Effects of inactivity on myosin heavy chain composition and size of rat soleus fibers
Elena J. Grossman BS
Department of Physiological Science, University of California, Los Angeles, Los Angeles, California 90095, USA
Search for more papers by this authorCorresponding Author
Roland R. Roy PhD
Brain Research Institute, UCLA School of Medicine, Center for the Health Sciences, 10833 Le Conte Avenue, Los Angeles, California 90095-1761, USA
Brain Research Institute, UCLA School of Medicine, Center for the Health Sciences, 10833 Le Conte Avenue, Los Angeles, California 90095-1761, USASearch for more papers by this authorRobert J. Talmadge PhD
Department of Physiological Science, University of California, Los Angeles, Los Angeles, California 90095, USA
Search for more papers by this authorHui Zhong MD
Brain Research Institute, UCLA School of Medicine, Center for the Health Sciences, 10833 Le Conte Avenue, Los Angeles, California 90095-1761, USA
Search for more papers by this authorV. Reggie Edgerton PhD
Department of Physiological Science, University of California, Los Angeles, Los Angeles, California 90095, USA
Brain Research Institute, UCLA School of Medicine, Center for the Health Sciences, 10833 Le Conte Avenue, Los Angeles, California 90095-1761, USA
Search for more papers by this authorElena J. Grossman BS
Department of Physiological Science, University of California, Los Angeles, Los Angeles, California 90095, USA
Search for more papers by this authorCorresponding Author
Roland R. Roy PhD
Brain Research Institute, UCLA School of Medicine, Center for the Health Sciences, 10833 Le Conte Avenue, Los Angeles, California 90095-1761, USA
Brain Research Institute, UCLA School of Medicine, Center for the Health Sciences, 10833 Le Conte Avenue, Los Angeles, California 90095-1761, USASearch for more papers by this authorRobert J. Talmadge PhD
Department of Physiological Science, University of California, Los Angeles, Los Angeles, California 90095, USA
Search for more papers by this authorHui Zhong MD
Brain Research Institute, UCLA School of Medicine, Center for the Health Sciences, 10833 Le Conte Avenue, Los Angeles, California 90095-1761, USA
Search for more papers by this authorV. Reggie Edgerton PhD
Department of Physiological Science, University of California, Los Angeles, Los Angeles, California 90095, USA
Brain Research Institute, UCLA School of Medicine, Center for the Health Sciences, 10833 Le Conte Avenue, Los Angeles, California 90095-1761, USA
Search for more papers by this authorAbstract
Myosin heavy chain (MHC) and fiber size properties of the adult rat soleus were determined after 4–60 days of complete inactivity, i.e., lumbar spinal cord isolation. Soleus atrophy was rapid and progressive, i.e., 25% and 64% decrease in weight and 33% and 75% decrease in fiber size after 4 and 60 days of inactivity, respectively. Changes in MHC occurred at a slower rate than the atrophic response. After 15 days there was de novo expression of type IIx MHC (∼10%). By 60 days, type IIx MHC accounted for 33% of the total MHC content, and 7% of the fibers contained only type IIx MHC. The relative amount of type I MHC was reduced from 93% in control to 49% after 60 days of inactivity. Therefore, the effects of 60 days of inactivity suggest that during this time period at least 75% of fiber size and ∼40% of type I MHC composition of the adult rat soleus can be attributed to activation-related events. © 1998 John Wiley & Sons, Inc. Muscle Nerve 21:375–389, 1998.
References
- 1 Alaimo MA, Smith JL, Roy RR, Edgerton VR: EMG activity of slow and fast ankle extensors following spinal cord transection. J Appl Physiol 1984; 56: 1608–1613.
- 2 Alford EK, Roy RR, Hodgson JA, Edgerton VR: Electromyography of rat soleus, medial gastrocnemius and tibialis anterior during hindlimb suspension. Exp Neurol 1987; 96: 635–649.
- 3 Ausoni S, Gorza L, Schiaffino S, Gundersen K, Lomo T: Expression of myosin heavy chain isoforms in stimulated fast and slow rat muscles. J Neurosci 1990; 10: 153–160.
