Dendritic development: Lessons from Drosophila and related branches

Current Opinion in Neurobiology

Volumn 14, Issue 1, 2004, Pages 74-82

  Grueber, Wesley B ^a   Jan, Yuh Nung ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

AdPN; Anterodorsal projection neuron; Da; Dendritic arborization; Ecdysone receptor; EcR; Es; External sensor; Lateral projection neuron; LPN; MB; Md; Multi dendritic; Mushroom body; Olfactory receptor neuron; ORN; Peripheral nervous system; PN; PNS; Projection neuron

Indexed keywords

CELL GROWTH; CELL SPECIFICITY; CHEMOSENSITIVITY; DENDRITE; DENDRITIC CELL; DROSOPHILA; MOLECULAR INTERACTION; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; REVIEW; SENSORY NERVE CELL; SYNAPTOGENESIS;

EID: 1342264171     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2004.01.001     Document Type: Review

References (67)

1. Levine R.B., Truman J.W. Metamorphosis of the insect nervous system: changes in morphology and synaptic interactions of identified neurons. Nature. 299:1982;250-252.
2. Truman J.W. Developmental neuroethology of insect metamorphosis. J. Neurobiol. 23:1992;1404-1422.
3. Gray J.R., Weeks J.C. Steroid-induced dendritic regression reduces anatomical contacts between neurons during synaptic weakening and the developmental loss of a behavior. J. Neurosci. 23:2003;1406-1415.
4. Landgraf M., Bossing T., Technau G.M., Bate M. The origin, location, and projections of embryonic abdominal motorneurons of Drosophila. J. Neurosci. 17:1997;9642-9655.
5. Gao F.-B., Brenman J.E., Jan L.Y., Jan Y.N. Genes regulating dendritic outgrowth, branching, and routing in Drosophila. Genes Dev. 13:1999;2549-2561.
6. •].
7. •], used highly specific neuronal markers to study the growth and dynamics of different groups of da neurons. Both studies provide experimental evidence that repulsive interactions between dendrites are necessary and sufficient for body wall tiling.
8. Landgraf M., Sanchez-Soriano N., Technau G.M., Urban J., Prokop A. Charting the Drosophila neuropile: a strategy for the standardised characterization of genetically amenable neurites. Dev. Biol. 260:2003;207-225.
9. Lee T., Luo L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron. 22:1999;451-461.
10. Jefferis G.S.X.E., Marin E.C., Stocker R.F., Luo L. Target neuron prespecification in the olfactory map of Drosophila. Nature. 414:2001;204-208.
11. Scott E.K., Raabe T., Luo L. Structure of the vertical and horizontal system neurons of the lobula plate in Drosophila. J. Comp. Neurol. 454:2002;470-481.
12. Grueber W.B., Jan L.Y., Jan Y.N. Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development. 129:2002;2867-2878.
13. Sweeney N.T., Li W., Gao F.-B. Genetic manipulation of single neurons in vivo reveals specific roles of Flamingo in neuronal morphogenesis. Dev. Biol. 247:2002;76-88.
14. Consoulas C., Restifo L.L., Levine R.B. Dendritic remodeling and growth of motoneurons during metamorphosis of Drosophila melanogaster. J. Neurosci. 22:2002;4906-4917.
15. Furrer M.-P., Kim S., Wolf B., Chiba A. Robo and Frazzled/DCC mediate dendritic guidance at the CNS midline. Nat. Neurosci. 6:2003;223-230 The authors show that dendritic and axon guidance at the midline share similar molecular components. The main distinctions between these two processes in central neurons might be the differential distribution of receptors in axons and dendrites.
16. Scott E.K., Luo L. How do dendrites take their shape? Nat. Neurosci. 4:2001;359-365.
17. Jan Y.N., Jan L.Y. Dendrites. Genes Dev. 15:2001;2627-2641.
18. Ghysen A. Dendritic arbors: a tale of living tiles. Curr. Biol. 13:2003;R427-R429.
19. Gao F.-B., Bogert B. Genetic control of dendritic morphogenesis in Drosophila. Trends Neurosci. 26:2003;262-268.
