Evolution of cholinergic proteins in developing slow and fast skeletal muscles in chick embryo (original) (raw)

Abstract

1. The cholinergic differentiation of two phenotypically muscles of the chick, the slow multiply innervated anterior latissimus dorsi (a.l.d.) and the fast focally innervated posterior latissimus dorsi (p.l.d.), was investigated during embryonic life and after hatching using both autoradiographical and biochemical methods. 2. The contents in total protein and in acetylcholinesterase activity follow similar development patterns in both muscles, but, after the 15th day in ovo, the accumulation of choline acetyltransferase activity and of acetylcholine nicotinic receptor sites as determined by alpha-bungarotoxin binding occurs at a faster rate in a.l.d. than in p.l.d. 3. In muscle of the p.l.d., a rapid increase of the total number of acetylcholine receptor clusters takes place after the 11th day of embryonic life although some clusters could be observed on myofibres as soon as the 4th day in ovo. 4. The rate of degradation of cholinergic receptor sites in chick muscle is constant around 28 hr up to the 10th day after hatching; thus the different rates of accumulation of acetylcholine receptor in a.l.d. and p.l.d., respectively, after the 15th day of embryonic life must be due to different rates of receptor synthesis. 5. The role of muscle activity in the biochemical differentiation of the developing motor end-plate was investigated in chick embryos which had been paralysed by repeated injections into the yolk sac of a curare-like agent, Flaxedil (May & Baker). 6. The total content in acetylcholinesterase of both a.l.d. and p.l.d. muscles is not significantly modified by paralysis. However, the histochemical staining of end-plates for acetylcholinesterase as well as the heavy form of this enzyme (19 . 5 S) are consistently reduced after Flaxedil injection. 7. In muscles from Flaxedil-treated embryos, the total content in acetylcholine receptor sites as determined by alpha-bungarotoxin binding is higher than in those from control embryos, whereas the rate of degradation of these sites is not significantly altered. 8. The localization of the acetylcholine receptors under the motor nerve terminals is not prevented by blocking muscle activity at the postsynaptic level. Clusters of receptor are still present, and there is no significant change in the number and distribution of these clusters along the myofibres of a.l.d. and p.l.d. muscles. 9. These results are discussed with respect to motor end-plate formation in multiply and focally innervated embryo muscles, and in relation to the control of cholinergic proteins distribution and synthesis by muscle activity.

197

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson M. J., Cohen M. W. Nerve-induced and spontaneous redistribution of acetylcholine receptors on cultured muscle cells. J Physiol. 1977 Jul;268(3):757–773. doi: 10.1113/jphysiol.1977.sp011880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anderson M. J., Cohen M. W., Zorychta E. Effects of innervation on the distribution of acetylcholine receptors on cultured muscle cells. J Physiol. 1977 Jul;268(3):731–756. doi: 10.1113/jphysiol.1977.sp011879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Atsumi S. Development of neuromuscular junctions of fast and slow muscles in the chick embryo: a light and electron microscopic study. J Neurocytol. 1977 Dec;6(6):691–709. doi: 10.1007/BF01176380. [DOI] [PubMed] [Google Scholar]
  4. Barnard E. A., Wieckowski J., Chiu T. H. Cholinergic receptor molecules and cholinesterase molecules at mouse skeletal muscle junctions. Nature. 1971 Nov 26;234(5326):207–209. doi: 10.1038/234207a0. [DOI] [PubMed] [Google Scholar]
  5. Bennett M. R., Pettigrew A. G. The formation of synapses in striated muscle during development. J Physiol. 1974 Sep;241(2):515–545. doi: 10.1113/jphysiol.1974.sp010670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Berg D. K., Hall Z. W. Fate of alpha-bungarotoxin bound to acetylcholine receptors of normal and denervated muscle. Science. 1974 Apr 26;184(4135):473–475. doi: 10.1126/science.184.4135.473. [DOI] [PubMed] [Google Scholar]
