Skip to main content
SpringerLink
Log in

Auto-oscillations of Skinned Myocardium Correlating with Heartbeat

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

Abstract

Skinned myocardium (or myofibrils) exhibits auto-oscillations of sarcomere length and developed force called SPOC (SPontaneousOscillatoryContraction) under partial activation conditions. In SPOC, each sarcomere repeats the cycle of slow shortening and rapid lengthening, and the lengthening phase propagates sequentially to the adjacent sarcomeres in waves (SPOC wave). In this study, we analyzed the sarcomeric oscillation in SPOC in skinned myocardium of various animal species (rat, rabbit, dog, pig, and cow) with different heart rates. The period of oscillation, the sarcomere shortening velocity, and the velocity of SPOC wave, strongly correlated with the resting heart rate of the animal species. The shortening velocity in particular was proportional to the resting heart rate. We then examined the motile activity of each cardiac myosin by an in vitro motility assay. The sliding velocity of actin filaments, which is an index of the motile activity of myosin, also correlated with the resting heart rate but the relationship was not proportional. As a result, the ratio of sarcomere shortening velocity in SPOC to the sliding velocity of actin filaments was not constant but became higher with a higher heart rate. This suggests that the sarcomere shortening velocity in SPOC is modulated by some additional factors besides the motile activity of myosin, resulting in the proportional relationship between the shortening velocity of the sarcomere and the resting heart rate.

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

Similar content being viewed by others

References

  1. Altman PL and Dittmer DS (eds) (1974) Biology Data Book, 2nd edn. (vol. 3, pp. 1686–1693) Federation of American Societies for Experiental Biology, Bethesda, MD.

  2. T Anazawa K Yasuda S Ishiwata (1992) ArticleTitleSpontaneous oscillation of tension and sarcomere length in skeletal myofibrils.Microscopic measurement and analysis Biophys J 61 1099–1108 Occurrence Handle1600075 Occurrence Handle1:STN:280:By2B1cfhs1w%3D

    PubMed  CAS  Google Scholar 

  3. M Barany (1967) ArticleTitleATPase Activity of Myosin Correlated with Speed of Muscle Shortening. J Gen Physiol 50 197–218 Occurrence Handle4227924 Occurrence Handle10.1085/jgp.50.6.197

    Article  PubMed  Google Scholar 

  4. O Cazorla A Freiburg M Helmes T Centner M McNabb Y Wu K Trombitas S Labeit H Granzier (2000) ArticleTitleDifferential expression of cardiac titin isoforms and modulation of cellular stiffness. Circ Res 86 59–67 Occurrence Handle10625306 Occurrence Handle1:CAS:528:DC%2BD3cXlt1egsw%3D%3D

    PubMed  CAS  Google Scholar 

  5. WH Dillmann (1984) ArticleTitleHormonal influences on cardiac myosin ATPase activity and myosin isoenzyme distribution Mol Cell Endocrinol 34 169–181 Occurrence Handle6232163 Occurrence Handle10.1016/0303-7207(84)90173-4 Occurrence Handle1:CAS:528:DyaL2cXhsFWisL4%3D

    Article  PubMed  CAS  Google Scholar 

  6. A Fabiato F Fabiato (1978) ArticleTitleMyofilament-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 Occurrence Handle739258 Occurrence Handle10.1085/jgp.72.5.667 Occurrence Handle1:CAS:528:DyaE1MXjslSmug%3D%3D

    Article  PubMed  CAS  Google Scholar 

  7. N Fukuda H Fujita T Fujita S Ishiwata (1996) ArticleTitleSpontaneous tension oscillation in skinned bovine cardiac muscle Pflügers Arch 433 1–8 Occurrence Handle9019709 Occurrence Handle10.1007/s004240050241 Occurrence Handle1:CAS:528:DyaK2sXhtVWhtr4%3D

