Skip to main content
SpringerLink
Log in

Spontaneous oscillatory contraction (SPOC) in cardiomyocytes

  • Review
  • Published:
Biophysical Reviews Aims and scope Submit manuscript

Abstract

SPOC (spontaneous oscillatory contraction) is a characteristic state of the contractile system of striated (skeletal and cardiac) muscle that exists between the states of relaxation and contraction. For example, Ca-SPOCs occur at physiological Ca2+ levels (pCa ∼6.0), whereas ADP-SPOC occurs in the virtual absence of Ca2+ (pCa ≥ 8; relaxing conditions in the presence of MgATP), but in the presence of inorganic phosphate (Pi) and a high concentration of MgADP. The concentration of Mg-ADP necessary for SPOC is nearly equal to or greater than the MgATP concentration for cardiac muscle and is several times higher for skeletal muscle. Thus, the cellular conditions for SPOC are broader in cardiac muscle than in skeletal muscle. During these SPOCs, each sarcomere in a myofibril undergoes length oscillation that has a saw-tooth waveform consisting of a rapid lengthening and a slow shortening phase. The lengthening phase of one half of a sarcomere is transmitted to the adjacent half of the sarcomere successively, forming a propagating wave (termed a SPOC wave). The SPOC waves are synchronized across the cardiomyocytes resulting in a visible wave of successive contractions and relaxations termed the SPOC wave. Experimentally, the SPOC period (and therefore the velocity of SPOC wave) is observed in demembranated cardiomyocytes and can be prepared from a wide range of animal hearts. These periods correlate well with the resting heartbeats of a wide range of mammals (rat, rabbit, dog, pig and cow). Preliminary experiments showed that the SPOC properties of human cardiomyocytes are similar to the heartbeat of a large dog or a pig. This correlation suggests that SPOCs may play a fundamental role in the heart. Here, we briefly summarize a range of SPOC parameters obtained experimentally, and relate them to a theoretical model to explain those characteristics. Finally, we discuss the possible significance of these SPOC properties in each and every heartbeat.

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

Access this article

Log in via an institution

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

  • Anazawa T, Yasuda K, Ishiwata S (1992) Spontaneous oscillation of tension and sarcomere length in skeletal myofibrils. Microscopic measurement and analysis. Biophys J 61:1099–1108

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barany M (1967) ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol 50:197–218

    Article  PubMed Central  PubMed  Google Scholar 

  • Bers DM (2001) In Excitation-contraction coupling and cardiac contractile force. 2nd. Kluwer-Academic, Dordrecht

  • Bremel RD, Weber A (1972) Cooperation within actin filament in vertebrate skeletal muscle. Nat New Biol 238:97–101

    Article  CAS  PubMed  Google Scholar 

  • Brenner B (1979) An indirect proof of stretch-induced Ca2+ release from the sarcoplasmic reticulum in glycerinated skeletal and heart muscle preparations. Basic Res Cardiol 74:177–202

    Article  CAS  PubMed  Google Scholar 

  • Cooke R, Pate E (1985) The effects of ADP and phosphate on the contraction of muscle fibers. Biophys J 48:789–798

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ebashi S, Endo M (1968) Calcium ions and muscle contraction. Prog Biophys Mol Biol 18:123–183

    Article  CAS  PubMed  Google Scholar 

  • Ebashi S, Endo M, Ohtsuki I (1969) Control of muscle contraction. Q Rev Biophys 2:351–384

    Article  CAS  PubMed  Google Scholar 

  • Endo M (1972a) Stretch-induced increase in activation of skinned muscle fibers by calcium. Nat New Biol 237:211–213

    Article  CAS  PubMed  Google Scholar 

  • Endo M (1972b) Length dependence of activation of skinned muscle fibers by calcium. Cold Spring Harb Symp Quant Biol 37:505–510

    Article  Google Scholar 

  • Fabiato A, Fabiato F (1978) Myofilament-generated tension oscillations during partial calcium activation and activation dependence of the sarcomere length-tension relation of skinned cardiac cells. J Gen Physiol 72:667–699

    Article  CAS  PubMed  Google Scholar 

  • Fuchs F, Wang YP (1996) Sarcomere length versus interfilament spacing as determinants of cardiac myofilament Ca2+ sensitivity and Ca2+ binding. J Mol Cell Cardiol 28:1375–1383

