Protein Synthesis in Presynaptic Endings of Squid Brain: Regulation by Ca2+ Ions

  • Juan Claudio Benech
  • Mariana Crispino
  • Barry B. Kaplan
  • Antonio Giuditta

Abstract

It is generally accepted that long-term synaptic plasticity induced by electrophysiological or behavioral stimulation requires the modulation of gene expression, eventually leading to modification of the set of synaptic proteins (Montarolo et al., 1986; Otani et al., 1989). These changes are believed to occur in presynaptic and postsynaptic sites (dendrites) of the neuron. The ability of dendrites to synthesize proteins, is largely accepted (Rao & Steward, 1991). On the other hand, the concept of protein synthesis in presynaptic terminals is still controversial. This possibility was considered in the past (Austin et al., 1967; Morgan & Austin, 1968; Gordon & Deanin, 1968; Bridgers et al., 1971; Cotman & Taylor, 1971), but failed to achieve acceptance as the protein synthetic activity of synaptosomal fractions could be attributed to contaminating fragments of glial cells or dendrites, rather than to nerve endings.

Keywords

Protein Synthesis Optic Lobe Orotic Acid Calcium Ionophore A23187 Retinal Photoreceptor 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Alvarez, J., and Benech, C. R. (1983). Axoplasmic incorporation of aminoacids in myelinated fiber exceeds that of its soma: an autoradiographic study. Exp. Neurol. 82:25–42.PubMedCrossRefGoogle Scholar
  2. Alvarez, J., and Torres, J. C. (1985). Slow axoplasmic transport: a fiction? J. Theor. Biol. 112:627–6651.PubMedCrossRefGoogle Scholar
  3. Austin, L., and Morgan, I.G. (1967). Incorporation of 14-C-labelled leucine into synaptosomes from rat cerebral cortex “in vitro”. J. Neurochem. 14:377–387.PubMedCrossRefGoogle Scholar
  4. Benech, C.R., Sad, E.A., and Franchi, C.M. (1968). In vivo local uptake of C-14 orotic acid by peripheral nerve. Exp. Neurol. 22:436–443.PubMedCrossRefGoogle Scholar
  5. Benech, C. R., Sotelo, J.R., Menéndez, J., and Correa-Luna, R. (1982). Autoradiographic study of RNA and protein synthesis in sectioned peripheral nerves. Exp. Neurol. 76:72–82.PubMedCrossRefGoogle Scholar
  6. Benech, J.C., Crispino, M., Chun, J.T., Kaplan, B.B., and Giuditta, A. (1994). Protein Synthesis in nerve endings from squid brain: modulation by calcium ions. Biol. Bull. 187:269.PubMedGoogle Scholar
  7. Benech, J.C., Crispino, M., Martin, R., Alvarez, J., Kaplan, B.B., and Giuditta, A. (1996). Protein synthesis in the presynaptic endings of the squid photoreceptor neuron: in vitro and in vivo modulation. Biol. Bull. 191:263.PubMedGoogle Scholar
  8. Bridgers, W.F., Cunningham, R.D., and Gressett, G. (1971). Properties distinguishing mitochondrial and synaptosomal protein synthesis. Biochem. Biophys. Res. Commun. 45:351–357.PubMedCrossRefGoogle Scholar
  9. Brostrom, C.O., Bocckino, S.B., and Brostrom, M. (1983). Identification of a calcium requirement for protein synthesis in eukaryotic cells. J. Biol. Chem. 258:14390–14399.PubMedGoogle Scholar
  10. Brostrom, C.O., and Brostrom, M. (1990). Calcium-dependent regulation of protein synthesis in intact mammalian cells. Annu. Rev. Physiol. 52:577–590.PubMedCrossRefGoogle Scholar
  11. Chin, K.V., Cade, C., Brostrom, M., Brostrom C.O. (1988). Regulation of protein synthesis in intact rat liver by calcium mobilizing agents. Int. J. Biochem. 20:1313–1319.PubMedCrossRefGoogle Scholar
