Skip to main content
NCBI home page
Cellular and Molecular Neurobiology logoLink to Cellular and Molecular Neurobiology
. 1991 Feb;11(1):35–54. doi: 10.1007/BF00712799

Interactions between intrinsic regulation and neural modulation of acetylcholinesterase in fast and slow skeletal muscles

Janez Sketelj 1, Neva Črne-Finderle 1, Samo Ribarič 1, Miro Brzin 1
PMCID: PMC11567393  PMID: 2013058

Abstract

  1. Initiation of subsynaptic sarcolemmal specialization and expression of different molecular forms of AChE were studied in fast extensor digitorum longus (EDL) and slow soleus (SOL) muscle of the rat under different experimental conditions in order to understand better the interplay of neural influences with intrinsic regulatory mechanisms of muscle cells.

  2. Former junctional sarcolemma still accumulated AChE and continued to differentiate morphologically for at least 3 weeks after early postnatal denervation of EDL and SOL muscles. In noninnervated regenerating muscles, postsynapticlike sarcolemmal specializations with AChE appeared (a) in the former junctional region, possibly induced by a substance in the former junctional basal lamina, and (b) in circumscribed areas along the whole length of myotubes. Therefore, the muscle cells seem to be able to produce a postsynaptic organization guiding substance, located in the basal lamina. The nerve may enhance the production or accumulation of this substance at the site of the future motor end plate.

  3. Significant differences in the patterns of AChE molecular forms in EDL and SOL muscles arise between day 4 and day 10 after birth. The developmental process of downregulation of the asymmetric AChE forms, eliminating them extrajunctionally in the EDL, is less efficient in the SOL. The presence of these AChE forms in the extrajunctional regions of the SOL correlates with the ability to accumulate AChE in myotendinous junctions. The typical distribution of the asymmetric AChE forms in the EDL and SOL is maintained for at least 3 weeks after muscle denervation.

  4. Different patterns of AChE molecular forms were observed in noninnervated EDL and SOL muscles regeneratingin situ. In innervated regenerates, patterns of AChE molecular forms typical for mature muscles were instituted during the first week after reinnervation.

  5. These results are consistent with the hypothesis that intrinsic differences between slow and fast muscle fibers, concerning the response of their AChE regulating mechanism to neural influences, may contribute to different AChE expression in fast and slow muscles, in addition to the influence of different stimulation patterns.

Key words: acetylcholinesterase, neuromuscular junction, nerve-muscle interaction, slow and fast muscles, muscle regeneration

