El acoplamiento excitación-contracción en el músculo esquelético: preguntas por responder a pesar de 50 años de estudio

Juan Camilo Calderón-Vélez, Lourdes Carolina Figueroa-Gordon, .

Palabras clave: músculo esquelético, contracción muscular, relajación muscular, calcio, canal liberador de calcio, canales de calcio tipo L, receptor de rianodina, fatiga muscular

Resumen

El mecanismo de acoplamiento excitación-contracción fue definido en el músculo esquelético como la secuencia de eventos que ocurre desde la generación del potencial de acción en la fibra muscular hasta que se inicia la generación de tensión. La regulación e interacción de dichos eventos entre sí ha sido estudiada durante los últimos 50 años utilizando diferentes técnicas, con las cuales se estableció la importancia y origen del ion calcio como activador contráctil, se conocen las principales proteínas involucradas y se inició el estudio de la base ultraestructural y de la regulación farmacológica; además, hay evidencias de que el acoplamiento excitación-contracción se altera en diferentes situaciones como en el envejecimiento, en la fatiga muscular y en algunas enfermedades musculares. Sin embargo, aún hay varias preguntas por responder: ¿cómo es el desarrollo y envejecimiento del mecanismo de acoplamiento excitación-contracción?, ¿cuál es su papel en la fatiga muscular y en algunas enfermedades musculares?, ¿cuál es la naturaleza de la interacción entre diferentes proteínas involucradas en el acoplamiento excitación-contracción?
La presente revisión describe el acoplamiento excitación-contracción en el músculo esquelético y las técnicas utilizadas para su estudio como introducción para discutir algunas de las preguntas que aún falta por responder al respecto.

Descargas

La descarga de datos todavía no está disponible.
  • Juan Camilo Calderón-Vélez Departamento de Fisiología y Bioquímica, Grupo de Fisiología del Ejercicio, Facultad de Medicina, Universidad de Antioquia, Medellín, Colombia. Laboratorio de Fisiología Celular, Centro de Biofísica y Bioquímica, Instituto Venezolano de Investigaci
  • Lourdes Carolina Figueroa-Gordon Laboratorio de Fisiología Celular, Centro de Biofísica y Bioquímica, Instituto Venezolano de Investigaciones Científicas, Estado Miranda, Venezuela

Referencias bibliográficas

1. Kahn A, Sandow A. The potentiation of muscular contraction by the nitrate-ion. Science. 1950;112:647-9.
2. Sandow A. Excitation-contraction coupling in muscular response. Yale J Biol Med. 1952;XXV:176-201.
3. Caputo C. Pharmacological investigations of excitation-contraction coupling. Chapter 14. En: Peachey L, Adrian R, editors. Handbook of physiology. Bethesda: American Physiological Society; 1983.
4. Berridge M, Lipp P, Bootman M. The versatility and universality of calcium signaling. Nature Rev Mol Cell Biol. 2000;1:11-21.
5. Weber A. On the role of calcium in the activity of adenosine 5´-triphosphate hydrolysis by actomyosin. J Biol Chem. 1959;234:2764-9.
6. Niedergerke R. Local muscular shortening by intracellularly applied calcium. J Physiol. 1955;128:12P-3P.
7. Hasselbach W. Relaxing factor and the relaxation of muscle. Prog Biophys Mol Biol. 1964;14:167-222.
8. Endo M, Tanaka M, Ogawa Y. Calcium induced release of calcium from the sarcoplasmic reticulum of skinned skeletal muscle fibres. Nature. 1970;228:34-6.
9. Ebashi S. Calcium ion and contractile proteins. Ann NY Acad Sci USA. 1988;522:51-9.
10. Stephenson D, Lamb G, Stephenson G. Events of the excitation-contraction-relaxation (E-C-R) cycle in fast- and slow-twitch mammalian muscle fibres relevant to muscle fatigue. Acta Physiol Scand. 1998;162:229-45.
11. Fill M, Copello J. Ryanodine receptor calcium release channels. Physiol Rev. 2002;82:893-922.
12. Horowicz P. Influence of ions on the membrane potential of muscle fibres. En: Shanes A, editor. Biophysics of physiological and pharmacological actions. Washington: American Association for the Advancement of Science; 1961. p. 217-34.
