Control of Muscle Size During Disuse, Disease, and Aging

H. Degens; S. E. Alway

doi:10.1055/s-2005-837571

International Journal of Sports Medicine, Inhaltsverzeichnis

Int J Sports Med 2006; 27(2): 94-99
DOI: 10.1055/s-2005-837571

Physiology & Biochemistry

Control of Muscle Size During Disuse, Disease, and Aging

H. Degens¹ ^, ² , S. E. Alway³

¹Institute for Biophysical and Clinical Research into Human Movement, Manchester Metropolitan University, Alsager Campus, Alsager, Cheshire, UK
²Departments of Physiology & Pulmonary Diseases, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
³Laboratory of Muscle Biology & Sarcopenia, Division of Exercise Physiology, West Virginia University School of Medicine, Morgantown, WV, USA

Abstract

Skeletal muscle is a highly plastic tissue. For example, muscle hypertrophies during strength training and increases its oxidative capacity in response to endurance training. Conditions associated with disuse, however, are also accompanied by adaptations, of which atrophy and a slow-to-fast transition are most prominent. Fast and slow muscles respond differently to disuse. The different response of muscle to different models of disuse reveals that loading is most important, but that also activity level, neurotrophic factors, and ageing play a part in determining the mass, morphology, contractile properties, and fatigability of a muscle. Muscle loss during disuse is a result, at least in part, of apoptosis. Finally, skeletal muscle wasting and remodelling during ageing and chronic disorders, such as chronic heart failure and chronic obstructive pulmonary disease, are not entirely attributable to disuse, but are also related to secondary consequences of the disease, most notably inflammation. Besides activating other pathways, we present evidence that inflammation during ageing and chronic disorders causes muscle wasting via alterations in abundance and/or activity of muscle specific transcription factors and induction of apoptosis, and that systemic inflammation rather than disuse is the primary cause of muscle wasting during ageing and chronic disorders.

