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Myofibrillar M-band proteins in rat skeletal muscles during development

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Summary

The distribution of three myofibrillar M-band proteins, myomesin, M-protein and the muscle isoform of creatine kinase, was investigated with immunocytochemical techniques in skeletal muscles of embryonic, fetal, newborn and four-week-old rats. Furthermore, muscles of newborn rats were denervated and examined at four weeks of age. In embryos, myomesin was present in all myotome muscle fibres of the somites, whereas M-protein was detected only in a small proportion of the myotome muscle fibres and muscle creatine kinase was not detected at all. In fetal and newborn muscles, all fibres contained all three M-band proteins. At four weeks of age, when fibre types (type 1 or slow twitch fibres and type 2 or fast twitch fibres) were clearly discernable, the pattern was changed. Myomesin and muscle creatine kinase were still observed in all fibres, whereas M-protein was present only in type 2 fibres. On the other hand, in muscle fibres denervated at birth all three M-band proteins were still detected. Our results suggest 1) that during the initial stages of myofibrillogenesis expression and incorporation of myomesin into the M-band precede that of M-protein and muscle creatine kinase; 2) that expression and incorporation of all three M-band proteins during fetal development is nerve independent and non coordinated to the expression of different forms of myosin heavy chains, and 3) that the suppression of M-protein synthesis during postnatal development is nerve dependent and reflects the maturation of slow twitch motor units.

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References

  • Arnold H, Pette D (1970) Binding of aldolase and TDA to F-actin and modificating of catalytic properties of aldolase. Eur J Biochem 15:360–366

    Google Scholar 

  • Bergh A, Helander HF, Wahlqvist L (1978) Studies on factors governing testicular descent in the rat — particularly the role of gubernaculum testis. Int J Androl 1:342–356

    Google Scholar 

  • Brooke MH, Kaiser KK (1970) Muscle fiber type: how many and what kind? Arch Neurol 23:369–379

    Google Scholar 

  • Brown MC, Booth CM (1983) Postnatal development of the adult pattern of motor axon distribution in rat muscle. Nature 304:741–742

    Google Scholar 

  • Butler-Browne GS, Whalen RG (1984) Myosin isozyme transitions occurring during the postnatal development of the rat soleus muscle. Dev Biol 102:324–334

    Google Scholar 

  • Bähler M, Wallimann T, Eppenberger HM (1985) Myofibrillar M-band proteins represent constituents of native thick filaments, frayed filaments and bare zone assemblages. J Muscle Res Cell Motil 6:783–800

    Google Scholar 

  • Carlsson E, Thornell L-E (1987) Diversification of the myofibrillar M-band in rat skeletal muscle during postnatal development. Cell Tissue Res 248:169–180

    Google Scholar 

  • Close RI (1964) Dynamic properties of fast and slow skeletal muscles of the rat during development. J Physiol 173:74–95

    Google Scholar 

  • Close RI (1972) Dynamic properties of mammalian skeletal muscle. Physiol Rev 52:129–197

    Google Scholar 

  • Dhoot GK (1986) Selective synthesis and degradation of slow skeletal muscle myosin heavy chains in developing muscle fibers. Muscle Nerve 9:155–164

    Google Scholar 

  • Drachman DB, Johnson DM (1973) Development of a mammalian fast muscle: dynamic and biochemical properties correlated. J Physiol 234:29–42

    Google Scholar 

  • Eppenberger HM, Perriard JC, Rosenberg UB, Strehler EE (1981) The Mr 165000 M-protein myomesin. A specific protein of cross-striated muscle cell. J Cell Biol 89:185–193

    Google Scholar 

  • Fairfield J (1948) Effects of cold on infant rats: body temperature, oxygen consumption, electrocardiograms. Am J Physiol 128:514

    Google Scholar 

  • Gambke B, Rubinstein NA (1984) A monoclonal antibody to the embryonic myosin heavy chain of rat skeletal muscle. J Biol Chem 259:12092–12100

    Google Scholar 

  • Gorza L (1990) Identification of a novel type 2 fiber population in mammalian skeletal muscle by combined use of histochemical myosin ATPase and antimyosin monoclonal antibodies. J Histochem Cytochem 38:257–265

