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Prolonged passive stretch of rat soleus muscle provokes an increase in the mRNA levels of the muscle regulatory factors distributed along the entire length of the fibers

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Abstract

The mRNA levels of the adult and the neonatal sarcoplasmic/endoplasmic reticulum Ca2+-ATPases (SERCA1a and SERCA1b, respectively) and those of the muscle regulatory factors (MRFs: myoD, myf-5, myogenin, MRF4) have been assessed by RT PCR in rat soleus muscles immobilized for 3 days in an extended position (passive stretch). The transcript level of the fast type SERCA1a Ca2+-transport ATPase decreased to half of its normal value, whereas that of neonatal SERCA1b isoform increased 5-fold above control in stretched muscles. Immunostaining of muscle cross sections showed that the fraction of fibers expressing the SERCA1a protein was decreased evenly along the length of the stretched muscles indicating that a transformation occurred of fast fibers to slow ones. The mRNA levels of MRFs were elevated 3- to 6-fold above the normal level and were distributed evenly along the length of the stretched muscles. However in the controls these transcripts were more abundant at both ends of the muscle. The stretch increased the level of myoD and immunocytochemistry showed the expression of myoD protein in a number of nuclei of the stretched muscles whereas it was practically undetectable by this method in the control muscles. Western blotting did not indicate a significant stretch-induced increase in the level of the myogenin protein, in spite of the fact that immunocytochemistry tended to show more myogenin-positive nuclei in stretched muscles as compared to the controls. These data indicate that after 3 days of passive stretch the central and the terminal parts of the soleus muscle adapt similarly by increasing the levels of the MRFs, by decreasing the overall levels of the fast SERCA1-type of ATPase and by partially re-establishing a neonatal mode of alternative SERCA1 transcript splicing resulting in an increased SERCA1b/1a ratio.

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References

  • Alway SE, Winchester PK, Davis ME and Gonyea WJ (1989) Regionalized adaptations and muscle fiber proliferation in stretch-induced enlargement. J Appl Physiol 66: 771-781.

    Google Scholar 

  • Cornelison DDW and Wold BJ (1997) Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle cells. Dev Biol 191: 270-283.

    Google Scholar 

  • Creuzet S, Lescaudron L, Li Z and Fontaine-Perus J (1998) MyoD, myogenin and desmin-nls-lacZ trangene emphasize the distinct patterns of satellite cell activation in growth and regeneration. Exp Cell Res 243: 241-253.

    Google Scholar 

  • Delp MD and Duan C (1996) Composition and size of type I, IIA, IID/X and IIB fibers and citrate synthetase activity of rat muscle. J Appl Physiol 80: 261-270.

    Google Scholar 

  • Dix DJ and Eisenberg BR (1990) Myosin mRNA accumulation and myofibrillogenesis at the myotendinous junction of stretched muscle fibers. J Cell Biol 111: 1885-1894.

    Google Scholar 

  • Dix DJ and Eisenberg BR (1991) Redistribution of myosin heavy chain mRNA in the midregion of stretched muscle fibers. Cell Tissue Res 263: 61-69.

    Google Scholar 

  • Fontaine B and Changeux J-P (1989) Localization of nicotinic acetylcholine receptor a-subunit transcripts during myogenesis and motor endplate development in the chick. J Cell Biol 108: 1025-1037.

    Google Scholar 

  • Füchtbauer E-M and Westphal H (1992) MyoD and myogenin are coexpressed in regenerating skeletal muscle of the mouse. Dev Dynamics 193: 34-39.

    Google Scholar 

  • Gerber AN, Klesert TR, Bergstrom DA and Tapscott SJ (1997) Two domains of myoD mediate transcriptional activation of genes in repressive chromatin: a mechanism for lineage determination in myogenesis. Genes & Dev 11: 436-450.

    Google Scholar 

  • Goblet C and Whalen RG (1995) Modifications of gene expression in myotonic murine skeletal muscle associated with abnormal expression of myogenic regulatory factors. Dev Biol 170: 262-273.

    Google Scholar 

  • Goldspink DF (1977) The influence of immobilization and stretch on protein turnover of rat skeletal muscle. J Physiol (Lond) 264: 267-282.

    Google Scholar 

  • Goldspink DF, Cox VM, Smith SK, Eaves LA, Osbaldeston NJ, Lee DM and Mantle D (1995) Muscle growth in response to mechanical stimuli. Am J Physiol 268: E288-E297.

