Patterns of Presynaptic Gene Expression Define Two Stages of Synaptic Differentiation

Molecular and Cellular Neuroscience

Volumn 6, Issue 3, 1995, Pages 252-262

  Lou, Xing Jian ^a,b   Bixby, John L ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLINE ACETYLTRANSFERASE; MESSENGER RNA; NEUROFILAMENT PROTEIN; SYNAPTOPHYSIN; SYNAPTOTAGMIN;

ANIMAL TISSUE; ARTICLE; CHICK EMBRYO; CILIARY GANGLION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; NERVE CELL DIFFERENTIATION; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN SYNTHESIS REGULATION; SYNAPSE VESICLE; SYNAPTOGENESIS;

AMINO ACID SEQUENCE; ANIMAL; CELL DIFFERENTIATION; CHICK EMBRYO; GENE EXPRESSION; MOLECULAR SEQUENCE DATA; PRESYNAPTIC TERMINALS; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; SUPPORT, U.S. GOV'T, NON-P.H.S.; SUPPORT, U.S. GOV'T, P.H.S.; SYNAPTOPHYSIN; TIME FACTORS;

EID: 0029148188     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1006/mcne.1995.1020     Document Type: Article

References (53)

1. Bajjalieh, S. M., Frantz, G. D., Weimann, J. M., Mc Connell, S. K., and Scheller, R. H. (1994). Differential expression of synaptic vesicle protein 2 (SV2) isoforms. J. Neurosci. 14(9): 5223-5235.
2. Bergmann, M., Lahr, G., Mayerhofer, A., and Gratzl, M. (1991), Expression of synaptophysin during die prenatal development of the rat spinal cord: Correlation with basic differentiation processes of neurons. Neuroscience 42: 569-582.
3. Bixby, J. L., and Reichardt, L. F. (1985). The expression and localization of synaptic vesicle antigens at neuromuscular junctions in vitro. J. Neurosci. 5: 3070-3080.
4. Bixby, J. L. (1992). Identification of an alternatively spliced avian member of the synaptophysin gene family. Brain Res. Mol. Brain Res. 13(4): 339-348.
5. Burt, A. M., and Narayanan, C. H. (1976). Choline acetyltransferase, choline kinase, and acetylcholinesterase activities during the development of the chick ciliary ganglion. Exp. Neurol. 53: 703-713.
6. Cavicchioli, L., Flanigan, T. P., Dickson, J. G., Vantini, G., Toso, R. D., Fusco, M., Walsh, F. S., and Leon, A. (1991). Choline acetyltransferase messenger RNA expression in developing and adult rat brain: Regulation by nerve growth factor. Mol. Brain Res. 9: 319-325.
7. Chiappinelli, V., Giacobini, E., Pilar, G„ and Uchimura, H. (1976). Induction of cholinergic enzymes in chick ciliary ganglion and iris muscle cells during synapse formation. J. Physiol, (London) 257(3): 749-766.
8. Coulombe, J., and Bronner-Fraser, M. (1990). Development of cholinergic traits in the quail ciliary ganglion: Expression of choline acetyl-transferase-like immunoreactivity. Neuroscience 37(1): 259-270.
9. 2+ level accompanying initial nerve-muscle contact in tissue culture. Neuron 10(5): 827-837.
10. Dai, Z., and Peng, H. B. (1994). Mobility of synaptic vesicles during presynaptic development in cultured neurons studied with FM1-43. Sci. Neurosci. Abstr. 632.
11. Devoto, S. H., and Barnstable, C. J. (1989). Expression of the growth cone specific epitope CDA1 and the synaptic vesicle protein svp38 in the developing mammalian cerebral cortex. J Comp. Neurol. 290: 154-168.
12. Eder-Colli, L., and Amato, S. (1985). Membrane-bound choline acetyl-transferase in Torpedo electric organ: A marker for synaptosomal plasma membrane? Neuroscience 15(2): 577-589.
13. Elferink, L. A., Peterson, M. R., and Scheller, R. H. (1993), A role for synaptotagmin (p65) in regulated exocytosis. Cell 72(1): 153-159.
14. Evers, J., Laser, M., Sun, Y. A., Xie, Z. P., and Poo, M. M. (1989), Studies of nerve-muscle interactions in Xenopus cell culture: Analysis of early synaptic currents. J. Neurosci. 9(5): 1523-1539.
