Single muscle fiber properties in aging and disuse

Scandinavian Journal of Medicine and Science in Sports

Volumn 20, Issue 1, 2010, Pages 10-19

  Canepari, M ^a   Pellegrino, M A ^a   D'Antona, G ^a   Bottinelli, R ^a  

^a UNIVERSITY OF PAVIA   (Italy)

Author keywords

Aging; Disuse; Muscle fibers; Myosin isoforms

Indexed keywords

ISOPROTEIN; MYOSIN; MYOSIN HEAVY CHAIN;

ADAPTATION; AGING; EXERCISE; HUMAN; METABOLISM; MUSCLE CONTRACTION; PHYSIOLOGY; RESISTANCE TRAINING; REVIEW; SKELETAL MUSCLE;

ADAPTATION, PHYSIOLOGICAL; AGING; EXERCISE; HUMANS; MUSCLE CONTRACTION; MUSCLE FIBERS, SKELETAL; MYOSIN HEAVY CHAINS; MYOSINS; PROTEIN ISOFORMS; RESISTANCE TRAINING;

EID: 75649122204     PISSN: 09057188     EISSN: 16000838     Source Type: Journal    
DOI: 10.1111/j.1600-0838.2009.00965.x     Document Type: Review

References (76)

1. Alkner BA, Tesch PA. Efficacy of a gravity-independent resistance exercise device as a countermeasure to muscle atrophy during 29-day bed rest. Acta Physiol Scand 2004 : 181 : 345 357.
2. Aoyagi Y, Shephard RJ. Aging and muscle function. Sports Med 1992 : 14 : 376 396.
3. Berg HE, Larsson L, Tesch PA. Lower limb skeletal muscle function after 6 wk of bed rest. J Appl Physiol 1997 : 82 : 182 188.
4. Bottinelli R. Functional heterogeneity of mammalian single muscle fibres: do myosin isoforms tell the whole story? Pflugers Arch 2001 : 443 : 6 17.
5. 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 1994a : 478 (Part 2) : 341 349. (Pubitemid 24232204)
6. Bottinelli R, Canepari M, Pellegrino MA, Reggiani C. Force-velocity properties of human skeletal muscle fibres: myosin heavy chain isoform and temperature dependence. J Physiol 1996 : 495 (Part 2) : 573 586.
7. Bottinelli R, Canepari M, Reggiani C, Stienen GJ. Myofibrillar ATPase activity during isometric contraction and isomyosin composition in rat single skinned muscle fibres. J Physiol (London) 1994b : 481 : 663 675.
8. 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 : 429 : 592 594.
9. Bottinelli R, Reggiani C. Human skeletal muscle fibres: molecular and functional diversity. Prog Biophys Mol Biol 2000 : 73 : 195 262.
10. Bottinelli R, Schiaffino S, Reggiani C. Force-velocity relations and myosin heavy chain isoform compositions of skinned fibres from rat skeletal muscle. J Physiol (London) 1991 : 437 : 655 672.
11. Bruce SA, Newton D, Woledge RC. Effect of age on voluntary force and cross-sectional area of human adductor pollicis muscle. Q J Exp Physiol 1989 : 74 : 359 362.
12. Campbell MJ, McComas AJ, Petito F Physiological changes in ageing muscles. J Neurol Neurosurg Psychiatry 1973 : 36 : 174 182.
13. Canepari M, Rossi R, Pellegrino MA, Bottinelli R, Schiaffino S, Reggiani C. Functional diversity between orthologous myosins with minimal sequence diversity. J Muscle Res Cell Motil 2000 : 21 : 375 382.
14. Canepari M, Rossi R, Pellegrino MA, Orrell RW, Cobbold M, Harridge S, Bottinelli R. Effects of resistance training on myosin function studied by the in vitro motility assay in young and older men. J Appl Physiol 2005 : 98 : 2390 2395.
15. Canepari M, Rossi R, Pellegrino MA, Reggiani C, Bottinelli R. Speeds of actin translocation in vitro by myosins extracted from single rat muscle fibres of different types. Exp Physiol 1999 : 84 : 803 806.
16. Coirault C, Guellich A, Barbry T, Samuel JL, Riou B, Lecarpentier Y. Oxidative stress of myosin contributes to skeletal muscle dysfunction in rats with chronic heart failure. Am J Physiol Heart Circ Physiol 2007 : 292 : H1009 H1017.
17. D'Antona G, Brocca L, Pansarasa O, Rinaldi C, Tupler R, Bottinelli R. Structural and functional alterations of muscle fibres in the novel mouse model of facioscapulohumeral muscular dystrophy. J Physiol 2007a : 584 : 997 1009.