Key words

Disuse - ageing - COPD - CHF - apoptosis - inflammation

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References

1 Aboudrar S, Desplanches D, Graber-von Bergen F, Favier R, Okyayuz-Baklouti I, Hoppeler H. Effects of torbafylline on muscle atrophy: prevention and recovery. Can J Physiol Pharmacol. 1992; 70 814-820
2 Agusti A G, Sauleda J, Miralles C, Gomez C, Togores B, Sala E, Batle S, Busquets X. Skeletal muscle apoptosis and weight loss in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2002; 166 485-489
3 Alway S E. Attenuation of Ca(2 +)-activated ATPase and shortening velocity in hypertrophied fast twitch skeletal muscle from aged Japanese quail. Exp Gerontol. 2002; 37 665-678
4 Alway S E, Degens H, Krishnamurthy G, Chaudhrai A. Denervation stimulates apoptosis but not Id2 expression in hindlimb muscles of aged rats. J Gerontol A Biol Sci Med Sci. 2003; 58 687-697
5 Alway S E, Degens H, Krishnamurthy G, Smith C A. Potential role for Id myogenic repressors in apoptosis and attenuation of hypertrophy in muscles of aged rats. Am J Physiol Cell Physiol. 2002; 283 C66-76
6 Alway S E, Degens H, Lowe D A, Krishnamurthy G. Increased myogenic repressor Id mRNA and protein levels in hindlimb muscles of aged rats. Am J Physiol Regul Integr Comp Physiol. 2002; 282 R411-422
7 Alway S E, Martyn J K, Ouyang J, Chaudhrai A, Murlasits Z S. Id2 expression during apoptosis and satellite cell activation in unloaded and loaded quail skeletal muscles. Am J Physiol Regul Integr Comp Physiol. 2003; 284 R540-549
8 Benezra R. The Id proteins: targets for inhibiting tumor cells and their blood supply. Biochim Biophys Acta. 2001; 1551 F39-47
9 Bernard S, LeBlanc P, Whittom F, Carrier G, Jobin J, Belleau R, Maltais F. Peripheral muscle weakness in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1998; 158 629-634
10 Bey L, Akunuri N, Zhao P, Hoffman E P, Hamilton D G, Hamilton M T. Patterns of global gene expression in rat skeletal muscle during unloading and low-intensity ambulatory activity. Physiol Genomics. 2003; 13 157-167
11 Bloomfield S A. Changes in musculoskeletal structure and function with prolonged bed rest. Med Sci Sports Exerc. 1997; 29 197-206
12 Blough E R, Linderman J K. Lack of skeletal muscle hypertrophy in very aged male Fischer 344 × Brown Norway rats. J Appl Physiol. 2000; 88 1265-1270
13 Booth F W, Gordon S E, Carlson C J, Hamilton M T. Waging war on modern chronic diseases: primary prevention through exercise biology. J Appl Physiol. 2000; 88 774-787
14 Bruunsgaard H, Bjerregaard E, Schroll M, Pedersen B K. Muscle strength after resistance training is inversely correlated with baseline levels of soluble tumor necrosis factor receptors in the oldest old. J Am Geriatr Soc. 2004; 52 237-241
15 Buller A J, Eccles J C, Eccles R M. Interactions between motoneurones and muscles in respect of the characteristic speeds of their responses. J Physiol. 1960; 150 417-439
16 Carmeli E, Coleman R, Reznick A Z. The biochemistry of aging muscle. Exp Gerontol. 2002; 37 477-489
17 Charge S B, Brack A S, Hughes S M. Aging-related satellite cell differentiation defect occurs prematurely after Ski-induced muscle hypertrophy. Am J Physiol Cell Physiol. 2002; 283 C1228-1241
18 Debigare R, Cote C H, Maltais F. Peripheral Muscle Wasting in Chronic Obstructive Pulmonary Disease. Clinical relevance and mechanisms. Am J Respir Crit Care Med. 2001; 164 1712-1717
19 Degens H. Age-related changes in the microcirculation of skeletal muscle. Adv Exp Med Biol. 1998; 454 343-348
20 Degens H, Alway S E. Skeletal muscle function and hypertrophy are diminished in old age. Muscle Nerve. 2003; 27 339-347
21 Degens H, Anderson R K, Alway S E. Capillarization in skeletal muscle of rats with cardiac hypertrophy. Med Sci Sports Exerc. 2002; 34 258-266
22 Degens H, Veerkamp J H. Changes in oxidative capacity and fatigue resistance in skeletal muscle. Int J Biochem. 1994; 26 871-878
23 Degens H, Yu F, Li X, Larsson L. Effects of age and gender on shortening velocity and myosin isoforms in single rat muscle fibres. Acta Physiol Scand. 1998; 163 33-40
24 Duscha B D, Annex B H, Green H J, Pippen A M, Kraus W E. Deconditioning fails to explain peripheral skeletal muscle alterations in men with chronic heart failure. J Am Coll Cardiol. 2002; 39 1170-1174