13. Hodgkin A, Huxley A. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952;117:500-44.
14. González-Serratos H. Inward spread of activation in vertebrate muscle fibres. J Physiol. 1971;212:777-99.
15. Bezanilla F, Caputo C, González-Serratos H, Venosa R. Sodium dependence of the inward spread of activation in isolated twitch muscle fibres of the frog. J Physiol. 1972;223:507-23.
16. Franzini-Armstrong C, Porter K. Sarcolemmal invaginations constituting the T system in fish muscle fibres. J Cell Biol. 1964;22:675-96.
17. Schneider M, Chandler W. Voltage dependent charge movement in skeletal muscle: a possible step in excitation-contraction coupling. Nature. 1973;242:244-6.
18. Ríos E, Brum G. Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature. 1987;325:717-20.
19. Ríos E, Pizarro G. Voltage sensor of excitation-contraction coupling in skeletal muscle. Physiol Rev. 1991;71:849-908.
20. Bezanilla F. The voltage sensor in voltage-dependent ion channels. Physiol Rev. 2000;80:555-92.
21. Lai F, Erickson H, Rousseau E, Liu Q, Meissner G. Purification and reconstitution of the calcium release channel from skeletal muscle. Nature. 1988; 331:315-9.
22. Takeshima H, Nishimura S, Matsumoto T, Ishida H, Kangawa K, Minamino N, et al. Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor. Nature. 1989;339:439-45.
23. Franzini-Armstrong C, Jorgensen A. Structure and development of e-c coupling units in skeletal muscle. Annu Rev Physiol. 1994;56:509-34.
24. Franzini-Armstrong C. The sarcoplasmic reticulum and the control of muscle contraction. FASEB J. 1999;13(Suppl):S266-S70.
25. Meissner G. Adenine nucleotide stimulation of Ca2+-induced Ca2+ release in sarcoplasmic reticulum. J Biol Chem. 1984;259:2365-74.
26. Coronado R, Morrissette J, Sukhareva, Vaughan D. Structure and function of ryanodine receptors. Am J Physiol. 1994;266:C1485-504.
27. Wei L, Varsányi M, Dulhunty A, Beard N. The conformation of calsequestrin determines its ability to regulate skeletal ryanodine receptors. Biophys J. 2006;91:1288-301.
28. Bleunven C, Treves S, Jinyu X, Leo E, Ronjat M, De Waard M, et al. SRP-27 is a novel component of the supramolecular signaling complex involved in skeletal muscle excitation-contraction coupling. Biochem J. 2008;411:343-49.
29. Prosser B, Wright N, Hernández-Ochoa E, Varney K, Liu Y, Olojo R, et al. S100A1 binds to the calmodulin binding site of ryanodine receptor and modulates skeletal muscle coupling. J Biol Chem. 2008;283:5046-57.
30. Fabiato A. Dependence of the Ca2+-induced release from the sarcoplasmic reticulum of skinned skeletal muscle fibres from the frog semitendinosus on the rate of change of free Ca2+ concentration at the outer surface of the sarcoplasmic reticulum. J Physiol. 1984;353-6P.
31. Baylor S, Hollingwoth S. Sarcoplasmic reticulum calcium release compared in slow-twitch and fast-twitch fibres of mouse muscle. J Physiol. 2003;551:125-38.
32. Caputo C, Bolaños P, González A. Inactivation of Ca2+ transients in amphibian and mammalian muscle fibres. J Muscle Res Cell Motil. 2004;25:315-28.
33. Miledi R, Parker I, Schalow G. Calcium transients in frog slow muscle fibres. Nature. 1977;268:750-2.
34. Klein M, Simon B, Szucs G, Schneider M. Simultaneous recording of calcium transients in skeletal muscle using high and low-affinity calcium indicators. Biophys J. 1988;53:971-88.
35. Delbono O, Stefani E. Calcium transients in single mammalian skeletal muscle fibres. J Physiol. 1993; 463: 689-707.
36. Shirokova N, García J, Pizarro G, Rios E. Ca2+ release from the sarcoplasmic reticulum compared in amphibian and mammalian skeletal muscle. J Gen Physiol. 1996;107:1-18.