- 4 Caiozzo VJ, Baker MJ, Herrick RE, Tao M, Baldwin KM: Effect of spaceflight on skeletal muscle: mechanical properties and myosin isoform content of a slow muscle. J Appl Physiol 1994; 76: 1764–1773.
- 5 Caiozzo VJ, Haddad F, Baker MJ, Herrick RE, Prietto N, Baldwin KM: Microgravity-induced transformations of myosin isoforms and contractile properties of skeletal muscle. J Appl Physiol 1996; 81: 123–132.
- 6 Covault J, Sanes JR: Neural cell adhesion molecule (N-CAM) accumulates in denervated and paralyzed skeletal muscles. Proc Natl Acad Sci USA 1985; 82: 4544–4548.
- 7 Edgerton VR, Roy RR: Neuromuscular adaptations to actual and simulated spaceflight, in MJ Fregly, CM Blatteis (eds): Handbook of Physiology. New York, Oxford University Press, 1996, pp 721–763.
- 8 Edgerton VR, Bodine-Fowler S, Roy RR, Ishihara A, Hodgson JA: Neuromuscular adaptation, in LB Rowell, JT Shepherd (eds): Handbook of Physiology. New York, Oxford University Press, 1996, pp 54–88.
- 9 Eldridge L, Mommaerts W: Ability of electrically silent nerves to specify fast and slow muscle characteristics, in D Pette (ed): Plasticity of Muscle. Berlin, Walter de Gruyter and Co., 1980, pp 325–337.
- 10 Eldridge L, Leibhold M, Steinback JH: Alterations in cat skeletal neuromuscular junctions following prolonged inactivity. J Physiol (Lond) 1981; 313: 529–545.
- 11 Fauteck SP, Kandarian SC: Sensitive detection of myosin heavy chain composition in skeletal muscle under different loading conditions. Am J Physiol 1995; 268: C419–C424.
- 12 Fournier M, Roy RR, Perham H, Simard CP, Edgerton VR: Is limb immobilization a model of muscle disuse? Exp Neurol 1983; 80: 147–156.
- 13 Grossman EJ, Roy RR, Talmadge RJ, Zhong VH, Edgerton VR: Effect of chronic inactivity on the myosin heavy chain profile of rat soleus fibers. FASEB J 1996; 10: A128.
- 14 Grossman EJ, Roy RR, Talmadge RJ, Zhong VH, Edgerton VR: Myosin heavy chain composition of inactive rat hindlimb muscles. Physiologist 1996; 39: A93.
- 15 Hnik P, Vejsada R, Goldspink DF, Kasicki S, Krekule I: Quantitative evaluation of electromyogram activity in rat extensor and flexor muscles immobilized at different lengths. Exp Neurol 1985; 88: 515–528.
- 16 Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227: 680–685.
- 17 Michel RN, Cowper G, Chi M, Manchester JK, Falter H, Lowry OH: Effects of tetrodotoxin-induced neural inactivation on single muscle fiber metabolic enzymes. Am J Physiol 1994; 267: C55–C66.
- 18 Michel RN, Parry DJ, Dunn SE: Regulation of myosin heavy chain expression in adult rat hindlimb muscles during shortterm paralysis: comparison of denervation and tetrodotoxin induced neural inactivation. FEBS Lett 1996; 391: 39–44.
- 19 Ohira Y, Jiang B, Roy RR, Oganov V, Ilyina-Kakueva E, Marini JF, Edgerton VR: Rat soleus muscle fiber responses to 14 days of spaceflight and hindlimb suspension. J Appl Physiol 1992; 73: 51S–57S.
- 20 Pette D, Vrbová G: Invited review: Neural control of phenotype expression in mammalian muscle fibers. Muscle Nerve 1985; 8: 676–689.
- 21 Pette D, Vrbová G: Adaptation of mammalian skeletal muscle fibers to chronic electrical stimulation. Rev Physiol Biochem Pharmacol 1992; 120: 116–202.
- 22 Pette D, Staron RS: Mammalian skeletal muscle fiber type transitions. Int Rev Cytol 1997; 170: 143–223.
