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A combined histochemical and immunohistochemical study on the dynamics of fast-to-slow fiber transformation in chronically stimulated rabbit muscle

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Summary

Chronically stimulated fast-twitch muscles of the rabbit were histochemically and immunohistochemically analyzed in serial cross sections (1) for percentages of fiber types, and (2) for the presence of myosin heavy chain isoforms during fast-to-slow transformation. By four weeks of stimulation the number of type-I fibers had increased more than fourfold, while only about 6% of the original IIB fibers remained. Type-IC and -IIC fibers transiently rose to 20% of the total fiber population. After 16 weeks, the number of type-I fibers had increased to 42%. With prolonged stimulation fewer fibers reacted with antibodies against embryonic and neonatal myosins and more with the antibody against slow myosin. The reaction for embryonic myosin was most often detected in the C fibers (IC, IIC). Immunohistochemical subtypes were observed for each fiber type in the stimulated muscles. The greatest number was seen in type-IIC fibers, which, in addition to their reaction for fast/neonatal and slow myosins, might also react with the antibodies against neonatal/embryonic and embryonic myosins. These findings indicated that the transforming fibers temporarily expressed myosin heavy chain isoforms normally not detectable in adult skeletal muscle. Myotubes reacted strongly with the antibodies against fast/neonatal and embryonic myosins, and some of them also with the antibody against slow myosin. Thus, it appears that under the influence of the low frequency stimulus pattern some of the newly formed myotubes developed into type-I fibers.

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References

  • Bandman E, Matsuda R, Strohman RC (1982) Developmental appearance of myosin heavy and light chain isoforms in vivo and in vitro in chicken skeletal muscle. Dev Biol 93:508–518

    Google Scholar 

  • Brooke MH, Kaiser KK (1970) Three “myosin adenosine triphosphatase” systems: the nature of their pH lability and sulfhydryl dependence. J Histochem Cytochem 18:670–672

    CAS  PubMed  Google Scholar 

  • Brown WE, Salmons S, Whalen RG (1983) The sequential replacement of myosin subunit isoforms during muscle type transformation induced by long term electrical stimulation. J Biol Chem 258:14686–14692

    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 

  • 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 

  • Heilmann C, Pette D (1979) Molecular transformations in sarcoplasmic reticulum of fast-twitch muscle by electro-stimulation. Eur J Biochem 93:437–446

    Google Scholar 

  • Hoh JFY, Yeoh GPS (1979) Rabbit skeletal myosin isoenzymes from fetal, fast-twitch and slow-twitch muscles. Nature (Lond) 280:321–322

    Google Scholar 

  • Izumo S, Nadal-Ginard B, Mahdavi V (1986) All members of the MHC multigene family respond to thyroid hormone in a highly tissue-specific manner. Science 231:597–600

    Google Scholar 

  • Leberer E, Pette D (1986) Immunochemical quantification of sarcoplasmic reticulum Ca-ATPase, of calsequestrin and of parvalbumin in rabbit skeletal muscles of defined fiber composition. Eur J Biochem 156:489–496

    Google Scholar 

  • Lowey S, Benfield PA, LeBlanc DD, Waller GS (1983) Myosin isozymes in avian skeletal muscles. I. Sequential expression of myosin isozymes in developing chicken pectoralis muscles. J Muscle Res Cell Motil 4:695–716

    Google Scholar 

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

    Google Scholar 

  • Mabuchi K, Szvetko D, Pinter K, Sréter FA (1982) Type-IIB to IIA fiber transformation in intermittently stimulated rabbit muscles. Am J Physiol 242:C373-C381

    Google Scholar 

  • Maier A, Pette D (1987) The time course of glycogen depletion in single fibers of chronically stimulated rabbit fast-twitch muscle. Pflügers Arch 408:338–342

    Google Scholar 

  • Maier A, Gambke B, Pette D (1986) Degeneration-regeneration as a mechanism contributing to the fast to slow conversion of chronically stimulated fast-twitch rabbit muscle. Cell Tissue Res 244:635–643

    Google Scholar 

  • Martin AF, Rabinowitz M, Blough R, Prior G, Zak R (1977) Measurements of half-life of rat cardiac myosin heavy chain with leucyl-tRNA used as precursor pool. J Biol Chem 252:3422–3429

    Google Scholar 

  • Matsuda R, Spector DH, Strohman RC (1983) Regenerating adult chicken skeletal muscle and satellite cell cultures express embryonic patterns of myosin and tropomyosin isoforms. Dev Biol 100:478–488

    Google Scholar 

  • Obinata T (1985) Changes in myofibrillar protein isoform expression during chicken skeletal muscle development. Zool Sci 2:833–847

    Google Scholar 

  • Pette D, Schnez U (1977) Coexistence of fast and slow type myosin light chains in single muscle fibres during transformation as induced by long term stimulation. FEBS Lett 83:128–130

    Google Scholar 

  • Pette D, Tyler KR (1983) Response of succinate activity in fibres of rabbit tibialis anterior muscle to chronic nerve stimulation. J Physiol (Lond) 338:1–9

    Google Scholar 

  • Pette D, Smith ME, Staudte HW, Vrbová G (1973) Effects of long-term electrical stimulation on some contractile and metabolic characteristics of fast rabbit muscles. Pflügers Arch 338:257–272