37. Ebashi S. Regulatory mechanism of muscle contraction with special reference to the Ca-troponin-tropomyosin system. Essays Biochem. 1974;10:1-36.
38. Berchtold M, Brinkmeier H, Müntener M. Calcium ion in skeletal muscle: its crucial role for muscle function, plasticity, and disease. Physiol Rev. 2000;80:1215-65.
39. Hasselbach W, Suko J, Stromer M, The R. Mechanism of calcium transport in sarcoplasmic reticulum. Ann NY Acad Sci. 1975;264:335-49.
40. Jorgensen A, Jones L. Localization of phospholamban in slow but not fast canine skeletal muscle fibers. J Biol Chem. 1986;261:3775-81.
41. Hasselbach W. The Ca2+-ATPase of the sarcoplasmic reticulum in skeletal and cardiac muscle. Ann NY Acad Sci. 1998;853:1-8.
42. Odermatt A, Becker S, Khanna V, Kurzydlowski K, Leisner E, Pette D, et al. Sarcolipin regulates the activity of SERCA1, the fast-twitch skeletal muscle sarcplasmic reticulum Ca2+-ATPase. J Biol Chem. 1998;273:12360-9.
43. Martonosi A, Pikula S. The structure of the Ca2+-ATPase of sarcoplasmic reticulum. Acta Biochim Pol. 2003;50:337-65.
44. Periasamy M, Kalyanasundaram A. Serca pump isoforms: their role in calcium transport and disease. Muscle Nerve. 2007;35:430-42.
45. Toyoshima H, Mizutani T. Crystal structure of the calcium pump with a bound ATP analogue. Nature. 2004;430:529-35.
46. MacLennan D, Brandl C, Korczak B, Green N. Amino-acid sequence of a Ca2++Mg2+-dependent ATPase from rabbit muscle sarcoplasmic reticulum, deduced from its complementary DNA sequence. Nature. 1985;316:696-700.
47. Dulhunty A. Excitation-contraction coupling from the 1950s into the new millennium. Clin Exp Pharmacol Physiol. 2006;33:763-72.
48. Bekoff A, Betz W. Physiological properties of dissociated muscle fibres obtained from innervated and denervated adult rat muscle. J Physiol. 1977;271:25-40.
49. Lännergren J, Westerblad H. The temperature dependence of isometric contractions of single, intact fibres dissected from a mouse foot muscle. J Physiol. 1987;390:285-93.
50. Wood DS, Zollman J, Reuben JP. Human skeletal muscle properties of the “chemically skinned” fiber. Science. 1975;187:1075-6.
51. Lamb G, Junankar P, Stephenson D. Raised intracellular Ca2+ abolishes excitation-contraction coupling in skeletal muscle fibres of rat and toad. J Physiol. 1995;489:349-62.
52. Lamb G. Excitation-contraction coupling and fatigue mechanisms in skeletal muscle: studies with mecanically skinned fibres. J Muscle Res Cell Motil. 2002;23:81-91.
53. Yaffe D, Saxel O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature. 1977;270:725-7.
54. Rando TA, Blau HM. Primary mouse myoblast purification, characterization and transplantation for cell-mediated gene therapy. J Cell Biol. 1994;125:1275-87.
55. Ridgway E, Ashley C. Calcium transients in single muscle fibres. Biochem Biophys Res Commun. 1967;29:229-34.
56. Grynkiewicz G, Poenie M, Tsien R. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985;260:3440-50.
57. Minta A, Kao J, Tsien R. Fluorescent indicators for cytosolic calcium based on rhodamine and fluorescein chromophores. J Biol Chem. 1989;264:8171-8.
58. Takahashi A, Camacho P, Lechleiter J, Herman B. Measurement of intracellular calcium. Physiol Rev. 1999;79:1089-125.
59. Katerinopoulos H, Foukaraki E. Polycarboxylate fluorescent indicators as ion concentration probes in biological systems. Current Med Chem. 2002;9:275-306.
