 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
Volume 17, Number 20, Issue of October 15, 1997 pp. 7839-7849
Copyright ©1997 Society for NeuroscienceIn Vitro Synaptogenesis between the Somata of Identified Lymnaea Neurons Requires Protein Synthesis But Not Extrinsic Growth Factors or Substrate Adhesion Molecules
Received June 26, 1997; revised July 18, 1997; accepted July 28, 1997.
Zhong-Ping Feng1, Judith Klumperman2, Ken Lukowiak1, and Naweed I. Syed1 1 Respiratory and Neuroscience Research Groups, Departments of Anatomy and Medical Physiology, Faculty of Medicine, University of Calgary, Calgary, Alberta, Canada T2N 4N1, and 2 Faculty of Biology, Free University Amsterdam, The Netherlands
Nerve growth factors, substrate and cell adhesion molecules, and protein synthesis are considered necessary for most developmental programs, including cell proliferation, migration, differentiation, axogenesis, pathfinding, and synaptic plasticity. Their direct involvement in synapse formation, however, has not yet been fully determined. The neurite outgrowth that precedes synaptogenesis is contingent on protein synthesis, the availability of externally supplied growth factors, and substrate adhesion molecules. It is therefore difficult to ascertain whether these factors are also needed for synapse formation. To examine this issue directly we reconstructed synapses between the cell somata of identified Lymnaea neurons. We show that when paired in the presence of brain conditioned medium (CM), mutual inhibitory chemical synapses between neurons right pedal dorsal 1 (RPeD1) and visceral dorsal 4 (VD4) formed in a soma-soma configuration (86%; n = 50). These synapses were reliable and target cell specific and were similar to those seen in the intact brain. To test whether synapse formation between RPeD1 and VD4 required de novo protein synthesis, the cells were paired in the presence of anisomycin (a nonspecific protein synthesis blocker). Chronic anisomycin treatment (18 hr) after cell pairing completely blocked synaptogenesis between RPeD1 and VD4 (n = 24); however, it did not affect neuronal excitability or responsiveness to exogenously applied transmitters (n = 7), nor did chronic anisomycin treatment affect synaptic transmission between pairs of cells that had formed synapses (n = 5). To test the growth and substrate dependence of synapse formation, RPeD1 and VD4 were paired in the absence of CM [defined medium; (n = 22)] on either plain plastic culture dishes (n = 10) or glass coverslips (n = 10). Neither CM nor any exogenous substrate was required for synapse formation. In summary, our data provide direct evidence that synaptogenesis in this system requires specific, cell contact-induced, de novo protein synthesis but does not depend on extrinsic growth factors or substrate adhesion molecules.
Key words: synapse formation; in vitro; growth factors; Lymnaea; soma-soma synapses; mollusks
This article has been cited by other articles:
K. Hui, G.-H. Fei, B. J. Saab, J. Su, J. C. Roder, and Z.-P. Feng
Neuronal calcium sensor-1 modulation of optimal calcium level for neurite outgrowth
Development, December 15, 2007; 134(24): 4479 - 4489.
[Abstract] [Full Text] [PDF]
P. Gardzinski, D. W. K. Lee, G.-H. Fei, K. Hui, G. J. Huang, H.-S. Sun, and Z.-P. Feng
The role of synaptotagmin I C2A calcium-binding domain in synaptic vesicle clustering during synapse formation
J. Physiol., May 15, 2007; 581(1): 75 - 90.
[Abstract] [Full Text] [PDF]
P. Lovell and L. L. Moroz
The largest growth cones in the animal kingdom: an illustrated guide to the dynamics of Aplysia neuronal growth in cell culture
Integr. Comp. Biol., December 1, 2006; 46(6): 847 - 870.
[Abstract] [Full Text] [PDF]
M. A. Colicos and N. I. Syed
Neuronal networks and synaptic plasticity: understanding complex system dynamics by interfacing neurons with silicon technologies
J. Exp. Biol., June 15, 2006; 209(12): 2312 - 2319.
[Abstract] [Full Text] [PDF]
R. Wiersma-Meems, J. Van Minnen, and N. I. Syed
Synapse Formation and Plasticity: The Roles of Local Protein Synthesis
Neuroscientist, June 1, 2005; 11(3): 228 - 237.
[Abstract] [PDF]
J. D. Spafford, J. van Minnen, P. Larsen, A. B. Smit, N. I. Syed, and G. W. Zamponi
Uncoupling of Calcium Channel {alpha}1 and {beta} Subunits in Developing Neurons
J. Biol. Chem., September 24, 2004; 279(39): 41157 - 41167.
[Abstract] [Full Text] [PDF]
M. Ghirardi, F. Benfenati, S. Giovedi, F. Fiumara, C. Milanese, and P. G. Montarolo
Inhibition of Neurotransmitter Release by a Nonphysiological Target Requires Protein Synthesis and Involves cAMP-Dependent and Mitogen-Activated Protein Kinases
J. Neurosci., May 26, 2004; 24(21): 5054 - 5062.
[Abstract] [Full Text] [PDF]
S. Sangha, A. Scheibenstock, R. Morrow, and K. Lukowiak
Extinction Requires New RNA and Protein Synthesis and the Soma of the Cell Right Pedal Dorsal 1 in Lymnaea stagnalis
J. Neurosci., October 29, 2003; 23(30): 9842 - 9851.
[Abstract] [Full Text] [PDF]
A. J. Woodall, H. Naruo, D. J. Prince, Z. P. Feng, W. Winlow, M. Takasaki, and N. I. Syed
Anesthetic Treatment Blocks Synaptogenesis But Not Neuronal Regeneration of Cultured Lymnaea Neurons
J Neurophysiol, October 1, 2003; 90(4): 2232 - 2239.
