Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-10T11:35:38.729Z Has data issue: false hasContentIssue false
  • English
  • Français

Determinants of surface membrane and transverse-tubular excitability in skeletal muscle: implications for high-intensity exercise

Published online by Cambridge University Press:  09 March 2007

Michael I. Lindinger
Michael I. Lindinger*
Affiliation:
Department of Human Biology and Nutritional Sciences, University of Guelph, Guelph, ON, Canada, N1G 2W1
*
*mlinding@uoguelph.ca
Get access

Abstract

The fatigue of high-intensity exercise is now believed to reside primarily within the excitation–contraction coupling processes associated with the plasma membrane of skeletal muscle (sarcolemm) and calcium-mediated events leading to myofilament sliding. This paper summarizes recent developments and advances in the identification of factors that contribute to changes in sarcolemmal excitability of mammalian skeletal muscle as a consequence of high-intensity exercise. There is an increasing recognition of the probable role that is played by the transverse tubular system (T-system), a system that comprises c. 80% of the total sarcolemmal surface capable of ion exchange. Furthermore, the fluid within the T-system has limited access to interstitial fluid bathing myofibres; hence, T-system fluid is probably markedly different from interstitial fluid during high-intensity exercise. Mechanically skinned fibre preparation is providing many new insights into functions of the surface membrane and T-system in fatigue. A scenario is developed whereby accumulation of potassium within the T-system ([K+]o) contributes to reduced membrane excitability, as well as lowering of T-system sodium and chloride, concomitant with loss of intracellular potassium ([K+]i) and accumulation of intracellular sodium ([Na+]) and chloride ([Cl−]). Lowering the [Na+]o/[Na+]i ratio and raising myoplasmic [Na+]i have been shown to decrease membrane excitability and impair action potential propagation. Maintained high [Cl−]o may also have a protective effect in maintaining membrane excitability, and this effect appears to be very pronounced in the presence of raised [K+]o. In contrast to dogma associating high [H+] to fatigue, recent studies have also shown that induced acidosis that results in increased [H+]o and [H+]i restores force production in muscles and skinned fibres fatigued by intermittent tetanic stimulation. This effect may be due to a decrease in surface membrane Cl− permeability that serves to restore membrane excitability. During high-intensity exercise, simultaneous changes in trans-membrane ion concentrations and membrane ion conductances may serve to reduce impairment of membrane excitability that provides for a maintained, though reduced, contractile function.

Keywords

membrane potentialpotassiumsodiumT-tubulecontractionchloride
Type
Research Article
Information
Equine and Comparative Exercise Physiology , Volume 2 , Issue 4 , November 2005 , pp. 209 - 217
Copyright
Copyright © Cambridge University Press 2005