60. Tsien R. A non-disruptive technique for loading calcium buffers and indicators into cells. Nature. 1981;290:527-8.
61. Pouvreau S, Collet C, Allard B, Jacquemond V. Whole-cell voltage clamp on skeletal muscle fibers with silicone-clamp technique. Meth Mol Biol. 2007;403:185-94.
62. Beam K, Franzini-Armstong C. Functional and structural approaches to the study of excitation-contraction coupling. Methods Cell Biol. 1997;52:283-306.
63. Bolaños P, Guillén A, Rojas H, Boncompagni S, Caputo C. The use of CalciumOrange-5N as a specific marker of mitochondrial Ca2+ in mouse skeletal muscle fibers. Pflugers Arch-Eur J Physiol. 2008;455:721-31.
64. Cheng H, Lederer W, Cannell M. Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science. 1993;262:740-4.
65. Klein M, Schneider M. Ca2+ sparks in skeletal muscle. Prog Biophys Mol Biol. 2006;92:308-32.
66. Papadopoulus S, Leuranguer V, Bannister R, Beam K. Mapping sites of potential proximity between the DHPR and RyR1 in muscle using a cyan fluorescent protein-yellow fluorescent protein tandem as a fluorescent resonance energy transfer probe. J Biol Chem. 2004;279:44046-56.
67. Launikonis BS, Zhou J, Royer L, Shannon T, Brum G, Rios E. Confocal imaging of [Ca2+] in cellular organelles by SEER, shifted excitation and emission ratioing of fluorescence. J Physiol. 2005;567:523-43.
68. Serysheva I, Chiu W, Ludtke S. Single-particle electron cryomicroscopy of the ion channels in the excitation-contraction coupling junction. Methods Cell Biol. 2007;79:407-35.
69. Anderson A, Altafaj X, Zheng Z, Wang Z, Delbono O, Ronjat M, et al. The junctional SR protein JP-45 affects the functional expression of the voltage-dependent Ca2+ channel Cav1.1. J Cell Sci. 2006;119:2145-55.
70. DiFranco M, Neco P, Capote J, Meera P, Vergara J. Quantitative evaluation of mammalian skeletal muscle as a heterologous protein expression system. Protein Expr Purif. 2006;47:281-8.
71. Flucher B, Franzini-Armstrong C. Formation of junctions involved in excitation-contraction coupling in skeletal and cardiac muscle. Proc Natl Acad Sci USA. 1996;93:8101-6.
72. Ríos E, Karhanek M, Ma J, González A. An Allosteric model of the molecular interactions of excitation-contraction coupling in skeletal muscle. J Gen Physiol. 1993;102:449-81.
73. Wagenknecht T, Grassucci R, Frank J, Saito A, Inui M, Fleischer S. Three-dimensional architecture of the calcium channel/foot structure of sarcoplasmic reticulum. Nature. 1989;338:167-70.
74. Ávila G, Dirksen R. Functional impact of the ryanodine receptor on the skeletal muscle L-type Ca2+ channel. J Gen Physiol. 2000;114: 467-80.
75. Wagenknecht T, Hsieh C-E, Rath B, Fleischer S, Marko M. Electron tomography of frozen-hydrated isolated triad junctions. Biophys J. 2002;83:2491-501.
76. Paolini C, Fessenden J, Pessah I, Franzini-Armstrong C. Evidence for conformational coupling between two calcium channels. Proc Natl Acad Sci USA. 2004;101:12748-52.
77. Tanabe T, Beam K, Adams B, Niidome T, Numa S. Regions of the skeletal dihydropyridine receptor critical for excitation-contraction coupling. Nature. 1990;346:567-9.
78. Leong P, MacLennan D. A 37-amino acid sequence in the skeletal muscle ryanodine receptor interacts with the cytoplasmic loop between domains II and III in the skeletal muscle dihydropyridine receptor. J Biol Chem. 1998;273:7791-4.
79. Casarotto M, Cui Y, Karunasekara Y, Harvey P, Norris N, Borrad P, et al. Structural and functional characterization of interactions between the dihydropyridine receptor II-III loop and the ryanodine receptor. Clin Exp Pharmacol Physiol. 2006;33:1114-7.
