Expression of Splice Variants of Insulin-Like Growth Factor I and the State of the Myosatellite Cell Pool in the Soleus Muscle in Rats during Gravitational Unweighting and Passive Stretching
Tóm tắt
Gravitational unweighting is known to induce atrophy and to suppress proliferative processes in the postural muscles; muscle stretching during unweighting allows this atrophy to be overcome. It has been suggested that stretching of the soleus muscle promotes proliferation of satellite cells with subsequent incorporation of their nuclei into fibers on functioning loading of the hindlimbs in rats. The numbers of satellite cells labeled with M-cadherin on cross-sections of single fibers were assessed. After two weeks of antiorthostatic suspension, the number of labeled cells decreased by 33% from the level seen in the control group. In passive stretching, the number of labeled cells was 2.5 times greater than that in suspended animals and 1.7 times greater than in that control animals. The key role in the activation of satellite cells is known to be played by growth factors, including insulin-like growth factor I (IGF-I). Levels of IGF-I expression were measured in the soleus muscle after suspension with stretching, which showed no changes as compared with the suspension without stretching or control groups. Thus, these experiments demonstrated that passive stretching stimulates increases in the proliferation of satellite cells in the soleus muscle of the stretched limb in rats as compared with the level seen in normal conditions, with no changes in the expression of IGF-I or its splice variant MGF.
Tài liệu tham khảo
A. M. Genin, A. E. Ilyin, A. S. Kaplanskii, T. B. Kasatkina, K. A. Kuznetsova, I. D. Pestov, and T. A. Smirnova, “Bioethical rules for studies on humans and animals in aviation, space, and marine medicine,” Aviakosmich., 35, 14–20 (2001).
K. S. Litvinova, P. P. Tarakin, N. M. Fokina,V. E. Istomina, I. M. Larina, and B. S. Shenkman, “Dynamic characteristics of soleus muscle fibers in rats and insulin-like growth factor I during readaptation after gravitational unweighting,” Ros. Fiziol. Zh. im. I. M. Sechenova, 93, No. 10, 1143–1155 (2007).
M. V. Tarakina, O. V. Turtikova, T. L. Nemirovskaya, A. A. Kokontsev, and B. S. Shenkman, “The role of precursor cells in supporting the morphological characteristics of the soleus muscle in passive muscle stretching on the background of gravitational unweighting,” Tsitologiya, 50, No. 2, 140–146 (2008).
O. V. Turtikova, E. G. Altaeva, M. V. Tarakina, A. M. Malashenko, T. L. Nemirovskaya, and B. S. Shenkman, “Cellular effects of functional unweighting and passive tension of the soleus muscle in dystrophin-deficient mice,” Tsitologiya, 50, No. 2, 132–138 (2008).
G. R. Adams, S. A. McCue, P. W. Bodell, M. Zeng, and K. M. Baldwin, “Effects of spaceflight and thyroid deficiency on hind limb development. I. Muscle mass and IGF-I expression,” J. Appl. Physiol., 88, 894–903 (2000).
D. L. Allen, S. R. Monke, R. J. Talmadge, R. R. Roy, and V. R. Edgerton, “Plasticity of myonuclear number in hypertrophied and atrophied mammalian skeletal muscle fibers,” J. Appl. Physiol., 78, 1969–1976 (1995).
B. Awede, J.-P. Thissen, P. Gailly, and J. Lebacq, “Regulation of IGF-I, IGFBP-4 and IGFBP-5 gene expression by loading in mouse skeletal muscle,” FEBS Lett., 461, 263–267 (1999).
E. R. Barton, “The ABCs of IGF-I isoforms: impact on muscle hypertrophy and implications for repair,” Appl. physiol. Nutr. Metab., 31, No. 6, 791–797 (2006).
E. R. Barton-Davis, D. I. Shoturma, and H. L. Sweeney, “Contribution of satellite cells to IGF-I induced hypertrophy of skeletal muscle,” Acta Physiol. Scand., 167, No. 4, 301–305 (1999).
