Expression of synapsin I correlates with maturation of the neuromuscular synapse

Neuroscience

Volumn 74, Issue 4, 1996, Pages 1087-1097

  Lu, B ^a,b,d   Czernik, A J ^a   Popov, S ^c,e   Wang, T ^b   Poo, M M ^c   Greengard, P ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b HOFFMANN LA ROCHE INC   (United States)

^c Och Spine at New York Presbyterian Hospitals   (United States)

^d EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^e UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Laminin; Nerve muscle co culture; Spinal neurons; Spontaneous synaptic currents; Synaptophysin

Indexed keywords

LAMININ; SYNAPSIN I;

ANIMAL TISSUE; ARTICLE; BRAIN HOMOGENATE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; GENE EXPRESSION; IMMUNOCYTOCHEMISTRY; MATURATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; TISSUE CULTURE; XENOPUS;

EID: 0030271819     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(96)00187-X     Document Type: Article

References (47)

1. 1. Bahler M. and Greengard P. (1987) Synapsin I bundles F-actin in a phosphorylation-dependent manner. Nature 326, 704-707.
2. 2. Bixby J. L. and Reichardt L. F. (1985) The expression and localization of synaptic vesicle antigens at neuromuscular junction in vitro. J. Neurosci. 5, 3070-3080.
3. 3. Buchanan J., Sun Y. and Poo M. (1989) Studies of nerve-muscle interactions in cell culture: fine structure of early functional contacts. J. Neurosci. 9, 1540-1554.
4. 4. Chin L., Li L., Ferreira A., Kosik K. S. and Greengard P. (1995) Impairment of axonal development and synaptogenesis in hippocampal neurons of synapsin I-deficient mice. Proc. natn. Acad. Sci. U.S.A. 92, 9230-9234.
5. 5. Czernik A. J., Pang D. T. and Greengard P. (1987) Amino acid sequences surrounding the cAMP-dependent and calcium/calmodulin-dependent phosphorylation sites in rat and bovine synapsin I. Proc. natn. Acad Sci. U.S.A. 84, 7518-7522.
6. 6. DeCamilli P., Cameron R. and Greengard P. (1983) Synapsin I (protein I), a nerve terminal-specific phosphoprotein: its general distribution in synapses of the central and peripheral nervous system demonstrated by immunofluorescence in frozen and plastic sections. J. Cell Biol. 96, 1337-1354.
7. 7. DeGennaro L. J., Kanazir S. D., Wallace W. C., Lewis R. M. and Greengard P. (1983) Neuro-specific phosphoproteins as model for neuronal gene expression. Cold Spring Harbor Symp. quant. Biol. 48, 337-345.
8. 8. Dennis M. J. (1981) Development of neuromuscular junction: inductive interaction between cells. A. Rev. Neurosci. 4, 43-68.
9. 9. Evers J., Laser M., Sun Y., Xie Z. and Poo M. (1989) Studies of nerve-muscle interaction in Xenopus cell culture: analysis of early synaptic currents. J. Neurosci. 9, 1523-1539.
10. 10. Ferreira A., Han H., Greengard P. and Kosik K. S. (1995) Suppression of synapsin II inhibits the formation and maintenance of synapses in hippocampal culture. Proc. natn. Acad. Sci. U.S.A. 92, 9225-9229.
11. 11. Ferreira A., Kosik K. S., Greengard P. and Han H. Q. (1994) Aberrant neurites and synaptic vesicle protein deficiency in synapsin II-depleted neurons. Science 264, 977-999.
12. 12. Flecher T. L., Cameron P., DeCamilli P. and Banker G. A. (1991) The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture. J. Neurosci. 11, 1617-1626.
13. 13. Greengard P., Valtorta F., Czernik A. J. and Benfenati F. (1993) Synaptic vesicle phophoproteins and regulation of synaptic function. Science 259, 780-785.
14. 14. Hackett J. T., Cochran S. L., Greenfield J., Brosius D. C. and Ueda T. (1990) Synapsin I injected presynaptically into goldfish Mauthner axons reduces quantal synaptic transmission. J. Neurophysiol. 63, 701-706.
15. 15. Hall Z. W. and Sanes J. R. (1993) Synaptic structure and development: the neuromuscular junction. Cell/Neuron Rev. 10 (Suppl.), 99-122.
16. 16. Hamill O. P., Marty A., Neher E., Sakmann B. and Sigworth F. J. (1981) Improved patch clamp techniques for high-resolution current recording from cell and cell-free membrane patches. Pflügers Arch. 391, 85-100.
17. 17. Han H. Q., Nichols R. A., Rubin M. R., Bahler M. and Greengard P. (1991) Induction of formation of presynaptic terminals in neuroblastoma cells by synapsin IIb. Nature 349, 697-700.
18. 18. Kelly A. M. and Zachs S. I. (1969) The fine structure of motor end-plate morphogenesis. J. Cell Biol. 42, 154-169.
19. 19. Kidokoro Y. (1984) Two types of miniature endplate potentials in Xenopus nerve muscle cultures. Neurosci. Res. 1, 157-170.
20. 20. Kidokoro Y., Anderson M. J. and Gruner R. (1980) Changes in synaptic potential properties during acetylcholine receptor accumulation and neurospecific interactions in Xenopus nerve-muscle cell culture. Devl Biol. 78, 464-483.