  12. Cohen, A.I. (1973). An ultrastructural analysis of the photoreceptors of the squid and their synaptic conections. Ill. Photoreceptor terminations in the optic lobes. J. Comp. Neurol. 147:399–426.PubMedCrossRefGoogle Scholar
  13. Cotman, C.W., and Taylor, D.A. (1971). Autoradiographic analysis of protein synthesis in synaptosomal fractions. Brain. Res. 29:366–372.PubMedCrossRefGoogle Scholar
  14. Crispino, M., Castigli, E., Perrone Capano, C., Martin, R., Menichini, E., Kaplan, B.B., and Giuditta, A. (1993a). Protein synthesis in a synaptosomal fraction from squid brain. Mol. Cell. Neurosci. 4:366–374.CrossRefGoogle Scholar
  15. Crispino, M., Perrone Capano, C., Kaplan, B.B., and Giuditta, A. (1993b). Neurofilament proteins are synthesized in the nerve endings from squid brain. J. Neurochem. 61:1144–1146.CrossRefGoogle Scholar
  16. Crispino, M., Kaplan, B.B., Martin, R., Alvarez, J., Chun, J.T., Benech, J.C., and Giuditta, A. (1997). Active polysomes are present in the large presynaptic endings of the synaptosomal fraction from squid brain. Submitted.Google Scholar
  17. Endo, M., Tanaka, M., and Ogawa, Y. (1970). Calcium induced release of calcium from the sarcoplasmic reticulum of skinned muscle fibres. Nature. 228:34–36.PubMedCrossRefGoogle Scholar
  18. Ehrlich, B.E., and Watras, J. (1988). Inositol 1,4,5-trisphosphate activates a channel from smooth muscle sarcoplasmic reticulum. Nature. 336:583–586.PubMedCrossRefGoogle Scholar
  19. Frankel, R.D., and Koenig, E. (1977). Identification of major indigenous protein components in mammalian axons and locally synthesized axonal proteins in hypoglossal nerve. Exp. Neurol. 57:282–295.PubMedCrossRefGoogle Scholar
  20. Frankel, R.D., and Koenig, E. (1978). Identification of locally synthesized proteins in proximal stumps axons of the neurotomized hypoglossal nerve. Brain. Res. 141:67–76.PubMedCrossRefGoogle Scholar
  21. Gordon, M.W., and Deanin, G.G. (1968). Protein synthesis by isolated rat brain mithochondria and synaptosomes. J. Biol. Chem. 243:4222–4226.PubMedGoogle Scholar
  22. Haghighat, N., Cohen, R.S., and Pappas, G.D. (1984). Fine structure of squid (Loligo pealei) optic lobe synapses. Neurosci. 13:527–546.CrossRefGoogle Scholar
  23. Hidaka, H; Sasaki, Y; Tanaka, T; Endo, T; Ohno, S; Fujii, Y. and Nagata, T. (1981). N-(6-aminohexyl)-5-chloro-1-naphtalenesulfonamide, a calmodulin antagonist, inhibits cell proliferation. Proc Natl. Acad. Sci. USA. 78:4354PubMedCrossRefGoogle Scholar
  24. Inui, M., Saito, A., and Fleischer, S. (1987). Purification of the ryanodine receptor and identity with feet structures of junctional terminal cisternae of sarcoplasmic reticulum from skeletal muscle. J. Biol. Chem. 262:1740–1747.PubMedGoogle Scholar
  25. Kimball, S. R., and Jefferson, L. (1991). Mechanism of inhibition of peptide chain initiation by amino acid deprivation in perfused rat liver. Regulation involving inhibition of eukaryotic initiation factor 2 alpha phosphatase activity. J. Biol. Chem. 266:1969–1974.PubMedGoogle Scholar
  26. Kimball, S. R., and Jefferson, L. (1992). Regulation of protein synthesis by modulation of intracellular calcium in rat liver. Am. J. Physiol. 263 (Endocrinol. Metab. 26):E958–E964.PubMedGoogle Scholar
