Extracellular Ca2+-induced force restoration in K+-depressed skeletal muscle of the mouse involves an elevation of [K+]i: Implications for fatigue

Journal of Applied Physiology

Volumn 118, Issue 6, 2015, Pages 662-674

  Cairns, Simeon P ^a   Leader, John P ^b   Loiselle, Denis S ^c,d   Higgins, Amanda ^e   Lin, Wei ^e   Renaud, Jean Marc ^e  

^a AUCKLAND UNIVERSITY OF TECHNOLOGY   (New Zealand)

^b UNIVERSITY OF OTAGO   (New Zealand)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

^d UNIVERSITY OF AUCKLAND   (New Zealand)

^e UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Action potential; Calcium; Excitability; Fiber type; Muscle fatigue; Potassium

Indexed keywords

CALCIUM; POTASSIUM;

ACTION POTENTIAL; ANIMAL; FEMALE; MALE; METABOLISM; MOUSE; MUSCLE CONTRACTION; MUSCLE FATIGUE; PHYSIOLOGY; SARCOLEMMA; SKELETAL MUSCLE;

ACTION POTENTIALS; ANIMALS; CALCIUM; FEMALE; MALE; MICE; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE FIBERS, SKELETAL; POTASSIUM; SARCOLEMMA;

EID: 84925355713     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00705.2013     Document Type: Article

References (71)

