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Journal of Cell Science, Vol 113, Issue 20 3583-3591, Copyright © 2000 by Company of Biologists
JOURNAL ARTICLES |
M Fluck, V Tunc-Civelek and M Chiquet
M. E. Muller-Institute for Biomechanics, Murtenstrasse 35, PO Box 30, CH-3010 Bern. flueck@mem.unibe.ch
Tenascin-C and tenascin-Y are two structurally related extracellular matrix glycoproteins that in many tissues show a complementary expression pattern. Tenascin-C and the fibril-associated minor collagen XII are expressed in tissues bearing high tensile stress and are located in normal skeletal muscle, predominantly at the myotendinous junction that links muscle fibers to tendon. In contrast, tenascin-Y is strongly expressed in the endomysium surrounding single myofibers, and in the perimysial sheath around fiber bundles. We previously showed that tenascin-C and collagen XII expression in primary fibroblasts is regulated by changes in tensile stress. Here we have tested the hypothesis that the expression of tenascin-C, tenascin-Y and collagen XII in skeletal muscle connective tissue is differentially modulated by mechanical stress in vivo. Chicken anterior latissimus dorsi muscle (ALD) was mechanically stressed by applying a load to the left wing. Within 36 hours of loading, expression of tenascin-C protein was ectopically induced in the endomysium along the surface of single muscle fibers throughout the ALD, whereas tenascin-Y protein expression was barely affected. Expression of tenascin-C protein stayed elevated after 7 days of loading whereas tenascin-Y protein was reduced. Northern blot analysis revealed that tenascin-C mRNA was induced in ALD within 4 hours of loading while tenascin-Y mRNA was reduced within the same period. In situ hybridization indicated that tenascin-C mRNA induction after 4 hours of loading was uniform throughout the ALD muscle in endomysial fibroblasts. In contrast, the level of tenascin-Y mRNA expression in endomysium appeared reduced within 4 hours of loading. Tenascin-C mRNA and protein induction after 4-10 hours of loading did not correlate with signs of macrophage infiltration. Tenascin-C protein decreased again with removal of the load and nearly disappeared after 5 days. Furthermore, loading was also found to induce expression of collagen XII mRNA and protein, but to a markedly lower level, with slower kinetics and only partial reversibility. The results suggest that mechanical loading directly and reciprocally controls the expression of extracellular matrix proteins of the tenascin family in skeletal muscle.
This article has been cited by other articles:
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  M. Fluck, S. Schmutz, M. Wittwer, H. Hoppeler, and D. Desplanches Transcriptional reprogramming during reloading of atrophied rat soleus muscle Am J Physiol Regulatory Integrative Comp Physiol, July 1, 2005; 289(1): R4 - R14. [Abstract] [Full Text] [PDF]
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 M. KJAeR Role of Extracellular Matrix in Adaptation of Tendon and Skeletal Muscle to Mechanical Loading Physiol Rev, April 1, 2004; 84(2): 649 - 698. [Abstract] [Full Text] [PDF]
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 M. Fluck, M. Kitzmann, C. Dapp, M. Chiquet, F. W. Booth, and A. Fernandez Transient induction of cyclin A in loaded chicken skeletal muscle J Appl Physiol, October 1, 2003; 95(4): 1664 - 1671. [Abstract] [Full Text] [PDF]
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 M. Chiquet and M. Fluck Ectopic expression of tenascin-C J. Cell Sci., October 1, 2003; 116(19): 3851 - 3851. [Full Text] [PDF]
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M. Chiquet and M. Fluck Rebuttal J. Cell Sci., October 1, 2003; 116(19): 3853 - 3853. [Full Text]
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T. A. H. Jarvinen, T. L. N. Jarvinen, P. Kannus, and H. Kalimo Reply J. Cell Sci., October 1, 2003; 116(19): 3851 - 3853. [Full Text]
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T. A. H. Jarvinen, L. Jozsa, P. Kannus, T. L. N. Jarvinen, T. Hurme, M. Kvist, M. Pelto-Huikko, H. Kalimo, and M. Jarvinen Mechanical loading regulates the expression of tenascin-C in the myotendinous junction and tendon but does not induce de novo synthesis in the skeletal muscle J. Cell Sci., March 1, 2003; 116(5): 857 - 866. [Abstract] [Full Text] [PDF]
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M. Fluck, M. Chiquet, S. Schmutz, M.-H. Mayet-Sornay, and D. Desplanches Reloading of atrophied rat soleus muscle induces tenascin-C expression around damaged muscle fibers Am J Physiol Regulatory Integrative Comp Physiol, March 1, 2003; 284(3): R792 - R801. [Abstract] [Full Text] [PDF]
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 M. Fluck, A. Ziemiecki, R. Billeter, and M. Muntener Fibre-type specific concentration of focal adhesion kinase at the sarcolemma: influence of fibre innervation and regeneration J. Exp. Biol., August 15, 2002; 205(16): 2337 - 2348. [Abstract] [Full Text] [PDF]
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