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Single skeletal muscle fiber behavior after a quick stretch in young and older men: a possible explanation of the relative preservation of eccentric force in old age

  • Skeletal Muscle
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An Erratum to this article was published on 05 October 2006

Abstract

The origins of the smaller age-related decrease in eccentric force compared to isometric and concentric conditions in vivo remain unclear. Could this originate from contractile elements of muscle cells? The main intent of the current investigation was to assess the force behavior of muscle cells with aging, during lengthening. Chemically skinned single muscle fibers (n=235) from m. vastus lateralis of six young (mean age 31.6 years) and six older men (mean age 66.1 years) were maximally activated with pCa 4.5 at 15°C. Maximal isometric force and cross-sectional area were measured allowing the calculation of the tension (T 0). A quick stretch (2 nm per half-sarcomere length) was applied and caused an immediate increase in tension followed by a decrease and a secondary delayed and transient rise in tension (phase 3); finally, the tension recovered a steady state value (phase 4). The tension enhancements during phase 3 (ΔT 3) and phase 4 (ΔT 4) were evaluated. The myosin heavy-chain isoform composition of each single fiber was determined by sodium dodecyl sulfate-polyacrylamide gel electrophoresis. ΔT 3 and ΔT 4 were preserved in older men for both type I and IIa fibers despite a reduction in T 0. Therefore, the age-related preservation of the tension increments after a quick stretch in single muscle fibers could explain in part the smaller decrease in force during eccentric contractions compared to isometric and concentric conditions in vivo with aging usually observed.

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References

  1. Alnaqueeb MA, Goldspink G (1986) Changes in fiber type number and diameter in developing and aging skeletal muscle. J Anat 153:31–45

    Google Scholar 

  2. Andruchov O, Andruchova O, Wang Y, Galler S (2005) Kinetic properties of myosin heavy chain isoforms in mouse skeletal muscle: comparison with rat, rabbit, and human and correlation with amino acid sequence. Am J Physiol Cell Physiol 287:1725–1732

    Article  CAS  Google Scholar 

  3. Bagni MA, Cecchi G, Colomo F, Poggesi C (1990) Tension and stiffness of frog muscle fibres at full filament overlap. J Muscle Res Cell Motil 11:371–377

    Article  PubMed  CAS  Google Scholar 

  4. Bergstrom J (1962) Muscle electrolytes in man. Scand J Clin Lab Invest 14(Suppl 68):1–110

    Google Scholar 

  5. D’Antona G, Pellegrino MA, Adami R, Rossi R, Carlizzi CN, Canepari M, Saltin B, Bottinelli R (2003) The effect of ageing and immobilization on structure and function of human skeletal muscle fibres. J Physiol 552:499–511

    Article  PubMed  CAS  Google Scholar 

  6. Doherty TJ (2003) Invited review: aging and sarcopenia. J Appl Physiol 95:1717–1727

    PubMed  CAS  Google Scholar 

  7. Evans WJ, Phinney SD, Young VR (1982) Suction applied to a muscle biopsy maximizes sample size. Med Sci Sports Exerc 14:101–102

    PubMed  CAS  Google Scholar 

  8. Fabiato A (1988) Computer programs for calculating total from specified free or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. Methods Enzymol 157:378–417

    Article  PubMed  CAS  Google Scholar 

  9. Frontera WR, Suh D, Krivickas LS, Hughes VA, Goldstein R, Roubenoff R (2000) Skeletal muscle fibre quality in older men and women. Am J Physiol Cell Physiol 279:611–618

    Google Scholar 

  10. Galler S, Schmitt T, Hilber K, Pette D (1997) Stretch activation and isoforms of myosin heavy chain and troponin T of rat skeletal muscle fibres. J Muscle Res Cell Motil 18:555–561

    Article  PubMed  CAS  Google Scholar 

  11. Hilber K, Galler S, Gohlsch B, Pette D (1999) Kinetic properties of myosin heavy chain isoforms in single fibers from human skeletal muscle. FEBS Lett 455:267–270

    Article  PubMed  CAS  Google Scholar 

  12. Hortobagyi T, Zheng D, Weidner M, Lambert N, Westbrook S, Houmard JA (1995) The influence of aging on muscle strength and muscle fiber characteristics with special reference to eccentric strength. J Gerontol A Biol Sci Med Sci 6:399–406

    Google Scholar 

  13. Huxley AF, Simmons RM (1971) Proposed mechanism of force generation in striated muscle. Nature 233:533–538

    Article  PubMed  CAS  Google Scholar 

  14. Kent-Braun JA, Ng VA, Young K (2000) Skeletal muscle contractile and non contractile components in young and older women and men. J Appl Physiol 88:662–668

    PubMed  CAS  Google Scholar 

  15. Klass M, Baudry S, Duchateau J (2005) Aging does not affect voluntary activation of the ankle dorsiflexors during isometric, concentric, and eccentric contractions. J Appl Physiol 99:31–38

    Article  PubMed  Google Scholar 

  16. Krivickas LS, Suh D, Wilkins J, Hughes VA, Roubenoff R, Frontera WR (2001) Age- and gender-related differences in maximum shortening velocity of skeletal muscle fibres. Am J Phys Med Rehabil 80:447–455

