Fatigue-induced change in T-system excitability and its major cause in rat fast-twitch skeletal muscle in vivo.
membrane excitability
muscle fatigue
skinned fibre
Journal
The Journal of physiology
ISSN: 1469-7793
Titre abrégé: J Physiol
Pays: England
ID NLM: 0266262
Informations de publication
Date de publication:
11 2020
11 2020
Historique:
received:
14
01
2020
accepted:
11
08
2020
pubmed:
25
8
2020
medline:
2
3
2021
entrez:
25
8
2020
Statut:
ppublish
Résumé
Using mechanically skinned rat muscle fibres, we investigated (i) transverse tubular-system (T-system) excitability after high-intensity contractions, and (ii) the mechanisms underlying the fatigue-induced alteration of the T-system excitability. T-system excitability estimated by using skinned fibres, which is highly regulated by T-system Na The purpose of this study was to investigate transverse tubular system (T-system) excitability after skeletal muscle contractions in vivo, and the contribution of S-glutathionylation of Na
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
5195-5211Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2020 The Authors. The Journal of Physiology © 2020 The Physiological Society.
Références
Allen DG, Lamb GD & Westerblad H (2008). Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88, 287-332.
Benziane B, Widegren U, Pirkmajer S, Henriksson J, Stepto NK & Chibalin AV (2011). Effect of exercise and training on phospholemman phosphorylation in human skeletal muscle. Am J Physiol Endocrinol Metab 301, E456-E466.
Bossuyt J, Despa S, Han F, Hou Z, Robia SL, Lingrel JB & Bers DM (2009). Isoform specificity of the Na/K-ATPase association and regulation by phospholemman. J Biol Chem 284, 26749-26757.
Cairns SP & Borrani F (2015). β-Adrenergic modulation of skeletal muscle contraction: key role of excitation-contraction coupling. J Physiol 593, 4713-4727.
Cheng AJ, Bruton JD, Lanner JT & Westerblad H (2015). Antioxidant treatments do not improve force recovery after fatiguing stimulation of mouse skeletal muscle fibres. J Physiol 593, 457-472.
Clausen T (2008). Role of Na+,K+-pumps and transmembrane Na+,K+-distribution in muscle function. The FEPS lecture - Bratislava 2007. Acta Physiol 192, 339-349.
Clausen T (2013). Quantification of Na+,K+ pumps and their transport rate in skeletal muscle: functional significance. J Gen Physiol 142, 327-345.
Crambert G, Fuzesi M, Garty H, Karlish S & Geering K (2002). Phospholemman (FXYD1) associates with Na,K-ATPase and regulates its transport properties. Proc Natl Acad Sci U S A 99, 11476-11481.
Dalle-Donne I, Rossi R, Giustarini D, Colombo R & Milzani A (2007). S-glutathionylation in protein redox regulation. Free Radic Biol Med 43, 883-898.
Dulhunty AF (1984). Heterogeneity of T-tubule geometry in vertebrate skeletal muscle fibres. J Muscle Res Cell Motil 5, 333-347.
Dutka TL & Lamb GD (2007). Na+-K+ pumps in the transverse tubular system of skeletal muscle fibers preferentially use ATP from glycolysis. Am J Physiol Cell Physiol 293, C967-C977.
Dutka TL, Mollica JP, Posterino GS & Lamb GD (2011). Modulation of contractile apparatus Ca2+ sensitivity and disruption of excitation-contraction coupling by S-nitrosoglutathione in rat muscle fibres. J Physiol 589, 2181-2196.
Dutka TL, Murphy RM, Stephenson DG & Lamb GD (2008). Chloride conductance in the transverse tubular system of rat skeletal muscle fibres: importance in excitation-contraction coupling and fatigue. J Physiol 586, 875-887.
Espinosa A, Henriquez-Olguin C & Jaimovich E (2016). Reactive oxygen species and calcium signals in skeletal muscle: A crosstalk involved in both normal signaling and disease. Cell Calcium 60, 172-179.
Geering K (2005). Function of FXYD proteins, regulators of Na,K-ATPase. J Bioenerg Biomembr 37, 387-392.
Grundy D (2015). Principles and standards for reporting animal experiments in The Journal of Physiology and Experimental Physiology. J Physiol 593, 2547-2549.
Hermansen L, Hultman E & Saltin B (1967). Muscle glycogen during prolonged severe exercise. Acta Physiol Scand 71, 129-139.
Jensen R, Nielsen J & Ortenblad N (2020). Inhibition of glycogenolysis prolongs action potential repriming period and impairs muscle function in rat skeletal muscle. J Physiol 598, 789-803.
