Abstract
Muscle fibres, isolated from frog tibialis anterior and mouse flexor digitorum brevis (FDB) were loaded with the fast dye MagFluo-4 to study the effects of potentiators caffeine, nitrate, Zn2+ and perchlorate on Ca2+ transients elicited by single action potentials. Overall, the potentiators doubled the transients amplitude and prolonged by about 1.5-fold their decay time. In contrast, as shown here for the first time, nitrate and Zn2+, but not caffeine, activated a late, secondary component of the transient rising phase of frog but not mouse, fibres. The rise time was increased from 1.9 ms in normal solution (NR) to 3.3 ms (nitrate) and 4.4 ms (Zn2+). In NR, a single exponential, fitted the rising phase of calcium transients of frog (τ1 = 0.47 ms) and mouse (τ1 = 0.28 ms). In nitrate and Zn2+ only frog transients showed a secondary exponential component, τ2 = 0.72 ms (nitrate) and 0.94 ms, (Zn2+). We suggest that nitrate and Zn2+ activate a late slower component of the ΔF/F signals of frog but not of mouse fibres, possibly promoting Ca2+ induced Ca2+ release at level of the RyR3, that in frog muscle fibres are localized in the para-junctional region of the triads and are absent in mouse FDB muscle fibres.
Similar content being viewed by others
References
Axelsson J, Thesleff S (1958) Activation of the contractile mechanism in striated muscle. Acta Physiol Scand 44:55–66
Baylor SM, Chandler WK, Marshall MW (1983) Sarcoplasmic reticulum calcium release in frog skeletal muscle fibres estimated from Arsenazo III calcium transients. J Physiol 344:625–666
Bekoff A, Betz WJ (1977) Physiological properties of dissociated muscle fibres obtained from innervated and denervated adult rat muscle. J Physiol 271:25–40
Bertocchini F, Ovitt CE, Conti A, Barone V, Scholer HR, Bottinelli R, Reggiani C, Sorrentino V (1997) Requirement for the ryanodine receptor type 3 for efficient contraction in neonatal skeletal muscles. EMBO J 16:6956–6963
Block BA, Imagawa T, Campbell KP, Franzini-Armstrong C (1988) Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle. J Cell Biol 107:2587–2600
Campbell KP, Knudson CM, Imagawa T, Leung AT, Sutko JL, Kahl SD, Raab CR, Madson L (1987) Identification and characterization of the high affinity [3H]ryanodine receptor of the junctional sarcoplasmic reticulum Ca2+ release channel. J Biol Chem 262:6460–6463
Caputo C, Gottschalk G, Lüttgau HC (1981) The control of contraction activation by the membrane potential. Experientia 37:580–581
Caputo C, Bolaños P, Gonzalez A (2004) Inactivation of Ca2+ transients in amphibian and mammalian muscle fibres. J Muscle Res Cell Motil 25:315–328
Carroll SL, Klein M, Schneider MF (1995) Calcium transients in intact rat skeletal muscle fibers in agarose gel. Am J Physiol 269:C28–C34
Cheung A, Dantzig JA, Hollingworth S, Baylor SM, Goldman YE, Mitchison TJ, Straight AF (2002) A small-molecule inhibitor of skeletal muscle myosin II. Nat Cell Biol 4:83–88
Csernoch L, Szentesi P, Kovacs L (1999) Differential effects of caffeine and perchlorate on excitation-contraction coupling in mammalian skeletal muscle. J Physiol 520(Pt 1):217–230
Delay M, Ribalet B, Vergara J (1986) Caffeine potentiation of calcium release in frog skeletal muscle fibres. J Physiol 375:535–559
Endo M (1975) Mechanism of action of caffeine on the sarcoplasmic reticulum of skeletal muscle. Proc Japan Acad 51:479–484