80. Protasi F, Paolini C, Nakai J, Beam K, Franzini-Armstrong C, Allen P. Multiple regions of RyR1 mediate functional and structural interactions with α1s-dihidropyridine receptors in skeletal muscle. Biophy J. 2002;83:3220-44.
81. Ludtke S, Serysheva I, Hamilton S, Chiu W. The pore structure of the closed RyR1 channel. Structure. 2005;13:1203-11.
82. Samsó M, Wagenknecht T, Allen D. Internal structure and visualization of transmembrane domains of the RyR1 calcium release channel by cryo-EM. Nat Struct Mol Biol. 2005;12:539-44.
83. Doyle D, Morais Cabral J, Pfuetzner R, Kuo A, Gulbis J, Cohen S, et al. The structure of potassium channel: molecular basis of K+ conduction and selectivity. Science. 1998;280:69-77.
84. Jiang Y, Lee A, Chen J, Cadene M, Chalt B, MacKinnon R. The open pore conformation of potassium channels. Nature. 2002;417:523-6.
85. Zorzato F, Fujii J, Otsu M, Phillips M, Green N, Lai F, et al. Molecular cloning of cDNA encoding human and rabbit forms of the Ca2+ release channel (ryanodine receptor) of skeletal muscle sarcoplasmic reticulum. J Biol Chem. 1990;265: 2244-56.
86. Fitts R. Cellular mechanisms of muscle fatigue. Physiol Rev. 1994;74:49-94.
87. Enoka R, Duchateau J. Muscle fatigue: what, why and how it influences muscle function. J Physiol. 2008;586:11-23.
88. Allen D, Lamb G, Westerblad. Skeletal muscle fatigue: cellular mechanisms. Physiol Rev. 2008;88:287-332.
89. Bigland-Ritchie B, Woods J. Changes in muscle contractile properties and neural control during human muscular fatigue. Muscle Nerve. 1984;7:691-9.
90. Abbiss C, Laursen P. Models to explain fatigue during prolonged endurance cycling. Sports Med. 2005;35:865-98.
91. Kent-Braun J. Central and peripheral contributions to muscle fatigue in humans during sustained maximal effort. Eur J Appl Physiol. 1999;80:57-63.
92. Luttgau H. The effect of metabolic inhibitors on the fatigue of the action potential in single muscle fibres. J Physiol. 1965;178:45-67.
93. Grabowski W, Lobsiger E, Luttgau H. The effect of repetitive stimulation at low frequencies upon the electrical and mechanical activity of single muscle fibres. Pflugers Arch. 1972;334:222-39.
94. Moussavi R, Carson P, Boska M, Weiner M, Miller R. Nonmetabolic fatigue in exercising human muscle. Neurology. 1989;39:1222-26.
95. Nassar-Gentina V, Passonneau J, Vergara J, Rapoport S. Metabolic correlates of fatigue and recovery from fatigue in single frog muscle fibers. J Gen Physiol. 1978;72:593-606.
96. Westerblad H, Allen D. Changes of myoplasmic calcium concentration during fatigue in single mouse muscle fibers. J Gen Physiol. 1991;98:615-35.
97. Green H. Cation pumps in skeletal muscle: potential role in muscle fatigue. Acta Physiol Scand. 1998;162:201-13.
98. Hill A, Kupalov P. Anaerobic and aerobic activity in isolated muscle. Proc R Soc London B. 1929;105:313-22.
99. Westerblad H. The role of pH and inorganic phosphate ions in skeletal muscle fatigue. Chapter 12. En: Hargreaves M, Thompson M, editors. Biochemistry of exercise X. Champaign: Human Kinetics; 1999. p. 147-54.
100. Westerblad H, Allen D, Lännergren J. Muscle fatigue: lactic acid or inorganic phosphate the major cause? News Physiol Sci. 2002;17:17-21.
101. Lamb G, Stephenson D. Lactic acid accumulation is an advantage during muscle activity. J Appl Physiol. 2006;100:1410-2.
102. Bangsbo J, Juel C. Lactic acid accumulation is a disadvantage during muscle activity. J Appl Physiol. 2006;100:1412-3.
