Extracellular Matrix and Myofibrils During Unloading and Reloading of Skeletal Muscle

Abstract

The aim of the study was to elucidate the effect of unloading and reloading on the collagen expression and synthesis rate of myofibrillar proteins in fast-twitch (FT) muscle in relation to changes in muscle strength and motor activity. Northern blot analysis was used for testing the specificity of cDNA probes and protein synthesis rate was measured according to incorporation of radioactive leucine into different protein fractions. Unloading depresses collagen type I and III (p<0.001), type IV (p<0.05) and reloading enhances collagen expression in fast-twitch skeletal muscle in comparison with unloading. Enhanced expression of matrix metalloproteinase-2 continued during the first week of reloading (p<0.01) and tissue inhibitor of metalloproteinase-2 during reloading (p<0.05). Changes in collagen expression in FT muscle are in good agreement with changes in myofibrillar protein synthesis during unloading and reloading. In conclusion alterations in extracellular matrix and myofibrillar apparatus in FT skeletal muscle are related to changes in muscle strength and motor activity, are significant in exercise training and determination of recovery periods in the training process as well as in athletes’ rehabilitation.

Key words

collagens - myofibrillar proteins - unloading - reloading

References

• 1 Baker AH, Edwards DR, Murphy G. Metalloproteinase inhibitors: biological actions and therapeutic opportunities.  J Cell Sci. 2002;  115 3719-3727
• 2 Bradford MM. A rapid sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.  Anal Biochem. 1976;  72 248-254
• 3 Choi Y-C, Dalakas MC. Expression of matrix metalloproteinases in the muscles of patients with inflammatory myopathies.  Neurology. 2000;  54 65-71
• 4 Chomczynsky PK, Mackey PK. One-hour downward capillary blotting of RNA at neutral pH.  Anal Biochem. 1994;  221 303-305
• 5 D’Antona G, Pellegrino MA, Rossi R, Carlizzi CN, Reggiani C, Bottinelli R. Disuse induced atrophy and contractile impairment of human skeletal muscle fibres.  Basic Appl Myol. 2000;  10 27-32
• 6 Dean RT, Fu S, Stocker R, Davies MJ. Biochemistry and pathology of radical-mediated protein oxidation.  Biochem J. 1997;  324 1-18
• 7 Degens H, Alway SE. Control of muscle size during disuse, disease, and ageing.  Int J Sports Med. 2006;  27 94-99
• 8 Fitts RH, Riley DR, Widrick JJ. Microcravity and skeletal muscle.  J Appl Physiol. 2000;  89 823-839
• 9 Fujino H, Ishihara A, Murakami S, Yasuhara T, Kondo H, Mohri S, Takeda I, Roy RR. Protective effects of exercise preconditioning on hindlimb unloading-induced atrophy of rat soleus muscle.  Acta Physiol (Oxf). 2009;  197 65-74
• 10 Gagliano N, Pelillo F, Chiriva-Internati M, Picciolini O, Costa F, Schutt C, Gioia M, Portinaro N. Expression profiling of genes involved in collagen turnover in tendons from cerebral palsy patients.  Connect Tissue Res. 2009;  50 203-208
• 11 Goto K, Okuyama R, Honda M, Uchida H, Akema T, Ohira Y, Yoshioka T. Profiles of connectin (titin) in atrophied soleus muscle induced by unloading of rats.  J Appl Physiol. 2003;  94 897-902
• 12 Gwang T, Lee K, Ju H, Shin H, Lee J-H, Choi I. Stress and signaling responses of rat skeletal muscle to brief endurance exercise during hindlimb unloading: a catch-up process for atrophied muscle.  Cell Physiol Biochem. 2009;  24 537-546
• 13 Harriss JD, Atkinson G. International Journal of Sports Medicine – Ethical Standards in Sport and Exercise Science Research.  Int J Sports Med. 2009;  30 701-702
• 14 Heinemeier K, Olesen JL, Haddad F, Schjerling P, Baldwin KM, Kjaer M. Effect of unloading followed by reloading on expression of collagen and related growth factors in rat tendon and muscle.  J Appl Physiol. 2009;  106 178-186
• 15 Järvinen TA, Józsa L, Kannus P, Järvinen TL-N, Järvinen M. Organization and distribution of intramuscular connective tissue in normal and immobilized skeletal muscles.  J Muscle Res Cell Motil. 2002;  23 245-254
• 16 Kagan HM, Li W. Lysyl oxidase: Properties, specificity, and biological roles inside and outside of the cell.  J Cell Biochem. 2002;  88 660-672