18. D'Antona G, Lanfranconi F, Pellegrino MA, Brocca L, Adami R, Rossi R, Moro G, Miotti D, Canepari M, Bottinelli R. Skeletal muscle hypertrophy and structure and function of skeletal muscle fibres in male body builders. J Physiol 2006 : 570 : 611 627.
19. D'Antona G, Pellegrino MA, Adami R, Rossi R, Carlizzi CN, Canepari M, Saltin B, Bottinelli R. The effect of ageing and immobilization on structure and function of human skeletal muscle fibres. J Physiol 2003 : 552 : 499 511.
20. D'Antona G, Pellegrino MA, Carlizzi CN, Bottinelli R. Deterioration of contractile properties of muscle fibres in elderly subjects is modulated by the level of physical activity. Eur J Appl Physiol 2007 : 100 : 603 611.
21. de Boer MD, Seynnes OR, di Prampero PE, Pisot R, Mekjavic IB, Biolo G, Narici MV. Effect of 5 weeks horizontal bed rest on human muscle thickness and architecture of weight bearing and non-weight bearing muscles. Eur J Appl Physiol 2008 : 104 : 401 407.
22. di Prampero PE, Narici MV. Muscles in microgravity: from fibres to human motion. J Biomech 2003 : 36 : 403 412.
23. Edgerton VR, Zhou MY, Ohira Y, Klitgaard H, Jiang B, Bell G, Harris B, Saltin B, Gollnick PD, Roy RR, Day MK, Greenisen M. Human fiber size and enzymatic properties after 5 and 11 days of spaceflight. J Appl Physiol 1995 : 78 : 1733 1739.
24. Fitts RH, Riley DR, Widrick JJ. Functional and structural adaptations of skeletal muscle to microgravity. J Exp Biol 2001 : 204 : 3201 3208.
25. Fluck M, Hoppeler H. Molecular basis of skeletal muscle plasticity-from gene to form and function. Rev Physiol Biochem Pharmacol 2003 : 146 : 159 216.
26. Ford LE, Nakagawa K, Desper J, Seow CY. Effect of osmotic compression on the force-velocity properties of glycerinated rabbit skeletal muscle cells. J Gen Physiol 1991 : 97 : 73 88.
27. Frontera WR, Reid KF, Phillips EM, Krivickas LS, Hughes VA, Roubenoff R, Fielding RA. Muscle fiber size and function in elderly humans: a longitudinal study. J Appl Physiol 2008 : 105 : 637 642.
28. Frontera WR, Suh D, Krivickas LS, Hughes VA, Goldstein R, Roubenoff R. Skeletal muscle fiber quality in older men and women. Am J Physiol Cell Physiol 2000 : 279 : C611 C618.
29. Harber MP, Gallagher PM, Creer AR, Minchev KM, Trappe SW. Single muscle fiber contractile properties during a competitive season in male runners. Am J Physiol Regul Integr Comp Physiol 2004 : 287 : R1124 1131.
30. Haus JM, Carrithers JA, Trappe SW, Trappe TA. Collagen, cross-linking, and advanced glycation end products in aging human skeletal muscle. J Appl Physiol 2007 : 103 : 2068 2076.
31. Hook P, Li X, Sleep J, Hughes S, Larsson L. In vitro motility speed of slow myosin extracted from single soleus fibres from young and old rats. J Physiol (London) 1999 : 520 (Part 2) : 463 471. (Pubitemid 29511910)
32. Hook P, Sriramoju V, Larsson L. Effects of aging on actin sliding speed on myosin from single skeletal muscle cells of mice, rats, and humans. Am J Physiol Cell Physiol 2001 : 280 : C782 C788.
33. Hortobagyi T, Dempsey L, Fraser D, Zheng D, Hamilton G, Lambert J, Dohm L. Changes in muscle strength, muscle fibre size and myofibrillar gene expression after immobilization and retraining in humans. J Physiol 2000 : 524 (Part 1) : 293 304.
34. Klein CS, Rice CL, Marsh GD. Normalized force, activation, and coactivation in the arm muscles of young and old men. J Appl Physiol 2001 : 91 : 1341 1349.
35. Klitgaard H, Zhou M, Schiaffino S, Betto R, Salviati G, Saltin B. Ageing alters the myosin heavy chain composition of single fibres from human skeletal muscle. Acta Physiol Scand 1990 : 140 : 55 62. (Pubitemid 20281050)
36. Kron SJ, Spudich JA. Fluorescent actin filaments move on myosin fixed to a glass surface. Proc Natl Acad Sci USA 1986 : 83 : 6272 6276.