    Article  PubMed  CAS  Google Scholar 

  8. N Fukuda S Ishiwata (1999) ArticleTitleEffects of pH on spontaneous tension oscillation in skinned bovine cardiac muscle Pflügers Arch 438 125–132 Occurrence Handle10370097 Occurrence Handle10.1007/s004240050889 Occurrence Handle1:CAS:528:DyaK1MXjsFKgtbw%3D

    Article  PubMed  CAS  Google Scholar 

  9. N Hamilton CD Ianuzzo (1991) ArticleTitleContractile and calcium regulating capacities of myocardia of different sized mammals scale with resting heart rate Mol Cell Biochem 106 133–141 Occurrence Handle1656210 Occurrence Handle10.1007/BF00230179 Occurrence Handle1:CAS:528:DyaK3MXmtVCnurw%3D

    Article  PubMed  CAS  Google Scholar 

  10. W Hasselbach G Schneider (1951) ArticleTitleL-Myosin and actin content of guinea-pig muscle Biochem Z 321 462–475 Occurrence Handle14858381 Occurrence Handle1:CAS:528:DyaG3sXkvVGnuw%3D%3D

    PubMed  CAS  Google Scholar 

  11. E Homsher M Nili IY Chen LS Tobacman (2003) ArticleTitleRegulatory proteins alter nucleotide binding to acto-myosin of sliding filaments in motility assays. Biophys J 85 1046–1052 Occurrence Handle12885651 Occurrence Handle1:CAS:528:DC%2BD3sXmtVyks7g%3D

    PubMed  CAS  Google Scholar 

  12. S Ishiwata N Okamura H Shimizu T Anazawa K Yasuda (1991) ArticleTitleSpontaneous oscillatory contraction (SPOC) of sarcomeres in skeletal muscle Adv Biophys 27 227–235 Occurrence Handle1755363 Occurrence Handle1:CAS:528:DyaK38XhslWjsbk%3D

    PubMed  CAS  Google Scholar 

  13. S Ishiwata K Yasuda (1993) ArticleTitleMechano-chemical coupling in spontaneous oscillatory contraction of muscle Phase Transitions 45 105–136 Occurrence Handle1:CAS:528:DyaK2MXjt1Kmuw%3D%3D

    CAS  Google Scholar 

  14. H Kondo S Ishiwata (1976) ArticleTitleUni-directional growth of F-actin J Biochem (Tokyo) 79 159–171 Occurrence Handle1:CAS:528:DyaE28XhtVWisrY%3D

    CAS  Google Scholar 

  15. WA Linke ML Bartoo GH Pollack (1993) ArticleTitleSpontaneous sarcomeric oscillations at intermediate activation levels in single isolated cardiac myofibrils Circ Res 73 724–734 Occurrence Handle8370125 Occurrence Handle1:CAS:528:DyaK2cXls1Wn

    PubMed  CAS  Google Scholar 

  16. K Maruyama (1997) ArticleTitleConnectin/titin, giant elastic protein of muscle FASEB J 11 341–345 Occurrence Handle9141500 Occurrence Handle1:CAS:528:DyaK2sXjtVWmtrw%3D

    PubMed  CAS  Google Scholar 

  17. N Okamura S Ishiwata (1988) ArticleTitleSpontaneous oscillatory contraction of sarcomeres in skeletal myofibrils. J Muscle Res Cell Motil 9 111–119 Occurrence Handle3138284 Occurrence Handle10.1007/BF01773733 Occurrence Handle1:STN:280:BieA3s7jsVY%3D

    Article  PubMed  CAS  Google Scholar 

  18. CA Opitz M Kulke MC Leake C Neagoe H Hinssen RJ Hajjar WA Linke (2003) ArticleTitleDamped elastic recoil of the titin spring in myofibrils of human myocardium. Proc Natl Acad Sci U S A 100 12688–12693 Occurrence Handle14563922 Occurrence Handle10.1073/pnas.2133733100 Occurrence Handle1:CAS:528:DC%2BD3sXoslKnt7g%3D