20. Jan Y.N., Jan L.Y. The control of dendrite development. Neuron. 40:2003;229-242.
21. Jefferis G.X.S.E., Marin E.C., Watts R.J., Luo L. Development of neuronal connectivity in Drosophila antennal lobes and mushroom bodies. Curr. Opin. Neurobiol. 12:2002;80-86.
22. Komiyama T., Johnson W.A., Luo L., Jefferis G.S.X.E. From lineage to wiring specificity: POU domain transcription factors control precise connections of Drosophila olfactory projections neurons. Cell. 112:2003;157-167 This study shows that two transcription factors, acj6 and drifter, are expressed in different lineages of olfactory projection neurons, and coordinate dendrite and axon morphogenesis within individual neurons.
23. Wong A.M., Wang J.W., Axel R. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell. 109:2002;229-241.
24. Marin E.C., Jefferis G.S.X.E., Komiyama T., Zhu H., Luo L. Representation of the glomerular olfactory map in the Drosophila brain. Cell. 109:2002;243-255.
25. Prokop A., Uhler J., Roote J., Bate M. The kakapo mutation affects terminal arborization and central dendritic sprouting of Drosophila motorneurons. J. Cell Biol. 143:1998;1283-1294.
26. Seeger M., Tear G., Ferres-Marco D., Goodman C.S. Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward or away from the midline. Neuron. 10:1993;409-426.
27. Hummel T., Schimmelpfeng K., Klambt C. Commissure formation in the embryonic CNS of Drosophila II. Function of the different midline cells. Development. 126:1999;771-779.
28. Moore A.W., Jan L.Y., Jan Y.N. hamlet, a binary genetic switch between single- and multiple-dendrite neuron morphology. Science. 297:2002;1355-1358 This study characterizes the hamlet (ham) gene, a zinc-finger putative transcription factor that controls the fate and morphogenesis of mono-dendritic external sensory organ neurons (in which it is expressed) versus multidendritic neurons (where it is not expressed) that arise from the same lineage.
29. Grueber W.B., Jan L.Y., Jan Y.N. Different levels of the homeodomain protein Cut regulate distinct dendrite branching patterns of Drosophila multidendritic neurons. Cell. 112:2003;805-818 Previously identified as necessary and sufficient for the morphological development of external sensory organs, Cut is shown, here, to be a crucial factor in the development of da neuron class-specific morphology.
30. Blochlinger K., Bodmer R., Jan L.Y., Jan Y.N. Patterns of expression of Cut, a protein required for external sensory organ development in wild-type and cut mutant Drosophila embryos. Genes Dev. 4:1990;1322-1331.
31. Brewster R., Bodmer R. Origin and specification of type II sensory neurons in Drosophila. Development. 121:1995;2923-2936.
32. Brewster R., Hardiman K., Deo M., Khan S., Bodmer R. The selector gene cut represses a neural cell fate that is specified independently of the Achaete-Scute-Complex and atonal. Mech. Dev. 105:2001;57-68.
33. Bodmer R., Jan Y.N. Morphological differentiation of the embryonic peripheral neurons in Drosophila. Rouxs Arch Dev. Biol. 196:1987;69-77.
34. Reuter J.E., Nardine T.M., Penton A., Billuart P., Scott E.K., Usui T., Uemura T., Luo L. A mosaic genetic screen for genes necessary for Drosophila mushroom body neuronal morphogenesis. Development. 130:2003;1203-1213.
35. Li W., Gao F.B. Actin filament stabilizing protein tropomyosin regulates the size of dendritic fields. J. Neurosci. 23:2003;6171-6175.
36. Chae J., Kim M.J., Goo J.H., Collier S., Gubb D., Charlton J., Adler P.N., Park W.J. The Drosophila tissue polarity gene starry night encodes a member of the protocadherin family. Development. 126:1999;5421-5429.