    Google Scholar 

  • Goldspink G, Scutt A, Loughna T, Wells DJ, Jaenicke T and Gerlach GF (1992) Gene expression in skeletal muscle in response to stretch and force generation. Am J Physiol 262: R356-R363.

    Google Scholar 

  • Grounds MD, Garrett KL, Lai MC, Wright WE and Beilharz MW (1992) Identification of skeletal muscle precursor cells in vivo by use of MyoD1 and myogenin probes. Cell Tissue Res 267: 99-104.

    Google Scholar 

  • Jacobs-EL J, Zhou M-Y and Russel B (1995) MRF4, Myf-5 and myogenin mRNAs in the adaptive responses of mature rat muscle. Am J Physiol 268: C1045-C1052.

    Google Scholar 

  • Kelly M(1978) Perisynaptic satellite cells in the developing and mature rat soleus muscle. Anat Rec 190: 891-904.

    Google Scholar 

  • Kennedy JM, Eisenberg BR, Reid SK, Sweeney LJ and Zak R (1988) Nascent muscle fiber appearance in overloaded chicken slow-tonic muscle. Am J Anat 181: 203-215.

    Google Scholar 

  • Koishi K, Zhang M, Mclennan IS and Harris J (1995) MyoD protein accumulates in satellite cells and is neurally regulated in regenerating myotubes and skeletal muscle fibers. Dev Dynamics 202: 244-254.

    Google Scholar 

  • Lazarides E (1980) Intermediate filaments as mechanical integrator of cellular space. Nature 238: 249-256.

    Google Scholar 

  • Li H and Capetanaki (1993) Regulation of the mouse desmin gene: transactivation by MyoD, myogenin, MRF4 and Myf-5. Nucleic Acids Res 21: 335-343.

    Google Scholar 

  • Li Z, Mericskay M, Agbulut O, Butler-Browne G, Carlsson L, Thornell L-E, Babinet C and Paulin D (1997) Desmin is essential for the tensile strength and integrity of myofibrils but not for myogenic commitment, differentiation and fusion of skeletal muscle. J Cell Biol 139: 129-144.

    Google Scholar 

  • Lin H, Yutzey KE and Konieczny SF (1991) Muscle-specific expression of the troponin I gene requires interactions between helix-loop-helix muscle regulatory factors and ubiquitous transcription factors. Mol Cell Biol 11: 267-280.

    Google Scholar 

  • Loughna PT, Izumo S, Goldspink G and Nadal-Ginard B (1990) Disuse and passive stretch cause rapid alterations in expression of developmental and adult contractile protein genes in skeletal muscle. Development 109: 217-223.

    Google Scholar 

  • Loughna PT and Brownson C (1996) Two myogenic regulatory factor transcripts exhibit muscle specific response to disuse and passive stretch in adult rats. FEBS Lett 390: 304-306.

    Google Scholar 

  • Lowe DA, Lund T and Alway SE (1998) Hypetrophy-stimulated myogenic regulatory factor mRNA increases are attenuated in fast muscle of aged quails. Am J Physiol 275C: 155-162.

    Google Scholar 

  • Ludolph DC and Konieczny SF (1995) Transcription factor families: muscling on the myogenic program. FASEB J 9: 1595-1604.

    Google Scholar 

  • Maione R and Amati P (1996) Interdependence between muscle differentiation and cell-cycle control. Biochem Biophys Acta 1332: M19-M30.

    Google Scholar 

  • Marsh DR, Criswell DS, Carson JA and Booth FW (1997) Myogenic regulatory factors during regeneration of skeletal muscle in young, adult, and old rats. J Appl Physiol 83: 1270-1275.

    Google Scholar 

  • Mendler L, Szakonyi G, Zador E, Gorbe A, Dux L and Wuytack F (1998) Expression of sarcoplasmic/endoplasmic reticulum Ca2+ ATPases in the rat extensor digitorum longus (EDL) muscle regenerating from notexin-induced necrosis. J Muscle Res & Cell Motil 19: 777-785.

    Google Scholar 

  • Mendler L, Zador E, Dux L and Wuytack F (1998) mRNA levels of myogenic regulatory factors in rat slow and fast muscles regenerating from notexin-induced necrosis. Neuromusc Disord 8: 533-541.

    Google Scholar 

  • Moss JB, Olson EN and Schwartz RJ (1996) The myogenic regulatory factor MRF4 represses the cardiac a-actin promoter through a negative-acting N-terminal protein domain. J Biol Chem 271: 31688-31694.

