Establishing and sculpting the synapse in Drosophila and C. elegans

Current Opinion in Neurobiology

Volumn 12, Issue 5, 2002, Pages 491-498

  Broadie, Kendal S ^a   Richmond, Janet E ^b  

^a VANDERBILT UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; GLUTAMIC ACID; PHOSPHATASE; POSTSYNAPTIC RECEPTOR; PROTEIN; PROTEIN LIPRIN; RECEPTOR; SPECTRIN; TYROSINE PHOSPHATASE; UNCLASSIFIED DRUG;

CAENORHABDITIS ELEGANS; DEGRADATION; DROSOPHILA; GENETIC PROCEDURES; LEUKOCYTE; NONHUMAN; PHYSIOLOGY; POLARIZATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; SCREENING; SYNAPSE; TRANSLATION REGULATION;

EID: 0036802605     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(02)00359-8     Document Type: Review

References (30)

1. Bate M., Broadie K. Wiring by fly: the neuromuscular system of the Drosophila embryo. Neuron. 15:1995;513-525.
2. Broadie K.S. Electrophysiological approaches to the neuromusculature. Sullivan W., Ashburner M., Hawley R.S., Drosophila Protocols. 1:2000;273-296 Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
3. Richmond J.E., Davis W.S., Jorgensen E.M. UNC-13 is required for synaptic vesicle fusion in C. elegans. Nat Neurosci. 2:1999;959-964.
4. Richmond J.E., Jorgensen E.M. One GABA and two acetylcholine receptors function at the C. elegans neuromuscular junction. Nat Neurosci. 2:1999;791-797.
5. Richmond JE, Broadie K: The synaptic vesicle cycle: EExocytosis and endocytosis in Drosophila and C. elegans. Curr Opin Neurobiol 2002, in press.
6. Broadie K., Bate M. Innervation directs receptor synthesis and localization in Drosophila embryo synaptogenesis. Nature. 361:1993;350-353.
7. Prokop A., Landgraf M., Rushton E., Broadie K., Bate M. Presynaptic development at the Drosophila neuromuscular junction: assembly and localization of presynaptic active zones. Neuron. 17:1996;617-626.
8. Zhen M., Jin Y. The liprin protein SYD-2 regulates the differentiation of presynaptic termini in C. elegans. Nature. 401:1999;371-375.
9. Crump J.G., Zhen M., Jin Y., Bargmann C.I. The SAD-1 kinase regulates presynaptic vesicle clustering and axon termination. Neuron. 29:2001;115-129. A forward screen in C. elegans used SV-associated synaptobrevin-GFP in chemosensory neurons to uncover synaptogenesis mutants. The largest complementation group was in the sad-1 gene, encoding a PAR1-like kinase. The SAD-1 product is present in presynaptic terminals; in sad-1-deficient mutants, SV clusters are misorganized or absent. SAD-1 overexpression causes ectopic SV clustering in dendrites and also premature axonal arrest. The SAD-1 kinase is most likely involved in microtubule mechanisms determining neuronal polarity and synaptogenesis.
10. Guo S., Kemphues K.J. par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell. 81:1995;611-620.
11. Kaufmann N., DeProto J., Ranjan R., Wan H., Van Vactor D. Drosophila Liprin-alpha and the receptor phosphatase Dlar control synapse morphogenesis. Neuron. 34:2002;27-38. The Drosophila receptor phosphatase dlar interacts with dliprin-α to regulate the formation of presynaptic active zones. These authors show that mutations in both genes cause a loss of regular active zone dimensions and a two-fold average increase in active zone area. Conversely, mutations in both genes suppress presynaptic SV fusion. dlar and dliprin-α are putatively involved in regulating cytoskeletal components required for active zone formation. Both proteins also play roles in NMJ morphogenesis, but these roles are not discussed in this review.
12. Zhou H.M., Brust-Mascher I., Scholey J.M. Direct visualization of the movement of the monomeric axonal transport motor UNC-104 along neuronal processes in living Caenorhabditis elegans. J Neurosci. 21:2001;3749-3755.
13. Byrd D.T., Kawasaki M., Walcoff M., Hisamoto N., Matsumoto K., Jin Y. UNC-16, a JNK-signaling scaffold protein, regulates vesicle transport in C. elegans. Neuron. 32:2001;787-800. The C. elegans gene unc-16 encodes a JIP3 homolog of Drosophila sunday driver. In this study, mutations in unc-16 cause SV mislocalization and defects in glutamate receptor localization. Comparable defects are observed in JNK and JNK kinase mutants. Surprisingly, unc-16 mutations suppress the trafficking defects of Unc-104/KIF1A. This study therefore suggests that Unc-16 may regulate the delivery of synaptic cargoes by integrating JNK signaling and kinesin-based microtubule transport.
14. Featherstone D.E., Davis W.S., Dubreuil R.R., Broadie K. Drosophila alpha- and beta-spectrin mutations disrupt presynaptic neurotransmitter release. J Neurosci. 21:2001;4215-4224. These authors show that Drosophila null mutants of either α-spectrin or β-spectrin dramatically impair synaptic transmission. Surprisingly, neither mutant shows detectable defects in either SV localization or postsynaptic neurotransmitter (glutamate) receptor localization. Thus, spectrins do not appear to be essential for these widely hypothesized functions, at least in Drosophila. Rather, spectrin mutants show gross mislocalization of numerous essential synaptic proteins; these proteins escape the normal tight, punctate restriction at synaptic contacts to diffuse throughout the cells. Thus, a spectrin cytoskeleton is essential for synaptic compartmentalization.