Endo M (1977) Calcium release from the Sarcoplasmic Reticulum. Physiol Rev 57:71–108
Falk G (1961) Electrical activity of skeletal muscle. Its relation to active state. In: Shanes AM (ed) Biophysics of Physiological and Pharmacological Actions. AAAS, Washington, DC, pp 259–279
Felder E, Franzini-Armstrong C (2002) Type 3 ryanodine receptors of skeletal muscle are segregated in a parajunctional position. Proc Natl Acad Sci USA 99:1695–1700
Fessenden JD, Wang Y, Moore RA, Chen SR, Allen PD, Pessah IN (2000) Divergent functional properties of ryanodine receptor types 1 and 3 expressed in a myogenic cell line. Biophys J 79:2509–2525
Figueroa L, Shkryl VM, Zhou J, Manno C, Momotake A, Brum G, Blatter LA, Ellis-Davies GC, Rios E (2012) Synthetic localized calcium transients directly probe signalling mechanisms in skeletal muscle. J Physiol 590:1389–1411
Franzini-Armstrong C, Nunzi G (1983) Junctional feet and particles in the triads of a fast-twitch muscle fibre. J Muscle Res Cell Motil 4:233–252
Franzini-Armstrong C, Protasi F (1997) Ryanodine receptors of striated muscles: a complex channel capable of multiple interactions. Physiol Rev 77:699–729
Gomolla M, Gottschalk G, Lüttgau HC (1983) Perchlorate-induced alterations in electrical and mechanical parameters of frog skeletal muscle fibres. J Physiol 343:197–214
Gonzalez A, Rios E (1993) Perchlorate enhances transmission in skeletal muscle excitation-contraction coupling. J Gen Physiol 102:373–421
Hodgkin AL, Horowicz P (1960) The effect of nitrate and other anions on the mechanical response of single muscle fibres. J Physiol (Lond) 153:404–412
Hodgkin AL, Nastuk WL (1949) Membrane potentials in single fibres of the frog’s sartorius muscle. J Physiol 108:42Proc
Hollingworth S, Baylor SM (2013) Comparison of myoplasmic calcium movements during excitation-contraction coupling in frog twitch and mouse fast-twitch muscle fibers. J Gen Physiol 141:567–583
Isaacson A, Sandow A (1963) Effects of zinc on responses of skeletal muscle. J Gen Physiol 46:655–677
Jacquemond V, Csernoch L, Klein MG, Schneider MF (1991) Voltage-gated and calcium-gated calcium release during depolarization of skeletal muscle fibers. Biophys J 60:867–873
Jong DS, Pape PC, Baylor SM, Chandler WK (1995) Calcium inactivation of calcium release in frog cut muscle fibers that contain millimolar EGTA or Fura-2. J Gen Physiol 106:337–388
Kahn AJ, Sandow A (1950) The potentiation of muscular contraction by the nitrate-ion. Science 112:647–649
Kashiyama T, Murayama T, Suzuki E, Allen PD, Ogawa Y (2010) Frog alpha- and beta-ryanodine receptors provide distinct intracellular Ca2+ signals in a myogenic cell line. PLoS One 5:e11526
Khan AR (1979) Effects of diethyl-stilboestrol on single fibres of frog skeletal muscle. Acta Physiol Scand 106:69–73
Klein MG, Simon BJ, Schneider MF (1990) Effects of caffeine on calcium release from the sarcoplasmic reticulum in frog skeletal muscle fibres. J Physiol 425:599–626
Konishi M, Hollingworth S, Harkins AB, Baylor SM (1991) Myoplasmic calcium transients in intact frog skeletal muscle fibers monitored with the fluorescent indicator furaptra. J Gen Physiol 97:271–301
Lüttgau HC, Oetliker H (1968) The action of caffeine on the activation of the contractile mechanism in striated muscle fibres. J Physiol 194:51–74
Melzer W, Rios E, Schneider MF (1984) Time course of calcium release and removal in skeletal muscle fibers. Biophys J 45:637–641