    Google Scholar 

  • Grove BK, Kurer V, Lehner C, Doetschman TC, Perriard JC, Eppenberger HM (1984) A new 185000-dalton skeletal muscle protein detected by monoclonal antibodies. J Cell Biol 98:518–524

    Google Scholar 

  • Grove BK, Cerny L, Perriard J-C, Eppenberger HM (1985) Myomesin and M-protein: expression of two M-band proteins in pectoral muscle and heart during development. J Cell Biol 101:1413–1421

    Google Scholar 

  • Grove BK (1989) Muscle differentiation and the origin of muscle fiber diversity. CRC Crit Rev Neurobiol 4:201–233

    Google Scholar 

  • Grove BK, Cerny L, Perriard J-C, Eppenberger HM, Thornell L-E (1989) Fiber type-specific distribution of M-band proteins in chicken muscle. J Histochem Cytochem 37:447–454

    Google Scholar 

  • Knappeis GG, Carlsen F (1968) The ultrastructure of the M-line in skeletal muscle. J Cell Biol 38:202–211

    Google Scholar 

  • Kugelberg E (1976) Adaptive transformation of rat soleus motor units during growth. Histochemistry and contraction speed. J Neurol Sci 27:269–289

    Google Scholar 

  • Luther P, Squire J (1978) Three-dimensional structure of the vertebrate muscle M-region. J Mol Biol 125:313–324

    Google Scholar 

  • Lyons GE, Haselgrove J, Kelly AM, Rubenstein NA (1983) Myosin transitions in developing fast and slow muscles of the rat hindlimb. Differentiation 25:168–175

    Google Scholar 

  • Masaki T, Takaiti O (1974) M-protein. J Biochem (Tokyo) 75:367–380

    Google Scholar 

  • Narusawa M, Fitzsimmons RB, Jzumo S, Nadal-Girard B, Rubinstein NA, Kelly AM (1987) Slow myosin in developing rat skeletal muscle. J Cell Biol 104:447–459

    Google Scholar 

  • Otsu N, Hirata M, Tuboi S, Miyazawa K (1989) Immunocytochemical localization of creatine kinase M in canine myocardial cells: most creatine kinase M is distributed in the A-band. J Histochem Cytochem 37:1465–1470

    Google Scholar 

  • Riley DA (1977) Multiple innervation of fiber types in the soleus muscles of postnatal rats. Exp Neurol 56:400–409

    Google Scholar 

  • Savabi F, Geiger PJ, Bessman SP (1983) Kinetic properties and functional role of creatine phosphokinase in glycerinated muscle fibers. Further evidence for compartmentation. Biochem Biophys Res Commun 114:785–790

    Google Scholar 

  • Schiaffino S, Gorza L, Sartore S, Saggin L, Ausoni S, Vianello M, Gundersen K, Lømo T (1989) Three myosin heavy chain isoforms in type 2 skeletal muscle fibres. J Muscle Res Cell Motil 10:197–205

    Google Scholar 

  • Sjöström M, Thornell L-E, Cedergren E (1973) The application of cryoultramicroscopy in the study of the fine structure of myofilaments. J Microsc 99:193–204

    Google Scholar 

  • Strehler EE, Carlsson E, Eppenberger HM, Thornell L-E (1983) Ultrastructural localization of M-band proteins in chicken breast muscle as revealed by combined immunocytochemistry and ultramicrotomy. J Mol Biol 166:141–158

    Google Scholar 

  • Termin A, Staron RS, Pette D (1989) Myosin heavy chain isoforms in histochemically defined fiber types of rat musclce. Histochemistry 92:453–457

    Google Scholar 

  • Thornell L-E, Butler-Browne GS, Carlsson E, Eppenberger HM, Fürst DO, Grove BK, Holmbom B, Small JV (1986) Cryoultramicrotomy and immunocyto-chemistry in the analysis of muscle fine structure. Scan Electron Microsc 9:1407–1418

    Google Scholar 

  • Thornell L-E, Carlsson E, Kugelberg E, Grove BK (1987) Myofibrillar M-band structure and composition of physiologically defined rat motor units. Am J Physiol 253:456–468