  7. Berg D. K., Hall Z. W. Loss of alpha-bungarotoxin from junctional and extrajunctional acetylcholine receptors in rat diaphragm muscle in vivo and in organ culture. J Physiol. 1975 Nov;252(3):771–789. doi: 10.1113/jphysiol.1975.sp011169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Betz H., Bourgeois J. P., Changeux J. P. Evidnece for degradation of the acetylcholine (nicotinic) receptor in skeletal muscle during the development of the chick embryo. FEBS Lett. 1977 May 15;77(2):219–224. doi: 10.1016/0014-5793(77)80238-x. [DOI] [PubMed] [Google Scholar]
  9. Betz H., Changeux J. P. Regulation of muscle acetylcholine receptor synthesis in vitro by cyclic nucleotide derivatives. Nature. 1979 Apr 19;278(5706):749–752. doi: 10.1038/278749a0. [DOI] [PubMed] [Google Scholar]
  10. Bevan S., Steinbach J. H. The distribution of alpha-bungarotoxin binding sites of mammalian skeletal muscle developing in vivo. J Physiol. 1977 May;267(1):195–213. doi: 10.1113/jphysiol.1977.sp011808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Bourgeois J. P., Betz H., Changuex J. P. Effets de la paralysie chronique de l'embryon de poulet par le flaxédil sur le développement de la jonction neuro-musculaire. C R Acad Sci Hebd Seances Acad Sci D. 1978 Mar 13;286(10):773–776. [PubMed] [Google Scholar]
  12. Bourgeois J. P., Popot J. L., Ryter A., Changeux J. P. Quantitative studies on the localization of the cholinergic receptor protein in the normal and denervated electroplaque from Electrophorus electricus. J Cell Biol. 1978 Oct;79(1):200–216. doi: 10.1083/jcb.79.1.200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Brockes J. P., Berg D. K., Hall Z. W. The biochemical properties and regulation of acetylcholine receptors in normal and denervated muscle. Cold Spring Harb Symp Quant Biol. 1976;40:253–262. doi: 10.1101/sqb.1976.040.01.026. [DOI] [PubMed] [Google Scholar]
  14. Brockes J. P., Hall Z. W. Acetylcholine receptors in normal and denervated rat diaphragm muscle. II. Comparison of junctional and extrajunctional receptors. Biochemistry. 1975 May 20;14(10):2100–2106. doi: 10.1021/bi00681a009. [DOI] [PubMed] [Google Scholar]
  15. Burden S. Acetylcholine receptors at the neuromuscular junction: developmental change in receptor turnover. Dev Biol. 1977 Nov;61(1):79–85. doi: 10.1016/0012-1606(77)90343-8. [DOI] [PubMed] [Google Scholar]
  16. Burden S. Development of the neuromuscular junction in the chick embryo: the number, distribution, and stability of acetylcholine receptors. Dev Biol. 1977 Jun;57(2):317–329. doi: 10.1016/0012-1606(77)90218-4. [DOI] [PubMed] [Google Scholar]
  17. Cardasis C. A., Cooper G. W. A method for the chemical isolation of individual muscle fibers and its application to a study of the effect of denervation on the number of nuclei per muscle fiber. J Exp Zool. 1975 Mar;191(3):333–346. doi: 10.1002/jez.1401910304. [DOI] [PubMed] [Google Scholar]
  18. Chang C. C., Huang M. C. Turnover of junctional and extrajunctional acetylcholine receptors of the rat diaphragm. Nature. 1975 Feb 20;253(5493):643–644. doi: 10.1038/253643a0. [DOI] [PubMed] [Google Scholar]
  19. Changeux J. P., Courrège P., Danchin A. A theory of the epigenesis of neuronal networks by selective stabilization of synapses. Proc Natl Acad Sci U S A. 1973 Oct;70(10):2974–2978. doi: 10.1073/pnas.70.10.2974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Changeux J. P., Danchin A. Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks. Nature. 1976 Dec 23;264(5588):705–712. doi: 10.1038/264705a0. [DOI] [PubMed] [Google Scholar]
  21. Cohen M. W. The development of neuromuscular connexions in the presence of D-tubocurarine. Brain Res. 1972 Jun 22;41(2):457–463. doi: 10.1016/0006-8993(72)90515-x. [DOI] [PubMed] [Google Scholar]
  22. Ellisman M. H., Rash J. E., Staehelin L. A., Porter K. R. Studies of excitable membranes. II. A comparison of specializations at neuromuscular junctions and nonjunctional sarcolemmas of mammalian fast and slow twitch muscle fibers. J Cell Biol. 1976 Mar;68(3):752–774. doi: 10.1083/jcb.68.3.752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Fischbach G. D., Berg D. K., Cohen S. A., Frank E. Enrichment of nerve--muscle synapses in spinal cord--muscle cultures and identification of relative peaks of ACh sensitivity at sites of transmitter release. Cold Spring Harb Symp Quant Biol. 1976;40:347–357. doi: 10.1101/sqb.1976.040.01.034. [DOI] [PubMed] [Google Scholar]