    Article  CAS  PubMed  Google Scholar 

  • Fujita H, Ishiwata S (1998) Spontaneous oscillatory contraction without regulatory proteins in actin filament-reconstituted fibers. Biophys J 75:1439–1445

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fujita H, Yasuda K, Niitsu S, Funatsu T, Ishiwata S (1996) Structural and functional reconstitution of thin filaments in the contractile apparatus of cardiac muscle. Biophys J 71:2307–2318

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fukuda N, Ishiwata S (1999) Effects of pH on spontaneous tension oscillation in skinned bovine cardiac muscle. Pflugers Arch 438:125–132

    Article  CAS  PubMed  Google Scholar 

  • Fukuda N, Fujita H, Fujita T, Ishiwata S (1996) Spontaneous tension oscillation in skinned bovine cardiac muscle. Pflugers Arch 433:1–8

    Article  CAS  PubMed  Google Scholar 

  • Fukuda N, Fujita H, Fujita T, Ishiwata S (1998) Regulatory roles of MgADP and calcium in tension development of skinned cardiac muscle. J Muscle Res Cell Motil 19:909–921

    Article  CAS  PubMed  Google Scholar 

  • Fukuda N, Sasaki D, Ishiwata S, Kurihara S (2001) Length dependence of tension generation in rat skinned cardiac muscle. Role of titin in the Frank–Starling mechanism of the heart. Circulation 104:1639–1645

    Article  CAS  PubMed  Google Scholar 

  • Fukuda N, Granzier HL, Ishiwata S, Kurihara S (2008) Physiological functions of the giant elastic protein titin in mammalian striated muscle. J Physiol Sci 58:151–159

    Article  CAS  PubMed  Google Scholar 

  • Funatsu T, Higuchi H, Ishiwata S (1990) Elastic filaments in skeletal muscle revealed by selective removal of thin filaments with plasma gelsolin. J Cell Biol 110:53–62

    Article  CAS  PubMed  Google Scholar 

  • Funatsu T, Kono E, Higuchi H, Kimura S, Ishiwata S, Yoshioka T, Maruyama K, Tsukita S (1993) Elastic filaments in situ in cardiac muscle: deep-etch replica analysis in combination with selective removal of actin and myosin filaments. J Cell Biol 120:711–724

    Article  CAS  PubMed  Google Scholar 

  • Günther S, Kruse K (2007) Spontaneous sarcomere dynamics. Chaos 20:045122

    Article  Google Scholar 

  • Huxley AF (1957) Muscle structure and theories of contraction. Prog Biophys Biophys Chem 7:255–318

    CAS  PubMed  Google Scholar 

  • Huxley HE, Hanson J (1954) Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature 173:973–977

    Article  CAS  PubMed  Google Scholar 

  • Huxley AF, Niedergerke R (1954) Structural changes in muscle during contraction: Interference microscopy of living muscle fibres. Nature 173:971–973

    Article  CAS  PubMed  Google Scholar 

  • Inoue T, Kobirumaki-Shimozawa F, Kagemoto T, Fujii T, Terui T, Kusakari Y, Hongo K, Morimoto S, Ohtsuki I, Hashimoto K, Fukuda N (2013) Depressed Frank-Starling mechanism in the left ventricular muscle of the knock-in mouse model of dilated cardiomyopathy with troponin T deletion mutation ΔK210. J Mol Cell Cardiol 63:69–78

    Article  CAS  PubMed  Google Scholar 

  • Ishiwata S, Yasuda K (1993) Mechano-chemical coupling in spontaneous oscillatory contraction of muscle. Phase Transit 45:105–136

    Article  CAS  Google Scholar 

  • Ishiwata S, Yasuda K, Shindo Y, Fujita H (1996) Microscopic analysis of the elastic properties of connectin/titin and nebulin in myofibrils. Adv Biophys 33:135–142

    Article  CAS  PubMed  Google Scholar 

  • Ishiwata S, Shimamoto Y, Suzuki M (2010) Molecular motors as an auto-oscillator. HFSP J 4:100–104

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ishiwata S, Shimamoto Y, Fukuda N (2011) Contractile system of muscle as an auto-oscillator. Prog Biophys Mol Biol 105:187–198. This is the most detailed review summarizing the characteristics of SPOC mainly experimentally obtained until 2011.