S. C. Bodine, “mTOR signaling and the molecular adaptation to resistance exercise,” Med. Sci. Sports Exerc., 38, No. 11, 1950–1957 (2006).
J. C. Bruusgaard and K. Gundersen, “In vivo time-lapse microscopy reveals no loss of murine myonuclei during weeks of muscle atrophy,” J. Clin. Invest., 118, No. 4, 1450 (2008).
K. L. Capkovic, S. Stevenson, M. C. Johnson, J. J. Thelen, and D. D. Cornelison, “Neural cell adhesion molecule (NCAM) marks adult myogenic cells committed to differentiation,” Exp. Cell. Res., 314, No. 7, 1553–1565 (2008).
K. C. Darr and E. Schultz, “Hindlimb suspension suppresses muscle growth and satellite cell proliferation,” J. Appl. Physiol., 67, 1827–1834 (1989).
D. F. Goldspink, “The influence of immobilization and stretch on protein turnover of rat skeletal muscle,” J. Physiol., 264, 267–282 (1977).
D. F. Goldspink, A. J. Morton, P. Loughna, and G. Goldspink, “The effect of hypokinesia and hypodynamia on protein turnover and the growth of four skeletal muscles of the rat,” Pflügers Arch., 407, 333–340 (1986).
G. Goldspink, “Changes in muscle mass and phenotype and the expression of autocrine and systemic growth factors by muscle in response to stretch and overload,” J. Anat., 194, 323–334 (1999).
N. Hagiwara, B. Ma, and A. Ly, “Slow and fast fiber isoform gene expression is systematically altered in skeletal muscle of the Sox6 mutant, p100H,” Dev. Dyn., 234, No. 2, 301–311 (2005).
B. Han, M. J. Zhu, C. Ma, and M. Du, “Rat hindlimb unloading down-regulates insulin like growth factor-1 signaling and AMP-activated protein kinase, and leads to severe atrophy of the soleus muscle,” Appl. Physiol. Nutr. Metab., 32, 1115–1123 (2007).
R. Hikida, S. Nostran, J. Murray, R. Staron, S. Gordon, and W. Kraemer, “Myonuclear loss in atrophied soleus muscle fibers,” Anat. Rec., 247, 350–354 (1997).
M. Hill and G. Goldspink, “Expression and splicing of the insulin-like growth factor gene in rodent muscle is associated with muscle satellite (stem) cell activation following local tissue damage,” J. Physiol., 549, 409–418 (2003).
M. Ishido, K. Kami, and M. Masuhara, “Localization of MyoD, myogenin and cell cycle regulatory factors in hypertrophying rat skeletal muscles,” Acta Physiol. Scand., 180, 281–289 (2004).
V. Jacquemin, D. Furling, A. Bigot, G. S. Butler-Browne, and V. Mouly, “IGF-I induces human myotube hypertrophy by increasing cell recruitment,” Exp. Cell. Res., 299, No. 1, 148–158 (2004).
C. E. Casper and L. Xun, “Cytoplasm-to-myonucleus ratios following microgravity,” J. Muscle Res. Cell. Motil., 17, No. 5, 595–602 (1996).
F. Kawano, Y. Takeno, N. Nakai, Y. Higo, M. Terada, T. Ohira, I. Nonaka, and Y. Ohira, “Essential role of satellite cells in the growth of rat soleus muscle fibers,” Am. J. Physiol. Cell. Physiol., 295, No. 2, 458–467 (2008).
R. Lalani, S. Bhastin, F. Byhower, R. Tarnuzzer, M. Grant, R. Shen, S. Asa, S. Ezzat, and N. F. Gonzalez-Cadavid, “Myostatin and insulin-like growth factor-I and II expression in the muscle of rat exposed to the microgravity environment of the NeuroLab space shuttle flight,” J. Endocrinol., 167, 417–428 (2000).
K. J. Livak and T. D. Schmittgen, “Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆Ct method,” Methods, 25, No. 4, 402–408 (2001).
P. T. Loughna, P. Mason, and P. C. Bates, “Regulation of insulin-like growth factor 1 gene expression in skeletal muscle,” Symp. Soc. Exp. Biol., 46, 319–330 (1992).
