Skip to main content
Log in

Differential effects of contractile potentiators on action potential-induced Ca2+ transients of frog and mouse skeletal muscle fibres

  • Original Paper
  • Published:
Journal of Muscle Research and Cell Motility Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bekoff A, Betz WJ (1977) Physiological properties of dissociated muscle fibres obtained from innervated and denervated adult rat muscle. J Physiol 271:25–40

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Caputo C, Gottschalk G, Lüttgau HC (1981) The control of contraction activation by the membrane potential. Experientia 37:580–581

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Carroll SL, Klein M, Schneider MF (1995) Calcium transients in intact rat skeletal muscle fibers in agarose gel. Am J Physiol 269:C28–C34

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delay M, Ribalet B, Vergara J (1986) Caffeine potentiation of calcium release in frog skeletal muscle fibres. J Physiol 375:535–559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Endo M (1975) Mechanism of action of caffeine on the sarcoplasmic reticulum of skeletal muscle. Proc Japan Acad 51:479–484

    CAS  Google Scholar 

  • Endo M (1977) Calcium release from the Sarcoplasmic Reticulum. Physiol Rev 57:71–108

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Franzini-Armstrong C, Protasi F (1997) Ryanodine receptors of striated muscles: a complex channel capable of multiple interactions. Physiol Rev 77:699–729

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gonzalez A, Rios E (1993) Perchlorate enhances transmission in skeletal muscle excitation-contraction coupling. J Gen Physiol 102:373–421

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Hodgkin AL, Nastuk WL (1949) Membrane potentials in single fibres of the frog’s sartorius muscle. J Physiol 108:42Proc

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Isaacson A, Sandow A (1963) Effects of zinc on responses of skeletal muscle. J Gen Physiol 46:655–677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kahn AJ, Sandow A (1950) The potentiation of muscular contraction by the nitrate-ion. Science 112:647–649

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan AR (1979) Effects of diethyl-stilboestrol on single fibres of frog skeletal muscle. Acta Physiol Scand 106:69–73

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Melzer W, Rios E, Schneider MF (1984) Time course of calcium release and removal in skeletal muscle fibers. Biophys J 45:637–641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murayama T, Ogawa Y (2002) Roles of two ryanodine receptor isoforms coexisting in skeletal muscle. Trends Cardiovasc Med 12:305–311

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ogawa Y, Kurebayashi N, Murayama T (2000) Putative roles of type 3 ryanodine receptor isoforms (RyR3). Trends Cardiovasc Med 10:65–70

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Persson A (1963) The negative after-potential of frog skeletal muscle firbres. Acta Physiol Scand 58:3

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Protasi F (2002) Structural interaction between RYRs and DHPRs in calcium release units of cardiac and skeletal muscle cells. Front Biosci 7:d650–d658

    Article  CAS  PubMed  Google Scholar 

  • Rios E, Brum G (1987) Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature 325:717–720

    Article  CAS  PubMed  Google Scholar 

  • Rios E, Pizarro G (1988) Voltage sensors and calcium channels of excitation-contraction coupling. News Physiol Sci 3:223–227

    Google Scholar 

  • Sandow A (1965) Excitation-contraction coupling in skeletal muscle. Pharmacol Rev 17:265–320

    CAS  PubMed  Google Scholar 

  • Sandow A, Taylor SR, Preiser H (1965) Role of the action potential in excitation-contraction coupling. Fed Proc 24:1116–1123

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Shirokova N, Rios E (1996) Activation of Ca2+ release by caffeine and voltage in frog skeletal muscle. J Physiol (Lond) 493:317–339

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Sutko JL, Ito K, Kenyon JL (1985) Ryanodine: a modifier of sarcoplasmic reticulum calcium release in striated muscle. Fed Proc 44:2984–2988

    CAS  PubMed  Google Scholar 

  • Taylor SR, Preiser H, Sandow A (1972) Action Potential parameters affecting excitation contraction coupling. J Gen Physiol 59:421–436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vergara JL, Difranco M (2006) Modulation by caffeine of calcium-release microdomains in frog skeletal muscle fibers. Biol Res 39:567–581

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Caputo Carlo.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 110 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10974-016-9455-3

Keywords

Navigation