[Abstract] [Full Text] [PDF]
S. Sangha, A. Scheibenstock, and K. Lukowiak
Reconsolidation of a Long-Term Memory in Lymnaea Requires New Protein and RNA Synthesis and the Soma of Right Pedal Dorsal 1
J. Neurosci., September 3, 2003; 23(22): 8034 - 8040.
[Abstract] [Full Text] [PDF]
D. W. Munno, D. J. Prince, and N. I. Syed
Synapse Number and Synaptic Efficacy Are Regulated by Presynaptic cAMP and Protein Kinase A
J. Neurosci., May 15, 2003; 23(10): 4146 - 4155.
[Abstract] [Full Text] [PDF]
S. Sangha, A. Scheibenstock, C. McComb, and K. Lukowiak
Intermediate and long-term memories of associative learning are differentially affected by transcription versus translation blockers inLymnaea
J. Exp. Biol., May 15, 2003; 206(10): 1605 - 1613.
[Abstract] [Full Text] [PDF]
R. Meems, D. Munno, J. van Minnen, and N. I. Syed
Synapse Formation Between Isolated Axons Requires Presynaptic Soma and Redistribution of Postsynaptic AChRs
J Neurophysiol, May 1, 2003; 89(5): 2611 - 2619.
[Abstract] [Full Text] [PDF]
J. D. Spafford, D. W. Munno, P. van Nierop, Z.-P. Feng, S. E. Jarvis, W. J. Gallin, A. B. Smit, G. W. Zamponi, and N. I. Syed
Calcium Channel Structural Determinants of Synaptic Transmission between Identified Invertebrate Neurons
J. Biol. Chem., January 31, 2003; 278(6): 4258 - 4267.
[Abstract] [Full Text] [PDF]
K. Lukowiak, Z. Haque, G. Spencer, N. Varshay, S. Sangha, and N. Syed
Long-Term Memory Survives Nerve Injury and the Subsequent Regeneration Process
Learn. Mem., January 1, 2003; 10(1): 44 - 54.
[Abstract] [Full Text] [PDF]
P. Lovell, B. McMahon, and N. I. Syed
Synaptic Precedence During Synapse Formation Between Reciprocally Connected Neurons Involves Transmitter-Receptor Interactions and AA Metabolites
J Neurophysiol, September 1, 2002; 88(3): 1328 - 1338.
[Abstract] [Full Text] [PDF]
S. Schacher and F. Wu
Synapse Formation in the Absence of Cell Bodies Requires Protein Synthesis
J. Neurosci., March 1, 2002; 22(5): 1831 - 1839.
[Abstract] [Full Text] [PDF]
M. A. Woodin, D. W. Munno, and N. I. Syed
Trophic Factor-Induced Excitatory Synaptogenesis Involves Postsynaptic Modulation of Nicotinic Acetylcholine Receptors
J. Neurosci., January 15, 2002; 22(2): 505 - 514.
[Abstract] [Full Text] [PDF]
G. E. Spencer, K. Lukowiak, and N. I. Syed
Transmitter-Receptor Interactions between Growth Cones of Identified Lymnaea Neurons Determine Target Cell Selection In Vitro
J. Neurosci., November 1, 2000; 20(21): 8077 - 8086.
[Abstract] [Full Text] [PDF]
T. Hamakawa, Z.-P. Feng, N. Grigoriv, T. Inoue, M. Takasaki, S. Roth, K. Lukowiak, S. U. Hasan, and N. I. Syed
Sevoflurane Induced Suppression of Inhibitory Synaptic Transmission Between Soma-Soma Paired Lymnaea Neurons
J Neurophysiol, November 1, 1999; 82(5): 2812 - 2819.
[Abstract] [Full Text] [PDF]
T. Hamakawa, M. A. Woodin, M. C. Bjorgum, S. D. Painter, M. Takasaki, K. Lukowiak, G. T. Nagle, and N. I. Syed
Excitatory Synaptogenesis between Identified Lymnaea Neurons Requires Extrinsic Trophic Factors and Is Mediated by Receptor Tyrosine Kinases
J. Neurosci., November 1, 1999; 19(21): 9306 - 9312.
[Abstract] [Full Text] [PDF]
M. A. Saver, J. L. Wilkens, and N. I. Syed
In Situ and In Vitro Identification and Characterization of Cardiac Ganglion Neurons in the Crab, Carcinus maenas
J Neurophysiol, June 1, 1999; 81(6): 2964 - 2976.
[Abstract] [Full Text] [PDF]
M. A. Woodin, T. Hamakawa, M. Takasaki, K. Lukowiak, and N. I. Syed
Trophic Factor-Induced Plasticity of Synaptic Connections Between Identified Lymnaea Neurons
Learn. Mem., May 1, 1999; 6(3): 307 - 316.
[Abstract] [Full Text]
N. S. Magoski and A. G. M. Bulloch
Trophic and Contact Conditions Modulate Synapse Formation Between Identified Neurons
J Neurophysiol, June 1, 1998; 79(6): 3279 - 3283.
[Abstract] [Full Text] [PDF]
R. E. van Kesteren, N. I. Syed, D. W. Munno, J. Bouwman, Z.-P. Feng, W. P. M. Geraerts, and A. B. Smit
Synapse Formation between Central Neurons Requires Postsynaptic Expression of the MEN1 Tumor Suppressor Gene
J. Neurosci., August 15, 2001; 21(16): RC161 - RC161.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|