P. O. Mitchell and G. K. Pavlath, “A muscle precursor cell-dependent pathway contributes to muscle growth after atrophy,” Am. J. Physiol. Cell. Physiol., 281, 1706–1715 (2001).
T. L. Nemirovskaya, B. S. Shenkman, A. Muchina, Y. Volodkovich, M. Sayapina, O. Larina, and E. Bratcseva, “Role of afferent control in maintaining structural and metabolic characteristics of stretched soleus in rats exposed to hindlimb suspension,” J. Gravit. Physiol., 9, 121–122 (2002).
V. E. Novikov and E. A. Ilyin, “Age-related reactions of rat bones to their unloading,” Aviat. Environ. Med., 52, 551–553 (1981).
Y. Ohira, B. Jiang, R. R. Roy, V. Oganov, E. Ilyina-Kakueva, J. F. Marini, and V. R. Edgerton, “Rat soleus muscle fiber responses to 14 days of spaceflight and hindlimb suspension,” J. Appl. Physiol., 73, 51–57 (1992).
Y. Ohira, T. Yoshinaga, T. Nomura, F. Kawano, A. Ishihara, I. Nonaka, R. R. Roy, and V. R. Edgerton, “Gravitational unloading effects on muscle fiber size, phenotype and myonuclear number,” Adv. Space Res., 30, 777–781 (2002).
D. A. Riley, G. R. Slocum, J. L. W. Bain, F. R. Sedlak, T. E. Sowa, and J. W. Mellender, “Rat hindlimb unloading: soleus histochemistry, ultrastructure and electromyography,” J. Appl. Physiol., 69, 58–66 (1990).
B. Rosser, M. Dean, and E. Bandman, “Myonuclear domain size varies along the lengths of maturing skeletal muscle fibers,” Int. J. Dev. Biol., 46, 747–754 (2002).
H. Schmalbruch and U. Hellhammer, “The number of nuclei in adult rat muscles with special reference to satellite cells,” Anat. Rec., 189, 169–176 (1977).
E. Schultz, K. C. Darr, and A. Macius, “Acute effects of hindlimb unweighting on satellite cells of growing skeletal muscle,” J. Appl. Physiol., 76, 266–270 (1994).
B. S. Shenkman, I. B. Kozlovskaya, S. L. Kuznetsov, T. L. Nemirovskaya, and D. Desplanches, “Plasticity of skeletal muscle fibres in space-flown primates,” J. Gravit. Physiol., 1, 64–66 (1994).
R. Tatsumi, X. Liu, A. Pulido, M. Morales, T. Sakata, S. Dial, A. Hattori, Y. Ikeuchi, and R. E. Allen, “Satellite cell activation in stretched skeletal muscle and the role of nitric oxide and hepatocyte growth factor,” Am. J. Physiol. Cell. Physiol., 290, No. 6, 1487–1494 (2006).
D. B. Thomason and F. W. Booth, “Influence of performance on gene expression in skeletal muscle: effects of force inactivity,” Adv. Myochem., 2, 79–82 (1989).
X. D. Wang, F. Kawano, Y. Matsuoka, K. Fukunaga, M. Terada, M. Sudoh, A. Ishihara, and Y. Ohira, “Mechanical load-dependent regulation of satellite cell and fiber size in rat soleus muscle,” Am. J. Physiol. Cell. Physiol., 290, No. 4, 981–989 (2006).
T. P. White and K. A. Esser, “Satellite cell and growth factor involvement in skeletal muscle growth,” Med. Sci. Sports Exerc., 21, 158–163 (1989).
H. Yang, M. Alnaqeeb, H. Simpson, and G. Goldspink, “Changes in muscle fibre type, muscle mass and IGF-I gene expression in rabbit skeletal muscle subjected to stretch,” J. Anat., 190, No. 4, 613–622 (1997).
T. Yimlamai, The Effects of Hindlimb Unweighting and Beta2-Agonist on the Ubiquitin-Proteasome Pathway and Insulin-Like Growth Factor I, PhD dissertation, University of Florida (2004).