  27. Kobayashi, E. (1989). Calphostin C (UCN-1028C), a novel microbial compound, is a highly specific inhibitor of protein kinase C. Biochem. Biophys. Res. Commun. 159:548–553.PubMedCrossRefGoogle Scholar
  28. Koenig, E., and Koelle, G.B. (1960). Acetylcholinesterase regeneration in peripheral nerve after irreversible inactivation. Science. 132:1249–1250.PubMedCrossRefGoogle Scholar
  29. Koenig, E. (1967a). Synthetic mechanisms in the axon. I. Local axonal synthesis ofacetylcholinesterase. J. Neurochem. 12:343–355.CrossRefGoogle Scholar
  30. Koenig, E. (1967b). Synthetic mechanisms in the axon. Ill. Stimulation of aeetylcholinesterase synthesis by actinomycin D in the hypoglossal nerve. J. Neurochem. 14:429–435.CrossRefGoogle Scholar
  31. Koenig, E. (1967c). Synthetic mechanisms in the axon. IV. In vitro incorporation of [3H]precursors into axonal proteins and RNA. J. Neurochem. 14:437–446.CrossRefGoogle Scholar
  32. Koenig, E. (1979). Ribosomal RNA in the Mauthner axon: implications for a protein synthesis machinery in the myelinated axons. Brain. Res. 174:95–107.PubMedCrossRefGoogle Scholar
  33. Koenig, E. (1984). Local synthesis of axonal proteins. In Lajtha, A. In: Handbook of Neurochemistry, 7:315–340, second edition. Plenum Press, New York.Google Scholar
  34. Koenig, E. (1991). Evaluation of local synthesis of axonal proteins in the goldfish Mauthner cell axon and axons of the dorsal and ventral roots of the rat in vitro. Mol. Cell. Neurosci. 2:384–394.PubMedCrossRefGoogle Scholar
  35. Koenig, E., and Martin, R. (1996). Cortical plaque-like structure identify ribosome-containing domains in the Mauthner cell axon. J. Neurosci. 16:1400–1411.PubMedGoogle Scholar
  36. Kumar, R. V; Panniers, R; Wolfman, A. and Henshaw, E. C. (1991). Inhibition of protein synthesis by antagonists of calmodulin in Ehrlich ascites tumor cells. Eur. J. Biochem. 195:313–319.PubMedCrossRefGoogle Scholar
  37. Liu, C., and Herman, T. E. (1978). Characterization of ionomycin as a calcium ionophore. J. Biol. Chem. 253:5892–5894.PubMedGoogle Scholar
  38. Lytton, J., Westlin, M. and Hanley, M.R. (1991). Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca2+ATPase family of calcium pumps. J. Biol. Chem. 266:17067–17071.PubMedGoogle Scholar
  39. Martin, R., Crispino, M., Kaplan, B.B., and Giuditta, A. (1997). Ribosome-like particles are present in axons and presynaptic endings of the squid photorreceptor neuron. Submitted.Google Scholar
  40. Morgan, I.G., and Austin, L. (1968). Synaptosomal protein synthesis in a cell-free system. J. Neurochem. 15:41–51.PubMedCrossRefGoogle Scholar
  41. Montarolo, P.G., Golet, P., Castelluci, V.F., Morgan, J., Kandel, E.R., and Schacher, S. (1986). A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplisia. Science 234:1249–1254.PubMedCrossRefGoogle Scholar
  42. Muallem, S., Khademazad, M. and Sachs, G. (1990). The route of Ca’’ entry during reloading of the intracellular Ca2’ pool in pancreatic acini. J. Biol. Chem. 265:2011–2016.PubMedGoogle Scholar
  43. Nygard, O.; Nilsson, A.; Carlberg, U.; Nilson, L. and Amons, R. (1991). Phosphorylation regulates the activity of the eEF-2 specific Cat+ - and calmoldulin-dependent protein kinase III. J. Biol. Chem. 266:16425–16430.PubMedGoogle Scholar
  44. Otani, S., Marshall, C.J., Tate, W.P., Goddard, G.V., and Abraham, W.C. (1989). Maintenance of long-term potentiation in rat dentate gyrus requires protein synthesis but not messenger RNA synthesis immediately posttetanization. Neuroscience 28:519–526.PubMedCrossRefGoogle Scholar
