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. 1991 Feb;11(1):191–201. doi: 10.1007/BF00712809

Two types of asymmetric acetylcholinesterase in chick hindlimb muscle: Developmental profiles,in Vivo and in cell culture, and recovery after inactivation

Xavier Busquets 1, Jordi Pérez-Tur 1, Paula Rosario 1, Galo Ramírez 1,
PMCID: PMC11567367  PMID: 2013057

Abstract

  1. We have analyzed the behavior of two types of asymmetric molecular forms (A forms) of acetylcholinesterase (AChE) during development of chick hindlimb muscle,in vivo and in cell culture, and upon irreversible inactivation of peroneal muscle AChE with diisopropylfluorophosphate (DFP)in vivo.

  2. In agreement with previous developmental studies on chick muscle, globular forms of AChE (G forms) are predominant in chick hindlimb at early embryonic ages, being gradually replaced by A forms as hatching (and, therefore, onset of locomotion) approaches. Of the two A-form types, AI appears and accumulates significantly earlier than AII, so that A/G and II/I ratios higher than 1 are attained only at about hatching time.

  3. Cultures prepared from 11-day chick embryo hindlimb myoblasts express both types of A forms, with a combined activity of 27% of total AChE after 12 days in culture. AI forms appear again earlier and are much more abundant than type II asymmetric species through the life span of cultures.

  4. All AChE activity in the peroneal muscle is irreversibly inactivated by injection of DFPin vivo. The recovery of A forms follows the same sequence described for normal development, with a delayed and slower recovery of AII forms as compared with AI.

  5. Several hypotheses involving tail polypeptides or tissue target molecules, or posttranslational interconversion, are proposed to help explain the earlier appearance and accumulation of AI forms in chick muscle.

Key words: acetylcholinesterase, asymmetric-form types, chick hindlimb muscle, development, cell culture, diisopropylfluorophosphate inactivation