103. McCully K, Clark B, Kent J, Wilson J, Chance B. Biochemical adaptations to training: implications for resisting muscle fatigue. Can J Physiol Pharmacol. 1991;69:274-8.
104. Lindinger M, Heigenhauser G. The roles of ion fluxes in skeletal muscle fatigue. Can J Physiol Pharmacol. 1991;69:246-53.
105. Kent-Braun J, Miller R, Weiner M. Phases of metabolism during progressive exercise to fatigue in human skeletal muscle. J Appl Physiol. 1993;75:573-80.
106. Knuth S, Dave H, Peters J, Fitts R. Low cell pH depresses peak power in rat skeletal muscle fibres at both 30°C and 15°C: implications for muscle fatigue. J Physiol. 2006;575:887-99.
107. Rousseau E, Pinkos J. pH modulates conducting and gating behaviour of single calcium release channels. Pflugers Arch-Eur J Physiol. 1990;415:645-7.
108. Caputo C, Edman K, Lou F, Sun Y. Variation in myoplasmic Ca concentration during contraction and relaxation studied by the indicator fluo-3 in frog muscle fibres. J Physiol. 1994;478:137-48.
109. Verburg E, Murphy R, Stephenson G, Lamb G. Disruption of excitation-contraction coupling and titin by endogenous Ca2+-activated proteases in toad muscle fibres. J Physiol. 2005;564:775-89.
110. Gollnick P, Korge P, Karpakka J, Saltin B. Elongation of skeletal muscle relaxation during exercise is linked to reduced calcium uptake by the sarcoplasmic reticulum in man. Acta Physiol Scand. 1991;142:135-6.
111. Leppik J, Aughey R, Medved I, Fairweather I, Carey M, McKenna M. Prolongued exercise to fatigue in humans impairs skeletal muscle Na-K ATPase activity, sarcoplasmic reticulum Ca release and Ca uptake. J Appl Physiol. 2004;97:1414-23.
112. Verburg E, Dutka T, Lamb G. Long-lasting muscle fatigue: partial disruption of excitation-contraction coupling by elevated cytosolic Ca2+ concentration during contractions. Am J Physiol. 2006;290:C1199-C208.
113. Westerblad H, Allen D. Myoplasmic free Mg2+ concentration during repetitive stimulation of single fibres from mouse skeletal muscle. J Physiol. 1992;453:413-34.
114. Lamb G, Stephenson D. Effects of intracellular pH and [Mg2+] on excitation-contraction coupling in skeletal muscle fibres of the rat. J Physiol. 1994; 478:331-9.
115. Fryer M, Owen V, Lamb G, Stephenson G. Effects of creatine phosphate and Pi on Ca movements and tension development in rat skinned skeletal muscle fibres. J Physiol. 1995;482:123-40.
116. Dutka T, Cole L, Lamb G. Calcium phosphate precipitation in the sarcoplasmic reticulum reduces action potential-mediated Ca2+ release in mammalian skeletal muscle. Am J Physiol. 2005;289:C1502-C12.
117. Barclay J, Hansel M. Free radicals may contribute to oxidative skeletal muscle fatigue. Can J Physiol Pharmacol. 1991;69:279-84.
118. Sen C. Oxidants and antioxidants in exercise. J Appl Physiol. 1995;79:675-86.
119. Reid M. Plasticity in skeletal, cardiac, and smooth muscle. Invited review: Redox modulation of skeletal muscle contraction: what we know and what we don’t. J Appl Physiol. 2001;90:724-31.
120. Darnley G, Duke A, Steele D, MacFarlane N. Effects of reactive oxygen species on aspects of excitation-contraction coupling in chemically skinned rabbit diaphragm muscle fibres. Exp Physiol. 2001;86:161-8.
121. Davies K, Quintanilha A, Brooks G, Packer L. Free radicals and tissue damage produced by exercise. Biochem Biophys Res Commun. 1982;107:1198-205.
122. M, Haack K, Kathleen F, Valberg P, Kobzik L, West S. Reactive oxygen in skeletal muscle. I. Intracellular oxidant kinetics and fatigue in vitro. J Appl Physiol. 1992;73:1797-804.