1. Ahmed J, Weisberg LS. Hyperkalemia in dialysis patients. Semin Dial 14: 348-356, 2001.
2. Albuquerque EX, Thesleff S. The effect of calcium on the skeletal muscle membrane after treatment with phospholipase C. Acta Physiol Scand 72: 310-321, 1968.
3. Allen DG, Lamb GD, Westerblad H. Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88: 287-332, 2008.
4. Balog EM, Fitts RH. Effects of depolarization and low intracellular pH on charge movement currents of frog skeletal muscle fibers. J Appl Physiol 90: 228-234, 2001.
5. Banas C, Clow B, Jasmin J, Renaud JM. The KATP channel Kir6.2 subunit protein content is higher in glycolytic than in oxidative skeletal muscle fibers. Am J Physiol Regul Integr Comp Physiol 301: R916-R925, 2011.
6. Bianchi CP, Narayan S. Muscle fatigue and the role of transverse tubules. Science 215: 295-296, 1982.
7. Boyle PJ, Conway EJ. Potassium accumulation in muscle and associated changes. J Physiol 100: 1-63, 1941.
8. 2+-induced inhibition of sodium pump: noncompetitive inhibition in respect of magnesium and sodium cations. Gen Physiol Biophys 17: 179-188, 1998.
9. o in mouse skeletal muscle: implications for fatigue. Am J Physiol Cell Physiol 285: C1131-C1141, 2003.
10. Cairns SP, Chin ER, Renaud JM. Stimulation pulse characteristics and electrode configuration determine site of excitation in isolated mammalian skeletal muscle: implications for fatigue. J Appl Physiol 103: 359-386, 2007.
11. Cairns SP, Dulhunty AF. High-frequency fatigue in rat skeletal muscle: role of extracellular ion concentrations. Muscle Nerve 18: 890-898, 1995.
12. o on membrane potential and contraction in mouse fast- and slow-twitch muscle. Am J Physiol Cell Physiol 273: C598-C611, 1997.
13. 2+] in fatigue of isolated mammalian skeletal muscle. J Appl Physiol 84: 1395-1406, 1998.
14. Cairns SP, Leader JP, Loiselle DS. Exacerbated potassium-induced paralysis of mouse soleus muscle at 37°C vis-à-vis 25°C: implications for fatigue. Pflügers Arch 461: 469-479, 2011.
15. Cairns SP, Lindinger MI. Do multiple ionic interactions contribute to skeletal muscle fatigue? J Physiol 586: 4039-4054, 2008.
16. Cairns SP, Robinson DM, Loiselle DS. Double-sigmoid model for fitting fatigue profiles in mouse fast- and slow-twitch muscle. Exp Physiol 93: 851-862, 2008.
17. Cairns SP, Taberner AJ, Loiselle DS. Changes of surface and t-tubular membrane excitability during fatigue with repeated tetani in isolated mouse fast- and slow-twitch muscle. J Appl Physiol 106: 101-112, 2009.
18. 2+ channels. Exp Physiol 93: 1126-1138, 2008.
19. + pump regulation and skeletal muscle contractility. Physiol Rev 83: 1269-1324, 2003.
20. +-pumps and fatigue in rat muscle. J Physiol 584: 295-304, 2007.
21. Danieli-Betto D, Germinario E, Esposito A, Megighian A, Midrio M, Ravara B, Damiani E, Libera LD, Sabbadini RA, Betto R. Sphingosine 1-phosphate protects mouse extensor digitorum longus skeletal muscle during fatigue. Am J Physiol Cell Physiol 288: C1367-C1373, 2005.
22. Delbono O, Obejero Paz CA, Muchnik S. The effect of verapamil and Ca free solution on mechanical and electrical properties in fast twitch mammalian skeletal muscle. Acta Physiol Pharmacol Ther Latinoam 37: 423-435, 1987.
23. Donaldson PJ, Leader JP. Intracellular ionic activities in the EDL muscle of the mouse. Pflügers Arch 400: 166-170, 1984.
24. Ducret T, Vandebrouck C, Cao ML, Lebacq J, Gailly P. Functional role of store-operated and stretch-activated channels in murine adult skeletal muscle fibres. J Physiol 575: 913-924, 2006.
25. Fitts RH. Cellular mechanisms of muscle fatigue. Physiol Rev 74: 49-94, 1994.
26. 2+ depletion in the transverse tubular system of mammalian muscle. Biophys J 80: 2046-2055, 2001.
27. Gamstorp I, Hauge M, Helweg-Larsen HF, Mjönes H, Sagild U. Adynamia Episodica Hereditaria. A disease clinically resembling familial periodic paralysis but characterized by increasing serum potassium during the paralytic attacks. Am J Med 23: 385-390, 1957.
28. 2+. Eur J Appl Physiol 104: 445-453, 2008.
29. 2+ influx in rat soleus and EDL muscle: mechanisms and effects on cellular integrity. Am J Physiol Regul Integr Comp Physiol 279: R917-R924, 2000.
30. - cotransport activity. News Physiol Sci 18: 196-200, 2003.
31. + conductance improves in vitro the contraction force of skeletal muscle in hypokalemic periodic paralysis. Muscle Nerve 13: 451-457, 1990.
32. Harrison AP, Flatman JA. Measurement of force and both surface and deep M wave properties in isolated rat soleus muscles. Am J Physiol Regul Integr Comp Physiol 277: R1646-R1653, 1999.
33. Hayward LJ, Kim JS, Lee MY, Zhou H, Kim JW, Misra K, Salajegheh M, Wu FF, Matsuda C, Reid V, Cros D, Hoffman EP, Renaud JM, Cannon SC, Brown RH. Targeted mutation of mouse skeletal muscle sodium channel produces myotonia and potassium-sensitive weakness. J Clin Invest 118: 1437-1449, 2008.
34. 2+ induced by depolarization of mouse skeletal muscle fibres. J Physiol 509: 93-102, 1998.
35. Juel C. Potassium and sodium shifts during in vitro isometric muscle contraction, and the time course of the ion-gradient recovery. Pflügers Arch 406: 458-463, 1986.
36. 2-adrenoceptor activation on ion-shifts and fatigue in mouse soleus muscles stimulated in vitro. Acta Physiol Scand 134: 209-216, 1988.
37. Juel C. Muscle action potential propagation velocity changes during activity. Muscle Nerve 11: 714-719, 1988.
