Long-term high-level exercise promotes muscle reinnervation with age

Journal of Neuropathology and Experimental Neurology

Volumn 73, Issue 4, 2014, Pages 284-294

  Mosole, Simone ^a   Carraro, Ugo ^a   Kern, Helmut ^b,c   Loefler, Stefan ^b   Fruhmann, Hannah ^b   Vogelauer, Michael ^c   Burggraf, Samantha ^b   Mayr, Winfried ^d   Krenn, Matthias ^d   Paternostro Sluga, Tatjana ^d   Hamar, Dusan ^e   Cvecka, Jan ^e   Sedliak, Milan ^e   Tirpakova, Veronika ^e   Sarabon, Nejc ^f   Musarò, Antonio ^g   Sandri, Marco ^a   Protasi, Feliciano ^h   Nori, Alessandra ^a   Pond, Amber ⁱ   Zampieri, Sandra ^a,b   more..

^a UNIVERSITY OF PADOVA   (Italy)

^b LUDWIG BOLTZMANN INSTITUTE FOR LUNG VASCULAR RESEARCH   (Austria)

^c WILHELMINEN HOSPITAL   (Austria)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

^e Faculty of Natural Sciences   (Slovakia)

^f UNIVERSITY OF PRIMORSKA   (Slovenia)

^g SAPIENZA UNIVERSITY OF ROME   (Italy)

^h UNIVERSITY OF CHIETI   (Italy)

ⁱ SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Coexpression of fast and slow myosin heavy chains; Denervation and reinnervation; Fiber type grouping; Human skeletal muscle; Recreational sport activity

Indexed keywords

MYOSIN HEAVY CHAIN;

ADULT; AGED; AGING; ARTICLE; COMPARATIVE STUDY; DEMOGRAPHY; EXERCISE; FAST MUSCLE FIBER; FUNCTIONAL MORPHOLOGY; GROUPS BY AGE; HUMAN; HUMAN EXPERIMENT; KNEE; MALE; MUSCLE BIOPSY; MUSCLE CELL; MUSCLE DENERVATION; MUSCLE FUNCTION; MUSCLE INNERVATION; MUSCLE REINNERVATION; MUSCLE STRENGTH; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECREATION; SEDENTARY LIFESTYLE; SLOW MUSCLE FIBER; ULTRASTRUCTURE; YOUNG ADULT;

ADULT; AGED; AGING; ANALYSIS OF VARIANCE; BIOPSY; EXERCISE; FEMALE; HUMANS; LAMININ; MALE; MOTOR ACTIVITY; MUSCLE FIBERS, SKELETAL; MUSCLE STRENGTH; MYOSIN HEAVY CHAINS; MYOSIN LIGHT CHAINS; NERVE REGENERATION; NEURAL CELL ADHESION MOLECULES; QUADRICEPS MUSCLE; YOUNG ADULT;

EID: 84897446849     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0000000000000032     Document Type: Article

References (56)

