Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1997 Jul 15;502(Pt 2):449–460. doi: 10.1111/j.1469-7793.1997.449bk.x

Chemo-mechanical energy transduction in relation to myosin isoform composition in skeletal muscle fibres of the rat.

C Reggiani 1, E J Potma 1, R Bottinelli 1, M Canepari 1, M A Pellegrino 1, G J Stienen 1
PMCID: PMC1159562  PMID: 9263923

Abstract

1. ATP consumption and force development were determined in single skinned muscle fibres of the rat at 12 degrees C. Myofibrillar ATPase consumption was measured photometrically from NADH oxidation which was coupled to ATP hydrolysis. Myosin heavy chain (MHC) and light chain (MLC) isoforms were identified by gel electrophoresis. 2. Slow fibres (n = 14) containing MHCI and fast fibres (n = 18) containing MHCIIB were compared. Maximum shortening velocity was 1.02 +/- 0.63 and 3.05 +/- 0.23 lengths s-1, maximum power was 1.47 +/- 0.22 and 9.59 +/- 0.84 W l-1, and isometric ATPase activity was 0.034 +/- 0.003 and 0.25 +/- 0.01 mM s-1 in slow and in fast fibres, respectively. 3. In fast as well as in slow fibres ATP consumption during shortening increased above isometric ATP consumption. The increase was much greater in fast fibres than in slow fibres, but became similar when expressed relative to the isometric ATPase rate. 4. Efficiency was calculated from mechanical power and free energy change associated with ATP hydrolysis. Maximum efficiency was larger in slow than in fast fibres (0.38 +/- 0.04 versus 0.28 +/- 0.03) and was reached at a lower shortening velocity. 5. Within the group of fast fibres efficiency was lower in fibres which contained more MLC3f. We conclude that both MHC and essential MLC isoforms contribute to determine efficiency of chemo-mechanical transduction.