Ji LL, Stratman FW & Lardy HA (1988). Antioxidant enzyme systems in rat liver and skeletal muscle. Influences of selenium deficiency, chronic training, and acute exercise. Arch Biochem Biophys 263, 150-160.
Jones AB & Curtis KS (2009). Differential effects of estradiol on drinking by ovariectomized rats in response to hypertonic NaCl or isoproterenol: Implications for hyper- vs. hypo-osmotic stimuli for water intake. Physiol Behav 98, 421-426.
Juel C (2009). Na+-K+-ATPase in rat skeletal muscle: muscle fiber-specific differences in exercise-induced changes in ion affinity and maximal activity. Am J Physiol Regul Integr Comp Physiol 296, R125-R132.
Juel C (2014). Oxidative stress (glutathionylation) and Na,K-ATPase activity in rat skeletal muscle. PLoS One 9, e110514.
Juel C, Hostrup M & Bangsbo J (2015). The effect of exercise and beta2-adrenergic stimulation on glutathionylation and function of the Na,K-ATPase in human skeletal muscle. Physiol Rep 3, e12515.
Juel C, Nordsborg NB & Bangsbo J (2013). Exercise-induced increase in maximal in vitro Na-K-ATPase activity in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol 304, R1161-R1165.
Kaplan JH (2002). Biochemistry of Na,K-ATPase. Annu Rev Biochem 71, 511-535.
Karatzaferi C, de Haan A, Ferguson RA, van Mechelen W & Sargeant AJ (2001). Phosphocreatine and ATP content in human single muscle fibres before and after maximum dynamic exercise. Pflugers Arch 442, 467-474.
Kinoshita E, Kinoshita-Kikuta E, Ujihara H & Koike T (2009). Mobility shift detection of phosphorylation on large proteins using a Phos-tag SDS-PAGE gel strengthened with agarose. Proteomics 9, 4098-4101.
Lamb GD & Stephenson DG (1990). Calcium release in skinned muscle fibres of the toad by transverse tubule depolarization or by direct stimulation. J Physiol 423, 495-517.
Lamb, GD & Stephenson, DG (2018). Measurement of force and calcium release using mechanically skinned fibers from mammalian skeletal muscle. J Appl Physiol 125, 1105-1127.
Lamb GD & Westerblad H (2011). Acute effects of reactive oxygen and nitrogen species on the contractile function of skeletal muscle. J Physiol 589, 2119-2127.
Launikonis BS, Barnes M & Stephenson DG (2003). Identification of the coupling between skeletal muscle store-operated Ca2+ entry and the inositol trisphosphate receptor. Proc Natl Acad Sci U S A 100, 2941-2944.
Lifshitz Y, Lindzen M, Garty H & Karlish SJ (2006). Functional interactions of phospholemman (PLM) (FXYD1) with Na+,K+-ATPase. Purification of alpha1/beta1/PLM complexes expressed in Pichia pastoris. J Biol Chem 281, 15790-15799.
Mano H, Watanabe D, Ishii Y, Hirano K, Matsunaga S & Wada M (2015). Endurance training-based tapering fails to improve fatigue resistance of rat skeletal muscle. Adv Exerc Sports Physiol 21, 37-45.
Manoharan P, Radzyukevich TL, Hakim Javadi H, Stiner CA, Landero Figueroa JA, Lingrel JB & Heiny JA (2015). Phospholemman is not required for the acute stimulation of Na+-K+-ATPase alpha2-activity during skeletal muscle fatigue. Am J Physiol Cell Physiol 309, C813-C822.
Mishima T, Yamada T, Sakamoto M, Sugiyama M, Matsunaga S & Wada M (2008). Time course of changes in in vitro sarcoplasmic reticulum Ca2+-handling and Na+-K+-ATPase activity during repetitive contractions. Pflugers Arch 456, 601-609.
Nielsen JJ, Mohr M, Klarskov C, Kristensen M, Krustrup P, Juel C & Bangsbo J (2004a). Effects of high-intensity intermittent training on potassium kinetics and performance in human skeletal muscle. J Physiol 554, 857-870.
Nielsen OB, Ortenblad N, Lamb GD & Stephenson DG (2004b). Excitability of the T-tubular system in rat skeletal muscle: roles of K+ and Na+ gradients and Na+-K+ pump activity. J Physiol 557, 133-146.
Ortenblad N, Westerblad H & Nielsen J (2013). Muscle glycogen stores and fatigue. J Physiol 591, 4405-4413.
