Early activation and redistribution of calpain activity in skeletal muscle during hindlimb unweighting and reweighting.

The aims of this study were the following: (i) to determine whether activation of the Ca2+-activated protease, calpain, is an early event during hindlimb unweighting (HU) in skeletal muscle; and (ii) to assess whether calpain activity is greater during reweighting compared with HU alone. Rats were exposed to 12, 24, and 72 h, or 9 d of HU, followed by reweighting for 0, 12, or 24 h. Calpain activities were assayed for total, soluble, and particulate fractions. Total calpain activity was increased in the soleus at all HU time points, whereas activities were elevated in the gastrocnemius only after 9 d of HU. With reweighting, calpain activity remained elevated at all time points for both muscles. In general, reweighting the gastrocnemius increased its calpain activity more than during HU only, whereas reweighting the soleus did not produce additional increases in its calpain activity. The increases in calpain activity were associated with a proportional increase in activity of the particulate (membrane- and protein-associated) fraction. The results suggest that calpain activation is an early event during HU in the soleus, and that the increases in calpain activity in both muscles are associated with a redistribution of activity from cytosolic to particulate fractions.

[1]  J M Steffen,et al.  Disuse atrophy, plasma corticosterone, and muscle glucocorticoid receptor levels. , 1987, Aviation, space, and environmental medicine.

[2]  R. Armstrong,et al.  Time course changes in [Ca2+]i, force, and protein content in hindlimb-suspended mouse soleus muscles. , 2001, Aviation, space, and environmental medicine.

[3]  F. Booth,et al.  Molecular Events Underlying Skeletal Muscle Atrophy and the Development of Effective Countermeasures , 1997, International journal of sports medicine.

[4]  D. Riley,et al.  Skeletal muscle fiber, nerve, and blood vessel breakdown in space‐flown rats , 1990, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[5]  D A Riley,et al.  Effect of a 17 day spaceflight on contractile properties of human soleus muscle fibres , 1999, The Journal of physiology.

[6]  R. Armstrong,et al.  Mechanisms of Exercise-Induced Muscle Fibre Injury , 1991, Sports medicine.

[7]  Emily R Morey-Holton,et al.  Hindlimb unloading rodent model: technical aspects. , 2002, Journal of applied physiology.

[8]  H. Ishii,et al.  Characterization of calpain I-binding proteins in human erythrocyte plasma membrane. , 1990, Journal of biochemistry.

[9]  Y Mounier,et al.  Ca2+ movements in sarcoplasmic reticulum of rat soleus fibers after hindlimb suspension. , 1992, Journal of applied physiology.

[10]  O. H. Lowry,et al.  Protein measurement with the Folin phenol reagent. , 1951, The Journal of biological chemistry.

[11]  P. Chase,et al.  Different mechanisms of increased proteolysis in atrophy induced by denervation or unweighting of rat soleus muscle. , 1990, Metabolism: clinical and experimental.

[12]  T P Stein,et al.  Protein kinetics during and after long-duration spaceflight on MIR. , 1999, American journal of physiology. Endocrinology and metabolism.

[13]  F. Booth,et al.  Protein metabolism and beta-myosin heavy-chain mRNA in unweighted soleus muscle. , 1989, The American journal of physiology.

[14]  T. Yoshioka,et al.  Calcium movement of sarcoplasmic reticulum from hindlimb suspended muscle. , 1996, Acta astronautica.

[15]  J. Tidball,et al.  Calpain II expression is increased by changes in mechanical loading of muscle in vivo , 1997, Journal of cellular biochemistry.

[16]  D. Riley Review of primary spaceflight-induced and secondary reloading-induced changes in slow antigravity muscles of rats. , 1998, Advances in space research : the official journal of the Committee on Space Research.

[17]  T. Raastad,et al.  Calpain/calpastatin activities and substrate depletion patterns during hindlimb unweighting and reweighting in skeletal muscle , 2007, European Journal of Applied Physiology.

[18]  T. Szilágyi,et al.  Effect of weightlessness on the function of rat skeletal muscles on the biosatellite "Cosmos-1129". , 1983, Acta physiologica Hungarica.