1. Morrison JH, Baxter MG. The ageing cortical synapse: Hallmarks and implications for cognitive decline. Nat Rev Neurosci 2012;13:240-50
2. Small SA, Schobel SA, Buxton RB, et al. A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat Rev Neurosci 2011;12:585-601
3. Balistreri CR, Candore G, Accardi G, et al. NF-JB pathway activators as potential ageing biomarkers: Targets for new therapeutic strategies. Immun Ageing 2013;10:24
4. Erickson KI, Voss MW, Prakash RS, et al. Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci USA 2011;108:3017-22
5. Aagaard P, Suetta C, Caserotti P, et al. Role of the nervous system in sarcopenia and muscle atrophy with aging: Strength training as a countermeasure. Scand J Med Sci Sports 2010;20:49-64
6. Ohlendieck K. Proteomic profiling of fast-To-slow muscle transitions during aging. Front Physiol 2011;2:105-
7. Gutmann E,Hanzlikova V.Motor unit in old age. Nature 1966;209:921-22
8. Tomlinson BE, Walton JN, Rebeiz JJ. The effects of ageing and of cachexia upon skeletal muscle. A histopathological study. J Neurol Sci 1969;9:321-46
9. Scelsi R, Marchetti C, Poggi P. Histochemical and ultrastructural aspects of m. vastus lateralis in sedentary old people (aged 65-89 years). Acta Neuropathol 1980;51:99-105
10. Urbanchek MG, Picken EB, Kalliainen LK, et al. Specific force deficit in skeletal muscles of old rats is partially explained by the existence of denervated muscle fibers. J Gerontol A Biol Sci Med Sci 2001;56: B191-97
11. Rowan SL, Rygiel K, Purves-Smith FM, et al. Denervation causes fiber atrophy and myosin heavy chain co-expression in senescent skeletal muscle. PLoS ONE 2012;7:e29082
12. Tomlinson BE, Irving D. The numbers of limb motor neurons in the human lumbosacral cord throughout life. J Neurol Sci 1977;34:213-19
13. Doherty TJ, Vandervoort AA, Taylor AW, et al. Effects of motor unit losses on strength in older men and women. J Appl Physiol 1993;74: 868-74
14. Larsson LX. Motor units: Remodeling in aged animals. J Gerontol A Biol Sci Med Sci 1993;50:91-95
15. Andersen JL. Muscle fibre type adaptation in the elderly human muscle. Scand J Med Sci Sports 2003;13:40-47
16. Luff AR. Age-Associated changes in the innervation of muscle fibers and changes in the mechanical properties of motor units. Ann N Y Acad Sci 1998;854:92-101
17. Mitchell WK, Williams J, Atherton P, et al. Sarcopenia, dynapenia, and the impact of advancing age on human skeletal muscle size and strength: A quantitative review. Front Physiol 2012;3:260
18. Zhou MY, Klitgaard H, Saltin B, et al. Myosin heavy chain isoforms of human muscle after short-Term spaceflight. J Appl Physiol 1995;78: 1740-44
19. Schiaffino S, Reggiani C. Fiber types in mammalian skeletal muscles. Physiol Rev 2011;91:1447-531
20. Kern H, Hofer C, Modlin M, et al. Stable muscle atrophy in long-Term paraplegics with complete upper motor neuron lesion from 3-To 20-year SCI. Spinal Cord 2008;46:293-304
21. Kern H, Carraro U, Adami N, et al. Home-based functional electrical stimulation rescues permanently denervated muscles in paraplegic patients with complete lower motor neuron lesion. Neurorehabil Neural Repair 2010;24:709-21
22. D'Antona G, Pellegrino MA, Adami R, et al. The effect of ageing and immobilization on structure and function of human skeletal muscle fibres. J Physiol (Lond) 2003;552:499-511
23. Carraro U, Catani C, Belluco S, et al. Slow-like electrostimulation switches on slow myosin in denervated fast muscle. Exp Neurol 1986;94: 537-53
24. Carraro U. Modulation of trophism and fiber type expression of denervated muscle by different patterns of electrical stimulation. Basic Appl Myol 2002;12:263-73
25. Mayne CN, Mokrusch T, Jarvis JC, et al. Stimulation-induced expression of slow muscle myosin in a fast muscle of the rat. Evidence of an unrestricted adaptive capacity. FEBS Lett 1993;327:297-300
26. Salmons S. Exercise, stimulation and type transformation of skeletal muscle. Int J Sports Med 1994;15:136-41
27. Midrio M. The denervated muscle: Facts and hypotheses. A historical review. Eur J Appl Physiol 2006;98:1-21
28. Meltzer DE. Age dependence of Olympic weightlifting ability. Med Sci Sports Exerc 1994;26:1053-67
29. McNeil CJ, Doherty TJ, Stashuk DW. Motor unit number estimates in the tibialis anterior muscle of young, old, and very old men. Muscle Nerve 2005;31:461-67
30. Leyk D, Ruther T, Wunderlich M, et al. Physical performance in middle age and old age: Good news for our sedentary and aging society. Dtsch Arztebl Int 2010;107:809-16
