The Library

Mutations in shaking-B prevent electrical synapse formation in the Drosophila giant fiber system

Tools

Phelan, Pauline, Nakagawa, Madoka, Wilkin, Marian B., Moffat, Kevin G., O'Kane, Cahir J. and Bacon, J. P. (Jonathan P.). (1996) Mutations in shaking-B prevent electrical synapse formation in the Drosophila giant fiber system. Journal of Neuroscience, Vol.16 (No.3). pp. 1101-1113. ISSN 0270-6474

[img] PDF
WRAP_Moffatt_mutations_in_Shaking-B.pdf - Requires a PDF viewer such as GSview, Xpdf or Adobe Acrobat Reader
Download (10Mb)

Abstract

The giant fiber system (GFS) is a simple network of neurons that mediates visually elicited escape behavior in Drosophila. The giant fiber (GF), the major component of the system, is a large, descending interneuron that relays visual stimuli to the motoneurons that innervate the tergotrochanteral jump muscle (TTM) and dorsal longitudinal flight muscles (DLMs). Mutations in the neural transcript from the shaking-B locus abolish the behavioral response by disrupting transmission at some electrical synapses in the GFS. This study focuses on the role of the gene in the development of the synaptic connections. Using an enhancer-trap line that expresses lacZ in the GFs, we show that the neurons develop during the first 30 hr of metamorphosis. Within the next 15 hr, they begin to form electrical synapses, as indicated by the transfer of intracellularly injected Lucifer yellow. The GFs dye-couple to the TTM motoneuron between 30 and 45 hr of metamorphosis, to the peripherally synapsing interneuron that drives the DLM motoneurons at approximately 48 hr, and to giant commissural interneurons in the brain at approximately 55 hr. Immunocytochemistry with shaking-B peptide antisera demonstrates that the expression of shaking-B protein in the region of GFS synapses coincides temporally with the onset of synaptogenesis; expression persists thereafter. The mutation shak-B2, which eliminates protein expression, prevents the establishment of dye coupling shaking-B, therefore, is essential for the assembly and/or maintenance of functional gap junctions at electrical synapses in the GFS.

Item Type: Journal Article
Subjects: Q Science > QL Zoology
R Medicine > RC Internal medicine > RC0321 Neuroscience. Biological psychiatry. Neuropsychiatry
Divisions: Faculty of Science > Life Sciences (2010- ) > Biological Sciences ( -2010)
Library of Congress Subject Headings (LCSH): Drosophila -- Physiology, Synapses, Gap junctions (Cell biology), Neurons -- Physiology, Startle reaction
Journal or Publication Title: Journal of Neuroscience
Publisher: Society for Neuroscience
ISSN: 0270-6474
Official Date: 1 February 1996
Volume: Vol.16
Number: No.3
Page Range: pp. 1101-1113
Status: Peer Reviewed
Access rights to Published version: Open Access
Funder: Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC), Wellcome Trust (London, England)
Grant number: 034310:2:91/Z (Wellcome)
References:

