Miniature Neurotransmission Regulates Drosophila Synaptic Structural Maturation

Neuron

Volumn 82, Issue 3, 2014, Pages 618-634

  Choi, BenJiwon ^a   Imlach, WendyL ^a   Jiao, Wei ^a   Wolfram, Verena ^b   Wu, Ying ^c   Grbic, Mark ^a   Cela, Carolina ^a   Baines, RichardA ^b   Nitabach, MichaelN ^c   McCabe, Brian D ^a  

^a Department of Pathology and Cell Biology College of Physicians and Surgeons Columbia University ^*  (United States)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE; IONOTROPIC RECEPTOR; RAC1 PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; IN VIVO STUDY; LARVAL STAGE; MOTONEURON; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; SYNAPTOSOME;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DROSOPHILA; MINIATURE POSTSYNAPTIC POTENTIALS; NEUROMUSCULAR JUNCTION; PRESYNAPTIC TERMINALS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84899846239     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.03.012     Document Type: Article

References (50)

1. Aberle H., Haghighi A.P., Fetter R.D., McCabe B.D., Magalhães T.R., Goodman C.S. wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 2002, 33:545-558.
2. Baek M., Enriquez J., Mann R.S. Dual role for Hox genes and Hox co-factors in conferring leg motoneuron survival and identity in Drosophila. Development 2013, 140:2027-2038.
3. Ball R.W., Warren-Paquin M., Tsurudome K., Liao E.H., Elazzouzi F., Cavanagh C., An B.-S., Wang T.-T., White J.H., Haghighi A.P. Retrograde BMP signaling controls synaptic growth at the NMJ by regulating trio expression in motor neurons. Neuron 2010, 66:536-549.
4. Beck E.S., Gasque G., Imlach W.L., Jiao W., Jiwon Choi B., Wu P.-S., Kraushar M.L., McCabe B.D. Regulation of Fasciclin II and synaptic terminal development by the splicing factor beag. J.Neurosci. 2012, 32:7058-7073.
5. Brose N. For better or for worse: complexins regulate SNARE function and vesicle fusion. Traffic 2008, 9:1403-1413.
6. Budnik V., Koh Y.H., Guan B., Hartmann B., Hough C., Woods D., Gorczyca M. Regulation of synapse structure and function by the Drosophila tumor suppressor gene dlg. Neuron 1996, 17:627-640.
7. Collins C.A., DiAntonio A. Synaptic development: insights from Drosophila. Curr. Opin. Neurobiol. 2007, 17:35-42.
8. Daniels R.W., Collins C.A., Chen K., Gelfand M.V., Featherstone D.E., DiAntonio A. A single vesicular glutamate transporter is sufficient to fill a synaptic vesicle. Neuron 2006, 49:11-16.
9. Davis G.W. Homeostatic signaling and the stabilization of neural function. Neuron 2013, 80:718-728.
10. Davis G.W., Goodman C.S. Synapse-specific control of synaptic efficacy at the terminals of a single neuron. Nature 1998, 392:82-86.
11. Dickman D.K., Lu Z., Meinertzhagen I.A., Schwarz T.L. Altered synaptic development and active zone spacing in endocytosis mutants. Curr. Biol. 2006, 16:591-598.
12. Egebjerg J., Bettler B., Hermans-Borgmeyer I., Heinemann S. Cloning of a cDNA for a glutamate receptor subunit activated by kainate but not AMPA. Nature 1991, 351:745-748.
13. Fatt P., Katz B. Spontaneous subthreshold activity at motor nerve endings. J.Physiol. 1952, 117:109-128.
14. Frank C.A., Kennedy M.J., Goold C.P., Marek K.W., Davis G.W. Mechanisms underlying the rapid induction and sustained expression of synaptic homeostasis. Neuron 2006, 52:663-677.
15. Haghighi A.P., McCabe B.D., Fetter R.D., Palmer J.E., Hom S., Goodman C.S. Retrograde control of synaptic transmission by postsynaptic CaMKII at the Drosophila neuromuscular junction. Neuron 2003, 39:255-267.
16. Hoang B., Chiba A. Single-cell analysis of Drosophila larval neuromuscular synapses. Dev. Biol. 2001, 229:55-70.
17. Huntwork S., Littleton J.T. A complexin fusion clamp regulates spontaneous neurotransmitter release and synaptic growth. Nat. Neurosci. 2007, 10:1235-1237.
18. Iyer J., Wahlmark C.J., Kuser-Ahnert G.A., Kawasaki F. Molecular mechanisms of COMPLEXIN fusion clamp function in synaptic exocytosis revealed in a new Drosophila mutant. Mol. Cell. Neurosci. 2013, 56:244-254.
19. Jiao W., Shupliakov A., Shupliakov O. A semi-correlative technique for the subcellular localization of proteins in Drosophila synapses. J.Neurosci. Methods 2010, 185:273-279.
20. Jin I., Puthanveettil S., Udo H., Karl K., Kandel E.R., Hawkins R.D. Spontaneous transmitter release is critical for the induction of long-term and intermediate-term facilitation in Aplysia. Proc. Natl. Acad. Sci. USA 2012, 109:9131-9136.
21. Kauwe G., Isacoff E.Y. Rapid feedback regulation of synaptic efficacy during high-frequency activity at the Drosophila larval neuromuscular junction. Proc. Natl. Acad. Sci. USA 2013, 110:9142-9147.
22. Kavalali E.T., Monteggia L.M. Synaptic mechanisms underlying rapid antidepressant action of ketamine. Am. J. Psychiatry 2012, 169:1150-1156.