  24. Freeman S. S., Engel A. G., Drachman D. B. Experimental acetylcholine blockade of the neuromuscular junction. Effects on end plate and muscle fiber ultrastructure. Ann N Y Acad Sci. 1976;274:46–59. doi: 10.1111/j.1749-6632.1976.tb47675.x. [DOI] [PubMed] [Google Scholar]
  25. GINSBORG B. L. Some properties of avian skeletal muscle fibres with multiple neuromuscular junctions. J Physiol. 1960 Dec;154:581–598. doi: 10.1113/jphysiol.1960.sp006597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. GREENWOOD F. C., HUNTER W. M., GLOVER J. S. THE PREPARATION OF I-131-LABELLED HUMAN GROWTH HORMONE OF HIGH SPECIFIC RADIOACTIVITY. Biochem J. 1963 Oct;89:114–123. doi: 10.1042/bj0890114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Giacobini-Robecchi M. G., Giacobini G., Filogamo G., Changeux J. P. Effets comparés de l'injection chronique de toxine alpha de Naja nigricollis et de toxine botulinique A sur le développement des racines dorsales et ventrales de la moelle épinière d'embryons de poulet. C R Acad Sci Hebd Seances Acad Sci D. 1976 Jul 19;283(3):271–274. [PubMed] [Google Scholar]
  28. Giacobini G., Filogamo G., Weber M., Boquet P., Changeux J. P. Effects of a snake alpha-neurotoxin on the development of innervated skeletal muscles in chick embryo. Proc Natl Acad Sci U S A. 1973 Jun;70(6):1708–1712. doi: 10.1073/pnas.70.6.1708. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Gordon T., Perry R., Tuffery A. R., Vrbová G G G. Possible mechanisms determining synapse formation in developing skeletal muscles of the chick. Cell Tissue Res. 1974;155(1):13–25. doi: 10.1007/BF00220281. [DOI] [PubMed] [Google Scholar]
  30. Gordon T., Purves R. D., Vrbová G. Differentiation of electrical and contractile properties of slow and fast muscle fibres. J Physiol. 1977 Aug;269(3):535–547. doi: 10.1113/jphysiol.1977.sp011913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. HESS A. Structural differences of fast and slow extrafusal muscle fibres and their nerve endings in chickens. J Physiol. 1961 Jul;157:221–231. doi: 10.1113/jphysiol.1961.sp006717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hall Z. W. Multiple forms of acetylcholinesterase and their distribution in endplate and non-endplate regions of rat diaphragm muscle. J Neurobiol. 1973;4(4):343–361. doi: 10.1002/neu.480040404. [DOI] [PubMed] [Google Scholar]
  33. Hall Z. W., Reiness C. G. Electrical stimulation of denervated muscles reduces incorporation of methionine into the ACh receptor. Nature. 1977 Aug 18;268(5621):655–657. doi: 10.1038/268655a0. [DOI] [PubMed] [Google Scholar]
  34. Hartzell H. C., Kuffler S. W., Yoshikami D. Post-synaptic potentiation: interaction between quanta of acetylcholine at the skeletal neuromuscular synapse. J Physiol. 1975 Oct;251(2):427–463. doi: 10.1113/jphysiol.1975.sp011102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Jansen J. K., Van Essen D. C., Brown M. C. Formation and elimination of synapses in skeletal muscles of rat. Cold Spring Harb Symp Quant Biol. 1976;40:425–434. doi: 10.1101/sqb.1976.040.01.040. [DOI] [PubMed] [Google Scholar]
  36. Kelly A. M. Perisynaptic satellite cells in the developing and mature rat soleus muscle. Anat Rec. 1978 Apr;190(4):891–903. doi: 10.1002/ar.1091900409. [DOI] [PubMed] [Google Scholar]
  37. King J., Laemmli U. K. Polypeptides of the tail fibres of bacteriophage T4. J Mol Biol. 1971 Dec 28;62(3):465–477. doi: 10.1016/0022-2836(71)90148-3. [DOI] [PubMed] [Google Scholar]
  38. Laing N. G., Prestige M. C. Prevention of spontaneous motoneurone death in chick embryos [proceedings]. J Physiol. 1978 Sep;282:33P–34P. [PubMed] [Google Scholar]
  39. McMahan U. J., Sanes J. R., Marshall L. M. Cholinesterase is associated with the basal lamina at the neuromuscular junction. Nature. 1978 Jan 12;271(5641):172–174. doi: 10.1038/271172a0. [DOI] [PubMed] [Google Scholar]
  40. Menez A., Morgat J. -L., Fromageot P., Ronseray A. -M., Boquet P., Changeux J. -P. Tritium labelling of the alpha-neurotoxin of Naja nigricollis. FEBS Lett. 1971 Oct 1;17(2):333–335. doi: 10.1016/0014-5793(71)80180-1. [DOI] [PubMed] [Google Scholar]
  41. O'Brien R. A., Vrbová G. Acetylcholine synthesis in nerve endings to slow and fast muscles of developing chicks: effect of muscle activity. Neuroscience. 1978;3(12):1227–1230. doi: 10.1016/0306-4522(78)90142-2. [DOI] [PubMed] [Google Scholar]
