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Fiber type and non-endplate acetylcholinesterase in normal and experimentally altered muscles

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Summary

The non-endplate (sarcoplasmic) acetylcholinesterase (AChE) was investigated in eight different muscles of the rat. Serial consecutive sections were stained for AChE, myofibrillar ATPase (after alkaline and acid preincubation), and cytochrome C-oxidase. The following general correlation could be established: within a given muscle the sarcoplasmic AChE was highest in type IIB fibers, lowest in type I and intermediate in type IIA. Additionally, the intensity of the reaction was directly proportional to the size of the type IIA fibers. The distribution of sarcoplasmic AChE was correlated to the ATPase fiber types but was complementary to the cytochrome C-oxidase staining pattern.

In single fiber preparations, accumulation of AChE at the myotendinous junction was found to occur in “caplike” form exclusively in fibers with very low or absent sarcoplasmic AChE.

To study the role of innervation in the expression of the sarcoplasmic AChE, we cross-reinnervated the extensor digitorum longus (EDL) muscle with the soleus (SOL) nerve and vice versa (X-EDL, X-SOL). In the X-EDL the sarcoplasmic AChE was transformed to that of a normal SOL as were also the ATPase and the cytochrome oxidase. Surprisingly, in the X-SOL the high AChE activity typical for a normal EDL was present after 3 weeks but decreased steadily to very low levels lacking any correlation with ATPase and cytochrome oxidase. The results suggest that the cytoplasmic AChE of the SOL muscle depends more on the load-bearing function of the muscle than on the imposed impulse pattern. There is additional evidence for a retrograde effect of the X-SOL upon its motoneurons.

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References

  • Armstrong RB, Phelps RO (1984) Muscle fiber type composition of the rat hindlimb. Am J Anat 171:259–272

    Google Scholar 

  • Bacou F, Vigneron P, Massoulié J (1982) Acetylcholinesterase forms in fast and slow rabbit muscle. Nature 296:661–664

    Google Scholar 

  • Bacou F, Vigneron P, Couraud JY (1985) Retrograde effect of muscle forms of acetylcholinesterase in peripheral nerves. J Neurochem 45:1178–1185

    Google Scholar 

  • Brimijoin S (1983) Molecular forms of acetylcholinesterase in brain, nerve and muscle: nature, localization and dynamics. Progr Neurobiol 21:291–322

    Google Scholar 

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

    Google Scholar 

  • Couteaux R (1953) Particularités histochimiques des zones d'insertion du muscle strié. CR Soc Biol 147:1974–1976

    Google Scholar 

  • Couteaux R, Nachmansohn N (1940) Changes of choline esterase at end plate of voluntary muscle following section of sciatic nerve. Proc Soc Exp Biol Med 43:177–181

    Google Scholar 

  • Dettbarn WD (1981) A distinct difference between slow and fast muscle in acetylcholinesterase recovery after reinnervation in the rat. Exp Neurol 74:33–50

    Google Scholar 

  • Entrikin RK, Patterson GT, Mouritsen JA, Wilson BW (1983) Water deprivation: beneficial effect on muscular dystrophy in chickens. Exp Neurol 79:746–752

    Google Scholar 

  • Gabella G (1964) Contribution à l'étude de la jonction musculotendineuse au cours du développement. CR Ass Anat 49e Réunion: 619–623

    Google Scholar 

  • Gerebtzoff MA, Ueten L (1954) Presence d'appareils cholin-estérasiques musculo-tendineux chez divers mammifères, notamment chez l'homme, et leur persistance après dénervation. CR Soc Biol 148:1896–1898

    Google Scholar 

  • Gisiger V, Stephens H (1982) Acetylcholinesterase content in both motor nerve and muscle is correlated with twitch properties. Neurosci Lett 31:301–305

    Google Scholar 

  • Gisiger V, Stephens H (1982–83) Correlation between the acetylcholinesterase content in motor nerves and their muscles. J Physiol (Paris) 78:720–728