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1Lamb, GD (1995). Excitation–contraction coupling and fatigue mechanisms in skeletal muscle: studies with mechanically skinned fibres. Journal of Muscle Research and Cell Motility 23: 81–91.Google Scholar
2Nielsen, OB, Ørtenblad, N, Lamb, GD and Stephenson, DG (2004). Excitability of the T-tubular system in rat skeletal muscle: roles of K + and Na + gradients and Na + –K + pump activity. Journal of Physiology 557: 133–146.Google Scholar
3Sejersted, OM and Sjogaard, G (2000). Dynamics and consequences of potassium shifts in skeletal muscle and heart during exercise. Physiological Reviews 80: 1411–1481.Google Scholar
4Renaud, JM (2002). Modulation of force development by Na +, K +, Na + –K + pump and K ATP channel. Canadian Journal of Applied Physiology 27: 296–315.CrossRefGoogle Scholar
5Gosmanov, AR, Lindinger, MI and Thomason, DB (2003). Riding the tides: [K + ] and volume regulation by Muscle Na + –K + –2Cl - cotransport activity. News in Physiological Sciences 18: 196–200.Google Scholar
6Clausen, T (2003). Na +, K + pump regulation and skeletal muscle contractility. Physiological Reviews 83: 1269–1324.CrossRefGoogle Scholar
7Green, HJ (2004). Membrane excitability, weakness, and fatigue. Canadian Journal of Applied Physiology 29: 291–307.CrossRefGoogle ScholarPubMed
8Yonemura, K (1967). Resting and action potentials in red and white muscle of the rat. Japanese Journal of Physiology 17: 708–719.Google Scholar
9Elliot, GF (1973). Donan and osmotic effects in muscle fibres without membranes. Journal of Mechanochemistry and Cell Motility 2: 83–89.Google Scholar
10Abe, H (2000). Role of histidine-related compounds as intracellular proton buffering constituents in vertebrate muscle. Biochemistry (Moscow) 65: 757–765.Google Scholar
11Beam, KG, Caldwell, JH and Campbell, DT (1985). Na channels in skeletal muscle concentrated near the neuromuscular junction. Nature 313: 588–590.Google Scholar
12Jacquemond, V and Allard, B (1998). Activation of Ca 2+ -activated K + channels by an increase in intracellular Ca 2+ induced by depolarization of mouse skeletal muscle fibres. Journal of Physiology 509: 93–102.CrossRefGoogle Scholar
13Rios, E and Pizarro, G (1991). Voltage sensor of excitation–contraction coupling in skeletal muscle. Physiological Reviews 71: 849–908.CrossRefGoogle ScholarPubMed
14Rios, E, Pizarro, G and Stefani, E (1992). Charge movement and the nature of signal transduction in skeletal muscle excitation–contraction coupling. Annual Reviews of Physiology 54: 109–133.CrossRefGoogle ScholarPubMed
15Nielsen, JJ, Kristensen, M, Hellsten, Y, Bangsbo, J and Juel, C (2003). Localization and function of ATP-sensitive potassium channels in human skeletal muscle. American Journal of Physiology 284: R558–R563Google Scholar
16Cairns, SP, Buller, SJ, Loiselle, DS and Renaud, JM (2003). Changes of action potentials and force at lowered [Na + ] o in mouse skeletal muscle: implications for fatigue. American Journal of Physiology 285: C1131–C1141Google Scholar
17Klocke, R, Steinmeyer, K, Jentsch, TJ and Jockusch, H (1994). Role of innervation, excitability, and myogenic factors in the expression of the muscular chloride channel CIC-1. Journal of Biological Chemistry 269: 27635–27639.Google Scholar
18Lindinger, MI, Hawke, TJ, Vickery, L, Bradford, L and Lipskie, SL (2001). An integrative, in situ approach to examining K + flux in resting skeletal muscle. Canadian Journal of Physiology and Pharmacology 79: 996–1006.CrossRefGoogle ScholarPubMed
19Maughan, D and Recchia, C (1985). Diffusible sodium, potassium, magnesium, calcium and phosphorus in frog skeletal muscle. Journal of Physiology 368: 545–563.Google Scholar
20Bretag, AH (1987). Muscle chloride channels. Physiological Reviews 67: 618–724.CrossRefGoogle ScholarPubMed
21Lindinger, MI and Heigenhauser, GJF (1991). The roles of ion fluxes in skeletal muscle fatigue. Canadian Journal of Physiology and Pharmacology 69: 246–253.Google Scholar
22Sen, CK, Hanninen, O and Orlov, SN (1995). Unidirectional sodium and potassium flux in myogenic L6 cells: mechanisms and volume-dependent regulation. Journal of Applied Physiology 78: 272–281.CrossRefGoogle ScholarPubMed
23Lang, F, Busch, GL, Ritter, M, Volkl, H, Waldegger, S, Gulbins, E and Haussinger, D (1998). Functional significance of cell volume regulatory mechanisms. Physiological Reviews 78: 247–306.Google Scholar