  45. Preston, G.F., and Berlin, R.D. (1992). An intracellular calcium store regulates protein synthesis in HeLa cells, but is not the hormone-sensitive store. Cell Calcium. 13:303–312.PubMedCrossRefGoogle Scholar
  46. Rao, A., and Steward, O. (1991). Evidence that protein constituents of postsynaptic membrane specializations arc locally synthesized: analysis of proteins synthesized within synaptosomes. J. Neurosci. 11:2881–2895.PubMedGoogle Scholar
  47. Sagara, Y. and mesi, G. (1991). Inhibition of the sarcoplasmic reticulum Ca“ transport ATPase by thapsigargin at subnanomolar concentrations. J. Biol. Chem. 266:13503–13506.PubMedGoogle Scholar
  48. Schweitzer, E. (1987). Coordinated release of ATP and ACh from cholinergic synaptosomes and its inhibition by calmodulin antagonists. J. Neurosci. 7:2948–2956.PubMedGoogle Scholar
  49. Sitges, M., and Talamo, B. R. (1993). Sphingosone, W7, and trifluoperazine inhibit the elevation in cytosolic calcium induced by high K’ depolarization in synaptosomes. J. Neurochem. 61:443–450.PubMedCrossRefGoogle Scholar
  50. Snelling, R., and Nicholls, D. (1984). The calmodulin antagonists, trifluoperazine and R24571, depolarize the mitochondria within guinea pig cerebral cortical synaptosomes. J. Neurochem. 42:1552–1557.PubMedCrossRefGoogle Scholar
  51. Sotelo, J.R., Benech, C.R., and Kun, A. (1992). Local radiolabeling of the 68kDa neurofilament protein in rat sciatic nerves. Neurosci. Let. 144:174–176.CrossRefGoogle Scholar
  52. Toeplitz, B. K., Cohen, A. I., Funke, P. T., Parker, W. L., and Gougoutas, J. Z. (1979). Structure of ionomycin: a novel diacidic polyether antibiotic having high affinity for calcium ions. J. Am. Chem. Soc. 101:3344–3353.CrossRefGoogle Scholar
  53. Tobias, G. S., and Koenig, E. (1975a). Axonal protein synthesizing activity during the early outgrowth period following neurotomy. Exp. Neurol. 49:221–234.CrossRefGoogle Scholar
  54. Tobias, G. S., and Koenig, E. (1975b). Influence of nerve cell body and neurilemma cells on local axonal protein synthesis following neurotomy. Exp. Neurol. 49:235–245.CrossRefGoogle Scholar
  55. Wang, J.K.T., Walaas, S.I., and Greengard, P. (1988). Protein phosphorylation in nerve terminals: comparison of calcium/calmodulin-dependent and calcium/diacylglycerol-dependent systems. J. Neurosci. 8:281–288.PubMedGoogle Scholar
  56. Young, J.Z. (1962). The retina of cephalopods and its degeneration after optic section. Phil. Trans. Roy. Soc. B. 245:281–288.Google Scholar
  57. Young, J.Z. (1974). The central nervous system of Loligo. 1. The optic lobe. Phil. Trans. Roy. Soc. B. 267:263–302.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1997

Authors and Affiliations

  • Juan Claudio Benech
    • 1
    • 2
  • Mariana Crispino
    • 4
  • Barry B. Kaplan
    • 3
  • Antonio Giuditta
    • 4
  1. 1.División BiofísicaInstituto de Investigaciones Biológicas Clemente EstableMontevideoUruguay
  2. 2.Area BiofísicaFacultad de VeterinariaMontevideoUruguay
  3. 3.Western Psychiatric Institute and ClinicUniversity of Pittsburgh Medical CenterPittsburghUSA
  4. 4.Department of General and Environmental PhysiologyUniversity of Naples “Federico II”NaplesItaly

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