15. Broadie K., Bate M. Activity-dependent development of the neuromuscular synapse during Drosophila embryogenesis. Neuron. 11:1993;607-619.
16. Saitoe M., Schwarz T.L., Umbach J.A., Gundersen C.B., Kidokoro Y. Absence of junctional glutamate receptor clusters in Drosophila mutants lacking spontaneous transmitter release. Science. 293:2001;514-517. Saitoe et al. report that spontaneous SV fusion is required for neurotransmitter (glutamate) receptor induction/localization during synaptogenesis. This result is controversial (see [17••] ).
17. Featherstone D.E., Rushton E., Broadie K. Developmental regulation of glutamate receptor field size by nonvesicular glutamate release. Nat Neurosci. 5:2002;141-146. A previous Drosophila forward genetic screen isolated gad mutants as defective in glutamate receptor field formation [18] . This study shows that mutation in a number of glutamate metabolizing enzymes alters presynaptic glutamate concentration to regulate postsynaptic glutamate receptor number. Increasing presynaptic glutamate concentration always decreased the number and field size of glutamate receptors; decreasing glutamate concentration presynaptically always increased glutamate receptor number and field size. Thus, glutamate is proposed to act as a negative regulator of its own receptor during synaptogenesis. Surprisingly, blocking SV fusion did not impair this regulation, suggesting that glutamate is being released via a nonvesicular mechanism, and confirming earlier studies that SV fusion is not required for glutamate receptor field formation or regulation. See also [16•], for an opposing point of view.
18. Featherstone D.E., Rushton E.M., Hilderbrand-Chae M., Phillips A.M., Jackson F.R., Broadie K. Presynaptic glutamic acid decarboxylase (GAD) is required for induction of the postsynaptic receptor field at a glutamatergic synapse. Neuron. 1:2000;71-84.
19. Featherstone D.E., Broadie K. Surprises from Drosophila: mechanisms of synaptic development and plasticity. Brain Res Bull. 53:2000;501-511.
20. Jabaudon D., Shimamoto K., Yasuda-Kamatani Y., Scanziani M., Gahwiler B.H., Gerber U. Inhibition of uptake unmasks rapid extracellular turnover of glutamate of nonvesicular origin. Proc Natl Acad Sci USA. 96:1999;8733-8738.
21. Sigrist S.J., Thiel P.R., Reiff D.F., Lachance P.E., Lasko P., Schuster C.M. Postsynaptic translation affects the efficacy and morphology of neuromuscular junctions. Nature. 405:2000;1062-1065.
22. Li Z., Zhang Y., Ku L., Wilkinson K.D., Warren S.T., Feng Y. The fragile X mental retardation protein inhibits translation via interaction with mRNA. Nucleic Acids Res. 29:2001;2276-2283.
23. Irwin S.A., Patel B., Idupulapati M., Harris J.B., Crisostomo R.A., Larsen B.P., Kooy F., Willems P.J., Cras P., Kozlowski P.B., et al. Abnormal dendritic spine characteristics in the temporal and visual cortices of patients with fragile-X syndrome: a quantitative examination. Am J Med Genet. 98:2001;161-167.
24. Zhang Y.Q., Bailey A.M., Matthies H.J., Renden R.B., Smith M.A., Speese S.D., Rubin G.M., Broadie K. Drosophila fragile X-related gene regulates the MAP1B homolog Futsch to control synaptic structure and function. Cell. 107:2001;591-603. The Drosophila ortholog of the FMRP (dfxr or dfmr) is here shown to encode a product with similar cellular expression and biochemical properties as the mammalian protein. As in mammals, null dfxr mutants are viable but defective in 'higher' neuronal properties. At the NMJ, null dfxr mutants displayed overgrowth and increased neurotransmission, whereas overexpression of dfxr caused opposite phenotypes. The dFXR protein binds futsch (MAP1B) mRNA and negatively regulates futsch translation in the nervous system. Double dfxr/futsch mutants, which have control levels of futsch protein, appear normal and lack all synaptic defects. These results suggest that dFXR acts as a negative translational regulator of futsch to control microtubule stability crucial for synaptic growth and function.
25. Hummel T., Krukkert K., Roos J., Davis G., Klambt C. Drosophila Futsch/22C10 is a MAP1B-like protein required for dendritic and axonal development. Neuron. 26:2000;357-370.
26. Roos J., Hummel T., Ng N., Klambt C., Davis G.W. Drosophila Futsch regulates synaptic microtubule organization and is necessary for synaptic growth. Neuron. 26:2000;371-382.
27. Rodesch C.K., Broadie K. Genetic studies in Drosophila: vesicle pools and cytoskeleton-based regulation of synaptic transmission. Neuroreport. 11:2000;45-53.
28. Wan H.I., DiAntonio A., Fetter R.D., Bergstrom K., Strauss R., Goodman C.S. Highwire regulates synaptic growth in Drosophila. Neuron. 26:2000;313-329.
29. Schaefer A.M., Hadwiger G.D., Nonet M.L. rpm-1, a conserved neuronal gene that regulates targeting and synaptogenesis in C. elegans. Neuron. 26:2000;345-356.
30. Cadavid A.L., Ginzel A., Fischer J.A. The function of the Drosophila fat facets deubiquitinating enzyme in limiting photoreceptor cell number is intimately associated with endocytosis. Development. 127:2000;1727-1736.