  42. Oppenheim R. W., Pittman R., Gray M., Maderdrut J. L. Embryonic behavior, hatching and neuromuscular development in the chick following a transient reduction of spontaneous motility and sensory input by neuromuscular blocking agents. J Comp Neurol. 1978 Jun 1;179(3):619–640. doi: 10.1002/cne.901790310. [DOI] [PubMed] [Google Scholar]
  43. Page S. G. A comparison of the fine structures of frog slow and twitch muscle fibers. J Cell Biol. 1965 Aug;26(2):477–497. doi: 10.1083/jcb.26.2.477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Pittman R. H., Oppenheim R. W. Neuromuscular blockade increases motoneurone survival during normal cell death in the chick embryo. Nature. 1978 Jan 26;271(5643):364–366. doi: 10.1038/271364a0. [DOI] [PubMed] [Google Scholar]
  45. Puro D. G., De Mello F. G., Nirenberg M. Synapse turnover: the formation and termination of transient synapses. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4977–4981. doi: 10.1073/pnas.74.11.4977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Puro D. G., Nirenberg M. On the specificity of synapse formation. Proc Natl Acad Sci U S A. 1976 Oct;73(10):3544–3548. doi: 10.1073/pnas.73.10.3544. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Rieger F., Vigny M. Solubilization and physicochemical characterization of rat brain acetylcholinesterase: development and maturation of its molecular forms. J Neurochem. 1976 Jul;27(1):121–129. doi: 10.1111/j.1471-4159.1976.tb01553.x. [DOI] [PubMed] [Google Scholar]
  48. Rutishauser U., Thiery J. P., Brackenbury R., Sela B. A., Edelman G. M. Mechanisms of adhesion among cells from neural tissues of the chick embryo. Proc Natl Acad Sci U S A. 1976 Feb;73(2):577–581. doi: 10.1073/pnas.73.2.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Salpeter M. M., Rogers A. W., Kasprzak H., McHenry F. A. Acetylcholinesterase in the fast extraocular muscle of the mouse by light and electron microscope autoradiography. J Cell Biol. 1978 Jul;78(1):274–285. doi: 10.1083/jcb.78.1.274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Shainberg A., Burstein M. Decrease of acetylcholine receptor synthesis in muscle cultures by electrical stimulation. Nature. 1976 Nov 25;264(5584):368–369. doi: 10.1038/264368a0. [DOI] [PubMed] [Google Scholar]
  51. Sheridan R. E., Lester H. A. Rates and equilibria at the acetylcholine receptor of Electrophorus electroplaques: a study of neurally evoked postsynaptic currents and of voltage-jump relaxations. J Gen Physiol. 1977 Aug;70(2):187–219. [PMC free article] [PubMed] [Google Scholar]
  52. Tsuji S. Sur la localisation des cholinestérases à l'aide d'iodures d'esters de thiocholine. C R Acad Sci Hebd Seances Acad Sci D. 1968 Aug 12;267(7):801–803. [PubMed] [Google Scholar]
  53. Van Essen D., Jansen J. K. Reinnervation of the rat diaphragm during perfusion with alpha-bungarotoxin. Acta Physiol Scand. 1974 Aug;91(4):571–573. doi: 10.1111/j.1748-1716.1974.tb05713.x. [DOI] [PubMed] [Google Scholar]
  54. Vigny M., Di Giamberardino L., Couraud J. Y., Rieger F., Koenig J. Molecular forms of chicken acetylcholinesterase: effect of denervation. FEBS Lett. 1976 Oct 15;69(1):277–280. doi: 10.1016/0014-5793(76)80703-x. [DOI] [PubMed] [Google Scholar]
  55. Vigny M., Koenig J., Rieger F. The motor end-plate specific form of acetylcholinesterase: appearance during embryogenesis and re-innervation of rat muscle. J Neurochem. 1976 Dec;27(6):1347–1353. doi: 10.1111/j.1471-4159.1976.tb02614.x. [DOI] [PubMed] [Google Scholar]
  56. Vogel Z., Sytkowski A. J., Nirenberg M. W. Acetylcholine receptors of muscle grown in vitro. Proc Natl Acad Sci U S A. 1972 Nov;69(11):3180–3184. doi: 10.1073/pnas.69.11.3180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Weber M., Changeux J. P. Binding of Naja nigricollis (3H)alpha-toxin to membrane fragments from Electrophorus and Torpedo electric organs. I. Binding of the tritiated alpha-neurotoxin in the absence of effector. Mol Pharmacol. 1974 Jan;10(1):1–14. [PubMed] [Google Scholar]
  58. Weber M., Changeux J. P. Binding of Naja nigricollis (3H)alpha-toxin to membrane fragments from Electrophorus and Torpedo electric organs. II. Effect of cholinergic agonists and antagonists on the binding of the tritiated alpha-neurotoxin. Mol Pharmacol. 1974 Jan;10(1):15–34. [PubMed] [Google Scholar]