31. Wroblewski AP, Amati F, Smiley MA, et al. Chronic exercise preserves lean muscle mass in masters athletes. Phys Sportsmed 2011;39:172-78
32. Lexell J, Downham DY. The occurrence of fiber-Type grouping in healthy human muscle: A quantitative study of cross-sections of whole vastus lateralis from men between 15 and 83 years. Acta Neuropathol (Berl) 1991;81:377-81
33. Sunnerhagen KS, Grimby G. Muscular effects in late polio. Acta Physiol Scand 2001;171:335-40
34. Vetter C, Reichmann H, Pette D. Microphotometric determination of enzyme activities in type-grouped fibres of reinnervated rat muscle. Histochemistry 1984;80:347-51
35. Coggan AR, Spina RJ, Rogers MA, et al. Histochemical and enzymatic characteristics of skeletal muscle in master athletes. J Appl Physiol 1990; 68:1896-901
36. Trappe S. Master athletes. Int J Sport Nutr Exerc Metab 2001;11: S196-207
37. Wright VJ, Perricelli BC. Age-related rates of decline in performance among elite senior athletes. Am J Sports Med 2008;36:443-50
38. Mosole S, Rossini K, Kern H, et al. Significant increase of vastus lateralis reinnervation in 70-year sportsmen with a lifelong history of high-level exercise. Eur J Transl Myol Basic Appl Myol 2013;23:117-22
39. Zampieri S, Rossini K, Carrao U, et al. Morphometry of skeletal muscle in sedentary elderly and senior sportsmen. Eur J Transl Myol Basic Appl Myol 2012;22:13
40. Kern H, Loefler S, Burggraf S, et al. Electrical stimulation counteracts muscle atrophy associated with aging in humans. Eur J Transl Myol Basic Appl Myol 2013;23:105-8
41. Boncompagni S, d'Amelio L, Fulle S, et al. Progressive disorganization of the excitation-contraction coupling apparatus in aging human skeletal muscle as revealed by electron microscopy: A possible role in the decline of muscle performance. J Gerontol A Biol Sci Med Sci 2006;61: 995-1008
42. Rossini K, Zanin ME, Podhorska-Okolow M, et al. To stage and quantify regenerative myogenesis in human long-Term permanent denervated muscle. Basic Appl Myol 2002;12:277-86
43. Boncompagni S, Kern H, Rossini K, et al. Structural differentiation of skeletal muscle fibers in the absence of innervation in humans. Proc Natl Acad Sci USA 2007;104:19339-44
44. Zampieri S, Valente M, Adami N, et al. Polymyositis, dermatomyositis and malignancy: A further intriguing link. Autoimmun Rev 2010;9: 449-53
45. Zampieri S, Doria A, Adami N, et al. Subclinical myopathy in patients affected with newly diagnosed colorectal cancer at clinical onset of disease: Evidence from skeletal muscle biopsies. Neurol Res 2010;32:20-25
46. Kern H, Boncompagni S, Rossini K, et al. Long-Term denervation in humans causes degeneration of both contractile and excitation-contraction coupling apparatus that can be reversed by functional electrical stimulation (FES). A role for myofiber regeneration? J Neuropathol Exp Neurol 2004;63:919-31
47. Kern H, Carraro U, Adami N, et al. One year of home-based daily FES in complete lower motor neuron paraplegia: Recovery of tetanic contractility drives the structural improvements of denervated muscle. Neurol Res 2010;32:5-12
48. Dickson G, Gower HJ, Barton CH, et al. Human muscle neural cell adhesion molecule (N-CAM): Identification of a muscle-specific sequence in the extracellular domain. Cell 1987;50:1119-30
49. Kern H, Pelosi L, Coletto L, et al. Atrophy/hypertrophy cell signaling in muscles of young athletes trained with vibrational-proprioceptive stimulation. Neurol Res 2011;33:998-1009
50. Gava P, Kern H, Carraro U. Age-related decline of muscle power in track and field master athletes indicates a lifespan of 110 years. Eur J Transl Myol Basic Appl Myol 2013;23:45
51. Carraro U, Catani C, Biral D. Selective maintenance of neurotrophically regulated proteins in denervated rat diaphragm. Exp Neurol 1979;63: 468-75
52. Carraro U, Catani C, Dalla Libera L. Myosin light and heavy chains in rat gastrocnemius and diaphragm muscles after chronic denervation or reinnervation. Exp Neurol 1981;72:401-12
53. Pette D, Vrbová G. What does chronic electrical stimulation teach us about muscle plasticity? Muscle Nerve 1999;22:666-77
54. Henneman E, Somjen G, Carpenter DO. Functional significance of cell size in spinal motoneurons. J Neurophysiol 1965;28:560-80
55. Herrera-Rincon C, Torets C, Sanchez-Jimenez A, et al. Chronic electrical stimulation of transected peripheral nerves preserves anatomy and function in the primary somatosensory cortex. Eur J Neurosci 2012;36: 3679-90
56. Wang XH, Mitch WE. Muscle wasting from kidney failureVA model for catabolic conditions. Int J Biochem Cell Biol 2013;45:2230-38