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. 1998 Oct;75(4):2098–2116. doi: 10.1016/S0006-3495(98)77652-0

Supercharging accelerates T-tubule membrane potential changes in voltage clamped frog skeletal muscle fibers.

A M Kim 1, J L Vergara 1
PMCID: PMC1299882  PMID: 9746552

Abstract

In voltage-clamp studies of single frog skeletal muscle fibers stained with the potentiometric indicator 1-(3-sulfonatopropyl)-4-[beta[2-(di-n-octylamino)-6-naphthyl] vinyl]pyridinium betaine (di-8 ANEPPS), fluorescence transients were recorded in response to both supercharging and step command pulses. Several illumination paradigms were utilized to study global and localized regions of the transverse tubule system (T-system). The rising phases of transients obtained from global illumination regions showed distinct accelerations when supercharging pulses were applied (95% of steady-state fluorescence achieved in 1.5 ms with supercharging pulses versus 14.6 ms with step pulses). When local transients were recorded at the edge of the muscle fiber, their kinetics resembled those of the applied waveform, but a similar relationship was not observed in transients from regions near the edge chosen to minimize the surface membrane contribution. We developed a model of the T-system capable of simulating membrane potential changes as a function of time and distance along the T-system cable and the associated fluorescence changes in regions corresponding to the experimental illumination strategies. A critical parameter was the access resistance term, for which values of 110-150 Omega.cm2 were adequate to fit the data. The results suggest that the primary mechanism through which supercharging pulses boost the kinetics of T-system voltage changes most likely involves their compensating the voltage attenuation across the access resistance at the mouth of the T-tubule.