    Google Scholar 

  • Pette D, Müller W, Leisner E, Vrbová G (1976) Time dependent effects on contractile properties, fibre population, myosin light chains and enzymes of energy metabolism in intermittently and continuously stimulated fast twitch muscle of the rabbit. Pflügers Arch 364:103–112

    Google Scholar 

  • Reichmann H, Srihari T, Pette D (1983) Ipsiand contralateral fibre transformations by cross-reinnervation. A principle of symmetry. Pflügers Arch 397:202–208

    Google Scholar 

  • Rubinstein N, Mabuchi K, Pepe F, Salmons S, Gergely J, Sréter F (1978) Use of type-specific antimyosins to demonstrate the transformation of individual fibers in chronically stimulated rabbit fast muscles. J Cell Biol 79:252–261

    Google Scholar 

  • Salmons S, Vrbová G (1969) The influence of activity on some contractile characteristics of mammalian fast and slow muscles. J Physiol (Lond) 201:535–549

    Google Scholar 

  • Sartore S, Gorza L, Schiaffino S (1982) Fetal myosin heavy chains in regenerating muscle. Nature (Lond) 298:294–296

    Google Scholar 

  • Schiaffino S, Gorza L, Pitton G, Saggin L, Ausoni S, Sartore S, Lömo T (1988) Embryonic and neonatal myosin heavy chain in denervated and paralyzed rat skeletal muscle. Dev Biol 127:1–11

    Google Scholar 

  • Schwarz G, Leisner E, Pette D (1983) Two telestimulation systems for chronic indirect muscle stimulation in caged rabbits and mice. Pflügers Arch 398:130–133

    Google Scholar 

  • Seedorf K, Seedorf U, Pette D (1983) Coordinate expression of alkali and DTNB myosin light chains during transformation of rabbit fast muscle by chronic stimulation. FEBS Lett 158:321–324

    Google Scholar 

  • Sréter FA, Gergely J, Salmons S, Romanul F (1973) Synthesis by fast muscle of myosin light chains characteristic of slow muscle in response to long-term stimulation. Nature New Biol (Lond) 241:17–19

    Google Scholar 

  • Srihari T, Seedorf U, Pette D (1981) Ipsiand contralateral changes in rabbit soleus myosins by cross-reinnervation. Pflügers Arch 390:246–249

    Google Scholar 

  • Staron RS, Hikida RS, Hagerman FC (1983) Reevaluation of human muscle fast-twitch subtypes: evidence for a continuum. Histochemistry 78:33–39

    Google Scholar 

  • Staron RS, Pette D (1986) Correlation between myofibrillar AT-Pase activity and myosin heavy chain composition in rabbit muscle fibers. Histochemistry 86:19–23

    Google Scholar 

  • Staron RS, Pette D (1987a) Nonuniform myosin expression along single fibers of chronically stimulated and contralateral rabbit tibialis anterior muscles. Pflügers Arch 409:67–73

    Google Scholar 

  • Staron RS, Pette D (1987b) The multiplicity of myosin light and heavy chain combinations in histochemically typed single fibres. Rabbit soleus muscle. Biochem J 243:687–693

    Google Scholar 

  • Staron RS, Gohlsch B, Pette D (1987) Myosin polymorphism in single fibers of chronically stimulated rabbit fast-twitch muscle. Pflügers Arch 408:444–450

    Google Scholar 

  • Sweeney HL, Kushmerick MJ, Mabuchi K, Gergely J, Sréter FA (1986) Velocity of shortening and myosin isozymes in two types of rabbit fast-twitch muscle fibers. Am J Physiol 251:C431-C434

    Google Scholar 

  • Whalen RG (1985) Myosin isoenzymes as molecular markers for muscle physiology. J Exp Biol 115:43–55

    Google Scholar 

  • Whalen RG, Schwartz K, Bouveret P, Sell SM, Gros F (1979) Contractile protein isozymes in muscle development: identification of an embryonic form of myosin heavy chain. Proc Natl Acad Sci USA 76:5197–5201

    Google Scholar 

  • Whalen RG, Sell SM, Butler-Browne GS, Schwartz K, Bouveret P, Pinset-Härström I (1981) Three myosin heavy-chain isozymes appear sequentially in rat muscle development. Nature (Lond) 292:805–809

    Google Scholar 

  • Winkelmann DA, Lowey S, Press JL (1983) Monoclonal antibodies localize changes on myosin heavy chain isozymes during avian myogenesis. Cell 34:295–306

    Google Scholar 

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Author notes

  1. Alfred Maier

    Present address: Department of Cell Biology and Anatomy, University of Alabama at Birmingham, AL 35294, Birmingham, USA

  2. Luisa Gorza & Stefano Schiaffino

    Present address: Institute of General Pathology, Via Loredan 16, I-35131, Padova, Italy

Authors and Affiliations

  1. Fakultät für Biologie, Universität Konstanz, Konstanz, Germany

    Alfred Maier, Luisa Gorza, Stefano Schiaffino &  Dirk Pette

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  1. Alfred Maier
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  2. Luisa Gorza
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  3. Stefano Schiaffino
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  4. Dirk Pette
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Maier, A., Gorza, L., Schiaffino, S. et al. A combined histochemical and immunohistochemical study on the dynamics of fast-to-slow fiber transformation in chronically stimulated rabbit muscle. Cell Tissue Res. 254, 59–68 (1988). https://doi.org/10.1007/BF00220017

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  • DOI: https://doi.org/10.1007/BF00220017

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