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. 1991 Mar 1;97(3):541–560. doi: 10.1085/jgp.97.3.541

Shortening velocity and power output of skinned muscle fibers from mammals having a 25,000-fold range of body mass

PMCID: PMC2216485  PMID: 2037839

Abstract

The shortening velocities of single, skinned, fast and slow skeletal muscle fibers were measured at 5-6 degrees C in five animal species having a 25,000-fold range of body size (mouse, rat, rabbit, sheep, and cow). While fiber diameter and isometric force showed no dependence on animal body size, maximum shortening velocity in both fast and slow fibers and maximum power output in fast fibers were found to vary with the -1/8 power of body size. Maximum power output in slow fibers showed a slightly greater (-1/5 power) dependence on body size. The isometric force produced by the fibers was correlated (r = 0.74) inversely with fiber diameter. For all sizes of animal the average maximum velocity was 1.7 times faster in fast fibers than in slow fibers. The large difference in mechanical properties found between fibers from large and small animals suggests that properties of the contractile proteins vary in a systematic manner with the body size. These size-dependent changes can be used to study the correlations of structure and function of these proteins. Experimental results also suggest that the different metabolic rates observed in different sizes of animals could be accounted for, at least in part, by the difference in the properties of the contractile proteins.

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Selected References

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  1. Biewener A. A. Scaling body support in mammals: limb posture and muscle mechanics. Science. 1989 Jul 7;245(4913):45–48. doi: 10.1126/science.2740914. [DOI] [PubMed] [Google Scholar]
  2. Brenner B. Technique for stabilizing the striation pattern in maximally calcium-activated skinned rabbit psoas fibers. Biophys J. 1983 Jan;41(1):99–102. doi: 10.1016/S0006-3495(83)84411-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brenner B. The necessity of using two parameters to describe isotonic shortening velocity of muscle tissues: the effect of various interventions upon initial shortening velocity (vi) and curvature (b). Basic Res Cardiol. 1986 Jan-Feb;81(1):54–69. doi: 10.1007/BF01907427. [DOI] [PubMed] [Google Scholar]
  4. Bárány M. ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol. 1967 Jul;50(6 Suppl):197–218. doi: 10.1085/jgp.50.6.197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chiu Y. C., Quinlan J., Ford L. E. System for automatic activation of skinned muscle fibers. Am J Physiol. 1985 Nov;249(5 Pt 1):C522–C526. doi: 10.1152/ajpcell.1985.249.5.C522. [DOI] [PubMed] [Google Scholar]
  6. Chiu Y. L., Asayama J., Ford L. E. A sensitive photoelectric force transducer with a resonant frequency of 6 kHz. Am J Physiol. 1982 Nov;243(5):C299–C302. doi: 10.1152/ajpcell.1982.243.5.C299. [DOI] [PubMed] [Google Scholar]
  7. Close R. I. Dynamic properties of mammalian skeletal muscles. Physiol Rev. 1972 Jan;52(1):129–197. doi: 10.1152/physrev.1972.52.1.129. [DOI] [PubMed] [Google Scholar]
  8. Cooke R., Pate E. The effects of ADP and phosphate on the contraction of muscle fibers. Biophys J. 1985 Nov;48(5):789–798. doi: 10.1016/S0006-3495(85)83837-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Elzinga G., Howarth J. V., Rall J. A., Wilson M. G., Woledge R. C. Variation in the normalized tetanic force of single frog muscle fibres. J Physiol. 1989 Mar;410:157–170. doi: 10.1113/jphysiol.1989.sp017526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Elzinga G., Stienen G. J., Wilson M. G. Isometric force production before and after chemical skinning in isolated muscle fibres of the frog Rana temporaria. J Physiol. 1989 Mar;410:171–185. doi: 10.1113/jphysiol.1989.sp017527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ferenczi M. A., Goldman Y. E., Simmons R. M. The dependence of force and shortening velocity on substrate concentration in skinned muscle fibres from Rana temporaria. J Physiol. 1984 May;350:519–543. doi: 10.1113/jphysiol.1984.sp015216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ford L. E., Huxley A. F., Simmons R. M. Tension responses to sudden length change in stimulated frog muscle fibres near slack length. J Physiol. 1977 Jul;269(2):441–515. doi: 10.1113/jphysiol.1977.sp011911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ford L. E., Nakagawa K., Desper J., Seow C. Y. Effect of osmotic compression on the force-velocity properties of glycerinated rabbit skeletal muscle cells. J Gen Physiol. 1991 Jan;97(1):73–88. doi: 10.1085/jgp.97.1.73. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ford L. E. Some consequences of body size. Am J Physiol. 1984 Oct;247(4 Pt 2):H495–H507. doi: 10.1152/ajpheart.1984.247.4.H495. [DOI] [PubMed] [Google Scholar]
  15. Godt R. E., Maughan D. W. Swelling of skinned muscle fibers of the frog. Experimental observations. Biophys J. 1977 Aug;19(2):103–116. doi: 10.1016/S0006-3495(77)85573-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Goldman Y. E., Simmons R. M. Control of sarcomere length in skinned muscle fibres of Rana temporaria during mechanical transients. J Physiol. 1984 May;350:497–518. doi: 10.1113/jphysiol.1984.sp015215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. HILL A. V. The heat of activation and the heat of shortening in a muscle twitch. Proc R Soc Lond B Biol Sci. 1949 Jun 23;136(883):195–211. doi: 10.1098/rspb.1949.0019. [DOI] [PubMed] [Google Scholar]
  18. Heglund N. C., Taylor C. R., McMahon T. A. Scaling stride frequency and gait to animal size: mice to horses. Science. 1974 Dec 20;186(4169):1112–1113. doi: 10.1126/science.186.4169.1112. [DOI] [PubMed] [Google Scholar]
  19. McMahon T. A. Using body size to understand the structural design of animals: quadrupedal locomotion. J Appl Physiol. 1975 Oct;39(4):619–627. doi: 10.1152/jappl.1975.39.4.619. [DOI] [PubMed] [Google Scholar]
  20. McMahon T. Size and shape in biology. Science. 1973 Mar 23;179(4079):1201–1204. doi: 10.1126/science.179.4079.1201. [DOI] [PubMed] [Google Scholar]
  21. Metzger J. M., Moss R. L. Greater hydrogen ion-induced depression of tension and velocity in skinned single fibres of rat fast than slow muscles. J Physiol. 1987 Dec;393:727–742. doi: 10.1113/jphysiol.1987.sp016850. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nosek T. M., Fender K. Y., Godt R. E. It is diprotonated inorganic phosphate that depresses force in skinned skeletal muscle fibers. Science. 1987 Apr 10;236(4798):191–193. doi: 10.1126/science.3563496. [DOI] [PubMed] [Google Scholar]
  23. Podolin R. A., Ford L. E. Influence of partial activation on force-velocity properties of frog skinned muscle fibers in millimolar magnesium ion. J Gen Physiol. 1986 Apr;87(4):607–631. doi: 10.1085/jgp.87.4.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sweeney H. L., Corteselli S. A., Kushmerick M. J. Measurements on permeabilized skeletal muscle fibers during continuous activation. Am J Physiol. 1987 May;252(5 Pt 1):C575–C580. doi: 10.1152/ajpcell.1987.252.5.C575. [DOI] [PubMed] [Google Scholar]

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