    Google Scholar 

  • Musaro A, Cusella de Angelis MG, Germani A, Ciccarelli C, Molinaro M and Zani BM (1995) Enhanced expression of myogenic regulatory genes in aging skeletal muscle. Exp Cell Res 221: 241-248.

    Google Scholar 

  • Newlands S, Levitt LK, Robinson CS, Karpf ABC, Hodgson VRM, Wade RP and Hardeman EC (1998) Transcription occurs in pulses in muscle fibers. Genes & Dev 12: 2748-2758.

    Google Scholar 

  • Osbaldeston JN, Lee DM, Cox VM, Hesketh JE, Morrison JFJ, Blairs GE and Goldspink DF (1995) The temporal and cellular expression of c-fos and c-jun in mechanically stimulated rabbit latissimus dorsi muscle. Biochem J 308: 465-471.

    Google Scholar 

  • Olson EN and Klein WH (1994) bHLH factors in muscle development: dead lines and commitments, what to leave in and what to leave out. Genes and Devel 8: 1-8.

    Google Scholar 

  • Rantanen J, Hurme T, Lukka R, Heino J and Kalimo H (1995) Satellite cell proliferation and the expression of myogenin and desmin in regenerating skeletal muscle: Evidence for two different populations of satellite cells. Lab Invest 72: 341-347.

    Google Scholar 

  • Rosser BWC, Waldbillig DM, Lovo SD, Armstrong JD and Bandman E (1995) Myosin heavy chain expression within the tapered ends of skeletal muscle fibers. Anat Rec 242: 462-470.

    Google Scholar 

  • Smith CK, Janney MJ and Allen RE (1994) Temporal expression of myogenic regulatory genes during activation, proliferation and differentiation of rat skeletal muscle satellite cells. J Cell Physiol 159: 379-385.

    Google Scholar 

  • Stickland NC (1983) The arrangement of muscle fibers and tendons in two muscles used for growth studies. J Anat 136: 175-179.

    Google Scholar 

  • Williams PE and Goldspink G (1971) Longitudinal growth of striated muscle fibers. J Cell Sci 9: 751-767.

    Google Scholar 

  • Williams PE and Goldspink G (1973) The effect of immobilization on the longitudinal growth of striated muscle fibers. J Anat 116: 45-55.

    Google Scholar 

  • Wuytack F, Raeymaekers L, Eggermont J, Van den Bosch L, Verboomen H and Mertens L (1998) Isoform diversity and regulation of organellar-type Ca2+-transport ATPases. Adv Mol Cell Biol 23A: 205-248.

    Google Scholar 

  • Yang S, Alnaqeeb M, Simpson H and Goldspink G (1996) Cloning and characterization of an IGF-1 isoform expressed in skeletal muscle subjected to stretch. J Muscle Res & Cell Motil 17: 487-495.

    Google Scholar 

  • Zador E, Mendler L, Ver Heyen M, Dux L and Wuytack F (1996) Changes in mRNA levels of the sarcoplasmic/endoplasmic-reticulum Ca2+ ATPase isoforms in the rat soleus muscle regenerating from notexin-induced necrosis. Biochem J 320: 461-464.

    Google Scholar 

  • Zador E, Szakonyi G, Racz G, Mendler L, Ver Heyen M, Lebacq J, Dux L and Wuytack F (1998) Expression of the sarcoplasmic reticulum Ca2+ transport ATPase protein isoforms during regeneration from notexin-induced necrosis of rat soleus muscle. Acta Histochem 100: 355-369.

    Google Scholar 

  • Zahradka P, Larson DE and Sells BH (1989) RNA polymerase II-directed gene transcription by rat skeletal muscle nuclear extracts. Exp Cell Res 185: 8-20.

    Google Scholar 

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Authors and Affiliations

  1. Inst. Biochem., Albert Szent-Gyorgyi Med. Univ., Szeged, Dom ter 9, P.O. Box 415, H-6701, Hungary

    ERNÖ ZÁDOR & LÁSZLÓ DUX

  2. Lab. Physiol., KULeuven, Campus Gasthuisberg, Leuven, B-3000, Belgium

    FRANK WUYTACK

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  1. ERNÖ ZÁDOR
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  2. LÁSZLÓ DUX
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  3. FRANK WUYTACK
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ZÁDOR, E., DUX, L. & WUYTACK, F. Prolonged passive stretch of rat soleus muscle provokes an increase in the mRNA levels of the muscle regulatory factors distributed along the entire length of the fibers. J Muscle Res Cell Motil 20, 395–402 (1999). https://doi.org/10.1023/A:1005541522599

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