15. Fykse, E. M., Takei, K., Walch-Solimena, C., Geppert, M., Jahn, J., De-Camilli, P., and Sudhof, T. C. (1993). Relative properties and localizations of synaptic vesicle protein isoforms: The case of the synaptophy-sins. J. Neurosci. 13: 4997-5007.
16. Geppert, M., Archer, B. T. Ill, and Sudhof, T. C. (1991). Synaptotagmin II, a novel differentially distributed form of synaptotagmin. J. Biol. Chem. 266(2): 13548-13552.
17. 2+ channels coupled to acetylcholine release. Neuron 8: 715-724.
18. Haas, C. A., DeGennaro, L. J., and Hollander, H. (1990). Synapsin I expression in the rat retina during postnatal development. Exp. Brain Res. 82: 25-32.
19. Habecker, B. A., and Landis, S. C. (1994), Noradrenergic regulation of cholinergic differentiation. Science 264:1602-1604.
20. Hall, Z. W., and Sanes, J. R. (1993). Synaptic structure and development: The neuromuscular junction. Neuron 10: 99-121.
21. Hruschak, K. A., Friedrich, V. L., Jr., and Giacobini, E. (1982), Synapto-genesis in cluck paravertebral sympathetic ganglia: A morphometric analysis. Brain Res. 256(2): 229-240.
22. Ibanez, C. F., Emfors, P., and Persson, H. (1991). Developmental and regional expression of choline acetyltransferase mRNA in the rat central nervous system, J. Neurosci. Res. 29:163-171.
23. Jahn, R., and Sudhof, T. C. (1994). Synaptic vesicles and exocytosis. Annu. Rev. Neurosci. 17: 219-246.
24. Kelly, A. M., and Zacks, S. I. (1969). The fine structure of motor endplate morphogenesis. J. Cell Biol. 42: 154-169.
25. Knaus, P., Marqueze-Pouey, B., Scherer, H., and Betz, H. (1990). Synap-toporin, a novel putative channel protein of synaptic vesicles. Neuron 5: 453-462.
26. Landmesser, L., and Pilar, G. (1972). The onset and development of transmission in the chick ciliary ganglion. J. Phisiol. 222: 691-713.
27. Landmesser, L., and Pilar, G. (1974). Synaptic transmission and cell death during normal ganglionic development. J. Physiol. 241: 737-749.
28. Landmesser, L., and Pilar, G. (1976). Fate of ganglionic synapses and ganglion cell axons during normal and induced cell death. J. Cell Biol. 68: 357-374.
29. Lou, X., and Bixby, J. L. (1993). Coordinate and noncoordinate regulation of synaptic vesicle protein genes during embryonic development. Dev. Biol 159: 327-337.
30. Mandell, J. W., Czemik, A. J., De Camilli, P., Greengard, P., and Townes-Anderson, E. (1992). Differential expression of synapsins I and II among rat retinal synapses. J. Neurosci. 12(5): 1736-1749.
31. Marazzi, G., and Buckley, K. M. (1993). Accumulation of mRNAs encoding synaptic vesicle-specific proteins precedes neurite extension during early neuronal development. Dev. Dyn. 197(2): 115-124.
32. Marqueze-Pouey, B., Wisden, W., Malosio, M. L., and Betz, H. (1991). Differential expression of synaptophysin and synaptoporin mRNAs in the postnatal rat central nervous system. J. Neurosci. 11(11): 3388-3397.
33. Meriney, S. D., and Pilar, G. (1987). Cholinergic innervation of the smooth muscle cell in the choroid coat of the chick eye and its development. J. Neurosci. 7(12): 3827-3839.
34. Mizuta, M., Inagaki, N., Nemoto, Y., Matsukura, S., Takahashi, M., and Seino, S. (1994). Synaptotagmin III is a novel isoform of rat synaptotagmin expressed in endocrine and neuronal cells. J. Biol. Chem. 269(16): 11675-11678.
35. Munz, K., Muller, U., and Waser, P. G. (1983). Electron microscopic localization of choline acetyltransferase activity in the electric organ of Torpedo marmorata. Histochemistry 78: 339-347.