23. Kittel R.J., Wichmann C., Rasse T.M., Fouquet W., Schmidt M., Schmid A., Wagh D.A., Pawlu C., Kellner R.R., Willig K.I., et al. Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release. Science 2006, 312:1051-1054.
24. Koch I., Schwarz H., Beuchle D., Goellner B., Langegger M., Aberle H. Drosophila ankyrin 2 is required for synaptic stability. Neuron 2008, 58:210-222.
25. Kummer T.T., Misgeld T., Sanes J.R. Assembly of the postsynaptic membrane at the neuromuscular junction: paradigm lost. Curr. Opin. Neurobiol. 2006, 16:74-82.
26. Kurdyak P., Atwood H.L., Stewart B.A., Wu C.F. Differential physiology and morphology of motor axons to ventral longitudinal muscles in larval Drosophila. J.Comp. Neurol. 1994, 350:463-472.
27. Mahr A., Aberle H. The expression pattern of the Drosophila vesicular glutamate transporter: a marker protein for motoneurons and glutamatergic centers in the brain. Gene Expr. Patterns 2006, 6:299-309.
28. McCabe B.D., Marqués G., Haghighi A.P., Fetter R.D., Crotty M.L., Haerry T.E., Goodman C.S., O'Connor M.B. The BMP homolog Gbb provides a retrograde signal that regulates synaptic growth at the Drosophila neuromuscular junction. Neuron 2003, 39:241-254.
29. Melom J.E., Akbergenova Y., Gavornik J.P., Littleton J.T. Spontaneous and evoked release are independently regulated at individual active zones. J.Neurosci. 2013, 33:17253-17263.
30. Miller M.B., Yan Y., Eipper B.A., Mains R.E. Neuronal Rho GEFs in synaptic physiology and behavior. Neuroscientist 2013, 19:255-273.
31. Otsu Y., Murphy T.H. Miniature transmitter release: accident of nature or careful design?. Sci. STKE 2003, 2003:pe54.
32. Peled E.S., Newman Z.L., Isacoff E.Y. Evoked and spontaneous transmission favored by distinct sets of synapses. Curr. Biol. 2014, 24:484-493.
33. Petersen S.A., Fetter R.D., Noordermeer J.N., Goodman C.S., DiAntonio A. Genetic analysis of glutamate receptors in Drosophila reveals a retrograde signal regulating presynaptic transmitter release. Neuron 1997, 19:1237-1248.
34. Ramirez D.M.O., Kavalali E.T. Differential regulation of spontaneous and evoked neurotransmitter release at central synapses. Curr. Opin. Neurobiol. 2011, 21:275-282.
35. Schmid A., Qin G., Wichmann C., Kittel R.J., Mertel S., Fouquet W., Schmidt M., Heckmann M., Sigrist S.J. Non-NMDA-type glutamate receptors are essential for maturation but not for initial assembly of synapses at Drosophila neuromuscular junctions. J.Neurosci. 2006, 26:11267-11277.
36. Schuster C.M., Davis G.W., Fetter R.D., Goodman C.S. Genetic dissection of structural and functional components of synaptic plasticity. I. Fasciclin II controls synaptic stabilization and growth. Neuron 1996, 17:641-654.
37. Stuart G., Sakmann B. Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons. Neuron 1995, 15:1065-1076.
38. Sutton M.A., Schuman E.M. Partitioning the synaptic landscape: distinct microdomains for spontaneous and spike-triggered neurotransmission. Sci. Signal. 2009, 2:pe19.
39. Sutton M.A., Ito H.T., Cressy P., Kempf C., Woo J.C., Schuman E.M. Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis. Cell 2006, 125:785-799.
40. Sweeney S.T., Broadie K., Keane J., Niemann H., O'Kane C.J. Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 1995, 14:341-351.
41. Tadross M.R., Dick I.E., Yue D.T. Mechanism of local and global Ca2+ sensing by calmodulin in complex with a Ca2+ channel. Cell 2008, 133:1228-1240.
42. Turrigiano G. Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. Cold Spring Harb. Perspect. Biol. 2012, 4:a005736.
43. Ueda A., Kidokoro Y. Longitudinal body wall muscles are electrically coupled across the segmental boundary in the third instar larva of Drosophila melanogaster. Invert. Neurosci. 1996, 1:315-322.
44. Verhage M., Maia A.S., Plomp J.J., Brussaard A.B., Heeroma J.H., Vermeer H., Toonen R.F., Hammer R.E., van den Berg T.K., Missler M., et al. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 2000, 287:864-869.
45. Walter A.M., Groffen A.J., Sørensen J.B., Verhage M. Multiple Ca2+ sensors in secretion: teammates, competitors or autocrats?. Trends Neurosci. 2011, 34:487-497.
46. Witzemann V., Chevessier F., Pacifici P.G., Yampolsky P. The neuromuscular junction: selective remodeling of synaptic regulators at the nerve/muscle interface. Mech. Dev. 2013, 130:402-411.
47. Wu Y., Cao G., Pavlicek B., Luo X., Nitabach M.N. Phase coupling of a circadian neuropeptide with rest/activity rhythms detected using a membrane-tethered spider toxin. PLoS Biol. 2008, 6:e273.
48. Yeh E., Gustafson K., Boulianne G.L. Green fluorescent protein as a vital marker and reporter of gene expression in Drosophila. Proc. Natl. Acad. Sci. USA 1995, 92:7036-7040.
49. Zito K., Parnas D., Fetter R.D., Isacoff E.Y., Goodman C.S. Watching a synapse grow: noninvasive confocal imaging of synaptic growth in Drosophila. Neuron 1999, 22:719-729.
50. Zucker R.S. Minis: whence and wherefore?. Neuron 2005, 45:482-484.