References

  1. Anglister, L., and McMahan, U. J. (1985). Basal lamina directs acetylcholinesterase accumulation at synaptic sites in regenerating muscle.J. Cell Biol.101735–743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bacou, F., Vigneron, P., and Massoulié, J. (1982). Acetylcholinesterase forms in fast and slow rabbit muscle.Nature296661–664. [DOI] [PubMed] [Google Scholar]
  3. Bennett, M., and Pettigrew, A. G. (1974). The formation of synapses in striated muscle during development.J. Physiol.241515–545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blondet, B., Rieger, F., Gautron, J., and Pinçon-Raymond, M. (1986). Difference in the ability of neonatal and adult denervated muscle to accumulate acetylcholinesterase at the old sites of innervation.Dev. Biol.8989–94. [DOI] [PubMed] [Google Scholar]
  5. Brenner, H. R., Meier, Th., and Vidmar, B. (1983). Early action of nerve determines motor endplate differentiation in rat muscle.Nature305536–537. [DOI] [PubMed] [Google Scholar]
  6. Brockman, S. K., Younkin, L. H., and Younkin, S. G. (1984). The effect of spontaneous electromechanical activity on the metabolism of acetylcholinesterase in cultured embryonic rat myotubes.J. Neurosci.4131–140. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bruner, J. M., and Bursztajn, S. (1986). Acetylcholine receptor clusters are associated with nuclei in rat myotubes.Dev. Biol.11535–43. [DOI] [PubMed] [Google Scholar]
  8. Brzin, M., and Pucihar, S. (1976). Iodide, thiocyanate and cyanide ions as capturing reagents in one-step copper-thiocholine method for cytochemical localization of cholinesterase activity.Histochemistry48283–292. [DOI] [PubMed] [Google Scholar]
  9. Brzin, M., Sketelj, J., Tennyson, V. M., Kiauta, T., and Budininkas-Schoenebeck, M. (1981). Activity, molecular forms and cytochemistry of cholinesterases in developing rat diaphragm.Muscle Nerve4505–513. [DOI] [PubMed] [Google Scholar]
  10. Brzin, M., Sketelj, J., and Klinar, B. (1983). Cholinesterases. InHandbook of Neurochemistry, (A. Lajtha, Ed.), Plenum Press, New York, pp. 251–292. [Google Scholar]
  11. Carlson, V. M. (1978). A review of muscle transplantation in mammals.Physiol. Bohemoslov.27387–400. [PubMed] [Google Scholar]
  12. Carlson, B. M., Hnik, P., Tuček, S., Vejsada, R., Bader, D. M., and Faulkner, J. A. (1981). Comparison between grafts with intact nerves and standard free grafts of the rat extensor digitorum longus muscle.Physiol. Bohemoslov.30505–513. [PubMed] [Google Scholar]
  13. Collins, P. L., and Younkin, S. G. (1982). Effect of denervation on the molecular forms of acetylcholinesterase in rat diaphragm.J. Biol. Chem.25713638–136644. [PubMed] [Google Scholar]
  14. De La Porte, S., Vigny, M., Massoulié, J., and Koenig, J. (1984). Action of veratridine on acetylcholinesterase in cultures of rat muscle cells.Dev. Biol.106450–456. [DOI] [PubMed] [Google Scholar]
  15. Dettbarn, W.-D., Groswald, D., Gupta, R. C., and Misulis, K. E. (1985). Use and disuse and control of acetylcholinesterase activity in fast and slow twitch muscle of rat. InMolecular Basis of Nerve Activity (J.-P. Changeux, F. Hucho, A. Maelicke, and E. Neumann, Eds.), Walter de Gruyter, Berlin, New York, pp. 567–587. [Google Scholar]
  16. Dhoot, G. J. K. (1986). Selective synthesis and degradation of slow skeletal myosin heavy chains in developing muscle fibers.Muscle Nerve9155–164. [DOI] [PubMed] [Google Scholar]
  17. Englander, L. L., and Rubin, L. L. (1987). Acetylcholine receptor clustering and nuclear movement in muscle fibres in cultures.J. Cell Biol.10487–95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Fallon, J. R., and Gelfman, C. E. (1989). Agrin-related molecules are concentrated at acetylcholine receptors in normal and aneural developing muscle.J. Cell Biol.1081527–1535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Fallon, J. R., Nitkin, R. M., Reist, N. E., Wallace, B. G., and McMahan, U. J. (1985). Acetylcholine receptor-aggregating factor is similar to molecules concentrated at neuromuscular junctions.Nature315571–574. [DOI] [PubMed] [Google Scholar]
  20. Fontaine, B., Klarsfeld, A., Hokfelt, T., and Changeux, J.-P. (1986). Calcitonin gene-related peptide, a peptide present in spinal cord motoneurons, increases the number of acetylcholine receptors in primary cultures of chick embryo myotubes.Neurosci. Lett.71159–65. [DOI] [PubMed] [Google Scholar]
  21. Grinell, A. D. (1986). Trophic interaction between nerve and muscle. InMyology (A. G. Engel, and B. Q. Banker, Eds.), McGraw-Hill, New York, pp. 359–391. [Google Scholar]