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Selected References

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  1. Adrian R. H., Chandler W. K., Hodgkin A. L. The kinetics of mechanical activation in frog muscle. J Physiol. 1969 Sep;204(1):207–230. doi: 10.1113/jphysiol.1969.sp008909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adrian R. H., Costantin L. L., Peachey L. D. Radial spread of contraction in frog muscle fibres. J Physiol. 1969 Sep;204(1):231–257. doi: 10.1113/jphysiol.1969.sp008910. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Adrian R. H., Peachey L. D. Reconstruction of the action potential of frog sartorius muscle. J Physiol. 1973 Nov;235(1):103–131. doi: 10.1113/jphysiol.1973.sp010380. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Armstrong C. M., Chow R. H. Supercharging: a method for improving patch-clamp performance. Biophys J. 1987 Jul;52(1):133–136. doi: 10.1016/S0006-3495(87)83198-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ashcroft F. M., Heiny J. A., Vergara J. Inward rectification in the transverse tubular system of frog skeletal muscle studied with potentiometric dyes. J Physiol. 1985 Feb;359:269–291. doi: 10.1113/jphysiol.1985.sp015585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. BLINKS J. R. INFLUENCE OF OSMOTIC STRENGTH ON CROSS-SECTION AND VOLUME OF ISOLATED SINGLE MUSCLE FIBRES. J Physiol. 1965 Mar;177:42–57. doi: 10.1113/jphysiol.1965.sp007574. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bastian J., Nakajima S. Action potential in the transverse tubules and its role in the activation of skeletal muscle. J Gen Physiol. 1974 Feb;63(2):257–278. doi: 10.1085/jgp.63.2.257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bedlack R. S., Jr, Wei M., Loew L. M. Localized membrane depolarizations and localized calcium influx during electric field-guided neurite growth. Neuron. 1992 Sep;9(3):393–403. doi: 10.1016/0896-6273(92)90178-g. [DOI] [PubMed] [Google Scholar]
  9. Bezanilla F., Caputo C., Gonzalez-Serratos H., Venosa R. A. Sodium dependence of the inward spread of activation in isolated twitch muscle fibres of the frog. J Physiol. 1972 Jun;223(2):507–523. doi: 10.1113/jphysiol.1972.sp009860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. FALK G., FATT P. LINEAR ELECTRICAL PROPERTIES OF STRIATED MUSCLE FIBRES OBSERVED WITH INTRACELLULAR ELECTRODES. Proc R Soc Lond B Biol Sci. 1964 Apr 14;160:69–123. doi: 10.1098/rspb.1964.0030. [DOI] [PubMed] [Google Scholar]
  11. Falk G. Predicted delays in the activation of the contractile system. Biophys J. 1968 May;8(5):608–625. doi: 10.1016/S0006-3495(68)86511-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. González-Serratos H. Inward spread of activation in vertebrate muscle fibres. J Physiol. 1971 Feb;212(3):777–799. doi: 10.1113/jphysiol.1971.sp009356. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. HUXLEY A. F., TAYLOR R. E. Local activation of striated muscle fibres. J Physiol. 1958 Dec 30;144(3):426–441. doi: 10.1113/jphysiol.1958.sp006111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Heiny J. A., Ashcroft F. M., Vergara J. T-system optical signals associated with inward rectification in skeletal muscle. Nature. 1983 Jan 13;301(5896):164–166. doi: 10.1038/301164a0. [DOI] [PubMed] [Google Scholar]
  15. Heiny J. A., Jong D. S. A nonlinear electrostatic potential change in the T-system of skeletal muscle detected under passive recording conditions using potentiometric dyes. J Gen Physiol. 1990 Jan;95(1):147–175. doi: 10.1085/jgp.95.1.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Heiny J. A., Vergara J. Dichroic behavior of the absorbance signals from dyes NK2367 and WW375 in skeletal muscle fibers. J Gen Physiol. 1984 Nov;84(5):805–837. doi: 10.1085/jgp.84.5.805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Heiny J. A., Vergara J. Optical signals from surface and T system membranes in skeletal muscle fibers. Experiments with the potentiometric dye NK2367. J Gen Physiol. 1982 Aug;80(2):203–230. doi: 10.1085/jgp.80.2.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hille B., Campbell D. T. An improved vaseline gap voltage clamp for skeletal muscle fibers. J Gen Physiol. 1976 Mar;67(3):265–293. doi: 10.1085/jgp.67.3.265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jong D. S., Stroffekova K., Heiny J. A. A surface potential change in the membranes of frog skeletal muscle is associated with excitation-contraction coupling. J Physiol. 1997 Mar 15;499(Pt 3):787–808. doi: 10.1113/jphysiol.1997.sp021969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kim A. M., Vergara J. L. Fast voltage gating of Ca2+ release in frog skeletal muscle revealed by supercharging pulses. J Physiol. 1998 Sep 1;511(Pt 2):509–518. doi: 10.1111/j.1469-7793.1998.509bh.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nakajima S., Gilai A. Action potentials of isolated single muscle fibers recorded by potential-sensitive dyes. J Gen Physiol. 1980 Dec;76(6):729–750. doi: 10.1085/jgp.76.6.729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Palade P., Vergara J. Arsenazo III and antipyrylazo III calcium transients in single skeletal muscle fibers. J Gen Physiol. 1982 Apr;79(4):679–707. doi: 10.1085/jgp.79.4.679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Peachey L. D. The sarcoplasmic reticulum and transverse tubules of the frog's sartorius. J Cell Biol. 1965 Jun;25(3 Suppl):209–231. doi: 10.1083/jcb.25.3.209. [DOI] [PubMed] [Google Scholar]
  24. Peachey L. D. Transverse tubules in excitation-contraction coupling. Fed Proc. 1965 Sep-Oct;24(5):1124–1134. [PubMed] [Google Scholar]
  25. Rohr S., Salzberg B. M. Multiple site optical recording of transmembrane voltage (MSORTV) in patterned growth heart cell cultures: assessing electrical behavior, with microsecond resolution, on a cellular and subcellular scale. Biophys J. 1994 Sep;67(3):1301–1315. doi: 10.1016/S0006-3495(94)80602-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Salzberg B. M., Bezanilla F. An optical determination of the series resistance in Loligo. J Gen Physiol. 1983 Dec;82(6):807–817. doi: 10.1085/jgp.82.6.807. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Simon B. J., Beam K. G. The influence of transverse tubular delays on the kinetics of charge movement in mammalian skeletal muscle. J Gen Physiol. 1985 Jan;85(1):21–42. doi: 10.1085/jgp.85.1.21. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Valdiosera R., Clausen C., Eisenberg R. S. Impedance of frog skeletal muscle fibers in various solutions. J Gen Physiol. 1974 Apr;63(4):460–491. doi: 10.1085/jgp.63.4.460. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Vergara J., Bezanilla F., Salzberg B. M. Nile blue fluorescence signals from cut single muscle fibers under voltage or current clamp conditions. J Gen Physiol. 1978 Dec;72(6):775–800. doi: 10.1085/jgp.72.6.775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Vergara J., Delay M. A transmission delay and the effect of temperature at the triadic junction of skeletal muscle. Proc R Soc Lond B Biol Sci. 1986 Oct 22;229(1254):97–110. doi: 10.1098/rspb.1986.0077. [DOI] [PubMed] [Google Scholar]
  31. Vergara J., DiFranco M., Compagnon D., Suarez-Isla B. A. Imaging of calcium transients in skeletal muscle fibers. Biophys J. 1991 Jan;59(1):12–24. doi: 10.1016/S0006-3495(91)82193-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Zampighi G., Vergara J., Ramón F. 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. 1975 Mar;64(3):734–740. doi: 10.1083/jcb.64.3.734. [DOI] [PMC free article] [PubMed] [Google Scholar]

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