    Google Scholar 

  • Gottschall J, Zenker W, Neuhuber W, Mysicka A, Müntener M (1980) The sternomastoid muscle of the rat and its innervation. Muscle fiber composition, perikarya and axons of efferent and afferent neurons. Anat Embryol 160:285–300

    Google Scholar 

  • Groswald DE, Dettbarn WD (1983) Characterization of acetylcholinesterase molecular forms in slow and fast muscle of rat. Neurochem Res 8:983–995

    Google Scholar 

  • Gruber H, Zenker W (1978) Acetylcholinesterase activity in motor nerve fibres in correlation to muscle fiber types in rat. Brain Res 141:325–334

    Google Scholar 

  • Gupta RC, Misulis KE, Dettbarn WD (1985) Changes in the cholinergic system of rat sciatic nerve and skeletal muscle following suspension-induced disuse. Exp Neurol 89:622–633

    Google Scholar 

  • Guth L, Brown WC (1965) The sequence of changes in cholinesterase activity during reinnervation of muscle. Exp Neurol 12:329–336

    Google Scholar 

  • Guth L, Samaha FJ (1970) Procedure for the histochemical demonstration of actomyosin ATPase. Exp Neurol 28:365–367

    Google Scholar 

  • Guth L, Albers RW, Brown WC (1964) Quantitative changes in cholinesterase activity of denervated muscle fibers and sole plates. Exp Neurol 10:236–250

    Google Scholar 

  • Karnovsky MJ, Roots L (1964) A “direct-coloring” thiocholine method for cholinesterases. J Histochem Cytochem 12:219–221

    Google Scholar 

  • Koelle GB, Friedenwald JS (1949) A histochemical method for localizing cholinesterase activity. Proc Soc Exp Biol Med 70:617–622

    Google Scholar 

  • Linkhart TA, Yee GW, Wilson BW (1975) Myogenic defect in acetylcholiensterase regulation in muscular dystrophy of the chicken. Science 187:549–551

    Google Scholar 

  • Lømo T, Massoulié J, Vigny M (1985) Stimulation of denervated rat soleus muscle with fast and slow activity patterns induces different expression of acetylcholinesterase molecular forms. J Neurosci 5:1180–1187

    Google Scholar 

  • Lubinska L (1967) Influence of denervation on acetylcholinesterase in developing fast and slow muscles of the rat: In: Milhorat (ed) Exploratory concepts in muscular dystrophy and related disorders, Harriman, New York

  • Lubinska L, Zelena J (1967) Acetylcholinesterase at muscle-tendon junctions during postnatal development in rats. J Anat 101:295–308

    Google Scholar 

  • Massoulié J, Bon S (1982) The molecular forms of cholinesterase and acetylcholinesterase in vertebrates. Ann Rev Neurosci 5:57–106

    Google Scholar 

  • Mayr R, Zenker W, Gruber H (1967) Zwischensehnenfreie Skeletmuskelfaserverbindungen. Cell Tissue Res 79: 319–325

    Google Scholar 

  • Misulis KE, Dettbarn WD (1985) Is fast fiber innervation responsible for increased acetylcholinesterase activity in reinnervating soleus muscles? Exp Neurol 89:204–212

    Google Scholar 

  • Mumenthaler M, Engel WK (1961) Cytological localization of cholinesterase in developing chick embryo skeletal muscle. Acta Anat 47:274–299

    Google Scholar 

  • Müntener M (1979) Variable pH dependence of the myosin ATPase in different muscles of the rat. Histochemistry 62:299–304

    Google Scholar 

  • Müntener M (1982) A rapid and reversible muscle fiber transformation in the rat. Exp Neurol 77:668–678

    Google Scholar 

  • Müntener M, Srihari T (1984) Changes of myosin and its ATPase in “neuronally” and “mechanically” contralateral muscles after cross-reinnervation in normal and capsaicin-treated rats. Exp Neurol 86:134–146