References

  1. Barat, A., Gómez-Barriocanal, J., and Ramírez, G. (1984). Two classes of collagen-tailed, asymmetric molecular forms of acetylcholinesterase in skeletal muscle: differential effects of denervation.Neurochem. Int.6403–412. [DOI] [PubMed] [Google Scholar]
  2. Barat, A., Escudero, E., and Ramírez, G. (1986). Heparin and the solubilization of asymmetric acetylcholinesterase.FEBS Lett.195209–214. [DOI] [PubMed] [Google Scholar]
  3. Brockman, S. K., Usiak, M. F., and Younkin, S. G. (1986). Assembly of monomeric acetylcholinesterase into tetrameric and asymmetric forms.J. Biol. Chem.2611201–1207. [PubMed] [Google Scholar]
  4. Bulger, J. E., Randall, W. R., Nieberg, P. S., Patterson, G. T., McNamee, M. G., and Wilson, B. W. (1982). Regulation of acetylcholinesterase forms in quail and chicken muscle cultures.Dev. Neurosci.5474–483. [DOI] [PubMed] [Google Scholar]
  5. Cisson, C. M., McQuarrie, C. H., Sketelj, J., McNamee, M. G., and Wilson, B. W. (1981). Molecular forms of acetylcholinesterase in chick embryonic fast muscle. Developmental changes and effects of DFP treatment.Dev. Neurosci.4157–164. [DOI] [PubMed] [Google Scholar]
  6. Fadić, R., and Inestrosa, N. C. (1989). Nerve regulation of class I and class II-asymmetric forms of acetylcholinesterase in rat skeletal muscles.J. Neurosci. Res.22449–455. [DOI] [PubMed] [Google Scholar]
  7. Fouvet, B. (1973). Innervation et morphogenèse de la patte chez l'embryon de poulet.Arch. Anat. Microsc.62269–280. [PubMed] [Google Scholar]
  8. Godfrey, E. W., Siebenlist, R. E., Wallskog, P. A., Walters, L. M., Bolender, D. L., and Yorde, D. E. (1988). Basal lamina components are concentrated in premuscle masses and at early acetylcholine receptor clusters in chick embryo hindlimb muscles.Dev. Biol.130471–486. [DOI] [PubMed] [Google Scholar]
  9. Gómez-Barriocanal, J., Barat, A., Escudero, E., Rodríguez-Borrajo, C., and Ramírez, G. (1981). Solubilization of collagen-tailed acetylcholinesterase from chick retina: Effect of different extraction procedures. J.Neurochem.371239–1249. [DOI] [PubMed] [Google Scholar]
  10. Kato, A. C., Vrachliotis, A., Fulpius, B., and Dunant, Y. (1980). Molecular forms of acetylcholinesterase in chick muscle and ciliary ganglion: Embryonic tissues and cultured cells.Dev. Biol.76222–228. [DOI] [PubMed] [Google Scholar]
  11. Landmesser, L., and Morris, D. G. (1975). The development of functional innervation in the hindlimb of the chick embryo.J. Physiol.249301–326. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lowry, O. H., Rosebrough, N. J., Farr, A. K., and Randall, R. J. (1951). Protein measurement with the Folin phenol reagent.J. Biol. Chem.193265–275. [PubMed] [Google Scholar]
  13. Lyles, J. M., Silman, I., and Barnard, E. A. (1979). Developmental changes in levels and forms of cholinesterases in muscles of normal and dystrophic chickens.J. Neurochem.33727–738. [DOI] [PubMed] [Google Scholar]
  14. Massoulié, J., and Bon, S. (1982). The molecular forms of cholinesterase and acetylcholinesterase in vertebrates.Annu. Rev. Neurosci.557–106. [DOI] [PubMed] [Google Scholar]
  15. Patterson, G. T., and Wilson, B. W. (1986). Serum regulation of acetylcholinesterase in cultured myotubes.Exp. Neurol.91308–318. [DOI] [PubMed] [Google Scholar]
  16. Ramírez, G., Gómez-Barriocanal, J., Barat, A., and Rodríguez-Borrajo, C. (1984). Two classes of collagen-tailed molecular forms of acetylcholinesterase. InCholinesterases: Fundamental and Applied Aspects (M. Brzin, E. A. Barnard, and D. Sket, Eds.), Walter de Gruyter, Berlin, pp. 115–128. [Google Scholar]
  17. Ramírez, G., Barat, A., and Fernández, H. L. (1990). Interaction of asymmetric and globular acetylcholinesterase species with glycosaminoglycans.J. Neurochem.541761–1768. [DOI] [PubMed] [Google Scholar]
  18. Rotundo, R. L. (1984). Asymmetric acetylcholinesterase is assembled in the Golgi apparatus.Proc. Natl. Acad. Sci. USA81479–483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rotundo, R. L., and Fambrough, D. (1979). Molecular forms of chicken embryo acetylcholinesterasein vitro andin vivo.J. Biol. Chem.2544790–4799. [PubMed] [Google Scholar]
  20. Sohal, G. S., and Wrenn, R. W. (1984). Appearance of high-molecular-weight acetylcholinesterase in aneural muscle developingin vivo.Dev. Biol.101229–234. [DOI] [PubMed] [Google Scholar]
  21. Toutant, J.-P., and Massoulié, J. (1988). Cholinesterases: Tissue and cellular distribution of molecular forms and their physiological regulation.Hand. Exp. Pharmacol.86225–265. [Google Scholar]
  22. Toutant, J.-P., Toutant, M., Fiszman, M. Y., and Massoulié, J. M. (1983). Expression of theA12 form of acetylcholinesterase by developing avian leg muscle cellsin vivo and during differentiation in primary cell cultures.Neurochem. Int.5751–762. [DOI] [PubMed] [Google Scholar]
  23. Vallette, F. M., Vigny, M., and Massoulié, J. (1986). Muscular differentiation of chicken myotubes in a simple defined synthetic culture medium and in serum supplemented media: Expression of the molecular forms of acetylcholinesterase.Neurochem. Int.8121–133. [DOI] [PubMed] [Google Scholar]
  24. Vallette, F. M., Fauquet, M., and Teillet, M. A. (1987). Difference in the expression of asymmetric acetylcholinesterase molecular forms during myogenesis in early avian dermomyotomes and limb budsin ovo andin vitro.Dev. Biol.12077–84. [DOI] [PubMed] [Google Scholar]

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