• 17 Kieseier BC, Schneider C, Clements JM, Gearing AJH, Gold R, Toyka KV, Hartung H-P. Expression of specific matrix metalloproteinases in inflammatory myopathies.  Brain. 2001;  124 341-351
• 18 Kjaer M, Magnusson P, Krogsgaard M, Møller JB, Olesen J, Heinemeier K, Hansen M, Haraldsson B, Koskinen S, Esmarck B, Langberg H. Extracellular matrix adaptation of tendon and skeletal muscle to exercise.  J Anat. 2006;  208 445-450
• 19 Koskinen SOA, Ahtikoski AM, Komulainen J, Hesslink MKC, Drost MR, Takala TES. Short-term effects of forced eccentric contractions on collagen synthesis and degradation in rat skeletal muscle.  Pflugers Arch. 2002;  444 59-72
• 20 Koskinen SOA, Wang W, Ahtikoski AM, Kjaer M, Han X-Y, Komulainen J, Kovanen V, Takala TES. Acute exercise induced changes in rat skeletal muscle mRNAs and protein regulating type IV collagen content.  Am J Physiol. 2001;  280 R1292-R1300
• 21 Mackey AL, Heinemeier KM, Koskinen SOA, Kjaer M. Dynamic adaptation of tendon and muscle connective tissue to mechanical loading.  Connect Tissue Res. 2008;  49 165-168
• 22 Maniatis T, Fritsch EF, Sambrook J. Molecular Cloning. A Laboratory Manual.. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; 1982
• 23 Matsuba Y, Goto K, Morioka S, Naito T, Akema T, Hashimoto N, Sugiura T, Ohira Y, Beppu M, Yoshioka T. Gravitational unloading inhibits the regenerative potential of atrophied soleus muscle in mice.  Acta Physiol (Oxf). 2009;  196 329-339
• 24 Morey-Holton ER, Globus RK. Hindlimb unloading rodent model: technical aspects.  J Appl Physiol. 2002;  92 1367-1377
• 25 Mozdziak PE, Pulvermacher PM, Shultz E. Muscle regeneration during hindlimb unloading results in a reduction in muscle size after reloading.  J Appl Physiol. 2001;  91 183-190
• 26 Riso E-M, Ahtikoski A, Alev K, Kaasik P, Pehme A, Seene T. Relationship between extracellular matrix, contractile apparatus, muscle mass and strength in case of glucocorticoid myopathy.  J Steroid Biochem Mol Biol. 2008;  108 117-120
• 27 Roy RR, Baldwin KM, Edgerton VR. Response of the neuromuscular unit to sapceflight: what has been learned from the rat model.  Exerc Sport Sci Rev. 1996;  24 399-425
• 28 Sakuma K, Watanabe K, Hotta N, Koike T, Ishida K, Katayama K, Akima H. The adaptive responses in several mediators linked with hypertrophy and atrophy of sekeletal muscle after lower limb unloading in humans.  Acta Physiol (Oxf). 2009;  197 151-159
• 29 Sanes JR. The basement membrane/basal lamina of skeletal muscle.  J Biol Chem. 2003;  278 12601-12604
• 30 Seene T, Kaasik P, Umnova M. Structural rearrangements in contractile apparatus and resulting skeletal muscle remodelling: effect of exercise training.  J Sports Med Phys Fitness. 2009;  49 410-423
• 31 Seene T, Umnova M, Kaasik P, Alev K, Pehme A. Overtraining injuries in athletic population. In: Tiidus PM (ed) Skeletal Muscle Damage and Repair Champaign (IL), Human Kinetics; 2008: 173-184 & 305–307
• 32 Seo Y, Lee K, Park K, Bae K, Choi I. A proteomic assessment of muscle contractile alterations during unloading and reloading.  J Biochem (Tokio). 2006;  139 71-80
• 33 Sugden PH, Fuller SJ. Regulation of protein turnover in skeletal and cardiac muscle.  Biochem J. 1991;  273 21-37
• 34 Trackman PC. Diverse biological functions of extracellular collagen processing enzymes.  J Cell Biochem. 2005;  96 927-937
• 35 Trappe T. Influence of aging and long-term unloading on the structure and function of human skeletal muscle.  Appl Physiol Nutr Metab. 2009;  34 459-464
• 36 Visse R, Nagase H. Matrix metalloproteinase and tissue inhibitors of metalloproteinases: Structure, function and biochemistry.  Circ Res. 2003;  92 827-839
• 37 Wang XD, Kawano F, Matsuoka Y, Fukunaga K, Terada M, Sudoh M, Ishihara A, Ohira Y. Mechanical load-dependent regulation of satellite cell and fibre size in rat soleus muscle.  Am J Physiol Cell Physiol. 2006;  290 C981-C989
• 38 Yamauchi H, Kariya F, Tabata J, Miyano S. Atrophy and expression of myosin heavy chain isoforms in antigravity muscles after long-term hindlimb unloading.  Jpn J Rehabil Med. 2002;  39 236-244

Correspondence