25 Faucher M, Steinberg J G, Barbier D, Hug F, Jammes Y. Influence of chronic hypoxemia on peripheral muscle function and oxidative stress in humans. Clin Physiol Funct Imaging. 2004; 24 75-84
26 Fisher J S, Hasser E M, Brown M. Effects of ovariectomy and hindlimb unloading on skeletal muscle. J Appl Physiol. 1998; 85 1316-1321
27 Fitts R H, Riley D R, Widrick J J. Functional and structural adaptations of skeletal muscle to microgravity. J Exp Biol. 2001; 204 3201-3208
28 Florio M, Hernandez M C, Yang H, Shu H K, Cleveland J L, Israel M A. Id2 promotes apoptosis by a novel mechanism independent of dimerization to basic helix-loop-helix factors. Mol Cell Biol. 1998; 18 5435-5444
29 Fluckey J D, Dupont-Versteegden E E, Montague D C, Knox M, Tesch P, Peterson C A, Gaddy-Kurten D. A rat resistance exercise regimen attenuates losses of musculoskeletal mass during hindlimb suspension. Acta Physiol Scand. 2002; 176 293-300
30 Goldspink G, Scutt A, Martindale J, Jaenicke T, Turay L, Gerlach G F. Stretch and force generation induce rapid hypertrophy and myosin isoform gene switching in adult skeletal muscle. Biochem Soc Trans. 1991; 19 368-373
31 Gosker H R, Kubat B, Schaart G, van der Vusse G J, Wouters E F, Schols A M. Myopathological features in skeletal muscle of patients with chronic obstructive pulmonary disease. Eur Respir J. 2003; 22 280-285
32 Gosker H R, Lencer N H, Franssen F M, van der Vusse G J, Wouters E F, Schols A M. Striking similarities in systemic factors contributing to decreased exercise capacity in patients with severe chronic heart failure or COPD. Chest. 2003; 123 1416-1424
33 Gosker H R, Wouters E F, van der Vusse G J, Schols A M. Skeletal muscle dysfunction in chronic obstructive pulmonary disease and chronic heart failure: underlying mechanisms and therapy perspectives. Am J Clin Nutr. 2000; 71 1033-1047
34 Gosselink R, Decramer M. Peripheral skeletal muscles and exercise performance in patients with chronic obstructive pulmonary disease. Monaldi Arch Chest Dis. 1998; 53 419-423
35 Heijdra Y F, Pinto-Plata V, Frants R, Rassulo J, Kenney L, Celli B R. Muscle strength and exercise kinetics in COPD patients with a normal fat-free mass index are comparable to control subjects. Chest. 2003; 124 75-82
36 Hnik P, Bass A, Vejsada R, Mackova E V, Goldspink D F, Teisinger J, Kasicki S. Is maintained stretch another factor determining muscle status?. Rose FC, Jones R, Vrbova G Comprehensive Neurologic Rehabilitation. New York; Demos 1989: 15-26
37 Hoh J F. Myogenic regulation of mammalian skeletal muscle fibres. News Physiol Sci. 1991; 6 1-6
38 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. 1999; 520 463-471
39 Hussain S P, Amstad P, He P, Robles A, Lupold S, Kaneko I, Ichimiya M, Sengupta S, Mechanic L, Okamura S, Hofseth L J, Moake M, Nagashima M, Forrester K S, Harris C C. p53-induced up-regulation of MnSOD and GPx but not catalase increases oxidative stress and apoptosis. Cancer Res. 2004; 64 2350-2356
40 Isfort R J, Wang F, Greis K D, Sun Y, Keough T W, Farrar R P, Bodine S C, Anderson N L. Proteomic analysis of rat soleus muscle undergoing hindlimb suspension-induced atrophy and reweighting hypertrophy. Proteomics. 2002; 2 543-550
41 Jackman R W, Kandarian S C. The molecular basis of skeletal muscle atrophy. Am J Physiol Cell Physiol. 2004; 287 C834-843
42 Jin H, Wu Z, Tian T, Gu Y. Apoptosis in atrophic skeletal muscle induced by brachial plexus injury in rats. J Trauma. 2001; 50 31-35
43 Kano Y, Shimegi S, Takahashi H, Masuda K, Katsuta S. Changes in capillary luminal diameter in rat soleus muscle after hind- limb suspension. Acta Physiol Scand. 2000; 169 271-276
44 Langen R C, Van Der Velden J L, Schols A M, Kelders M C, Wouters E F, Janssen-Heininger Y M. Tumor necrosis factor-alpha inhibits myogenic differentiation through MyoD protein destabilization. Faseb J. 2004; 18 227-237
45 Larsen A I, Lindal S, Aukrust P, Toft I, Aarsland T, Dickstein K. Effect of exercise training on skeletal muscle fibre characteristics in men with chronic heart failure. Correlation between skeletal muscle alterations, cytokines and exercise capacity. Int J Cardiol. 2002; 83 25-32
46 Larsson L, Ansved T. Effects of ageing on the motor unit. Prog Neurobiol. 1995; 45 397-458