Full text

PDF
449

Images in this article

452Figure 2
on p.452

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alberty R. A. Standard Gibbs free energy, enthalpy, and entropy changes as a function of pH and pMg for several reactions involving adenosine phosphates. J Biol Chem. 1969 Jun 25;244(12):3290–3302. [PubMed] [Google Scholar]
  2. Barclay C. J., Constable J. K., Gibbs C. L. Energetics of fast- and slow-twitch muscles of the mouse. J Physiol. 1993 Dec;472:61–80. doi: 10.1113/jphysiol.1993.sp019937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bottinelli R., Betto R., Schiaffino S., Reggiani C. Unloaded shortening velocity and myosin heavy chain and alkali light chain isoform composition in rat skeletal muscle fibres. J Physiol. 1994 Jul 15;478(Pt 2):341–349. doi: 10.1113/jphysiol.1994.sp020254. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bottinelli R., Canepari M., Reggiani C., Stienen G. J. Myofibrillar ATPase activity during isometric contraction and isomyosin composition in rat single skinned muscle fibres. J Physiol. 1994 Dec 15;481(Pt 3):663–675. doi: 10.1113/jphysiol.1994.sp020472. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bottinelli R., Reggiani C. Force-velocity properties and myosin light chain isoform composition of an identified type of skinned fibres from rat skeletal muscle. Pflugers Arch. 1995 Feb;429(4):592–594. doi: 10.1007/BF00704166. [DOI] [PubMed] [Google Scholar]
  6. Buschman H. P., Elzinga G., Woledge R. C. The effects of the level of activation and shortening velocity on energy output in type 3 muscle fibres from Xenopus laevis. Pflugers Arch. 1996 Nov-Dec;433(1-2):153–159. doi: 10.1007/s004240050261. [DOI] [PubMed] [Google Scholar]
  7. Curtin N. A., Gilbert C., Kretzschmar K. M., Wilkie D. R. The effect of the performance of work on total energy output and metabolism during muscular contraction. J Physiol. 1974 May;238(3):455–472. doi: 10.1113/jphysiol.1974.sp010537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fenn W. O. The relation between the work performed and the energy liberated in muscular contraction. J Physiol. 1924 May 23;58(6):373–395. doi: 10.1113/jphysiol.1924.sp002141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Finer J. T., Simmons R. M., Spudich J. A. Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature. 1994 Mar 10;368(6467):113–119. doi: 10.1038/368113a0. [DOI] [PubMed] [Google Scholar]
  10. Gibbs C. L., Gibson W. R. Energy production of rat soleus muscle. Am J Physiol. 1972 Oct;223(4):864–871. doi: 10.1152/ajplegacy.1972.223.4.864. [DOI] [PubMed] [Google Scholar]
  11. Glyn H., Sleep J. Dependence of adenosine triphosphatase activity of rabbit psoas muscle fibres and myofibrils on substrate concentration. J Physiol. 1985 Aug;365:259–276. doi: 10.1113/jphysiol.1985.sp015770. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Greaser M. L., Moss R. L., Reiser P. J. Variations in contractile properties of rabbit single muscle fibres in relation to troponin T isoforms and myosin light chains. J Physiol. 1988 Dec;406:85–98. doi: 10.1113/jphysiol.1988.sp017370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Heglund N. C., Cavagna G. A. Mechanical work, oxygen consumption, and efficiency in isolated frog and rat muscle. Am J Physiol. 1987 Jul;253(1 Pt 1):C22–C29. doi: 10.1152/ajpcell.1987.253.1.C22. [DOI] [PubMed] [Google Scholar]
  14. Holroyd S. M., Gibbs C. L., Luff A. R. Shortening heat in slow- and fast-twitch muscles of the rat. Am J Physiol. 1996 Jan;270(1 Pt 1):C293–C297. doi: 10.1152/ajpcell.1996.270.1.C293. [DOI] [PubMed] [Google Scholar]
  15. Homsher E., Irving M., Wallner A. High-energy phosphate metabolism and energy liberation associated with rapid shortening in frog skeletal muscle. J Physiol. 1981 Dec;321:423–436. doi: 10.1113/jphysiol.1981.sp013994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Irving M., Woledge R. C. The dependence on extent of shortening of the extra energy liberated by rapidly shortening frog skeletal muscle. J Physiol. 1981 Dec;321:411–422. doi: 10.1113/jphysiol.1981.sp013993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kushmerick M. J., Davies R. E. The chemical energetics of muscle contraction. II. The chemistry, efficiency and power of maximally working sartorius muscles. Appendix. Free energy and enthalpy of atp hydrolysis in the sarcoplasm. Proc R Soc Lond B Biol Sci. 1969 Dec 23;174(1036):315–353. doi: 10.1098/rspb.1969.0096. [DOI] [PubMed] [Google Scholar]
  18. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  19. Linari M., Woledge R. C. Comparison of energy output during ramp and staircase shortening in frog muscle fibres. J Physiol. 1995 Sep 15;487(Pt 3):699–710. doi: 10.1113/jphysiol.1995.sp020911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Metzger J. M., Moss R. L. Calcium-sensitive cross-bridge transitions in mammalian fast and slow skeletal muscle fibers. Science. 1990 Mar 2;247(4946):1088–1090. doi: 10.1126/science.2309121. [DOI] [PubMed] [Google Scholar]