123. Kanter M, Nolte L, Holloszy J. Effects of an antioxidant vitamin mixture on lipid peroxidation at rest and postexercise. J Appl Physiol. 1993;74:965-9.
124. Jackson M, Pye D, Palomero J. The production of reactive oxygen species by skeletal muscle. J Appl Physiol. 2007;102:1664-70.
125. Brotto M, Nosek T. Hydrogen peroxide disrupts Ca2+ release from the sarcoplasmic reticulum of rat skeletal muscle fibers. J Appl Physiol. 1996;81:731-7.
126. Oba T, Kurono C, Nakajima R, Takaishi T, Ishida K, Fuller G, et al. H2O2 activates ryanodine receptor but has little effect on recovery of release Ca2+ content after fatigue. J Appl Physiol. 2002;93:1999-2008.
127. Hidalgo C. Cross talk between Ca2+ and redox signaling cascades in muscle and neurons through the combined activation of ryanodine receptors/Ca2+ release channels. Phil Trans R Soc B. 2005;360:2237-46.
128. Moopanar T, Allen D. Reactive oxygen species reduce myofibrillar Ca2+ sensitivity in fatiguing mouse skeletal muscle at 37°C. J Physiol. 2005;564:189-99.
129. Moopanar T, Allen D. The activity-induced reduction of myofibrillar Ca2+ sensitivity in Mouse skeletal muscle is reversed by dithiothreitol. J Physiol. 2006;571:191-200.
130. Posterino G, Lamb G. Effects of reducing agents and oxidants on excitation-contraction coupling in skeletal muscle fibres of rat and toad. J Physiol. 1996;496:809-25.
131. Andrade F, Reid M, Allen D, Westerblad H. Effects of hydrogen peroxide and dithiotreitol on contractile function of single skeletal muscle fibres from the mouse. J Physiol. 1998;509:565-75.
132. Andrade F, Reid M, Allen D, Westerblad H. Effect of nitric oxide on single skeletal muscle fibres from the mouse. J Physiol. 1998;509:577-86.
133. Andrade F, Reid M, Westerblad H. Contractile response of skeletal muscle to low peroxide concentrations: myofibrillar calcium sensitivity as a likely target for redox-modulation. FASEB J. 2001;15:309-11.
134. Ward K, Wareham A. Changes in membrane potential and potassium and sodium activities during postnatal development of mouse skeletal muscle. Exp Neurol. 1985;89:554-8.
135. Brown M, Jansen J, Van Essen D. Polyneural innervation of skeletal muscle in newborn rats and its elimination during maturation. J Physiol. 1976;261:387-422.
136. Kjeldsen K, Norgaard A, Clausen T. Age dependent changes in the number of [H3] ouabain binding sites in rat soleus muscle. Biochem Biophys Acta. 1982;686:253-356.
137. Harris J, Marshall M. Tetrodotoxin-resistant action potentials in newborn rat muscle. Nature New Biol. 1973;243:191-2.
138. Capote J, Bolanos P, Schuhmeier R, Melzer W, Caputo C. Calcium transients in developing mouse skeletal muscle fibres. J Physiol. 2005;564:451-64.
139. Kano M, Yamamoto M. Development of spike potentials in skeletal muscle cells differentiated in vitro from chick embryo. J Cell Physiol. 1977;90:439-44.
140. Franzini-Armstrong C. Simultaneous maturation of transverse tubules and sarcoplasmic reticulum during muscle differentiation in the mouse. Dev Biol. 1991;146:353-63.
141. Bertocchini F, Ovitt C, Conti A, Barone V, Schöler H, Bottinelli R, et al. Requirement for the ryanodine receptor type 3 for efficient contraction in neonatal skeletal muscles. EMBO J. 1997;16:6956-63.
142. Chaudhari N, Beam K. mRNA for cardiac calcium channels is expressed during development of skeletal muscle. Dev Biol. 1993;155:507-15.
143. Cognard C, Lazdunski M, Romey G. Different types of Ca2+ channels in mammalian skeletal muscle cells in culture. Proc Natl Acad Sci USA. 1986;83:517-21.