47 Larsson L, Li X, Berg H E, Frontera W R. 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
48 Larsson L, Li X, Frontera W R. Effects of aging on shortening velocity and myosin isoform composition in single human skeletal muscle cells. Am J Physiol. 1997; 272 C638-649
49 Larsson L, Li X, Yu F, Degens H. Age-related changes in contractile properties and expression of myosin isoforms in single skeletal muscle cells. Muscle Nerve. 1997; 5 (Suppl) S74-78
50 Lee H C, Wei Y H. Mitochondrial alterations, cellular response to oxidative stress and defective degradation of proteins in aging. Biogerontology. 2001; 2 231-244
51 Leeuwenburgh C. Role of apoptosis in sarcopenia. J Gerontol A Biol Sci Med Sci. 2003; 58 999-1001
52 Lewis D M, al-Amood W S, Schmalbruch H. Effects of long-term phasic electrical stimulation on denervated soleus muscle: guinea-pig contrasted with rat. J Muscle Res Cell Motil. 1997; 18 573-586
53 Lowe D A, Alway S E. Stretch-induced myogenin, MyoD, and MRF4 expression and acute hypertrophy in quail slow-tonic muscle are not dependent upon satellite cell proliferation. Cell Tissue Res. 1999; 296 531-539
54 Lowe D A, Surek J T, Thomas D D, Thompson L V. Electron paramagnetic resonance reveals age-related myosin structural changes in rat skeletal muscle fibers. Am J Physiol Cell Physiol. 2001; 280 C540-547
55 Lowe D A, Warren G L, Snow L M, Thompson L V, Thomas D D. Muscle activity and aging affect myosin structural distribution and force generation in rat fibers. J Appl Physiol. 2004; 96 498-506
56 Mador M J, Bozkanat E. Skeletal muscle dysfunction in chronic obstructive pulmonary disease. Respir Res. 2001; 2 216-224
57 Marcell T J, Harman S M, Urban R J, Metz D D, Rodgers B D, Blackman M R. Comparison of GH, IGF-I, and testosterone with mRNA of receptors and myostatin in skeletal muscle in older men. Am J Physiol Endocrinol Metab. 2001; 281 E1159-1164
58 McDonald K S, Blaser C A, Fitts R H. Force-velocity and power characteristics of rat soleus muscle fibers after hindlimb suspension. J Appl Physiol. 1994; 77 1609-1616
59 McDonald K S, Delp M D, Fitts R H. Fatigability and blood flow in the rat gastrocnemius-plantaris-soleus after hindlimb suspension. J Appl Physiol. 1992; 73 1135-1140
60 Mozdziak P E, Pulvermacher P M, Schultz E. Muscle regeneration during hindlimb unloading results in a reduction in muscle size after reloading. J Appl Physiol. 2001; 91 183-190
61 Ohira M, Hanada H, Kawano F, Ishihara A, Nonaka I, Ohira Y. Regulation of the properties of rat hind limb muscles following gravitational unloading. Jpn J Physiol. 2002; 52 235-245
62 Ohnishi T, Takahashi A, Wang X, Ohnishi K, Ohira Y, Nagaoka S. Accumulation of a tumor suppressor p53 protein in rat muscle during a space flight. Mutat Res. 1999; 430 271-274
63 Panton L B, Golden J, Broeder C E, Browder K D, Cestaro-Seifer D J, Seifer F D. The effects of resistance training on functional outcomes in patients with chronic obstructive pulmonary disease. Eur J Appl Physiol. 2004; 91 443-449
64 Reid M B, Lannergren J, Westerblad H. Respiratory and limb muscle weakness induced by tumor necrosis factor-alpha: involvement of muscle myofilaments. Am J Respir Crit Care Med. 2002; 166 479-484
65 Riley D A, Bain J L, Thompson J L, Fitts R H, Widrick J J, Trappe S W, Trappe T A, Costill D L. Disproportionate loss of thin filaments in human soleus muscle after 17-day bed rest. Muscle Nerve. 1998; 21 1280-1289
66 Roy R R, Zhong H, Monti R J, Vallance K A, Edgerton V R. Mechanical properties of the electrically silent adult rat soleus muscle. Muscle Nerve. 2002; 26 404-412
67 Salmons S, Sreter F A. Significance of impulse activity in the transformation of skeletal muscle type. Nature. 1976; 263 30-34
68 Schols A M. Pulmonary cachexia. Int J Cardiol. 2002; 85 101-110
69 Serres I, Gautier V, Varray A, Prefaut C. Impaired skeletal muscle endurance related to physical inactivity and altered lung function in COPD patients. Chest. 1998; 113 900-905
70 Serres I, Hayot M, Prefaut C, Mercier J. Skeletal muscle abnormalities in patients with COPD: contribution to exercise intolerance. Med Sci Sports Exerc. 1998; 30 1019-1027
71 Simonini A, Long C S, Dudley G A, Yue P, McElhinny J, Massie B M. Heart failure in rats causes changes in skeletal muscle morphology and gene expression that are not explained by reduced activity. Circ Res. 1996; 79 128-136
