The Na conductance in the sarcolemma and the transverse tubular system membranes of mammalian skeletal muscle fibers

Journal of General Physiology

Volumn 138, Issue 4, 2011, Pages 393-419

  DiFranco, Marino ^a   Vergara, Julio L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 (3 SULFONATOPROPYL) 4 (BETA (2 (DI N OCTYLAMINO) 6 NAPHTHYL)VINYL)PYRIDINIUM BETAINE; 1-(3-SULFONATOPROPYL)-4-(BETA-(2-(DI-N-OCTYLAMINO)-6-NAPHTHYL)VINYL)PYRIDINIUM BETAINE; FLUORESCENT DYE; LITHIUM; PYRIDINIUM DERIVATIVE; SODIUM; SODIUM CHANNEL;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; CELL MEMBRANE POTENTIAL; CHANNEL GATING; ELECTROPHYSIOLOGY; INTRACELLULAR MEMBRANE; METABOLISM; MOUSE; PHYSIOLOGY; SARCOLEMMA; SKELETAL MUSCLE;

ANIMALS; ELECTROPHYSIOLOGICAL PROCESSES; FLUORESCENT DYES; INTRACELLULAR MEMBRANES; ION CHANNEL GATING; LITHIUM; MEMBRANE POTENTIALS; MICE; MODELS, BIOLOGICAL; MUSCLE FIBERS, SKELETAL; PYRIDINIUM COMPOUNDS; SARCOLEMMA; SODIUM; SODIUM CHANNELS;

EID: 80054082682     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201110682     Document Type: Article

References (50)