21. 21. Kullberg R. W., Lentz T. L. and Cohen M. W. (1977) Development of myotomal neuromuscular junction in Xenopus laevis: an electrophysiological and fine structural study. Devl Biol. 60, 101-129.
22. 22. Li L., Chin L., Shupliakov O., Brodin L., Sihra T., Hvalby O., Jensen V., Zheng D., McNamara J. O., Greengard P. and Andersen P. (1995) Impairment of synaptic vesicle clustering and of synaptic transmission, and increased seizure propensity, in synapsin 1-deficient mice. Proc. natn. Acad. Sci. U.S.A. 92, 9235-9239.
23. 23. Lin J., Sugimori M., Llinas R. R., McGuinness T. L. and Greengard P. (1990) Effects of synapsin I and calcium/calmodulin-dependent protein kinase II on spontaneous neurotransmitter release in the squid giant synapse. Proc. natn. Acad. Sci. U.S.A. 87, 8257-8261.
24. 24. Llinas R., McGuinness T. L., Leonard C. S., Sugimori M. and Greengard P. (1985) Intra-terminal injection of synapsin I or calcium/calmodulin-dependent protein kinase II alters neurotransmitter release at the squid giant synapse. Proc. natn. Acad. Sci. U.S.A. 82, 3035-3039.
25. 2+-calmodulin-dependent protein kinase II of transmitter release in squid giant synapse. J. Physiol. 439, 257-282.
26. 26. Lohmann S. M., Ueda T. and Greengard P. (1978) Ontogeny of synaptic phosphoproteins in brain. Proc. natn. Acad. Sci. U.S.A. 75, 4037-4041.
27. 27. Lu B., Greengard P. and Poo M. (1992) Exogenous synapsin I promotes functional maturation of developing neuromuscular synapses. Neuron 8, 521-529.
28. 28. Mason C. A. (1986) Axon development in mouse cerebellum: embryonic axon forms and expression of synapsin I. Neuroscience 19, 1319-1333.
29. 29. McMahan U. J. (1990) The agrin hypothesis. Cold Spring Harbor Symp. quant. Biol. 55, 407-418.
30. 30. Nakajima Y., Kidokoro Y. and Klier F. G. (1980) The development of functional neuromuscular junction in vitro: an ultrastructural and physiological study. Devl Biol. 77, 52-72.
31. 31. Nichols R. A., Chilcote T. J., Czernik A. J. and Greengard P. (1992) Synapsin I regulates glutamate release from rat brain synaptosomes. J. Neurochem. 58, 783-785.
32. 32. Nieuwkoop P. and Faber P. (1967) Normal Table of Xenopus laevis. North Holland, Amsterdam.
33. 33. Pieribone V. A., Shupliakov O., Brodin L., Hilfiker-Rothenfiuh S., Czernik A. J. and Greengard P. (1995) Distinct pools of synaptic vesicles in neurotransmitter release. Nature 375, 493-497.
34. 34. Popov S., Brown A. and Poo M. (1993) Forward plasma membrane flow in growing nerve processes. Science 259, 244-246.
35. 35. Reichardt L. F. and Tomaselli K. J. (1991) Extracellular matrix molecules and their receptors: functions in neural development. A. Rev. Neurosci. 14, 531-570.
36. 36. Rosahl T. W., Geppert M., Spillane D., Herz J., Hammer R. E., Malenka R. C. and Sudhof T. C. (1994) Short-term synaptic plasticity is altered in mice lacking synapsin I. Cell 75, 661-670.
37. 37. Rosahl T. W., Spillane D., Missler M., Herz J., Selig D. K., Wolff J. R., Hammer R. E., Malenka R. C. and Sudhof T. C. (1995) Essential function of synapsins I and II in synaptic vesicle regulation. Nature 375, 488-493.
38. 38. Sanes J. R. (1989) Extracellular martrix molecules that influence neural development. A. Rev. Neurosci. 12, 491-516.
39. 39. Sanes J. R. and Chiu A. Y. (1983) The basal lamina of the neuromuscular junction. Cold Spring Harbor Symp. quant. Biol. 48, 667-678.
40. 40. Schaeffer E., Alder J., Greengard P. and Poo M. (1994) Synpasin IIa accelerates functional development of neuromuscular synapses. Proc. natn. Acad. Sci. U.S.A. 91, 3882-3886.
41. 41. Schubert D. (1991) The possible role of adhesion in synaptic modification. Trends Neurosci. 4, 127-130.
42. 42. Sudhof T. C. and Jahn R. (1991) Proteins of synaptic vesicles involved in exocytosis and membrane recyling. Neuron 6, 665-677.
43. 43. Tabti N. and Poo M. (1991) Culturing spinal neurons and muscle cells from Xenopus embryos. In Culture of Nerve Cells (eds Barker G. and Goslin K.), pp. 137-153. MIT Press, Boston, MA.
44. 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, 473-481.
45. 45. Valtorta F., Lezzi N., Benfenati F., Lu B., Poo M. and Greengard P. (1995) Accelerated structural maturation induced by synapsin I at developing neuromuscular synapses of Xenopus laevis. Eur. J. Neurosci. 7, 261-270.
46. 46. Valtorta F., Villa A., Jahn R., DeCamilli P. and Greengard P. (1988) Localization of synapsin I at the frog neuromuscular junction. Neuroscience 24, 593-603.
47. 47. Weiss S., Pin J., Sebben M., Kemp D. E. and Sladeczek F. (1986) Synaptogenesis of cultured striatal neurons in serum-free medium: a morphological study. Proc. natn. Acad. Sci. U.S.A. 83, 2238-2242.