Murayama T, Ogawa Y (2002) Roles of two ryanodine receptor isoforms coexisting in skeletal muscle. Trends Cardiovasc Med 12:305–311
O’Brien J, Meissner G, Block BA (1993) The fastest contracting muscles of nonmammalian vertebrates express only one isoform of the ryanodine receptor. Biophys J 65:2418–2427
Ochi K (1984) Effects of twitch potentiators and repetitive stimulation on arsenazo III Ca-transients in Xenopus skeletal muscle fibers. Jpn J Physiol 34:857–870
Ogawa Y, Kurebayashi N, Murayama T (2000) Putative roles of type 3 ryanodine receptor isoforms (RyR3). Trends Cardiovasc Med 10:65–70
Paolini C, Protasi F, Franzini-Armstrong C (2004) The relative position of RyR feet and DHPR tetrads in skeletal muscle. J Mol Biol 342:145–153
Persson A (1963) The negative after-potential of frog skeletal muscle firbres. Acta Physiol Scand 58:3
Pinniger GJ, Bruton JD, Westerblad H, Ranatunga KW (2005) Effects of a myosin-II inhibitor (N-benzyl-p-toluene sulphonamide, BTS) on contractile characteristics of intact fast-twitch mammalian muscle fibres. J Muscle Res Cell Motil 26:135–141
Protasi F (2002) Structural interaction between RYRs and DHPRs in calcium release units of cardiac and skeletal muscle cells. Front Biosci 7:d650–d658
Rios E, Brum G (1987) Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature 325:717–720
Rios E, Pizarro G (1988) Voltage sensors and calcium channels of excitation-contraction coupling. News Physiol Sci 3:223–227
Sandow A (1965) Excitation-contraction coupling in skeletal muscle. Pharmacol Rev 17:265–320
Sandow A, Taylor SR, Preiser H (1965) Role of the action potential in excitation-contraction coupling. Fed Proc 24:1116–1123
Schwartz LM, McCleskey EW, Almers W (1985) Dihydropyridine receptors in muscle are voltage-dependent but most are not functional calcium channels. Nature 314:747–751
Shirokova N, Rios E (1996) Activation of Ca2+ release by caffeine and voltage in frog skeletal muscle. J Physiol (Lond) 493:317–339
Shirokova N, Garcia J, Pizarro G, Rios E (1996) Ca2+ release from the sarcoplasmic reticulum compared in amphibian and mammalian skeletal muscle. J Gen Physiol 107:1–18
Simon BJ, Klein MG, Schneider MF (1989) Caffeine slows turn-off of calcium release in voltage clamped skeletal muscle fibers. Biophys J 55:793–797
Smith JS, Imagawa T, Ma J, Fill M, Campbell KP, Coronado R (1988) Purified ryanodine receptor from rabbit skeletal muscle is the calcium-release channel of sarcoplasmic reticulum. J Gen Physiol 92:1–26
Sutko JL, Ito K, Kenyon JL (1985) Ryanodine: a modifier of sarcoplasmic reticulum calcium release in striated muscle. Fed Proc 44:2984–2988
Taylor SR, Preiser H, Sandow A (1972) Action Potential parameters affecting excitation contraction coupling. J Gen Physiol 59:421–436
Vergara JL, Difranco M (2006) Modulation by caffeine of calcium-release microdomains in frog skeletal muscle fibers. Biol Res 39:567–581
Weber A, Herz R (1968) The relationship between caffeine contracture of intact muscle and the effect of caffeine on reticulum. J Gen Physiol 52:750–759
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Carlo, C., Pura, B., Magaly, R. et al. Differential effects of contractile potentiators on action potential-induced Ca2+ transients of frog and mouse skeletal muscle fibres. J Muscle Res Cell Motil 37, 169–180 (2016). https://doi.org/10.1007/s10974-016-9455-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10974-016-9455-3