- 23 Pierotti DJ, Roy RR, Bodine-Fowler SC, Hodgson JA, Edgerton VR: Mechanical and morphological properties of chronically inactive cat tibialis anterior motor units. J Physiol (Lond) 1991; 444: 175–192.
- 24 Roy RR, Baldwin KM, Edgerton VR: The plasticity of skeletal muscle: effects of neuromuscular Sactivity, in JO Holloszy (ed): Exercise and Sport Sciences Reviews. Baltimore, Williams and Wilkins, 1991, pp 269–312.
- 25 Roy RR, Hodgson JA, Lauretz SD, Pierotti DJ, Gayek RJ, Edgerton VR: Chronic spinal cord-injured cats: surgical procedures and management. Lab Anim Sci 1992; 42: 335–343.
- 26 Roy RR, Pierotti DJ, Flores V, Rudolph W, Edgerton VR: Fibre size and type adaptations to spinal isolation and cyclical passive stretch in cat hindlimb. J Anat 1992; 180: 491–499.
- 27
Roy RR,
Eldridge L,
Baldwin KM,
Edgerton VR:
Neural influence on slow muscle properties: inactivity with and without cross-reinnervation.
Muscle Nerve
1996;
19:
707–714.
10.1002/(SICI)1097-4598(199606)19:6<707::AID-MUS4>3.0.CO;2-E CAS PubMed Web of Science® Google Scholar
- 28 Salmons S, Henriksson J: The adaptive response of skeletal muscle to increased use. Muscle Nerve 1981; 4: 94–105.
- 29 Schiaffino S, Gorza L, Sartore S, Saggin L, Ausoni S, Vianello M, Gunderson K, Lomo T: Three myosin heavy chain isoforms in type 2 skeletal muscle fibers. J Musc Res Cell Motil 1989; 10: 197–205.
- 30
Sketelj J,
Leisner E,
Gohlsch B,
Skorjanc D,
Pette D:
Specific impulse patterns regulate acetylcholinesterase activity in skeletal muscles of rats and rabbits.
J Neurosci Res
1997;
47:
49–57.
10.1002/(SICI)1097-4547(19970101)47:1<49::AID-JNR5>3.0.CO;2-F CAS PubMed Web of Science® Google Scholar
- 31 Talmadge RJ, Roy RR: Electrophoretic separation of rat skeletal muscle myosin heavy-chain isoforms. J Appl Physiol 1993; 75: 2337–2340.
- 32 Talmadge RJ, Roy RR, Bodine-Fowler SC, Pierotti DJ, Edgerton VR: Adaptations in myosin heavy chain profile in chronically unloaded muscles. Basic Appl Myol 1995; 5: 114–134.
- 33 Talmadge RJ, Roy RR, Edgerton VR: Prominence of myosin heavy chain hybrid fibers in soleus muscle of spinal cordtransected rats. J Appl Physiol 1995; 78: 1256–1265.
- 34 Talmadge RJ, Roy RR, Baldwin KM, Edgerton VR: Myosin heavy chain profile of cat soleus following chronic reduced activity or inactivity. Muscle Nerve 1996; 19: 980–988.
- 35 Talmadge RJ, Roy RR, Edgerton VR: Distribution of myosin heavy chain isoforms in non-weight bearing rat soleus muscle fibers. J Appl Physiol 1996; 81: 2540–2546.
- 36 Thomason DB, Herrick RE, Surdyka D, Baldwin KM: Time course of soleus muscle myosin expression during hindlimb suspension and recovery. J Appl Physiol 1987; 63: 130–137.
- 37 Thomason DB, Biggs RB, Booth FW: Protein metabolism and β-myosin heavy chain mRNA in unweighted soleus muscle. Am J Physiol 1989; 257: R300–R305.
- 38 Thomason DB, Booth FW: Atrophy of the soleus muscle by hindlimb unweighting. J Appl Physiol 1990; 68: 1–12.
- 39 Tower SS: Function and structure in the chronically isolated lumbo-sacral spinal cord of the dog. J Comp Neurol 1937; 67: 109–131.