144. Beam K, Knudson C. Calcium currents in embryonic and neonatal mammalian skeletal muscle. J Gen Physiol. 1988;91:781-98.
145. Beam K, Knudson C. Effect of postnatal development on calcium currents and slow charge movement in mammalian skeletal muscle. J Gen Physiol. 1988;91:799-815.
146. Romey G, Garcia L, Dimitriadou V, Pincon-Raymond M, Rieger F, Lazdunski M. Ontogenesis and localization of Ca2+ channels in mammalian skeletal muscle in culture and role in excitation-contraction coupling. Proc Natl Acad Sci USA. 1989;86:2933-7.
147. Dangain J, Neering I. Effect of caffeine and high potassium on normal and dystrophic mouse EDL muscles at various developmental stages. Muscle Nerve. 1992;16:33-42.
148. Ma J, Pan Z. Retrograde activation of store-operated calcium channel. Cell Calcium. 2003;33:375-84.
149. Whalen R, Sell S, Butler-Browne G, Schwartz K, Bouveret P, Pinset-Harstom I. Three myosin heavy-chain isozymes appear sequentially in rat muscle development. Nature. 1981;292:805-9.
150. Dhoot G, Perry S. The components of the troponin complex and development in skeletal muscle. Exp Cell Res. 1980;127:75-87.
151. Roy R, Sreter F, Sarkar S. Changes in tropomyosin subunits and myosin light chains during development of chicken and rabbit striated muscles. Dev Biol. 1979;69:15-30.
152. Berchtold M, Means A. The Ca2+-binding protein parvalbumin: molecular cloning and developmental regulation of mRNA abundance. Proc Natl Acad Sci USA. 1985;82:1414-8.
153. Figueroa LC, Bolaños P, Guillen A, Caputo C. Efecto del calcio extracelular sobre transitorios de Ca2+ de fibras musculares esqueléticas y miotubos durante el desarrollo. Acta Científica Venezolana. 2006;57:19.
154. Sandow A, Taylor S, Preiser H. Role of the action potential in excitation-contraction coupling. Fed Proc. 1965;24:1116-23.
155. Marx S, Reiken S, Hisamatsu Y, Jayaraman T, Burkhoff D, Rosemblit N, et al. PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell. 2000;101:365-76.
156. Stange M, Xu L, Balshaw D, Yamaguchi N, Meissner G. Characterization of recombinant skeletal muscle (Ser-2843) and cardiac muscle (Ser-2809) ryanodine receptor phosphorylation mutants. J Biol Chem. 2003;278:51693-702.
157. Dipolo R, Beaugé L. Sodium/calcium exchanger: influence of metabolic regulation on ion carrier interaction. Physiol Rev. 2006;86:155-203.
158. Bruton J, Tavi P, Aydin J, Wasterblad H, Lanergren J. Mitochondrial and myoplasmic [Ca2+] in single fibers from Mouse limb muscles during repeated tetanic contraction. J Physiol. 2003;551:179-90.
159. Caputo C, Bolaños P. Effect of mitochondria poisoning by FCCP on Ca2+ signaling in muse skeletal muscle fibers. Pflugers Arch-Eur J Physiol. 2008;455:733-43.
160. Caputo C, Bolaños P. Effect of external sodium and calcium on calcium efflux in frog striated muscle. J Membr Biol. 1978;41:1-14.
161. Balnave Ch, Allen D. Evidence for Na+/Ca2+ Exchange in intact single skeletal muscle fibers from the mouse. Am J Physiol Cell Physiol. 1998;274:940-6.
162. Cifuentes F, Vergara J, Hidalgo C. Sodium/calcium Exchange in amphibian skeletal muscle fibers and isolated transverse tubules. Am J Physiol Cell Physiol. 2000;279:C89-97.
Cómo citar
1.
Calderón-Vélez JC, Figueroa-Gordon LC. El acoplamiento excitación-contracción en el músculo esquelético: preguntas por responder a pesar de 50 años de estudio. biomedica [Internet]. 1 [citado 8 de diciembre de 2021];29(1):140-6. Disponible en: https://revistabiomedica.org/index.php/biomedica/article/view/50

Más sobre este tema

Sección
Revisión de tema