37. Larsson L, Li X, Berg HE, Frontera WR. Effects of removal of weight-bearing function on contractility and myosin isoform composition in single human skeletal muscle cells. Pflugers Arch 1996 : 432 : 320 328.
38. Larsson L, Li X, Frontera WR. Effects of aging on shortening velocity and myosin isoform composition in single human skeletal muscle cells. Am J Physiol 1997 : 272 : C638 C649.
39. LeBlanc A, Rowe R, Schneider V, Evans H, Hedrick T. Regional muscle loss after short duration spaceflight. Aviat Space Environ Med 1995 : 66 : 1151 1154.
40. Lexell J. Human aging, muscle mass, and fiber type composition. J Gerontol A Biol Sci Med Sci 1995 : 50 (Spec No) : 11 16.
41. Lowe DA, Surek JT, Thomas DD, Thompson LV. Electron paramagnetic resonance reveals age-related myosin structural changes in rat skeletal muscle fibers. Am J Physiol Cell Physiol 2001 : 280 : C540 C547.
42. Magnusson SP, Narici MV, Maganaris CN, Kjaer M. Human tendon behaviour and adaptation, in vivo. J Physiol 2008 : 586 : 71 81.
43. Metzger JM, Moss RL. Shortening velocity in skinned single muscle fibers. Influence of filament lattice spacing. Biophys J 1987 : 52 : 127 131.
44. Narici MV, Maganaris CN. Plasticity of the muscle-tendon complex with disuse and aging. Exerc Sport Sci Rev 2007 : 35 : 126 134.
45. Narici MV, Maganaris CN, Reeves ND, Capodaglio P. Effect of aging on human muscle architecture. J Appl Physiol 2003 : 95 : 2229 2234.
46. Narici MV, Reeves ND, Morse CI, Maganaris CN. Muscular adaptations to resistance exercise in the elderly. J Musculoskelet Neuronal Interact 2004 : 4 : 161 164.
47. Pansarasa O, Rinaldi C, Parente V, Miotti D, Capodaglio P, Bottinelli R. Resistance training of long duration modulates force and unloaded shortening velocity of single muscle fibres of young women. J Electromyogr Kinesiol 2009 : 19 : e290 300.
48. Parente V, D'Antona G, Adami R, Miotti D, Capodaglio P, De Vito G, Bottinelli R. Long-term resistance training improves force and unloaded shortening velocity of single muscle fibres of elderly women. Eur J Appl Physiol 2008 : 104 : 885 893.
49. Pette D, Staron RS. Cellular and molecular diversities of mammalian skeletal muscle fibers. Rev Physiol Biochem Pharmacol 1990 : 116 : 1 76.
50. Ramamurthy B, Hook P, Jones AD, Larsson L. Changes in myosin structure and function in response to glycation. FASEB J 2001 : 15 : 2415 2422.
51. Renganathan M, Messi ML, Delbono O. Dihydropyridine receptor-ryanodine receptor uncoupling in aged skeletal muscle. J Membr Biol 1997 : 157 : 247 253.
52. Riley DA, Bain JL, Thompson JL, Fitts RH, Widrick JJ, Trappe SW, Trappe TA, Costill DL. Disproportionate loss of thin filaments in human soleus muscle after 17-day bed rest. Muscle Nerve 1998 : 21 : 1280 1289.
53. Round JM, Barr FM, Moffat B, Jones DA. Fibre areas and histochemical fibre types in the quadriceps muscle of paraplegic subjects. J Neurol Sci 1993 : 116 : 207 211.
54. Sampaolesi M, Blot S, D'Antona G, Granger N, Tonlorenzi R, Innocenzi A, Mognol P, Thibaud JL, Galvez BG, Barthelemy I, Perani L, Mantero S, Guttinger M, Pansarasa O, Rinaldi C, Cusella De Angelis MG, Torrente Y, Bordignon C, Bottinelli R, Cossu G. Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 2006 : 444 : 574 579.
55. Sampaolesi M, Torrente Y, Innocenzi A, Tonlorenzi R, D'Antona G, Pellegrino MA, Barresi R, Bresolin N, De Angelis MG, Campbell KP, Bottinelli R, Cossu G. Cell therapy of alpha-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science 2003 : 301 : 487 492.
56. Schiaffino S, Reggiani C. Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol Rev 1996 : 76 : 371 423.
57. Shoepe TC, Stelzer JE, Garner DP, Widrick JJ. Functional adaptability of muscle fibers to long-term resistance exercise. Med Sci Sports Exerc 2003 : 35 : 944 951.