Overgaard K, Nielsen OB, Flatman JA & Clausen T (1999). Relations between excitability and contractility in rat soleus muscle: role of the Na+-K+ pump and Na+/K+ gradients. J Physiol 518, 215-225.
Pedersen TH, de Paoli FV, Flatman JA & Nielsen OB (2009a). Regulation of ClC-1 and KATP channels in action potential-firing fast-twitch muscle fibers. J Gen Physiol 134, 309-322.
Pedersen TH, Macdonald WA, de Paoli FV, Gurung IS & Nielsen OB (2009b). Comparison of regulated passive membrane conductance in action potential-firing fast- and slow-twitch muscle. J Gen Physiol 134, 323-337.
Pedersen TH, Riisager A, de Paoli FV, Chen TY & Nielsen OB (2016). Role of physiological ClC-1 Cl− ion channel regulation for the excitability and function of working skeletal muscle. J Gen Physiol 147, 291-308.
Petrushanko IY, Yakushev S, Mitkevich VA, Kamanina YV, Ziganshin RH, Meng X, Anashkina AA, Makhro A, Lopina OD, Gassmann M, Makarov AA & Bogdanova A (2012). S-glutathionylation of the Na,K-ATPase catalytic alpha subunit is a determinant of the enzyme redox sensitivity. J Biol Chem 287, 32195-32205.
Pirkmajer S & Chibalin AV (2016). Na,K-ATPase regulation in skeletal muscle. Am J Physiol Endocrinol Metab 311, E1-E31.
Posterino GS, Lamb GD & Stephenson DG (2000). Twitch and tetanic force responses and longitudinal propagation of action potentials in skinned skeletal muscle fibres of the rat. J Physiol 527, 131-137.
Radzyukevich TL, Neumann JC, Rindler TN, Oshiro N, Goldhamer DJ, Lingrel JB & Heiny JA (2013). Tissue-specific role of the Na,K-ATPase alpha2 isozyme in skeletal muscle. J Biol Chem 288, 1226-1237.
Rasmussen MK, Kristensen M & Juel C (2008). Exercise-induced regulation of phospholemman (FXYD1) in rat skeletal muscle: implications for Na+/K+-ATPase activity. Acta Physiol 194, 67-79.
Rich MM & Pinter MJ (2003). Crucial role of sodium channel fast inactivation in muscle fibre inexcitability in a rat model of critical illness myopathy. J Physiol 547, 555-566.
Sejersted OM & Sjogaard G (2000). Dynamics and consequences of potassium shifts in skeletal muscle and heart during exercise. Physiol Rev 80, 1411-1481.
Stephenson DG (2006). Tubular system excitability: an essential component of excitation-contraction coupling in fast-twitch fibres of vertebrate skeletal muscle. J Muscle Res Cell Motil 27, 259-274.
Watanabe D, Aibara C, Okada N & Wada M (2018). Thermal pretreatment facilitates recovery from prolonged low-frequency force depression in rat fast-twitch muscle. Physiol Rep 6, e13853.
Watanabe D, Aibara C & Wada M (2019a). Treatment with EUK-134 improves sarcoplasmic reticulum Ca2+ release but not myofibrillar Ca2+ sensitivity after fatiguing contraction of rat fast-twitch muscle. Am J Physiol Regul Integr Comp Physiol 316, R543-R551.
Watanabe D, Kanzaki K, Kuratani M, Matsunaga S, Yanaka N & Wada M (2015). Contribution of impaired myofibril and ryanodine receptor function to prolonged low-frequency force depression after in situ stimulation in rat skeletal muscle. J Muscle Res Cell Motil 36, 275-286.
Watanabe D, Lamboley CR & Lamb GD (2019b). Effects of S-glutathionylation on the passive force-length relationship in skeletal muscle fibres of rats and humans. J Muscle Res Cell Motil (in press; https://doi.org/10.1007/s10974-019-09563-5).
Watanabe D & Wada M (2016). Predominant cause of prolonged low-frequency force depression changes during recovery after in situ fatiguing stimulation of rat fast-twitch muscle. Am J Physiol Regul Integr Comp Physiol 311, R919-R929.
Williams MW, Resneck WG, Kaysser T, Ursitti JA, Birkenmeier CS, Barker JE & Bloch RJ (2001). Na,K-ATPase in skeletal muscle: two populations of beta-spectrin control localization in the sarcolemma but not partitioning between the sarcolemma and the transverse tubules. J Cell Sci 114, 751-762.