  21. Potma E. J., Stienen G. J., Barends J. P., Elzinga G. Myofibrillar ATPase activity and mechanical performance of skinned fibres from rabbit psoas muscle. J Physiol. 1994 Jan 15;474(2):303–317. doi: 10.1113/jphysiol.1994.sp020023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Potma E. J., Stienen G. J. Increase in ATP consumption during shortening in skinned fibres from rabbit psoas muscle: effects of inorganic phosphate. J Physiol. 1996 Oct 1;496(Pt 1):1–12. doi: 10.1113/jphysiol.1996.sp021660. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Potma E. J., van Graas I. A., Stienen G. J. Influence of inorganic phosphate and pH on ATP utilization in fast and slow skeletal muscle fibers. Biophys J. 1995 Dec;69(6):2580–2589. doi: 10.1016/S0006-3495(95)80129-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rall J. A., Schottelius B. A. Energetics of contraction in phasic and tonic skeletal muscles of the chicken. J Gen Physiol. 1973 Sep;62(3):303–323. doi: 10.1085/jgp.62.3.303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rall J. A. Sense and nonsense about the Fenn effect. Am J Physiol. 1982 Jan;242(1):H1–H6. doi: 10.1152/ajpheart.1982.242.1.H1. [DOI] [PubMed] [Google Scholar]
  26. Rayment I., Rypniewski W. R., Schmidt-Bäse K., Smith R., Tomchick D. R., Benning M. M., Winkelmann D. A., Wesenberg G., Holden H. M. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science. 1993 Jul 2;261(5117):50–58. doi: 10.1126/science.8316857. [DOI] [PubMed] [Google Scholar]
  27. Reiser P. J., Moss R. L., Giulian G. G., Greaser M. L. Shortening velocity in single fibers from adult rabbit soleus muscles is correlated with myosin heavy chain composition. J Biol Chem. 1985 Aug 5;260(16):9077–9080. [PubMed] [Google Scholar]
  28. Salviati G., Betto R., Danieli Betto D., Zeviani M. Myofibrillar-protein isoforms and sarcoplasmic-reticulum Ca2+-transport activity of single human muscle fibres. Biochem J. 1984 Nov 15;224(1):215–225. doi: 10.1042/bj2240215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schiaffino S., Reggiani C. Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol Rev. 1996 Apr;76(2):371–423. doi: 10.1152/physrev.1996.76.2.371. [DOI] [PubMed] [Google Scholar]
  30. Stienen G. J., Kiers J. L., Bottinelli R., Reggiani C. Myofibrillar ATPase activity in skinned human skeletal muscle fibres: fibre type and temperature dependence. J Physiol. 1996 Jun 1;493(Pt 2):299–307. doi: 10.1113/jphysiol.1996.sp021384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Stienen G. J., Roosemalen M. C., Wilson M. G., Elzinga G. Depression of force by phosphate in skinned skeletal muscle fibers of the frog. Am J Physiol. 1990 Aug;259(2 Pt 1):C349–C357. doi: 10.1152/ajpcell.1990.259.2.C349. [DOI] [PubMed] [Google Scholar]
  32. Stienen G. J., Zaremba R., Elzinga G. ATP utilization for calcium uptake and force production in skinned muscle fibres of Xenopus laevis. J Physiol. 1995 Jan 1;482(Pt 1):109–122. doi: 10.1113/jphysiol.1995.sp020503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sweeney H. L., Kushmerick M. J., Mabuchi K., Sréter F. A., Gergely J. Myosin alkali light chain and heavy chain variations correlate with altered shortening velocity of isolated skeletal muscle fibers. J Biol Chem. 1988 Jun 25;263(18):9034–9039. [PubMed] [Google Scholar]
  34. Toyoshima Y. Y., Kron S. J., McNally E. M., Niebling K. R., Toyoshima C., Spudich J. A. Myosin subfragment-1 is sufficient to move actin filaments in vitro. Nature. 1987 Aug 6;328(6130):536–539. doi: 10.1038/328536a0. [DOI] [PubMed] [Google Scholar]
  35. VanBuren P., Waller G. S., Harris D. E., Trybus K. M., Warshaw D. M., Lowey S. The essential light chain is required for full force production by skeletal muscle myosin. Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12403–12407. doi: 10.1073/pnas.91.26.12403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wendt I. R., Barclay J. K. Effects of dantrolene on the energetics of fast- and slow-twitch muscles of the mouse. Am J Physiol. 1980 Jan;238(1):C56–C61. doi: 10.1152/ajpcell.1980.238.1.C56. [DOI] [PubMed] [Google Scholar]
  37. Wendt I. R., Gibbs C. L. Energy production of rat extensor digitorum longus muscle. Am J Physiol. 1973 May;224(5):1081–1086. doi: 10.1152/ajplegacy.1973.224.5.1081. [DOI] [PubMed] [Google Scholar]
  38. Woledge R. C. The energetics of tortoise muscle. J Physiol. 1968 Aug;197(3):685–707. doi: 10.1113/jphysiol.1968.sp008582. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES