wray, D. W., Rossman, M. J., & Richardson, R. S. (2016). Symmorphosis and skeletal muscle V˙O2 max : In vivo and in vitro measures reveal differing constraints in the exercise-trained and untrained human. The Journal of Physiology, 594(6), 1741.
Glenmark, B., Hedberg, G., & Jansson, E. (1992). Changes in muscle fibre type from adolescence to adulthood in women and men. Acta Physiologica Scandinavica, 146(2), 251-259.
Hayot, M. (2005). Skeletal muscle microbiopsy: A validation study of a minimally invasive technique. European Respiratory Journal, 25(3), 431-440.
Hill, D. W. (1993). The critical power concept: A review. Sports Medicine, 16(4), 237-254.
Hoffmann, M. D., Colley, R. C., Doyon, C. Y., Wong, S. L., Tomkinson, G. R., & Lang, J. J. (2019). Normative-referenced percentile values for physical fitness among Canadians. Health Reports, 30(10), 14-22.
Hunter, S. K. (2014). Sex differences in human fatigability: Mechanisms and insight to physiological responses. Acta Physiologica (Oxf), 210(4), 768-789.
Hunter, S. K. (2016). The relevance of sex differences in performance fatigability. Medicine and Science in Sports and Exercise, 48(11), 2247-2256.
Iannetta, D., Inglis, E. C., Mattu, A. T., Fontana, F. Y., Pogliaghi, S., Keir, D. A., & Murias, J. M. (2020). A critical evaluation of current methods for exercise prescription in women and men. Medicine and Science in Sports and Exercise, 52(2), 466-473.
Ivy, J. L., Withers, R. T., Van Handel, P. J., Elger, D. H., & Costill, D. L. (1980). Muscle respiratory capacity and fiber type as determinants of the lactate threshold. Journal of Applied Physiology, 48(3), 523-527.
James, J. J., Leach, O. K., Young, A. M., Newman, A. N., Mpongo, K. L., Quirante, J. M., Wardell, D. B., Ahmadi, M., & Gifford, J. R. (2023). The exercise power-duration relationship is equally reproducible in eumenorrheic female and male humans. Journal of Applied Physiology, 134(2), 230-241.
Jones, A. M., Vanhatalo, A., Burnley, M., Morton, R. H., & Poole, D. C. (2010). Critical power: Implications for determination of V˙O2max and exercise tolerance. Medicine and Science in Sports and Exercise, 42(10), 1876-1890.
Jones, A. M., Wilkerson, D. P., Dimenna, F., Fulford, J., & Poole, D. C. (2008). Muscle metabolic responses to exercise above and below the “critical power” assessed using 31P-MRS. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 294(2), R585-R593.
Joumaa, V., Power, G. A., Hisey, B., Caicedo, A., Stutz, J., & Herzog, W. (2015). Effects of fiber type on force depression after active shortening in skeletal muscle. Journal of Biomechanics, 48(10), 1687-1692.
Junker, A., Wang, J., Gouspillou, G., Ehinger, J. K., Elmér, E., Sjövall, F., Fisher-Wellman, K., Neufer, P. D., Molina, A. J. A., Ferrucci, L., & Picard, M. (2021). Human studies of mitochondrial biology demonstrate an overall lack of binary sex differences: A multivariate meta-analysis. https://www.medrxiv.org/content/10.1101/2021.11.03.21265871v1
Kontro, H., Bertagnolli, C., Murias, J. M., & Macinnis, M. J. (2022). Impairment in maximal lactate steady state after carbon monoxide inhalation is related to training status. Experimental Physiology, 107(11), 1265-1282.
Koo, T. K., & Li, M. Y. (2016). A guideline of selecting and reporting intraclass correlation coefficients for reliability research. Journal of Chiropractic Medicine, 15(2), 155-163.
Krüger, R. L., Aboodarda, S. J., Jaimes, L. M., Vaz, M. A., Samozino, P., & Millet, G. Y. (2020). Age-related neuromuscular fatigue and recovery after cycling: Measurements in isometric and dynamic modes. Experimental Gerontology, 133, 110877.
Kumagai, H., Tobina, T., Ichinoseki-Sekine, N., Kakigi, R., Tsuzuki, T., Zempo, H., Shiose, K., Yoshimura, E., Kumahara, H., Ayabe, M., Higaki, Y., Yamada, R., Kobayashi, H., Kiyonaga, A., Naito, H., Tanaka, H., & Fuku, N. (2018). Role of selected polymorphisms in determining muscle fiber composition in Japanese men and women. Journal of Applied Physiology, 124(5), 1377-1384.
Larsen, S., Nielsen, J., Hansen, C. N., Nielsen, L. B., Wibrand, F., Stride, N., Schroder, H. D., Boushel, R., Helge, J. W., Dela, F., & Hey-Mogensen, M. (2012). Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. The Journal of Physiology, 590(14), 3349-3360.
Macinnis, M. J., Zacharewicz, E., Martin, B. J., Haikalis, M. E., Skelly, L. E., Tarnopolsky, M. A., Murphy, R. M., & Gibala, M. J. (2017). Superior mitochondrial adaptations in human skeletal muscle after interval compared to continuous single-leg cycling matched for total work. The Journal of Physiology, 595(9), 2955-2968.
Makin, T. R., & Orban De Xivry, J.-J. (2019). Ten common statistical mistakes to watch out for when writing or reviewing a manuscript. Elife, 8, e48175.
Mcnulty, K. L., Elliott-Sale, K. J., Dolan, E., Swinton, P. A., Ansdell, P., Goodall, S., Thomas, K., & Hicks, K. M. (2020). The effects of menstrual cycle phase on exercise performance in eumenorrheic women: A systematic review and meta-analysis. Sports Medicine, 50(10), 1813-1827.
Micklewright, D., St Clair Gibson, A., Gladwell, V., & Al Salman, A. (2017). Development and validity of the rating-of-fatigue scale. Sports Medicine, 47(11), 2375-2393.
Mira, J., Aboodarda, S. J., Floreani, M., Jaswal, R., Moon, S. J., Amery, K., Rupp, T., & Millet, G. Y. (2018). Effects of endurance training on neuromuscular fatigue in healthy active men. Part I: Strength loss and muscle fatigue. European Journal of Applied Physiology, 118(11), 2281-2293.
Mitchell, E. A., Martin, N. R. W., Bailey, S. J., & Ferguson, R. A. (2018). Critical power is positively related to skeletal muscle capillarity and type I muscle fibers in endurance-trained individuals. Journal of Applied Physiology (1985), 125(3), 737-745.
Mollica, J. P., Oakhill, J. S., Lamb, G. D., & Murphy, R. M. (2009). Are genuine changes in protein expression being overlooked? Reassessing Western blotting. Analytical Biochemistry, 386(2), 270-275.
Montero, D., Madsen, K., Meinild-Lundby, A.-K., Edin, F., & Lundby, C. (2018). Sexual dimorphism of substrate utilization: Differences in skeletal muscle mitochondrial volume density and function. Experimental Physiology, 103(6), 851-859.
Moritani, T., Nagata, A., Devries, H. A., & Muro, M. (1981). Critical power as a measure of physical work capacity and anaerobic threshold. Ergonomics, 24(5), 339-350.
Murphy, R. M. (2011). Enhanced technique to measure proteins in single segments of human skeletal muscle fibers: Fiber-type dependence of AMPK-α1 and -β1. Journal of Applied Physiology, 110(3), 820-825.
Ørtenblad, N., Nielsen, J., Saltin, B., & Holmberg, H.-C. (2011). Role of glycogen availability in sarcoplasmic reticulum Ca2+ kinetics in human skeletal muscle. The Journal of Physiology, 589(3), 711-725.
Ørtenblad, N., Westerblad, H., & Nielsen, J. (2013). Muscle glycogen stores and fatigue. The Journal of Physiology, 591(18), 4405-4413.
Pethick, J., Winter, S. L., & Burnley, M. (2020). Physiological evidence that the critical torque is a phase transition, not a threshold. Medicine and Science in Sports and Exercise, 52(11), 2390-2401.
Poole, D. C., Burnley, M., Vanhatalo, A., Rossiter, H. B., & Jones, A. M. (2016). Critical power: An important fatigue threshold in exercise physiology. Medicine and Science in Sports and Exercise, 48(11), 2320-2334.
Schäfer, L. U., Hayes, M., & Dekerle, J. (2019). The magnitude of neuromuscular fatigue is not intensity dependent when cycling above critical power but relates to aerobic and anaerobic capacities. Experimental Physiology, 104(2), 209-219.
Shansky, R. M., & Murphy, A. Z. (2021). Considering sex as a biological variable will require a global shift in science culture. Nature Neuroscience, 24(4), 457-464.
Simoneau, J. A., Lortie, G., Boulay, M. R., Thibault, M.-C., Thériault, G., & Bouchard, C. (1985). Skeletal muscle histochemical and biochemical characteristics in sedentary male and female subjects. Canadian Journal of Physiology and Pharmacology, 63(1), 30-35.
Simoneau, J. A., & Bouchard, C. (1989). Human variation in skeletal muscle fiber-type proportion and enzyme activities. American Journal of Physiology, 257(4 Pt 1), E567-E572.
Smith, J., Dangelmaier, B., & Hill, D. (1999). Critical power is related to cycling time trial performance. International Journal of Sports Medicine, 20(06), 374-378.
Staron, R. S., Hagerman, F. C., Hikida, R. S., Murray, T. F., Hostler, D. P., Crill, M. T., Ragg, K. E., & Toma, K. (2000). Fiber type composition of the vastus lateralis muscle of young men and women. Journal of Histochemistry and Cytochemistry, 48(5), 623-629.
Strojnik, V., & Komi, P. V. (1998). Neuromuscular fatigue after maximal stretch-shortening cycle exercise. Journal of Applied Physiology (1985), 84(1), 344-350.
Tamm, A. S., Lagerquist, O., Ley, A. L., & Collins, D. F. (2009). Chronotype influences diurnal variations in the excitability of the human motor cortex and the ability to generate torque during a maximum voluntary contraction. Journal of Biological Rhythms, 24(3), 211-224.
Tarnopolsky, L. J., Macdougall, J. D., Atkinson, S. A., Tarnopolsky, M. A., & Sutton, J. R. (1990). Gender differences in substrate for endurance exercise. Journal of Applied Physiology, 68(1), 302-308.
Tarnopolsky, M. (1998). Chapter 1 Introduction. In Gender differences in metabolism: Practical and nutritional implications. CRC Press.
Tarnopolsky, M. A. (2008). Sex differences in exercise metabolism and the role of 17-beta estradiol. Medicine and Science in Sports and Exercise, 40(4), 648-654.
Tarnopolsky, M. A., Rennie, C. D., Robertshaw, H. A., Fedak-Tarnopolsky, S. N., Devries, M. C., & Hamadeh, M. J. (2007). Influence of endurance exercise training and sex on intramyocellular lipid and mitochondrial ultrastructure, substrate use, and mitochondrial enzyme activity. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 292(3), R1271-R1278.
Toursel, T., Bastide, B., Stevens, L., Rieger, F., & Mounier, Y. (2000). Alterations in contractile properties and expression of myofibrillar proteins in wobbler mouse muscles. Experimental Neurology, 162(2), 311-320.
Townsend, N. E., Nichols, D. S., Skiba, P. F., Racinais, S., & Périard, J. D. (2017). Prediction of critical power and W′ in hypoxia: Application to work-balance modelling. Frontiers in Physiology, 8, 180.
Tripp, T. R., Frankish, B. P., Lun, V., Wiley, J. P., Shearer, J., Murphy, R. M., & Macinnis, M. J. (2022). Time course and fibre type-dependent nature of calcium-handling protein responses to sprint interval exercise in human skeletal muscle. The Journal of Physiology, 600(12), 2897-2917.
Wells, J. C. K. (2007). Sexual dimorphism of body composition. Best Practice & Research Clinical Endocrinology & Metabolism, 21(3), 415-430.
Westerblad, H., Allen, D. G., & Lännergren, J. (2002). Muscle fatigue: Lactic acid or inorganic phosphate the major cause? Physiology, 17(1), 17-21.
Wyckelsma, V. L., Levinger, I., Mckenna, M. J., Formosa, L. E., Ryan, M. T., Petersen, A. C., Anderson, M. J., & Murphy, R. M. (2017). Preservation of skeletal muscle mitochondrial content in older adults: Relationship between mitochondria, fibre type and high-intensity exercise training. The Journal of Physiology, 595(11), 3345-3359.