  • Jülicher F, Prost J (1997) Spontaneous oscillations of collective motor units. Phys Rev Lett 78:4510–4513

    Article  Google Scholar 

  • Kobirumaki-Shimozawa F, Oyama K, Serizawa T, Mizuno A, Kagemoto T, Shimozawa T, Ishiwata S, Kurihara S, Fukuda N (2012) Sarcomere imaging by quantum dots for the study of cardiac muscle physiology. J Biomed Biotechnol 2012:1–7

    Article  Google Scholar 

  • Kobirumaki-Shimozawa F, Inoue T, Shintani SA, Oyama K, Terui T, Minamisawa S, Ishiwata S, Fukuda N (2014) Cardiac thin filament regulation and the Frank–Starling mechanism. J Physiol Sci 64:221–232

    Article  PubMed Central  PubMed  Google Scholar 

  • Linke WA, Bartoo ML, Pollack GH (1993) Spontaneous sarcomeric oscillations at intermediate activation levels in single isolated cardiac myofibrils. Circ Res 73:724–734

    Article  CAS  PubMed  Google Scholar 

  • Malmqvist UP, Aronshtam A, Lowey S (2004) Cardiac myosin isoforms from different species have unique enzymatic and mechanical properties. Biochemistry 43:15058–15065

    Article  CAS  PubMed  Google Scholar 

  • Maruyama K, Natori R, Nonomura Y (1976) New elastic protein from muscle. Nature 262:58–60

    Article  CAS  PubMed  Google Scholar 

  • Okamura N, Ishiwata S (1988) Spontaneous oscillatory contraction of sarcomeres in skeletal myofibrils. J Muscle Res Cell Motil 9:111–119

    Article  CAS  PubMed  Google Scholar 

  • Sasaki D, Fujita H, Fukuda N, Kurihara S, Ishiwata S (2005) Auto-oscillations of skinned myocardium correlating with heartbeat. J Muscle Res Cell Motil 26:93–101

    Article  PubMed  Google Scholar 

  • Sasaki D, Fukuda N, Ishiwata S (2006) Myocardial sarcomeres spontaneously oscillate with the period of heartbeat under physiological conditions. Biochem Biophys Res Commun 343:1146–1152

    Article  CAS  PubMed  Google Scholar 

  • Sato K, Ohtaki M, Shimamoto Y, Ishiwata S (2011) A theory on auto-oscillation and contraction in striated muscle. Prog Biophys Mol Biol 105:199–207. This paper proposed the concrete model that has succeeded in explaining almost all the SPOC properties, i.e., the oscillation waveform and the phase diagram, on a single sarcomere (termed a unit-model).

  • Sato K, Kuramoto Y, Ohtaki M, Shimamoto Y, Ishiwata S (2013) Locally and globally coupled oscillators in muscle. Phys Rev Lett 111:108104. This is a paper that presented the model to explain the SPOC properties, i.e., the oscillation pattern (SPOC wave), on a single myofibril (termed a connected model). This model is an extension of the unit model that was visco-elastically connected in series (Sato et al., 2011).

  • Serizawa T, Terui T, Kagemoto T, Mizuno A, Shimozawa T, Kobirumaki F, Ishiwata S, Kurihara S, Fukuda N (2011) Real-time measurement of the length of a single sarcomere in rat ventricular myocytes: a novel analysis with quantum dots. Am J Physiol Cell Physiol 301:C1116–C1127

    Article  CAS  PubMed  Google Scholar 

  • Shimamoto Y, Kono F, Suzuki M, Ishiwata S (2007) Non-linear force-length relationship in the ADP-induced contraction of skeletal myofibrils. Biophys J 93:4330–4341

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shimamoto Y, Suzuki M, Ishiwata S (2008) Length-dependent activation and auto-oscillation in skeletal myofibrils at partial activation by Ca2+. Biochem Biophys Res Commun 366:233–238

    Article  CAS  PubMed  Google Scholar 

  • Shimamoto Y, Suzuki M, Mikhailenko SV, Yasuda K, Ishiwata S (2009) Inter-sarcomere coordination in muscle revealed through individual sarcomere response to quick stretch. Proc Natl Acad Sci U S A 106:11954–11959

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shimizu H, Fujita T, Ishiwata S (1992) Regulation of tension development by MgADP and Pi without Ca2+. Role in spontaneous tension oscillation of skeletal muscle. Biophys J 61:1087–1098