  22. Groswald, D. E., and Dettbarn, W.-D. (1983). Characterization of acetylcholinesterase molecular forms in slow and fast muscle of rat.Neurochem. Res.8983–995. [DOI] [PubMed] [Google Scholar]
  23. Grove, B. K. (1989). Muscle differentation and origin of muscle fiber diversity.CRC Crit. Rev. Neurobiol.4201–234. [PubMed] [Google Scholar]
  24. Hall, Z. W. (1973). Multiple forms of acetylcholinesterase and their distribution in endplate and non-plate regions of rat diaphragm muscle.J. Neurobiol.4343–361. [DOI] [PubMed] [Google Scholar]
  25. Harris, D. A., Falls, D. L., and Fischbach, G. D. (1989). Differential activation of myotube nuclei following exposure to an acetylcholine receptor-inducing factor.Nature337173–176. [DOI] [PubMed] [Google Scholar]
  26. Inestrosa, N. C., Miller, J. B., Silberstein, L., Ziskind-Conhaim, L., and Hall, Z. W. (1983). Developmental regulation of 16 S acetylcholinesterase and acetylcholine receptors in a mouse muscle cell line.Exp. Res.147393–405. [DOI] [PubMed] [Google Scholar]
  27. Kelly, A. M., and Zacks, S. I. (1969). The fine structure of motor endplate morphogenesis.J. Cell Biol.42154–169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Koelle, G. B., and Friedenwald, J. S. (1949). A histochemical method for localization cholinesterase activity.Proc. Soc. Exp. Biol. (N.Y.)70617–622. [DOI] [PubMed] [Google Scholar]
  29. Koenig, J., and Rieger, F. (1981). Biochemical stability of AChE molecular forms after cytochemical staining: Postnatal focalization of the 16 S AChE in rat muscle.Dev. Neurosci.4249–257. [DOI] [PubMed] [Google Scholar]
  30. Kugelberg, E. (1976). Adaptive transformation of rat soleus motor units during growth.J. Neurol. Sci.27269–289. [DOI] [PubMed] [Google Scholar]
  31. Kupfer, C., and Koelle, G. B. (1951). A histochemical study of cholinesterase during formation of motor endplate of the albino rat.J. Exp. Zool.116397–407. [DOI] [PubMed] [Google Scholar]
  32. Lai, J., Jedrzejczyk, J., Pizzey, J. A., Green, D., and Barnard, E. A. (1986). Neural control of the forms of acetylcholinesterase in slow mammalian muscles.Nature32172–74. [DOI] [PubMed] [Google Scholar]
  33. Lappin, R. I., and Rubin, L. L. (1985). Molecular forms of acetylcholinesterase in Xenopus muscle.Dev. Biol.110269–274. [DOI] [PubMed] [Google Scholar]
  34. Lentz, T. L. (1969). Development of neuromuscular junction. I. Cytological and cytochemical studies on the junction of differentiating muscle in the regenerating limb of the newt Triturus.J. Cell Biol.42431–443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Lømo, T., and Slater, C. R. (1980). Control of junctional acetylcholinesterase by neural and muscular influences in the rat.J. Physiol.303191–202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Lømo, T., Gundersen, K., Hennig, R., and Westgaard, R. (1984). The role of impulse patterns in maintaining and regulating contractile properties in intact and chronically denervated and stimulated rat skeletal muscles. InRecent Achievement in Restorative Neurology: Upper Motor Neurone Functions and Disfunctions, (J. C. Eccles, and M. R. Dimitrijević, Eds.), Karger AG, Basel, pp. 249–262. [Google Scholar]
  37. Lømo, T., Massoulié, J., and Vigny, M. (1985). Stimulation of denervated rat soleus muscle with fast and slow activity patterns induces different expression of acetylcholinesterase molecular forms.J. Neurosci.51180–1187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Marnay, A., and Nachmansohn, D. (1938). Choline esterase in voluntary muscle.J. Physiol. (Lond.),9237–47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Miller, J. B., and Stockdale, F. E. (1987). What muscle cells know that nerves don't tell them.TINS110325–329. [Google Scholar]
  40. Moss, F. P., and Leblond, C. P. (1971). Satellite cells as the source of nuclei in muscles of growing rats.Anat. Res.170421–436. [DOI] [PubMed] [Google Scholar]
  41. Murray, M. A., and Robbins, N. (1982). Cell proliferation in denervated muscle: Identity and origin of dividing cells.Neurosocience7 1823–1833. [DOI] [PubMed] [Google Scholar]
  42. Narusawa, M., Fitzsimons, R. B., Izumo, C., Nadal-Ginard, B., Rubinstein, N. A., and Kelly, A. M. (1987). Slow myosin in developing rat skeletal muscle.J. Cell Biol.104447–459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Navarrete, R., and Vrbova, G. (1983). Changes of activity patterns in slow and fast muscles during postnatal development.Dev. Brain Res.811–19. [Google Scholar]
  44. New, H. V., and Mudge, A. W. (1986). Calcitonin gene-related peptide regulates muscle acetylcholin receptor synthesis.Nature323809–811. [DOI] [PubMed] [Google Scholar]