1. Adrian, R.H., and L.D. Peachey. 1973. Reconstruction of the action potential of frog sartorius muscle. J. Physiol. 235:103-131.
2. Adrian, R.H., W.K. Chandler, and A.L. Hodgkin. 1969. The kinetics of mechanical activation in frog muscle. J. Physiol. 204: 207-230.
3. Ashcroft, F.M., J.A. Heiny, and J. Vergara. 1985. Inward rectification in the transverse tubular system of frog skeletal muscle studied with potentiometric dyes. J. Physiol. 359:269-291.
4. Barry, P.H., and R.H. Adrian. 1973. Slow conductance changes due to potassium depletion in the transverse tubules of frog muscle fibers during hyperpolarizing pulses. J. Membr. Biol. 14:243-292. http://dx.doi.org/10.1007/BF01868081
5. Bedlack, R.S., Jr., M. Wei, and L.M. Loew. 1992. Localized membrane depolarizations and localized calcium influx during electric fieldguided neurite growth. Neuron. 9:393-403. http://dx.doi.org/10 .1016/0896-6273(92)90178-G
6. Bezanilla, F., J. Vergara, and R.E. Taylor. 1982. Voltage clamping of excitable membranes. In Methods of Experimental Physics. Volume 20. G. Ehrenstein and H. Lecar, editors. Academic Press, New York. 445-511.
7. Campbell, D.T. 1976. Ionic selectivity of the sodium channel of frog skeletal muscle. J. Gen. Physiol. 67:295-307. http://dx.doi.org/10.1085/jgp.67.3.295
8. Cannon, S.C. 2006. Pathomechanisms in channelopathies of skeletal muscle and brain. Annu. Rev. Neurosci. 29:387-415. http://dx.doi.org/10.1146/annurev.neuro.29.051605.112815
9. Capote, J.C., M. DiFranco, and J.L. Vergara. 2011. Differential recording of voltage changes at the surface and transverse tubular system membranes of mammalian skeletal muscle fibers using di-8-ANEPPS and global and TIRFM. Biophys. J. 100:590a. http:// dx.doi.org/10.1016/j.bpj.2010.12.3404
10. Crank, J. 1975. The Mathematics of Diffusion. Oxford University Press, Oxford. 414 pp.
11. del Castillo, J., and G. Escalona de Motta. 1978. A new method for excitation-contraction uncoupling in frog skeletal muscle. J. Cell Biol. 78:782-784. http://dx.doi.org/10.1083/jcb.78.3.782
12. DiFranco, M., D. Novo, and J.L. Vergara. 2002. Characterization of the calcium release domains during excitation-contraction coupling in skeletal muscle fibres. Pflugers Arch. 443:508-519. http:// dx.doi.org/10.1007/s004240100719
13. DiFranco, M., J. Capote, and J.L. Vergara. 2005. Optical imaging and functional characterization of the transverse tubular system of mammalian muscle fibers using the potentiometric indicator di-8-ANEPPS. J. Membr. Biol. 208:141-153. http://dx.doi.org/10.1007/ s00232-005-0825-9
14. DiFranco, M., J. Capote, M. Quiñonez, and J.L. Vergara. 2007. Voltage-dependent dynamic FRET signals from the transverse tubules in mammalian skeletal muscle fibers. J. Gen. Physiol. 130: 581-600. http://dx.doi.org/10.1085/jgp.200709831
15. DiFranco, M., M. Quinonez, J. Capote, and J. Vergara. 2009. DNA transfection of mammalian skeletal muscles using in vivo electroporation. J. Vis. Exp. 32:1520.
16. DiFranco, M., A. Herrera, and J.L. Vergara. 2011a. Chloride currents from the transverse tubular system in adult mammalian skeletal muscle fibers. J. Gen. Physiol. 137:21-41. http://dx.doi.org/10.1085/jgp.201010496
17. DiFranco, M., P. Tran, M. Quiñonez, and J.L. Vergara. 2011b. Functional expression of transgenic α1sDHPR channels in adult mammalian skeletal muscle fibres. J. Physiol. 589:1421-1442. http://dx.doi.org/10.1113/jphysiol.2010.202804
18. Escobar, A.L., J.R. Monck, J.M. Fernandez, and J.L. Vergara. 1994. Localization of the site of Ca2+ release at the level of a single sarcomere in skeletal muscle fibres. Nature. 367:739-741. http:// dx.doi.org/10.1038/367739a0
19. Falk, G. 1968. Predicted delays in the activation of the contractile system. Biophys. J. 8:608-625. http://dx.doi.org/10.1016/S0006-3495(68)86511-7
20. Falk, G., and P. Fatt. 1964. Linear electrical properties of striated muscle fibres observed with intracellular electrodes. Proc. R. Soc. Lond. B Biol. Sci. 160:69-123. http://dx.doi.org/10.1098/rspb.1964.0030
21. Fluhler, E., V.G. Burnham, and L.M. Loew. 1985. Spectra, membrane binding, and potentiometric responses of new charge shift probes. Biochemistry. 24:5749-5755. http://dx.doi.org/10.1021/bi00342a010
22. Franzini-Armstrong, C., R.A. Venosa, and P. Horowicz. 1973. Morphology and accessibility of the 'transverse' tubular system in frog sartorius muscle after glycerol treatment. J. Membr. Biol. 14:197-212. http://dx.doi.org/10.1007/BF01868078
23. Franzini-Armstrong, C., L. Landmesser, and G. Pilar. 1975. Size and shape of transverse tubule openings in frog twitch muscle fibers. J. Cell Biol. 64:493-497. http://dx.doi.org/10.1083/jcb.64.2.493
24. Friedrich, O., T. Ehmer, D. Uttenweiler, M. Vogel, P.H. Barry, and R.H. Fink. 2001. Numerical analysis of Ca2+ depletion in the transverse tubular system of mammalian muscle. Biophys. J. 80:2046-2055. http://dx.doi.org/10.1016/S0006-3495(01)76178-4
25. Fu, Y., A. Struyk, V. Markin, and S. Cannon. 2011. Gating behaviour of sodium currents in adult mouse muscle recorded with an improved two-electrode voltage clamp. J. Physiol. 589:525-546. http://dx.doi.org/10.1113/jphysiol.2010.199430