    Google Scholar 

  • Thornell L-E, Carlsson E, Pedrosa F (1990) M-band structure and composition in relation to fiber types. In: Pette D (ed) The dynamic state of muscle fibers. Walter de Gruyte, Berlin New York, pp 369–383

    Google Scholar 

  • Tokuyasu KT (1980) Immunochemistry on ultrathin frozen sections. Histochem J 12:381–403

    Google Scholar 

  • Turner DC, Wallimann T, Eppenberger HM (1973) A protein that binds specifically to the M-line of skeletal muscle is identified as the muscle form of creatine kinase. Proc Natl Acad Sci USA 70:702–705

    Google Scholar 

  • Wallimann T, Turner DC, Eppenberger HM (1975) Creatine kinase and M-line structure. In: Biro EVA (ed) Proteins of contractile systems. Proc 9th Eur Meeting, Budapest, Hungary 1974. FEBS 31:119–124

    Google Scholar 

  • Wallimann T, Turner DC, Eppenberger HM (1977a) Localization of creatine kinase isoenzymes in myofibrils. I. Chicken skeletal muscle. J Cell Biol 75:297–317

    Google Scholar 

  • Wallimann T, Kuhn HJ, Pelloni G, Turner DC, Eppenberger HM (1977b) Localization of creatine kinase isoenzymes in myofibrils. I. Chicken heart muscle. J Cell Biol 75:318–325

    Google Scholar 

  • Wallimann T, Pelloni G, Turner DC, Eppenberger HM (1978) Monovalent antibodies against MM-creatine kinase remove the M-line from myofibrils. Proc Natl Acad Sci USA 75:4296–4300

    Google Scholar 

  • Wallimann T, Doetschman TC, Eppenberger HM (1983) Novel staining pattern of skeletal muscle M-lines upon incubation with antibodies against MM-creatine kinase. J Cell Biol 96:1772–1779

    Google Scholar 

  • Wallimann T, Eppenberger HM (1985) Localization and function of M-line-bound creatine kinase. M-band model and creatine phosphate shuttle. Cell Muscle Motil 6:239–285

    Google Scholar 

  • Wallimann T, Schnyder T, Schlegel J, Wyss M, Wegmann G, Rossi A-M, Hemmer W, Eppenberger HM, Quest AFG (1989) Subcellular compartmentation of creatine kinase isoenzymes, regulation of CK and octameric structure of mitochondrial CK: important aspects of thephosphoryl-creatine circuit. In: Paul RJ, Elzinga G, Yamada K (eds) Progress in clinical and biological research. Muscle Energetics, vol. 315. Alan R. Liss, New York, pp 159–176

    Google Scholar 

  • Wegman R, Kishino Y, Samannoudy FA (1974) Histochemical study on creatine kinase of developing and denervated rat muscle as compared with glycolytic and oxidative enzymes. Ann Histochem 19:227–238

    Google Scholar 

  • Wegmann E, Eppenberger HM, Wallimann T (1987) In situ localization of creatine kinase (CK) in skeletal muscle. J Muscle Res Cell Motil 8:90

    Google Scholar 

  • Woodhead JL, Lowey S (1982) Size and shape of skeletal bound M-protein. J Mol Biol 157:149–154

    Google Scholar 

  • Ziter FA (1974) Creatine kinease in developing skeletal and cardiac muscle of the rat. Exp Neurol 43:539–546

    Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy, University of Ume», S-90187, Ume», Sweden

    E. Carlsson, B. K. Grove & L. E. Thornell

  2. Institute for Cell Biology, ETH, CH-8093, Zürich, Switzerland

    T. Wallimann & H. M. Eppenberger

Authors
  1. E. Carlsson
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  2. B. K. Grove
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  3. T. Wallimann
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  4. H. M. Eppenberger
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  5. L. E. Thornell
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Carlsson, E., Grove, B.K., Wallimann, T. et al. Myofibrillar M-band proteins in rat skeletal muscles during development. Histochemistry 95, 27–35 (1990). https://doi.org/10.1007/BF00737225

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