72 Siu P M, Alway S E. Id2 and p53 participate in apoptosis during unloading-induced muscle atrophy. Am J Physiol Cell Physiol. 2005; in press
73 Siu P M, Bryner R W, Martyn J K, Alway S E. Apoptotic adaptations from exercise training in skeletal and cardiac muscles. Faseb J. 2004; 18 1150-1152
74 Siu P M, Pistilli E E, Butler D C, Alway S E. Aging influences the cellular and molecular responses of apoptosis to skeletal muscle unloading. Am J Physiol Cell Physiol. 2005; 288 C338-C349
75 Stein T, Schluter M, Galante A, Soteropoulos P, Tolias P, Grindeland R, Moran M, Wang T, Polansky M, Wade C. Energy metabolism pathways in rat muscle under conditions of simulated microgravity. J Nutr Biochem. 2002; 13 471
76 Steinborn W, Anker S D. Cardiac cachexia: pathophysiology and clinical implications. Basic and Applied Myology. 2003; 13 191-201
77 Stevens L, Bastide B, Bozzo C, Mounier Y. Hybrid fibres under slow-to-fast transformations: expression is of myosin heavy and light chains in rat soleus muscle. Pflugers Arch. 2004; 448 507-514
78 Stevens L, Bastide B, Kischel P, Pette D, Mounier Y. Time-dependent changes in expression of troponin subunit isoforms in unloaded rat soleus muscle. Am J Physiol Cell Physiol. 2002; 282 C1025-1030
79 Stevens L, Firinga C, Gohlsch B, Bastide B, Mounier Y, Pette D. Effects of unweighting and clenbuterol on myosin light and heavy chains in fast and slow muscles of rat. Am J Physiol Cell Physiol. 2000; 279 C1558-1563
80 Syrovy I, Hodny Z. Non-enzymatic glycosylation of myosin: effects of diabetes and ageing. Gen Physiol Biophys. 1992; 11 301-307
81 Talmadge R J, Roy R R, Bodine-Fowler S C, Pierotti D J, Edgerton V R. Adaptations in myosin heavy chain profile in chronically unloaded muscles. Basic Appl Myol. 1995; 5 117-137
82 Tesch P A, Trieschmann J T, Ekberg A. Hypertrophy of chronically unloaded muscle subjected to resistance exercise. J Appl Physiol. 2004; 96 1451-1458
83 Tyml K, Mathieu-Costello O. Structural and functional changes in the microvasculature of disused skeletal muscle. Front Biosci. 2001; 6 D45-52
84 Tzeng S F, Kahn M, Liva S, De Vellis J. Tumor necrosis factor-alpha regulation of the Id gene family in astrocytes and microglia during CNS inflammatory injury. Glia. 1999; 26 139-152
85 Vermeulen K, Berneman Z N, Van Bockstaele D R. Cell cycle and apoptosis. Cell Prolif. 2003; 36 165-175
86 Vescovo G, Serafini F, Facchin L, Tenderini P, Carraro U, Dalla Libera L, Catani C, Ambrosio G B. Specific changes in skeletal muscle myosin heavy chain composition in cardiac failure: differences compared with disuse atrophy as assessed on microbiopsies by high resolution electrophoresis. Heart. 1996; 76 337-343
87 Vescovo G, Zennaro R, Sandri M, Carraro U, Leprotti C, Ceconi C, Ambrosio G B, Dalla Libera L. Apoptosis of skeletal muscle myofibers and interstitial cells in experimental heart failure. J Mol Cell Cardiol. 1998; 30 2449-2459
88 Visser M, Pahor M, Taaffe D R, Goodpaster B H, Simonsick E M, Newman A B, Nevitt M, Harris T B. Relationship of interleukin-6 and tumor necrosis factor-alpha with muscle mass and muscle strength in elderly men and women: the Health ABC Study. J Gerontol A Biol Sci Med Sci. 2002; 57 M326-332
89 Walters T J, Sweeney H L, Farrar R P. Influence of electrical stimulation on a fast-twitch muscle in aging rats. J Appl Physiol. 1991; 71 1921-1928
90 Widrick J J, Knuth S T, Norenberg K M, Romatowski J G, Bain J L, Riley D A, Karhanek M, Trappe S W, Trappe T A, Costill D L, Fitts R H. Effect of a 17 day spaceflight on contractile properties of human soleus muscle fibres. J Physiol. 1999; 516 915-930
91 Wittwer M, Fluck M, Hoppeler H, Muller S, Desplanches D, Billeter R. Prolonged unloading of rat soleus muscle causes distinct adaptations of the gene profile. Faseb J. 2002; 16 884-886
92 Yang H, Alnaqeeb M, Simpson H, Goldspink G. Changes in muscle fibre type, muscle mass and IGF-I gene expression in rabbit skeletal muscle subjected to stretch. J Anat. 1997; 190 613-622

Dr. Hans Degens

Institute for Biophysical and Clinical Research into Human Movement, Manchester Metropolitan University, Alsager Campus, Alsager

Cheshire

UK

Telefon: + 441612475686

Fax: + 44 16 12 47 63 75

eMail: h.degens@mmu.ac.uk