Bacon JP, Strausfeld NJ (1986) The Dipteran “giant fibre” pathway:
neurons and signals. J Comp Physiol (Aj 15X:529-548. - -
Bainbridge SP, Bownes M (1981) Staeine the metamoruhosis of Drosophil~
meiuno~u.s~er. J Em’bryol’ Exp M&phol 6657-80:
Baird DH, Koto M, Wyman RJ (1993) Dendritic reduction in Pussover, a
Drosophilu mutant with a defective giant fibrc neuronal pathway. J Neurobiol
24:971-0X4.
Baird DH, Schalet AP, Wyman RJ (1990) The Pussover locus in Drosophilu
melumgasier: complex complcmentation and different effects on the
giant fibre neural pathway. Genetics 126:1045-1059.
Balakrishnan R, Rodrigues V (1991) The shuker and shaking-B genes
specify elements in the processing of gustatory information in Drosoplli&
r melutrogrrsfer. J Exp Biol 157: Ihl-181.
Baptista CA, Macagno ER (198X) Modulation of the pattern of axonal
projections of a leech motor neuron by ablation or transplantation of its
target. Neuron 1:94Y-962.
Brand AH, Perrimon N (lYY3) Targeted gene expression as a means of
altering cell fates and generating dominant phenotypes. Development
118:401-415.
Broadie KS, Bate M (lYY3) Devclopmcnt of the embryonic neuromuscular
synapse of Drosophila meluno~uster. J Neurosci 13: 144-166.
Crompton DE, Grithn A, Davies JA, Miklos GLG (1992) Analysis of a
cDNA from the neurologically active locus shukin~-B (Pussover) of
Drosophilu melurro~us~er. Gene 122~385-386.
Crompton DE, Todman MT, Wilkin MB, Ji S, Davies JA (1995) Essential
and neural transcripts from the Drosophilu shaking-B locus are
differentially exprcsscd in the embryonic mesoderm and pupal nervous
system. Dev Biol 170:142-158.
Fischer JA, Giniger E, Maniatis T, Ptashne M (1988) GAL4 activates
transcription in Drusophiiu. Nature 332:853-856.
Goodman CS, Shatz CJ (1993) Developmental mechanisms that generate
precise patterns of neuronal connectivity. Cell 72:77-98.
Halpcrn ME, Chiba A, Johansen J, Keshishian H (1YYl) Growth cone
hehaviour underlying the development of stereotypic synaptic connections
in Drowphiku embryos. J Neurosci 11:3227-3238.
Haydon PC, Drapeau P (1995) From contact to connection: early events
during synaptogcncsis. Trends Neurosci 18:196-201.
Homyk T, Szidonya J, Suzuki DT (1980) Behavioural mutants of Drosophilu
melunquster. III. Isolation and mapping of mutations by direct
visual observation of behavioural phenotypes. Mel Gen Genet
177:553-Sb7.
Ito K, Hotta Y (1992) Proliferation pattern of postembryonic neuroblasts
in the brain of Drosophilu melunoguster. Dev Biol 149:134-148.
King DC, Wyman RJ (1980) Anatomy of the giant fibre pathway in
Drosophilu. I. Three thoracic components of the pathway. J. Neurocytol
9:753-770.
Koto M, Tanouye MA, Ferrus A, Thomas JB, Wyman RJ (1981) The
morphology of the cervical giant fibre neuron of Drosophila. Brain Res
221:213-217.
Krishnan SN, Frei E, Schalet AP, Wyman RJ (1995) Molecular basis of
intracistronic complementation in the Passover locus of Drosophila. Proc
Nat] Acad Sci USA 92:2021-2025.
Krishnan SN, Frei E, Swain GP, Wyman RJ (1993) Pussover: a gene
required for synaptic connectivity in the giant Iibre system of Drosophilu.
Cell 731967-977.
Lipshitz HD, Kankel DR (1985) Specificity of gene action during central
netvous system dcvclopment in Drosophilu melurrogaster: analysis of the
lelhul (I) optic ganglion reduced locus. Dev Biol 108:56-77.
Martin KA, Poeck B, Roth H, Ebens AJ, Conlcy Ballard L, Zipursky SL
(1995) Mutations disrupting neuronal connectivity in the Drosophilu
visual system. Neuron 14:229-240.
Myers CM, Whitington PM, Ball EE (1990) Embryonic dcvclopment of
the innervation of the locust extensor tibiae muscle by identitled neurons:
formation and elimination of inappropriate axon branches. Dev
Biol 137:194-206.
Myers PZ, Bastiani MJ (1993) Cell-cell interactions during the migration
of an identified commissural growth cone in the embryonic grasshopper.
J Neurosci 13:115-126.
Nastuk MA, Fallon JR (1993) Agrin and the molecular choreography of
synapse formation. Trends Neurosci l6:72-76.
Peinado A, Yuste R, Katz LC (1993) Extensive dye coupling between rat
neocorticai neurons during the period of circuit formation. Neuron
10:103-114.
Penn AA, Wong ROL, Shatz CJ (1994) Neuronal coupling in the developing
mammalian retina. J Neurosci 14:3805-3815.
Phillis RW, Bramlage AT, Wotus C, Whittaker A, Grametcs LS, Scppala
D, Farahanchi F, Caruccio P, Murphey RK (1993) Isolation of mutants
affecting neural circuitry required for grooming behaviour in Drosophiku
melunogusfer. Genetics 133:581-592.
Power ME (1948) The thoracico-abdominal nervous system of an adult
insect, Drosophila melunogaster. J Comp Neural 88:347-409.
Raper Hummon M, Costello WJ (1987) Induced disruption in the connectivity
of an identified neuron in the Drosophila ts mutant shihire.
J Neurosci 7:3633-3638.
Schwarzman G, Wiegandt H, Rose B, Zimmerman A. Ben-Haim D,
Loewenstein WR (1981) Diameter of the cell-to-cell junctional membrane
channels as probed with neutral molecules. Science 213:551-553.
Sink H, Whitington PM (19Yla) Pathfinding in the central nervous system
and periphery by identified embryonic Drosophilu motor axons.
Development 112:307-316.
Sink H, Whitington PM (1991b) Early ablation of target muscles modulates
the arborization pattern of an idcntitied embryonic Drosophilu
motor axon. Development 113:701-707.
Starich TA, Herman RK, Shaw JE (1993) Molecular and genetic analysis
of uric-7, a Cuenorhuhditis elegurrs gene required for coordinated locomotion.
Genetics 133:527-541.
Strausfeld NJ, Bassemir UK (1983) Cobalt-coupled neurons of a giant
fibre system in Diptera. J Neurocytol 12:971-991.
Tanouye MA, Wyman RJ (1980) Motor outputs of giant nerve fibrc in
Drosophila. J Neurophysiol 44:405-421.
Tepass U, Hartenstein V (1994) The dcvclopment of cellular junctions in
the Drosophila embryo. Dev Biol 161:563-569.
Thomas JB,. Wyman RJ (1994) Mutations altering synaptic connectivity
between identified neurons in Drosophila. J Ncurosci 14:530-53X.
Truman JW, Bate M (1988) Spatial and temporal patterns of neurogenesis
in the central nervous system of Drosophila me/uno~us/er. Dcv Biol
125:145-157.
Van Vactor D, Sink H, Fambrough D, Tsoo R, Goodman CS (1993)
Genes that control neuromuscular specificity in Drosophilu. Cell
73:1137-l 153.
Watanabe T, Kankcl DR (1990) Molecular cloning and analysis of l(1)
ogre, a locus of Drosophila melunoguster with prominent effects on the
postembryonic development of the central nervous system. Genetics
126:1033-1044.
Watanabe T, Kankel DR (1992) The I(l)o gene of Drosopldu me/unoguster
is expressed in postembryonic neuroblasts. Dev Biol
152:172-183.
White K, Kankel DR (1978) Patterns of cell division and ccl1 movement
in the formation of the imaginal nervous system in Drosophila mekurzogu.
ster. Dev Biol 65:296-321.
URI: http://wrap.warwick.ac.uk/id/eprint/2714

Request changes or add full text files to a record

Actions (login required)

View Item View Item

Document Downloads

More statistics for this item...