[19]  R. Armstrong,et al.  Intracellular Ca2+ transients in mouse soleus muscle after hindlimb unloading and reloading. , 1999, Journal of applied physiology.

[20]  A. Belcastro,et al.  Striated muscle calcium-stimulated cysteine protease (calpain-like) activity promotes myeloperoxidase activity with exercise , 1998, Pflügers Archiv.

[21]  M. Mingari,et al.  Characterization of the calpain/calpastatin system in human hemopoietic cell lines. , 2006, Archives of biochemistry and biophysics.

[22]  S. Jaspers,et al.  Role of glucocorticoids in the response of rat leg muscles to reduced activity , 1986, Muscle & nerve.

[23]  D. Balcerzak,et al.  Myoblast fusion requires fibronectin degradation by exteriorized m-calpain. , 1997, Experimental cell research.

[24]  B. Bastide,et al.  Properties of ryanodine receptor in rat muscles submitted to unloaded conditions. , 2000, Biochemical and biophysical research communications.

[25]  A. Belcastro,et al.  Exercise promotes a subcellular redistribution of calcium-stimulated protease activity in striated muscle , 1999 .

[26]  M. Tischler,et al.  Time course of the response of myofibrillar and sarcoplasmic protein metabolism to unweighting of the soleus muscle. , 1993, Metabolism: clinical and experimental.

[27]  D A Riley,et al.  Review of spaceflight and hindlimb suspension unloading induced sarcomere damage and repair. , 1995, Basic and applied myology : BAM.

[28]  I. Nonaka,et al.  Space shuttle flight (STS‐90) enhances degradation of rat myosin heavy chain in association with activation of ubiquitin‐proteasome pathway , 2001, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[29]  E. Melloni,et al.  Modulation of the calpain autoproteolysis by calpastatin and phospholipids. , 1996, Biochemical and biophysical research communications.

[30]  K M Baldwin,et al.  Effects of zero gravity on myofibril content and isomyosin distribution in rodent skeletal muscle , 1990, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[31]  A. Belcastro Skeletal muscle calcium-activated neutral protease (calpain) with exercise. , 1993, Journal of applied physiology.

[32]  W. Reid,et al.  Diaphragm injury and myofibrillar structure induced by resistive loading. , 1994, Journal of applied physiology.

[33]  D. Thomason,et al.  Soleus muscle nascent polypeptide chain elongation slows protein synthesis rate during non-weight-bearing activity. , 1994, The American journal of physiology.

[34]  F. B. Davis,et al.  Thyroid hormone induces activation of mitogen-activated protein kinase in cultured cells. , 1999, American journal of physiology. Cell physiology.

[35]  G. Goldspink,et al.  The effect of hypokinesia and hypodynamia on protein turnover and the growth of four skeletal muscles of the rat , 1986, Pflügers Archiv.

[36]  Y. Murata,et al.  Urinary excretion of stress hormones of rats in tail-suspension. , 1993, Environmental medicine : annual report of the Research Institute of Environmental Medicine, Nagoya University.

[37]  H. Hoppeler,et al.  Rat soleus muscle ultrastructure after hindlimb suspension. , 1990, Journal of applied physiology.

[38]  S. Barnoy,et al.  Association of calpain (Ca2+‐dependent thiol protease) with its endogenous inhibitor calpastatin in myoblasts , 1999, Journal of cellular biochemistry.

[39]  S. Kandarian,et al.  Regulation of sarcoplasmic reticulum calcium pump gene expression by hindlimb unweighting. , 1993, The American journal of physiology.

[40]  C. Guézennec,et al.  Coordinate activation of lysosomal, Ca 2+-activated and ATP-ubiquitin-dependent proteinases in the unweighted rat soleus muscle. , 1996, The Biochemical journal.

[41]  J. Schollmeyer Possible role of calpain I and calpain II in differentiating muscle. , 1986, Experimental cell research.

[42]  R. Armstrong,et al.  Rat skeletal muscle mitochondrial [Ca2+] and injury from downhill walking. , 1990, Journal of applied physiology.

[43]  Z. Jia,et al.  Crystal structure of calpain reveals the structural basis for Ca2+‐dependent protease activity and a novel mode of enzyme activation , 1999, The EMBO journal.