  45. Nitkin, R. M., Smith, M. A., Magill, C., Fallon, J. R., Yao, Y.-M., Wallace, B. G., and McMahan, U. J. (1987). Identification of agrin, a synaptic organizing protein in Torpedo electric organ.J. Cell Biol.1052471–2478. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Pette, D. (1986). Skeletal muscle adaptation in response to chronic stimulation. InElectrical Stimulation and Neuromuscular Disorders, (W. A. Nix, and G. Vrbova, Eds.), Springer-Verlag, Berlin, Heidelberg, pp. 12–20. [Google Scholar]
  47. Pette, D., and Vrbova, G. (1985). Invited review: Neural control of phenotypic expression in mammalian muscle fibers.Muscle Nerve8676–689. [DOI] [PubMed] [Google Scholar]
  48. Phillips, W. D., and Bennett, M. R. (1989). The distribution of intracellular acetylcholine receptor and nuclei in developing avian fast-twitch muscle fibres during synapse elimination.J. Neurocytol.18241–255. [DOI] [PubMed] [Google Scholar]
  49. Randall, W. R., Lai, J., and Barnard, E. A. (1985). Acetylcholinesterase of muscle and nerve. InMolecular Basis of Nerve Activity, (J.-P. Changeux, F. Hucho, A. Maelicke, and E. Neumann, Eds.), Walter de Gruyter, Berlin, pp. 595–617. [Google Scholar]
  50. Rieger, F., Koenig, J., and Vigny, M. (1980). Spontaneous contractile activity and the presence of the 16 S form of acetylcholinesterase in rat muscle cells in culture: Reversible suppersive action of tetrodotoxin.Dev. Biol.76358–365. [DOI] [PubMed] [Google Scholar]
  51. Rubin, L. (1985). Increases in muscle Ca mediate changes in acetylcholinesterase and acetylcholine receptors caused by muscle contraction.Proc. Natl. Acad. Sci. USA827121–7125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Rubinstein, N. A., and Kelly, A. A. (1981). Development of muscle fiber specialization in the rat hindlimb.J. Cell Biol.901128–144. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Sketelj, J., and Brzin, M. (1980). 16 S acetylcholinesterase in endplate free regions of developing rat diaphragm.Neurochem. Res.5653–658. [DOI] [PubMed] [Google Scholar]
  54. Sketelj, J., and Brzin, M. (1985). Asymmetric molecular forms of acetylcholinesterase in mammalian skeletal muscles.J. Neurosci. Res.1495–103. [DOI] [PubMed] [Google Scholar]
  55. Sketelj, J., Črne, N., and Brzin, M. (1987). Molecular forms and localization of acetylcholinesterase and nonspecific cholinesterase in regenerating skeletal muscles.Neurochem. Res.12159–165. [DOI] [PubMed] [Google Scholar]
  56. Sketelj, J., Črne, N., and Brzin, M. (1988). Two types of focal accumulations of acetylcholinesterase appear in noninnervated regenerating skeletal muscles of the rat.J. Neurosci. Res.2090–101. [DOI] [PubMed] [Google Scholar]
  57. Slater, C. R. (1982). Neural influence on the postnatal changes in acetylcholine receptor distribution at nerve-muscle junctions in the mouse.Dev. Biol.9423–30. [DOI] [PubMed] [Google Scholar]
  58. Tennyson, V. M., Brzin, M., and Slotwiner, P. (1971). The appearance of acetylcholinesterase in the myotome of the embryonic rabbit. An electron microscope cytochemical and biochemical study.J. Cell Biol.51703–721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Tennyson, V. M., Brzin, M., and Kremzner, L. T. (1973). Acetylcholinesterase activity in myotube and muscle satellite cells of the fetal rabbit: An electron microscopic-cytochemical and biochemical study.J. Histochem. Cytochem.21634–652. [DOI] [PubMed] [Google Scholar]
  60. Teräväinen, H., and Juntunen, J. (1978). Effect of temporary denervation on the development of the acetylcholinesterase-positive structures of the rat myoneural junction.Histochemie15261–269. [DOI] [PubMed] [Google Scholar]
  61. Toth, V. L., and Karcsu, S. (1979). Ultrastructural localization of the acetylcholinesterase activity in the diaphragm of the rat embryo.Acta Histochem. (Jena)64148–156. [PubMed] [Google Scholar]
  62. Toutant, J.-P., and Massoulié, J. (1987). Acetylcholinesterase. InMammalian Ectoenzymes (Kenny and Turner, Eds.), Elsevier (Biomedical Division), Amsterdam, pp. 289–328. [Google Scholar]
  63. Vigny, M., Koenig, J., and Rieger, F. (1976). The motor endplate specific form of acetylcholinesterase: Appearance during embryogenesis and reinnervation of rat muscle.J. Neurochem.271347–1353. [DOI] [PubMed] [Google Scholar]
  64. Wake, K. (1979). Formation of myoneural and myotendinous junctions in the chick.Cell Tissue Res.173383–400. [DOI] [PubMed] [Google Scholar]
  65. Wallace, B. G., Nitkin, R. M., Reist, N. E., Fallon, J. R., Moayeri, N. N., and McMahan, U. J. (1985). Aggregates of acetylcholinesterase induced by acetylcholin receptor-aggregating factor.Nature315574–577. [DOI] [PubMed] [Google Scholar]

Articles from Cellular and Molecular Neurobiology are provided here courtesy of Springer

RESOURCES