36. Napolitano, E. W., Chin, S. S. M., Colman, D. R., and Liem, K. H, (1987). Complete amino acid sequence and in vitro expression of rat NF-M, the middle molecular weight neurofilament protein. J. Neurosci. 7(8): 2590-2599.
37. Ovtscharoff, W., Bergmann, M., Marqueze-Pouey, B., Knaus, P., Betz, H., Grabs, D., Reisert, L, and Gratzl, M. (1993). Ontogeny of synaptophysin and synaptoporin in the central nervous system: Differential expression in striatal neurons and their afferents during development Dev. Brain Res. 72; 219-225.
38. Pilar, G., Chiappinelli, V., Uchimura, H., and Giacobini, E. (1974). Changes of acetylcholinesterase (AChE) and cholineacetyltransferase (ChAc) correlated with the formation of cholinergic synapses in the chick embryo. Physiologist 17: 307.
39. Pilar, G., Nunez, R., McLennan, I. S., and Meriney, S. D. (1987). Muscarinic and nicotinic synaptic activation of the developing chicken iris. J. Neurosci. 7(12): 3813-3826.
40. Puro, D. G., De Mello, F. G., and Nirenberg, M. (1977). Synapse turn-over: The formation and termination of transient synapses. Proc. Natl. Acad. Sci. USA 74(11): 4977-4981.
41. Rao, M. S., Patterson, P. H., and Landis, S. C. (1992). Multiple cholinergic differentiation factors are present in footpad extracts: Comparison with known cholinergic factors. Development 116(3): 731-744.
42. Salvaterra, P. M., and Vaughn, J. E. (1989). Regulation of choline acetyl-transferase. Int. Rev. Neurobiol. 31: 81-143.
43. Sanes, J. R., Johnson, Y. R., Kotzbauer, P. T., Mudd, J., Hanley, T., Martinou, J. C„ and Merlie, J. P. (1991). Selective expression of an acetylcholine receptor-lacZ transgene in synaptic nuclei of adult muscle fibers. Development 113(4): 1181-1191.
44. Takahashi, T., Nakajima, Y., Hirosawa, K., Nakajima, S., and Onodera, K. (1987), Structure and physiology of developing neuromuscular synapses in culture. J. Neurosci. 7(2): 473-481.
45. Thomas, L., Hartung, K., Langosch, D., Rehm, H., Bamberg, E., Franke, W. W., and Betz, H. (1988). Identification of synaptophysin as a hex-americ channel protein of the synaptic vesicle membrane. Science 242(4881): 1050-1053.
46. Thomas, W. S., O'Dowd, D. K., and Smith, M. A. (1993). Developmental expression and alternative splicing of chick agrin RNA. Dev. Biol. 158(2): 523-535.
47. Tsay, H-J., and Schmidt, J. (1989). Skeletal muscle denervation activates receptor genes. J. Cell Biol. 108:1523-1526.
48. Ullrich, B., Li, C., Zhang, J. Z., McMahon, H., Anderson, R. G. W., Geppert, M., and Siidhof, T. C. (1994). Functional properties of multiple synaptotagmins in brain. Neuron 13: 1281-1291.
49. Xie, Z. P., and Poo, M. M, (1986). Initial events in the formation of neuromuscular synapse: Rapid induction of acetylcholine release from embryonic neuron. Proc. Natl. Acad. Sci. USA 83(18): 7069-7073.
50. Yamada, T., Pfaff, S., Edlund, T., and Jessell, T. M. (1993). Control of cell pattern in the neural tube: Motor neuron induction by diffusible factors from notochord and floor plate. Cell 73: 673-686.
51. Zopf, D., Hermans-Borgmeyer, I., Gundelfinger, E. D., and Betz, H. (1987). Identification of gene products expressed in the developing chick visual system: Characterization of a middle-molecular-weight neurofilament cDNA. Genes Dev. 1: 699-708.
52. Zoran, M. J., Funte, L. R., Kater, S. B., and Haydon, P. G. (1993). Neu-ron-muscle contact changes presynaptic resting calcium set-point. Dev. Biol. 158(1): 163-171.
53. Zurmohle, U-M., Herms, J., Schlingensiepen, R., Schlingensiepen, K-H., and Brysch, W. (1994). Changes of synapsin I messenger RNA expression during rat brain development. Exp. Brain Res. 99:17-24.