24Lindinger, MI and Heigenhauser, GJF (1988). Ion fluxes during tetanic stimulation in the isolated perfused rat hindlimb. American Journal of Physiology 254: R117–R126.Google Scholar
25Metzger, JM and Fitts, RH (1986). Fatigue from high and low frequency stimulation: role of sarcolemma action potentials. Experimental Neurology 93: 320–333.Google Scholar
26Cairns, SP, Flatman, JA and Clausen, T (1995). Relation between extracellular [K + ], membrane potential and contraction in rat soleus muscle: modulation by the Na + –K + pump. Pflugers Archivs 430: 909–915.CrossRefGoogle ScholarPubMed
27Korge, P and Campbell, KB (1995). The importance of ATPase microenvironment in muscle fatigue: a hypothesis. International Journal of Sports Medicine and Physiological Biochemistry 16: 172–179.Google Scholar
28Tricarico, D, Mallamaci, R, Barbieri, M and Conte-Camerino, D (1997). Modulation of ATP-sensitive K + channel by insulin in rat skeletal muscle fibres. Biochemistry and Biophysics Research Communications 232: 536–539.CrossRefGoogle Scholar
29Weiss, JN and Lamp, ST (1989). Cardiac ATP-sensitive K + channels. Evidence for preferential regulation by glycolysis. Journal of General Physiology 94: 911–935.Google Scholar
30James, JH, Wagner, KR, King, J, Leffler, RE, Upputuri, RK, Balasubramaniam, A, Friend, LA, Shelly, DAPRJ and Fisher, JE (1999). Stimulation of both aerobic glycolysis and Na + –K + –ATPase activity in skeletal muscle by epinephrine or amylin. American Journal of Physiology 277: E176–E186Google Scholar
31Semb, SO and Sejersted, OM (1996). Fuzzy space and control of Na +, K + -pump rate in heart and skeletal muscle. Acta Physiologica Scandinavica 156: 213–225.Google Scholar
32Silverman, BZ, Warley, A, Miller, JIA, James, AF and Shattock, MJ (2003). Is there a transient rise in sub-sarcolemmal Na and activation of Na/K pump current following activation of I Na in ventricular myocardium? Cardiovascular Research 57: 1025–1034.CrossRefGoogle Scholar
33Lindinger, MI, Hawke, TJ, Lipskie, SL, Schaefer, HD and Vickery, L (2002). K + transport and volume regulatory response by NKCC in resting rat hindlimb skeletal muscle. Cellular Physiology and Biochemistry 12: 279–292.Google Scholar
34Franzini-Armstrong, C and Jorgensen, AO (1994). Structure and development of E–C coupling units in skeletal muscle. Annual Reviews of Physiology 56: 509–534.Google Scholar
35Launikonis, BS and Stephenson, DG (2002). Properties of the vertebrate skeletal muscle tubular system as a sealed compartment. Cell Biology International 26: 921–929.CrossRefGoogle ScholarPubMed
36Soeller, C and Cannell, MB (1999). Examination of the transverse tubular system in living rat myocytes by 2-photon microscopy and digital image-processing techniques. Circulation Research 84: 266–275.CrossRefGoogle ScholarPubMed
37Launikonis, BS and Stephenson, DG (2004). Osmotic properties of the sealed tubular system of tad and rat skeletal muscle. Journal of General Physiology 123: 231–247.Google Scholar
38Sjogaard, G (1991). Role of exercise-induced potassium fluxes underlying muscle fatigue: a brief review. Canadian Journal of Physiology and Pharmacology 69: 238–245.Google Scholar
39Dulhunty, AF (1979). Distribution of potassium and chloride permeability over the surface and T-tubule membranes of mammalian skeletal muscle. Journal of Membrane Biology 45: 293–310.Google Scholar
40Renaud, JM and Light, P (1992). Effects of K + on the twitch and tetanic contraction in the sartorius muscle of the frog, Rana pipiens. Implication for fatigue in vivo. Canadian Journal of Physiology and Pharmacology 70: 1236–1246.CrossRefGoogle ScholarPubMed
41Ruff, RL (1997). Sodium channel regulation of skeletal muscle membrane excitability. Annals of the New York Academy of Sciences 835: 64–76.Google Scholar
42Clark, RB, Tremblay, A, Melnyk, P, Allen, BG, Giles, WR and Fiset, C (2001). T-tubule localization of the inward-rectifier K + channel in mouse ventricular myocytes: a role in K + accumulation. Journal of Physiology 537: 979–992.Google Scholar
43Mohr, M, Nordsberg, N, Nielsen, JJ, Pedersen, LD, Fischer, C, Krustrup, P and Bangsbo, J (2004). Potassium kinetics in human muscle interstitium during repeated intense exercise in relation to fatigue. Pflugers Archivs 448: 452–456.Google Scholar
44Hnik, P, Holas, M, Krekule, I, Kriz, N, Mejsnar, J, Smiesko, V, Ujec, E and Vyskocil, F (1976). Work-induced potassium changes in skeletal muscle and effluent venous blood assessed by liquid ion-exchanger microelectrodes. Pflugers Archivs 362: 85–94.Google Scholar
45Vyskocil, F, Hnik, P, Rehfeldt, H, Vejsada, R and Ujec, E (1983). The measurement of K + e concentration changes in human skeletal muscles during volitional contractions. Pflugers Archivs 399: 235–237.Google Scholar
46Cairns, SP, Hing, WA, Slack, JR, Mills, RG and Loiselle, DS (1997). Different effects of raised [K + ] o on membrane potential and contraction in mouse fast- and slow-twitch muscle. American Journal of Physiology 273: C598–C611.Google Scholar
47Gonzalez-Serratos, H, Somlyo, AV, McClellan, G, Shuman, H, Borrero, LM and Somlyo, AP (1978). Composition of vacuoles and sarcoplasmic reticulum in fatigued muscle: electron probe analysis. Proceedings of the National Academy of Sciences 75: 1329–1333.Google Scholar
48Sembrowich, WL, Johnson, D, Wang, E and Hutchison, TE (1982). Electron microprobe analysis of fatigued fast- and slow-twitch muscle. In: Knuttgen, HG, Vogel, JA & Poort-mans, J (eds), Biochemistry of Exercise. Champaign, IL: Human Kinetics Vol. 13 pp. 571–576.Google Scholar
49Cairns, SP, Dulhunty, AF and Renaud, JM (1995). High-frequency fatigue in rat skeletal muscle: role of extracellular ion concentrations. Muscle & Nerve 18: 890–898.Google Scholar
50Posterino, GS, Lamb, GD and Stephensen, DG (2000). Twitch and tetanic force responses and longitudinal propagation of action potentials in skinned skeletal muscle fibres of the rat. Journal of Physiology 527: 131–137.Google Scholar
51Nielsen, OB, de Paoli, F and Overgaard, K (2001). Protective effects of lactic acid on force production in rat skeletal muscle. Journal of Physiology 536: 161–166.Google Scholar
52Renaud, JM and Mainwood, GW (1985). The interactive effects of fatigue and pH on the ionic conductance of frog sartorius muscle fibres. Canadian Journal of Physiology and Pharmacology 63: 1444–1453.Google Scholar
53Fink, R and Luttgau, HC (1976). An evaluation of the membrane constants and the potassium conductance in metabolically exhausted muscle fibres. Journal of Physiology 263: 215–238.CrossRefGoogle ScholarPubMed
54Coonan, JR and Lamb, GD (1998). Effect of transverse-tubular chloride conductance on excitability in skinned skeletal muscle fibres of rat and toad. Journal of Physiology 509: 551–564.Google Scholar
55Pedersen, TH, Nielsen, OB, Lamb, GD and Stephensen, DG (2004). Intracellular acidosis enhances the excitability of working muscle. Science 305: 1144–1147.Google Scholar
56Pedersen, TH, de Paoli, T and Nielsen, OB (2005). Increased excitability of acidified skeletal muscle: role of chloride conductance. Journal of General Physiology 125: 237–246.Google Scholar
57Fahlke, C, Durr, C and George, AL Jr (1997). Mechanism of ion permeation in skeletal muscle chloride channels. Journal of General Physiology 110: 551–564.Google Scholar
58Lehmann-Horn, F and Jurkat-Rott, K (1999). Voltage-gated ion channels and hereditary disease. Physiological Reviews 79: 1317–1372.Google Scholar
59Gurnett, CA, Kahl, SD, Anderson, RD and Campbell, KP (1995). Absence of skeletal muscle sarcolemma chloride channel CIC-1 in myotonic mice. Journal of Biological Chemistry 270: 9035–9038.CrossRefGoogle Scholar
60Milton, RL and Behforouz, MA (1995). Na channel density in extrajunctional sarcolemma of fast and slow twitch mouse skeletal muscle fibres: functional implications and plasticity after fast motoneuron transplantation on to a slow muscle. Journal of Muscle Research and Cell Motility 16: 430–439.Google Scholar
61Cairns, SP, Ruzhynsky, V and Renaud, JM (2004). Protective role of extracellular chloride in fatigue of isolated mammalian skeletal muscle. American Journal of Physiology 287: C762–C770Google Scholar
62van Emst, MG, Klarenbeek, S, Schot, A, Plomp, JJ, Doornenbal, A and Everts, ME (2004). Reducing chloride conductance prevents hyperkalaemia-induced loss of twitch force in rat slow-twitch muscle. Journal of Physiology 561: 169–181.Google Scholar
63Gosmanov, AR, Nordvedt, NC, Brown, R and Thomson, DB (2002). Exercise effects on muscle beta-adrenergic signalling for MAPK-dependent NKCC activity are rapid and persistent. Journal of Applied Physiology 93: 1457–1465.Google Scholar
64Lundvall, J, Mellander, S, Westling, H and White, T (1972). Fluid transfer between blood and tissues during exercise. Acta Physiologica Scandinavica 85: 258–269.Google Scholar
65Bergstrom, J and Hultman, E (1966). The effect of exercise on muscle glycogen and electrolytes in normals. Scandinavian Journal of Clinical and Laboratory Investigation 18: 1–5.Google Scholar