58. Smerdu V, Karsch-Mizrachi I, Campione M, Leinwand L, Schiaffino S. Type IIx myosin heavy chain transcripts are expressed in type IIb fibers of human skeletal muscle. Am J Physiol 1994 : 267 : C1723 C1728.
59. Stelzer JE, Widrick JJ. Effect of hindlimb suspension on the functional properties of slow and fast soleus fibers from three strains of mice. J Appl Physiol 2003 : 95 : 2425 2433.
60. Stienen GJ, Kiers JL, Bottinelli R, Reggiani C. Myofibrillar ATPase activity in skinned human skeletal muscle fibres: fibre type and temperature dependence. J Physiol 1996a : 493 (Part 2) : 299 307.
61. Stienen GJ, Kiers JL, Bottinelli R, Reggiani C. Myofibrillar ATPase activity in skinned human skeletal muscle fibres: fibre type and temperature dependence. J Physiol (London) 1996b : 493 : 299 307.
62. Trappe S, Costill D, Thomas R. Effect of swim taper on whole muscle and single muscle fiber contractile properties. Med Sci Sports Exerc 2000a : 32 : 48 56.
63. Trappe S, Gallagher P, Harber M, Carrithers J, Fluckey J, Trappe T. Single muscle fibre contractile properties in young and old men and women. J Physiol 2003 : 552 : 47 58.
64. Trappe S, Godard M, Gallagher P, Carroll C, Rowden G, Porter D. Resistance training improves single muscle fiber contractile function in older women. Am J Physiol Cell Physiol 2001 : 281 : C398 C406.
65. Trappe S, Harber M, Creer A, Gallagher P, Slivka D, Minchev K, Whitsett D. Single muscle fiber adaptations with marathon training. J Appl Physiol 2006 : 101 : 721 727.
66. Trappe S, Trappe T, Gallagher P, Harber M, Alkner B, Tesch P. Human single muscle fibre function with 84 day bed-rest and resistance exercise. J Physiol 2004 : 557 : 501 513.
67. Trappe S, Williamson D, Godard M, Porter D, Rowden G, Costill D. Effect of resistance training on single muscle fiber contractile function in older men. J Appl Physiol 2000b : 89 : 143 152.
68. Weiss A, Schiaffino S, Leinwand LA. Comparative sequence analysis of the complete human sarcomeric myosin heavy chain family: implications for functional diversity. J Mol Biol 1999 : 290 : 61 75.
69. Widrick JJ, Knuth ST, Norenberg KM, Romatowski JG, Bain JL, Riley DA, Karhanek M, Trappe SW, Trappe TA, Costill DL, Fitts RH. Effect of a 17 day spaceflight on contractile properties of human soleus muscle fibres. J Physiol 1999 : 516 (Part 3) : 915 930.
70. Widrick JJ, Romatowski JG, Bain JL, Trappe SW, Trappe TA, Thompson JL, Costill DL, Riley DA, Fitts RH. Effect of 17 days of bed rest on peak isometric force and unloaded shortening velocity of human soleus fibers. Am J Physiol 1997 : 273 : C1690 C1699.
71. Widrick JJ, Romatowski JG, Norenberg KM, Knuth ST, Bain JL, Riley DA, Trappe SW, Trappe TA, Costill DL, Fitts RH. Functional properties of slow and fast gastrocnemius muscle fibers after a 17-day spaceflight. J Appl Physiol 2001 : 90 : 2203 2211.
72. Widrick JJ, Stelzer JE, Shoepe TC, Garner DP. Functional properties of human muscle fibers after short-term resistance exercise training. Am J Physiol Regul Integr Comp Physiol 2002 : 283 : R408 R416.
73. Widrick JJ, Trappe SW, Blaser CA, Costill DL, Fitts RH. Isometric force and maximal shortening velocity of single muscle fibers from elite master runners. Am J Physiol 1996a : 271 : C666 C675.
74. Widrick JJ, Trappe SW, Costill DL, Fitts RH. Force-velocity and force-power properties of single muscle fibers from elite master runners and sedentary men. Am J Physiol 1996b : 271 : C676 C683.
75. Zhong S, Lowe DA, Thompson LV. Effects of hindlimb unweighting and aging on rat semimembranosus muscle and myosin. J Appl Physiol 2006 : 101 : 873 880.
76. Zhong S, Thompson LV. The roles of myosin ATPase activity and myosin light chain relative content in the slowing of type IIB fibers with hindlimb unweighting in rats. Am J Physiol Cell Physiol 2007 : 293 : C723 C728.