    Google Scholar 

  • Müntener M, Gottschall J, Neuhuber W, Mysicka A, Zenker W (1980) The ansa cervicalis and the infrahyoid muscles of the rat. I. Anatomy; distribution, number and diameter of fiber types. Anat Embryol 159:49–57

    Google Scholar 

  • Müntener M, Berchtold MW, Heizmann CW (1985) Parvalbumin in cross-reinnervated muscles. Muscle & Nerve 8:132–137

    Google Scholar 

  • Nemeth PM, Pette D (1980) The interrelationship of two systems of fiber classification in rat EDL muscle. J Histochem Cytochem 28:193

    Google Scholar 

  • Nemeth PM, Pette D (1981) The limited correlation of myosin-based and metabolism-based classifications of skeletal muscle fibers. J Histochem Cytochem 29:89–90

    Google Scholar 

  • Nishikawa M (1981) Histo-and cytochemistry of acetylcholinesterase activity at the myotendinous junction in skeletal muscles of rats. Acta Histochem Cytochem 14:670–686

    Google Scholar 

  • Patterson GT, Wilson BW (1976a) Distribution of extrajunctional acetylcholinesterase in muscle of normal and dystrophic chickens. Exp Neurol 50:214–225

    Google Scholar 

  • Patterson GT, Wilson BW (1976b) Distribution of acetylcholinesterase activity in normal, dystrophic, and denervated muscles of the chicken. Exp Neurol 52:250–262

    Google Scholar 

  • Pierobon Bormioli S, Schiaffino S (1977) Myomuscular junctions in re-innervated rat skeletal muscle. J Anat 124:359–370

    Google Scholar 

  • Pullen AH (1977a) The distribution and relative sizes of three histochemical fibre types in the rat tibialis anterior muscle. J Anat 123:1–19

    Google Scholar 

  • Pullen AH (1977b) The distribution and relative sizes of fibre types in the extensor digitorum longus and soleus muscles of the adult rat. J Anat 123:467–486

    Google Scholar 

  • Schwarzacher HG (1960) Untersuchungen über die Skeletmuskel-Sehnenverbindung. II. Histochemische Lokalisation der Acetylcholinesterase und Untersuchungen über ihre mögliche Funktion an der Muskelfaser-Sehnenverbindung. Acta Anat 42:318–332

    Google Scholar 

  • Spurway N (1981) Interrelationship between myosin-based and metabolism-based classifications of skeletal muscle fibers. J Histochem Cytochem 29:87–88

    Google Scholar 

  • Teräväinen H (1969) Localisation of acetylcholinesterase activity in myotendinous and myomyous junctions of the striated skeletal muscles of the rat. Experientia 25:524–525

    Google Scholar 

  • Weidoff PM Jr, Wilson BW (1977) Influence of muscle activity in trophic regulation of acetylcholinesterase activity in dystrophic chickens. Exp Neurol 57:1–12

    Google Scholar 

  • Wong-Riley M (1979) Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res 171:11–28

    Google Scholar 

  • Wooten GF, Cheng CH (1980) Transport and turnover of acetylcholinesterase and choline acetyltransferase in rat sciatic nerve and skeletal muscle. J Neurochem 34:359–566

    Google Scholar 

  • Zelena J (1965) Development of acetylcholinesterase activity at muscle-tendon junctions. Nature 205:295–296

    Google Scholar 

Download references

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Dedicated to Professor Walle J.H. Nauta, Newton, on occasion his 70th birthday

This work was supported in part by the Hartmann Müller-Stiftung für medizinische Forschung

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Müntener, M., Zenker, W. Fiber type and non-endplate acetylcholinesterase in normal and experimentally altered muscles. Anat Embryol 173, 377–383 (1986). https://doi.org/10.1007/BF00318922

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