    Article  PubMed  CAS  Google Scholar 

  17. Larsson L, Moss RL (1993) Maximum velocity of shortening in relation to myosin isoform composition in single fibres from human skeletal muscles. J Physiol 472:595–614

    PubMed  CAS  Google Scholar 

  18. Larsson L, Li X, Yu F, Degens H (1997) Age-related changes in contractile properties and expression of myosin isoforms in single skeletal muscle cells. Muscle Nerve 5:74–78

    Article  Google Scholar 

  19. Lexell J, Downham DY (1991) The occurrence of fibre-type grouping in healthy human muscle: a quantitative study of cross-sections of whole vastus lateralis from men between the age of 15 and 83 years. Acta Neuropathol (Berl) 81:377–381

    Article  CAS  Google Scholar 

  20. Linari M, Reedy MK, Reedy MC, Lombardi V, Piazzesi G (2004) Ca-activation and stretch-activation in insect flight muscle. Biophys J 87:1101–1111

    Article  PubMed  CAS  Google Scholar 

  21. Linari M, Bottinelli R, Pellegrino MA, Reconditi M, Reggiani C, Lombardi V (2004) The mechanism of the force response to stretch in human skinned muscle fibres with different myosin isoforms. J Physiol 554:335–352

    Article  PubMed  CAS  Google Scholar 

  22. Liu J, Reedy MC, Goldman YE, Franzini-Armstrong C, Sasaki H, Tregear RT, Lucaveche C, Winkler H, Baumann BA, Squire JM, Irving TC, Reedy MK, Taylor KA (2004) Electron tomography of fast frozen, stretched rigor fibers reveals elastic distortions in the myosin crossbridges. J Struct Biol 147:268–282

    Article  PubMed  CAS  Google Scholar 

  23. Lowe DA, Surek JT, Thomas DD, Thompson LV (2001) Electron paramagnetic resonance reveals age-related myosin structural changes in rat skeletal muscle fibres. Am J Physiol Cell Physiol 280:540–547

    Google Scholar 

  24. Macaluso A, De Vito G (2004) Muscle strength, power and adaptations to resistance training in older people. Eur J Appl Physiol 91:450–472

    Article  PubMed  Google Scholar 

  25. Moss RL (1979) Sarcomere length–tension relations of frog skinned muscle fibres during calcium activation at short lengths. J Physiol 292:177–192

    PubMed  CAS  Google Scholar 

  26. Porter MM, Vandervoort AA, Lexell J (1995) Aging of human muscle: structure, function and adaptability. Scand J Med Sci Sports 5:129–142

    Article  PubMed  CAS  Google Scholar 

  27. Porter MM, Vandervoort AA, Kramer JF (1997) Eccentric peak torque of plantar and dorsiflexors is maintained in older women. J Gerontol A Biol Sci Med Sci 52:125–131

    Google Scholar 

  28. Pousson M, Lepers R, Van Hoecke J (2001) Changes in isokinetic torque and muscular activity of elbow flexors muscles with age. Exp Gerontol 36:1687–1698

    Article  PubMed  CAS  Google Scholar 

  29. Rassier DE, Herzog W (2005) Relationship between force and stiffness in muscle fibers after stretch. J Appl Physiol 99:1769–1775

    Article  PubMed  Google Scholar 

  30. Rice CL, Cunningham DA, Paterson D, Lefcoe MS (1989) Arm and leg composition determined by computed tomography in young and elderly men. Clin Physiol 9:207–220

    Article  PubMed  CAS  Google Scholar 

  31. Roos MR, Rice CL, Connelly DM, Vandervoort AA (1999) Quadriceps muscle strength, contractile properties, and motor unit firing rates in young and old men. Muscle Nerve 22:1094–1103

    Article  PubMed  CAS  Google Scholar 

  32. Trappe S, Gallagher P, Harber M, Carrithers J, Fluckey J, Trappe T (2003) Single muscle fibre contractile properties in young and old men and women. J Physiol 552:47–58

    Article  PubMed  CAS  Google Scholar 

  33. Vandervoort AA, Kramer JF, Wharram ER (1990) Eccentric knee strength of elderly females. J Gerontol 45:125–128

    Google Scholar 

  34. White DC (1983) The elasticity of relaxed insect fibrillar flight muscle. J Physiol 343:31–57

    PubMed  CAS  Google Scholar 

  35. Wood DS, Zollman J, Reuben JP (1975) Human skeletal muscle: properties of the “chemically skinned” fiber. Science 187:1075–1076

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The authors gratefully acknowledge Dr. Stefan Galler (Department of Cell Biology, University of Salzburg, Austria) for his valuable suggestions in refining the methods. The authors also wish to thank Gomathi Krishnan and Andreas Johansson for their valuable help with experiments. This work was supported by grants from the National Institute of Health (#AG18844-01).

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Correspondence to Julien Ochala.

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An erratum to this article can be found at http://dx.doi.org/10.1007/s00424-006-0167-1

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Ochala, J., Dorer, D.J., Frontera, W.R. et al. Single skeletal muscle fiber behavior after a quick stretch in young and older men: a possible explanation of the relative preservation of eccentric force in old age. Pflugers Arch - Eur J Physiol 452, 464–470 (2006). https://doi.org/10.1007/s00424-006-0065-6

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  • DOI: https://doi.org/10.1007/s00424-006-0065-6

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