38. Kristensen M, Hansen T, Juel C. Membrane proteins involved in potassium shifts during muscle activity and fatigue. Am J Physiol Regul Integr Comp Physiol 290: R766-R772, 2006.
39. Kristensen M, Juel C. Potassium-transporting proteins in skeletal muscle: cellular location and fibre-type differences. Acta Physiol (Oxf) 198: 105-123, 2010.
40. 2+ entry in skeletal muscle. Pflügers Arch 460: 813-823, 2010.
41. 2+ flux through the transverse tubular membrane, activated by individual action potentials in mammalian skeletal muscle. J Physiol 587: 2299-2312, 2009.
42. Leader JP, Bray JJ, Macknight ADC, Mason DR, McCaig D, Mills RG. Cellular ions in intact and denervated muscles of the rat. J Membr Biol 81: 19-27, 1984.
43. Lindinger MI, Heigenhauser GJF. Ion fluxes during tetanic stimulation in isolated perfused rat hindlimb. Am J Physiol Regul Integr Comp Physiol 254: R117-R126, 1988.
44. Lindinger MI, Leung M, Trajcevski KE, Hawke TJ. Volume regulation in mammalian skeletal muscle: the role of sodium-potassium-chloride cotransporters during exposure to hypertonic solutions. J Physiol 589: 2887-2899, 2011.
45. + pump inactivation: implications for fatigue. J Appl Physiol 104: 288-295, 2008.
46. 2+ ions in excitation-contraction coupling of skeletal muscle fibres. Biochim Biophys Acta 1241: 59-116, 1995.
47. 2+ influx and muscle damage in the rat: loss of membrane integrity and impaired force recovery. J Physiol 559: 271-285, 2004.
48. 2+ in skeletal myogenic cells. Am J Physiol Cell Physiol 284: C969-C976, 2003.
49. Nielsen HB, Bredmose PR, Strømstad M, Volianitis S, Quistorff B, Secher NH. Bicarbonate attenuates arterial desaturation during maximal exercise in humans. J Appl Physiol 93: 724-731, 2002.
50. - currents in frog parathyroid cells through the mediation of arachidonic acid cascade. PLos One 6: e19158, 2011.
51. Pan Z, Yang D, Nagaraj RY, Nosek TA, Nishi M, Takeshima H, Cheng H, Ma J. Dysfunction of store-operated calcium channel in muscle cells lacking mg29. Nat Cell Biol 4: 379-383, 2002.
52. Pearson CM. The periodic paralyses: differential features and pathological observations in permanent myopathic weakness. Brain 87: 341-354, 1964.
53. +] in rat muscle: effect of temperature, lactic acid and β2-agonist. J Physiol 551: 277-286, 2003.
54. 2+ influx and muscle fatigue. Pflügers Arch 461: 115-122, 2011.
55. 2+transients of fast skeletal muscle fibers. Implications for muscle fatigue. J Muscle Res Cell Motil 31: 13-33, 2010.
56. Radzyukevich T, Lipska E, Pavelkova J, Zacharova D. Characterization of tension decline in different types of fatigue-resistant skeletal muscle fibres of the frog. Low extracellular calcium effects. Gen Physiol Biophys 12: 473-490, 1993.
57. + on the twitch and tetanic contraction in the sartorius muscle of the frog, Rana pipiens. Implication for fatigue in vivo. Can J Physiol Pharmacol 70: 1236-1246, 1992.
58. Rich MM, Pinter MJ. Crucial role of sodium channel fast inactivation in muscle fibre inexcitability in a rat model of critical illness myopathy. J Physiol 547: 555-566, 2003.
59. Ruff RL, Simoncini L, Stühmer W. Slow sodium channel inactivation in mammalian muscle: a possible role in regulating excitability. Muscle Nerve 11: 502-510, 1988.
60. Sejersted OM, Sjøgaard G. Dynamics and consequences of potassium shifts in skeletal muscle and heart during exercise. Physiol Rev 80: 1411-1481, 2000.
61. Shah VN, Wingo TL, Weiss KL, Williams CK, Balser JR, Chazin WJ. Calcium-dependent regulation of the voltage-gated sodium channel hH1: intrinsic and extrinsic sensors use a common molecular switch. Proc Natl Acad Sci USA 103: 3592-3597, 2006.
62. Shalton PM, Wareham AC. Intracellular activity of potassium in normal and dystrophic skeletal muscle from C57BL/6J mice. Exp Neurol 74: 673-687, 1981.
63. - cotransporter in human nasal epithelia. J Biol Chem 279: 18567-18574, 2004.
64. Stankovičovə T, Zemková H, Breier A, Amler E, Burkhard M, Vyskočil F. The effects of calcium and calcium channel blockers on sodium pump. Pflügers Arch 429: 716-721, 1995.
65. Stiber J, Hawkins A, Zhang ZS, Wang S, Burch J, Graham V, Ward CC, Seth M, Finch E, Malouf N, Williams RS, Eu JP, Rosenburg P. STIM1 signalling controls store-operated calcium entry required for development and contractile function in skeletal muscle. Nat Cell Biol 10: 688-697, 2008.
66. 2+ modulates charge movement in skeletal muscle. Gen Physiol Biophys 16: 59-77, 1997.
67. Usher-Smith JA, Xu W, Fraser JA, Huang CLH. Alterations in calcium homeostasis reduce membrane excitability in amphibian skeletal muscle. Pflügers Arch 453: 211-221, 2006.
68. Williams JH, Ward CW. Dihydropyridine effects on skeletal muscle fatigue. J Physiol (Paris) 85: 235-238, 1991.
69. Zanou N, Shapovalov G, Louis M, Tajeddine N, Gallo C, Van Schoor M, Anguish I, Cao ML, Schakman O, Dietrich A, Lebacq J, Ruegg U, Roulet E, Birnbaumer L, Gailly P. Role of TRPC1 channel in skeletal muscle function. Am J Physiol Cell Physiol 298: C149-C162, 2010.
70. Zhang SJ, Bruton JD, Katz A, Westerblad H. Limited oxygen diffusion accelerates fatigue development in mouse skeletal muscle. J Physiol 572: 551-559, 2006.
71. Zhao X, Yoshida M, Brotto L, Takeshima H, Weisleder N, Hirata Y, Nosek TM, Ma J, Brotto M. Enhanced resistance to fatigue and altered calcium handing properties of sarcalumenin knockout mice. Physiol Genomics 23: 72-78, 2005.