    Article  PubMed  CAS  Google Scholar 

  19. M Sata S Sugiura H Yamashita S Momomura T Serizawa (1993) ArticleTitleDynamic interaction between cardiac myosin isoforms modifies velocity of actomyosin sliding in vitro. Circ Res 73 696–704 Occurrence Handle8370124 Occurrence Handle1:CAS:528:DyaK2cXls1Wg

    PubMed  CAS  Google Scholar 

  20. R Stehle M Krüger G Pfitzer (2002) ArticleTitleForce kinetics and individual sarcomere dynamics in cardiac myofibrils after rapid Ca2+ changes. Biophys J 83 2152–2161 Occurrence Handle12324432 Occurrence Handle1:CAS:528:DC%2BD38XnslSrtr0%3D

    PubMed  CAS  Google Scholar 

  21. S Sugiura N Kobayakawa S Momomura S Chaen M Omata H Sugi (1996) ArticleTitleDifferent cardiac myosin isoforms exhibit equal force-generating ability in vitro. Biochim Biophys Acta 1273 73–76 Occurrence Handle8611591

    PubMed  Google Scholar 

  22. C Svensson I Morano A Arner (1997) ArticleTitleIn vitro motility assay of atrial and ventricular myosin from pig. J Cell Biochem 67 241–247 Occurrence Handle9328829 Occurrence Handle10.1002/(SICI)1097-4644(19971101)67:2<241::AID-JCB9>3.0.CO;2-X Occurrence Handle1:CAS:528:DyaK2sXmsV2rsbc%3D

    Article  PubMed  CAS  Google Scholar 

  23. P VanBuren DE Harris NR Alpert DM Warshaw (1995) ArticleTitleCardiac V1 and V3 myosins differ in their hydrolytic and mechanical activities in vitro. Circ Res 77 439–444 Occurrence Handle7614728 Occurrence Handle1:CAS:528:DyaK2MXntFartLc%3D

    PubMed  CAS  Google Scholar 

  24. K Wang (1996) ArticleTitleTitin/connectin and nebulin: giant protein rulers of muscle structure and function. Adv Biophys 33 123–134 Occurrence Handle8922107 Occurrence Handle1:CAS:528:DyaK28Xnt1eju74%3D

    PubMed  CAS  Google Scholar 

  25. K Yasuda Y Shindo S Ishiwata (1996) ArticleTitleSynchronous behavior of spontaneous oscillations of sarcomeres in skeletal myofibrils under isotonic conditions. Biophys J 70 1823–1829 Occurrence Handle8785342 Occurrence Handle1:CAS:528:DyaK28XhvVGjs70%3D Occurrence Handle10.1016/S0006-3495(96)79747-3

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Integrative Bioscience and Biomedical Engineering, Graduate School of Science and Engineering, Waseda University, 3-4-1 Okubo, Shinjuku-ku, Tokyo, 169-8555, Japan

    Daisuke Sasaki

  2. Tohoku University Biomedical Engineering Research Organization, 2-1 Seiryou-machi, Aobaku Sendai, Miyagi, 980-8575, Japan

    Hideaki Fujita

  3. Department of Physiology (II), The Jikei University School of Medicine, 3-25-8 Nishishinbashi, Minato-ku, Tokyo, 105-8461, Japan

    Norio Fukuda & Satoshi Kurihara

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

    Shin’ichi Ishiwata

  5. Advanced Research Institute for Science and Engineering, Waseda University, 3-4-1 Okubo, Shinjuku-ku, Tokyo, 169-8555, Japan

    Shin’ichi Ishiwata

Authors
  1. Daisuke Sasaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hideaki Fujita
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Norio Fukuda
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Satoshi Kurihara
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shin’ichi Ishiwata
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shin’ichi Ishiwata.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sasaki, D., Fujita, H., Fukuda, N. et al. Auto-oscillations of Skinned Myocardium Correlating with Heartbeat. J Muscle Res Cell Motil 26, 93–101 (2005). https://doi.org/10.1007/s10974-005-0249-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10974-005-0249-2

Keywords

Search

Navigation