 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
Volume 17, Number 21, Issue of November 1, 1997 pp. 8408-8426
Copyright ©1997 Society for NeuroscienceTransition from Growth Cone to Functional Motor Nerve Terminal in Drosophila Embryos
Received May 14, 1997; revised Aug. 22, 1997; accepted Aug. 22, 1997.
Motojiro Yoshihara1, Mary B. Rheuben2, and Yoshiaki Kidokoro1 1 Gunma University School of Medicine, Maebashi 371, Japan, and 2 Department of Anatomy, College of Veterinary Medicine, Michigan State University, East Lansing, Michigan 48824
As a motor axon grows from the CNS to its target muscle, the terminal has the form of a flattened growth cone with a planar central region, lamellipodia, and filopodia. A mature terminal usually has a stereotyped shape that may be elongated with varicosities, as in several invertebrate species, or have short branches with boutons, as in mammals. We examined in Drosophila the developmental changes between growth cone and mature terminal using ultrastructural and immunocytochemical methods.
The transition period, which occurs 2-3 hr after the first growth cone reaches its target muscle, is marked by the formation of "prevaricosities," smoothly contoured enlargements of the axons at the point where the nerve trunk first contacts the muscle fiber (MF). There is a 15-30 min ventral-to-dorsal gradient in the formation of prevaricosities on the individual abdominal MFs. Multineuronal innervation of each MF has occurred by this time, and two or more different axons undergo prevaricosity formation while they are intimately intertwined at the nerve entry point (NEP). Presynaptic active zones, both nerve-nerve and nerve-muscle, occur within the prevaricosities along broad contact regions. Synaptotagmin immunoreactive clusters form concurrently.
The first varicosities then develop as a result of constrictions of the larger prevaricosities rather than as enlargement of discrete portions of the filopodia or neurites. The prevaricosity stage therefore may include the key steps that lead to the differentiation of functional differences in terminal subtypes as well as those leading to the formation of a stable neuromuscular junction.
Key words: Drosophila; neuromuscular junction; synaptogenesis; growth cone; development; immunohistochemistry
This article has been cited by other articles:
B. Ing, A. Shteiman-Kotler, M. Castelli, P. Henry, Y. Pak, B. Stewart, G. L. Boulianne, and D. Rotin
Regulation of Commissureless by the Ubiquitin Ligase DNedd4 Is Required for Neuromuscular Synaptogenesis in Drosophila melanogaster
Mol. Cell. Biol., January 15, 2007; 27(2): 481 - 496.
[Abstract] [Full Text] [PDF]
A. Ueda and C.-F. Wu
Distinct frequency-dependent regulation of nerve terminal excitability and synaptic transmission by IA and IK potassium channels revealed by Drosophila Shaker and Shab mutations.
J. Neurosci., June 7, 2006; 26(23): 6238 - 6248.
[Abstract] [Full Text] [PDF]
M. Yoshihara, B. Adolfsen, K. T. Galle, and J. T. Littleton
Retrograde Signaling by Syt 4 Induces Presynaptic Release and Synapse-Specific Growth
Science, November 4, 2005; 310(5749): 858 - 863.
[Abstract] [Full Text] [PDF]
J. C. Choi, D. Park, and L. C. Griffith
Electrophysiological and Morphological Characterization of Identified Motor Neurons in the Drosophila Third Instar Larva Central Nervous System
J Neurophysiol, May 1, 2004; 91(5): 2353 - 2365.
[Abstract] [Full Text] [PDF]
G. E. Rieckhof, M. Yoshihara, Z. Guan, and J. T. Littleton
Presynaptic N-type Calcium Channels Regulate Synaptic Growth
J. Biol. Chem., October 17, 2003; 278(42): 41099 - 41108.
[Abstract] [Full Text] [PDF]
B. Berke and C.-F. Wu
Regional Calcium Regulation within Cultured Drosophila Neurons: Effects of Altered cAMP Metabolism by the Learning Mutations dunce and rutabaga
J. Neurosci., June 1, 2002; 22(11): 4437 - 4447.
[Abstract] [Full Text] [PDF]
M. Yoshihara, K. Suzuki, and Y. Kidokoro
Two Independent Pathways Mediated by cAMP and Protein Kinase A Enhance Spontaneous Transmitter Release at Drosophila Neuromuscular Junctions
J. Neurosci., November 15, 2000; 20(22): 8315 - 8322.
[Abstract] [Full Text] [PDF]
M. B. Steketee and K. W. Tosney
Contact with Isolated Sclerotome Cells Steers Sensory Growth Cones by Altering Distinct Elements of Extension
J. Neurosci., May 1, 1999; 19(9): 3495 - 3506.
[Abstract] [Full Text] [PDF]
C. Desai, P. Garrity, H Keshishian, S. Zipursky, and K Zinn
The Drosophila SH2-SH3 adapter protein Dock is expressed in embryonic axons and facilitates synapse formation by the RP3 motoneuron
Development, January 4, 1999; 126(7): 1527 - 1535.
[Abstract] [PDF]
A. Prokop, J. Uhler, J. Roote, and M. Bate
The kakapo Mutation Affects Terminal Arborization and Central Dendritic Sprouting of Drosophila Motorneurons
J. Cell Biol., November 30, 1998; 143(5): 1283 - 1294.
[Abstract] [Full Text] [PDF]
C. Consoulas and R. B. Levine
Presynaptic Function during Muscle Remodeling in Insect Metamorphosis
J. Neurosci., August 1, 1998; 18(15): 5817 - 5831.
[Abstract] [Full Text] [PDF]
E. Shishido, M. Takeichi, and A. Nose
Drosophila Synapse Formation: Regulation by Transmembrane Protein with Leu-Rich Repeats, CAPRICIOUS
Science, June 26, 1998; 280(5372): 2118 - 2121.
[Abstract] [Full Text]
B Wolf, M. Seeger, and A Chiba
Commissureless endocytosis is correlated with initiation of neuromuscular synaptogenesis
Development, January 10, 1998; 125(19): 3853 - 3863.
[Abstract] [PDF]
|
|
|
|
 |
|