The ultrastructural interactions of identified pre- and postsynaptic cells during synaptic target recognition in Drosophila embryos.
During the development of neural networks, what sets synaptogenic interactions apart from nonsynaptogenic interactions is not well understood at the subcellular level. Using a combination of intracellular dye injection and electron microscopy, we show that a specific motoneuron (RP3) and its synaptic partners (muscles 6 and 7), both often bearing microprocesses, develop intimate membrane contact sites characterized by junctional structures, prior to their initiating synaptogenesis in Drosophila embryos. Other motoneuron growth cones that extend alongside the RP3 growth cone to innervate surrounding muscles do not form such contacts with muscles 6 and 7. We also examined how specific target recognition molecules affect the development of these ultrastructural associations between synaptic partner cells. When Fasciclin III (Fas3), a "positive" target recognition molecule for RP3, is ectopically expressed in neighboring muscles, the RP3 growth cone ectopically develops membrane contact sites with Fas3-misexpressing muscles with which it would not normally associate. In contrast, when Toll, a "negative" target recognition molecule normally expressed by a subset of muscles that surrounds muscles 6 and 7, is misexpressed on muscles 6 and 7, the RP3 growth cone fails to exhibit its normal close contact with these muscles. We propose that the formation of close membrane associations and junctional structures can be regulated under the influence of synaptic target recognition molecules and signifies the beginning of subcellular events during synaptic target recognition.
Suzuki
E
E
Department of Fine Morphology, Institute of Medical Science, The University of Tokyo, Tokyo 108-8639, and CREST, JST, Japan.
Rose
D
D
Chiba
A
A
D000818:Animals; D015816:Cell Adhesion Molecules, Neuronal / Q000096:biosynthesis; D002462:Cell Membrane / Q000378:metabolism / Q000648:ultrastructure; D029721:Drosophila Proteins; D004331:Drosophila melanogaster / Q000196:embryology*; D020439:Growth Cones / Q000378:metabolism / Q000648:ultrastructure; D019476:Insect Proteins / Q000096:biosynthesis; D007365:Intercellular Junctions / Q000648:ultrastructure; D008562:Membrane Glycoproteins / Q000096:biosynthesis; D008854:Microscopy, Electron; D009046:Motor Neurons / Q000166:cytology / Q000378:metabolism / Q000648:ultrastructure*; D009132:Muscles / Q000294:innervation / Q000378:metabolism / Q000648:ultrastructure; D011956:Receptors, Cell Surface; D013569:Synapses / Q000378:metabolism / Q000648:ultrastructure*; D051193:Toll-Like Receptors
D015816:Cell Adhesion Molecules, Neuronal; D029721:Drosophila Proteins; C061565:Fas3 protein, Drosophila; D019476:Insect Proteins; D008562:Membrane Glycoproteins; D011956:Receptors, Cell Surface; C068721:Tl protein, Drosophila; D051193:Toll-Like Receptors