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shintani SA, Oyama K, Kobirumaki-Shimozawa F, Ohki T, Ishiwata S, Fukuda N (2014) Sarcomere length nanometry in rat neonatal cardiomyocytes expressed with α-actinin-AcGFP in Z-discs. J Gen Physiol 143:513–524

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Smith DA, Stephenson DG (2009) The mechanism of spontaneous oscillatory contractions in skeletal muscle. Biophys J 96:3682–3691

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stehle R, Krüger M, Pfitzer G (2002) Force kinetics and individual sarcomere dynamics in cardiac myofibrils after rapid Ca2+ changes. Biophys J 83:2152–2161

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sweitzer NK, Moss RL (1990) The effect of altered temperature on Ca2+-sensitive force in permeabilized myocardium and skeletal muscle. Evidence for force dependence of thin filament activation. J Gen Physiol 96:1221–1245

    Article  CAS  PubMed  Google Scholar 

  • Terui T, Sodnomtseren M, Matsuba D, Udaka J, Ishiwata S, Ohtsuki I, Kurihara S, Fukuda N (2008) Troponin and titin coordinately regulate length-dependent activation in skinned porcine ventricular muscle. J Gen Physiol 131:275–283

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Terui T, Shimamoto Y, Yamane M, Kobirumaki F, Ohtsuki I, Ishiwata S, Kurihara S, Fukuda N (2010) Regulatory mechanism of length-dependent activation in skinned porcine ventricular muscle: role of thin filament cooperative activation in the Frank-Starling relation. J Gen Physiol 136:469–482

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vilfan A, Duke T (2003) Synchronization of active mechanical oscillators by an inertial lode. Phys Rev Lett 91:114101

    Article  PubMed  Google Scholar 

  • Wang K, Ramirez-Mitchell R, Palter D (1984) Titin is an extraordinarily long, flexible, and slender myofibrillar protein. Proc Natl Acad Sci USA 81: 3685-3689

  • Wolfe JE, Ishiwata S, Braet F, Whan R, Su Y, Lal S, dos Remedios CG (2011) SPontaneous Oscillatory Contraction (SPOC): auto-oscillations observed in striated muscle at partial activation. Biophys Rev 3:53–62

    Article  Google Scholar 

  • Yasuda K, Shindo Y, Ishiwata S (1996) Synchronous behavior of spontaneous oscillations of sarcomeres in skeletal myofibrils under isotonic conditions. Biophys J 70:1823–1829

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Compliance with Ethical Standards

ᅟ

Funding

This work was supported in part by Grants-in-Aid for Specially Promoted Research and Scientific Research (S) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (to SI) and from the National Heart Foundation of Australia (to LA).

Conflict of interest

Tatsuya Kagemoto, Amy Li, Cris dos Remedio, and Shin’ichi Ishiwata declare that they have no conflict of interest.

Ethical approval

The human heart was provided by Sydney Heart Bank directed by Cris dos Remedios, which has been approved by Human Research Ethics Committee of The University of Sydney. This research has also been approved by Human Ethics Committee at Waseda University.

Author contributions

Tatsuya Kagemoto, Amy Li, Cris dos Remedio, and Shin’ichi Ishiwata discussed all contents of this review and prepared the manuscript.

Author information

Authors and Affiliations

  1. Department of Physics, Faculty of Science and Engineering, Waseda University, 3-4-1, Okubo, Shinjuku-ku, Tokyo, 169-8555, Japan

    Tatsuya Kagemoto & Shin’ichi Ishiwata

  2. Waseda Bioscience Research Institute in Singapore (WABIOS), 11 Biopolis Way, #05-01/02 Helios, Singapore, 138667, Singapore

    Shin’ichi Ishiwata

  3. Muscle Research Unit, Discipline of Anatomy & Histology, Bosch Institute, University of Sydney, Sydney, 2006, Australia

    Amy Li & Cris dos Remedios

Authors
  1. Tatsuya Kagemoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amy Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cris dos Remedios
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shin’ichi Ishiwata
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shin’ichi Ishiwata.

Additional information

Special Issue: Biophysics of Human Heart Failure

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kagemoto, T., Li, A., dos Remedios, C. et al. Spontaneous oscillatory contraction (SPOC) in cardiomyocytes. Biophys Rev 7, 15–24 (2015). https://doi.org/10.1007/s12551-015-0165-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12551-015-0165-7

Keywords

Search

Navigation