26. Gerald, C.F. 1978. Applied Numerical Analysis. Addison-Wesley Publishing Company, Boston. 518 pp.
27. Heiny, J.A., and J. Vergara. 1982. Optical signals from surface and T system membranes in skeletal muscle fibers. Experiments with the potentiometric dye NK2367. J. Gen. Physiol. 80:203-230. http:// dx.doi.org/10.1085/jgp.80.2.203
28. Heiny, J.A., F.M. Ashcroft, and J. Vergara. 1983. T-system optical signals associated with inward rectification in skeletal muscle. Nature. 301:164-166. http://dx.doi.org/10.1038/301164a0
29. Hille, B. 1972. The permeability of the sodium channel to metal cations in myelinated nerve. J. Gen. Physiol. 59:637-658. http:// dx.doi.org/10.1085/jgp.59.6.637
30. Hodgkin, A.L., and A.F. Huxley. 1952a. Currents carried by sodium and potassium ions through the membrane of the giant axon of Loligo. J. Physiol. 116:449-472.
31. Hodgkin, A.L., and A.F. Huxley. 1952b. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117:500-544.
32. Huxley, A.F., and R.E. Taylor. 1958. Local activation of striated muscle fibres. J. Physiol. 144:426-441.
33. Jong, D.S., K. Stroffekova, and J.A. Heiny. 1997. A surface potential change in the membranes of frog skeletal muscle is associated with excitation-contraction coupling. J. Physiol. 499:787-808.
34. Kim, A.M., and J.L. Vergara. 1998. Supercharging accelerates T-tubule membrane potential changes in voltage clamped frog skeletal muscle fibers. Biophys. J. 75:2098-2116. http://dx.doi .org/10.1016/S0006-3495(98)77652-0
35. Lueck, J.D., A.E. Rossi, C.A. Thornton, K.P. Campbell, and R.T. Dirksen. 2010. Sarcolemmal-restricted localization of functional ClC-1 channels in mouse skeletal muscle. J. Gen. Physiol. 136:597-613. http://dx.doi.org/10.1085/jgp.201010526
36. Obaid, A.L., T. Koyano, J. Lindstrom, T. Sakai, and B.M. Salzberg. 1999. Spatiotemporal patterns of activity in an intact mammalian network with single-cell resolution: optical studies of nicotinic activity in an enteric plexus. J. Neurosci. 19:3073-3093.
37. Peachey, L.D. 1965. Transverse tubules in excitation-contraction coupling. Fed. Proc. 24:1124-1134.
38. Rohr, S., and B.M. Salzberg. 1994. Multiple site optical recording of transmembrane voltage (MSORTV) in patterned growth heart cell cultures: assessing electrical behavior, with microsecondresolution, on a cellular and subcellular scale. Biophys. J. 67:1301-1315. http://dx.doi.org/10.1016/S0006-3495(94)80602-2
39. Ross, W.N., B.M. Salzberg, L.B. Cohen, A. Grinvald, H.V. Davila, A.S. Waggoner, and C.H. Wang. 1977. Changes in absorption, fluorescence, dichroism, and birefringence in stained giant axons: optical measurement of membrane potential. J. Membr. Biol. 33:141-183. http://dx.doi.org/10.1007/BF01869514
40. Salzberg, B.M., H.V. Davila, and L.B. Cohen. 1973. Optical recording of impulses in individual neurones of an invertebrate central nervous system. Nature. 246:508-509. http://dx.doi.org/10.1038/246508a0
41. Schneider, M.F. 1970. Linear electrical properties of the transverse tubules and surface membrane of skeletal muscle fibers. J. Gen. Physiol. 56:640-671. http://dx.doi.org/10.1085/jgp.56.5.640
42. Takahashi, M.P., and S.C. Cannon. 2001. Mexiletine block of disease-associated mutations in S6 segments of the human skeletal muscle Na(+) channel. J. Physiol. 537:701-714. http://dx.doi .org/10.1113/jphysiol.2001.012541
43. Tsau, Y., P. Wenner, M.J. O'Donovan, L.B. Cohen, L.M. Loew, and J.P. Wuskell. 1996. Dye screening and signal-to-noise ratio for retrogradely transported voltage-sensitive dyes. J. Neurosci. Methods. 70:121-129. http://dx.doi.org/10.1016/S0165-0270(96)00109-4
44. Vergara, J., and F. Bezanilla. 1976. Fluorescence changes during electrical activity in frog muscle stained with merocyanine. Nature. 259:684-686. http://dx.doi.org/10.1038/259684a0
45. Vergara, J.L., and F. Bezanilla. 1981. Optical studies of E-C coupling with potentiometric dyes. In The Regulation of Muscle Contraction: Excitation-Contraction Coupling. A.G.M. Brazier, editor. Academic Press, New York. 66-77.
46. Vergara, J., F. Bezanilla, and B.M. Salzberg. 1978. Nile blue fluorescence signals from cut single muscle fibers under voltage or current clamp conditions. J. Gen. Physiol. 72:775-800.
47. Vergara, J.L., M. Delay, J.A. Heiny, and B. Ribalet. 1983. Optical studies of T-system potential and calcium release in skeletal muscle fibers. In The Physiology of Excitable Cells. A.D. Moody, editor. Alan R. Liss, Inc., New York. 343-355.
48. Woods, C.E., D. Novo, M. DiFranco, and J.L. Vergara. 2004. The action potential-evoked sarcoplasmic reticulum calcium release is impaired in mdx mouse muscle fibres. J. Physiol. 557:59-75. http://dx.doi.org/10.1113/jphysiol.2004.061291
49. Wu, F.F., E. Gordon, E.P. Hoffman, and S.C. Cannon. 2005. A C-terminal skeletal muscle sodium channel mutation associated with myotonia disrupts fast inactivation. J. Physiol. 565:371-380. http://dx.doi.org/10.1113/jphysiol.2005.082909
50. Zampighi, G., J. Vergara, and F. Ramón. 1975. On the connection between the transverse tubules and the plasma membrane in frog semitendinosus skeletal muscle. Are caveolae the mouths of the transverse tubule system? J. Cell Biol. 64:734-740. http://dx.doi .org/10.1083/jcb.64.3.734