37. Usui T., Shima Y., Shimada Y., Hirano S., Burgess R.W., Schwarz T.L., Takeichi M., Uemura T. Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell. 98:1999;585-595.
38. Brenman J.E., Gao F.-B., Jan L.Y., Jan Y.N. Sequoia, a Tramtrack-related zinc finger protein, functions as a pan-neural regulator for dendrite and axon morphogenesis in Drosophila. Dev. Cell. 1:2001;667-677.
39. Lee T., Winter C., Marticke S.S., Lee A., Luo L. Essential roles of Drosophila RhoA in the regulation of neuroblast proliferation and dendritic but not axonal morphogenesis. Neuron. 25:2000;307-316.
40. Gao F.-B., Kohwi M., Brenman J.E., Jan L.Y., Jan Y.N. Control of dendritic field formation in Drosophila: the roles of flamingo and competition between homologous neurons. Neuron. 28:2000;91-101.
41. Goldberg J.L., Klassen M.P., Hua Y., Barres B.A. Amacrine-signaled loss of intrinsic axon growth ability by retinal ganglion cells. Science. 296:2002;1860-1864.
42. Mizrahi A., Ben-ner E., Katz M.J., Kedem K., Glusman J.G., Libersat F. Comparative analysis of dendritic architecture of identified neurons using the Hausdorff distance metric. J. Comp. Neurol. 422:2000;415-428.
43. Kramer A.P., Stent G.S. Developmental arborization of sensory neurons in the leech Haementeria ghilianii II. Experimentally induced variations in the branching pattern. J. Neurosci. 5:1985;768-775.
44. Gan W.-B., Macagno E. Interactions between segmental homologs and between isoneuronal branches guide the formation of terminal sensory fields. J. Neurosci. 15:1995;3243-3253.
45. Wang H., Macagno E.R. A detached branch stops being recognized as self by other branches of a neuron. J. Neurobiol. 35:1998;53-64.
46. Grueber W.B., Truman J.W. Development and organization of a nitric-oxide-sensitive peripheral neural plexus in larvae of the moth, Manduca sexta. J. Comp. Neurol. 404:1999;127-141.
47. Blackshaw S.E., Nicholls J.G., Parnas I. Expanded receptive fields of cutaneous mechanoreceptor cells after single neurone deletion in leech central nervous system. J. Physiol. 326:1982;261-268.
48. Wassle H., Boycott B.B. Functional architecture of the mammalian retina. Physiol. Rev. 71:1991;447-478.
49. Grueber W.B., Graubard K., Truman J.W. Tiling of the body wall by multidendritic sensory neurons in Manduca sexta. J. Comp. Neurol. 440:2001;271-283.
50. •].
51. •].
52. •] pathways.
53. Perry V.H., Linden R. Evidence for dendritic competition in the developing retina. Nature. 297:1982;683-685.
54. Hitchcock P.F. Exclusionary dendritic interactions in the retina of the goldfish. Development. 106:1989;589-598.
55. Mizrahi A., Libersat F. Synaptic reorganization induced by selective photoablation of an identified neuron. J. Neurosci. 21:2001;9280-9290.
56. Koelle M.R., Talbot W.S., Segraves W.A., Bender M.T., Cherbas P., Hogness D.S. The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell. 67:1991;59-77.
57. Yao T.P., Segraves W.A., Oro A.E., McKeown M., Evans R.M. Drosophila ultraspiracle modulates ecdysone receptor function via heterodimer formation. Cell. 71:1992;63-72.
58. Talbot W.S., Swyryd E.A., Hogness D.S. Drosophila tissues with different metamorphic responses to ecdysone express different ecdysone receptor isoforms. Cell. 73:1993;1323-1337.
59. Truman J.W., Talbot W.S., Fahrbach S.E., Hogness D.S. Ecdysone receptor expression in the CNS correlates with stage-specific responses to ecdysteroids during Drosophila and Manduca development. Development. 120:1994;219-234.
60. Bender M., Imam F.B., Talbot W.S., Ganetzky B.S., Hogness D.S. Drosophila ecdysone receptor mutations reveal functional differences among receptor isoforms. Cell. 91:1997;777-788.
61. Schubiger M., Wade A.A., Carney G.E., Truman J.W., Bender M. Drosophila EcR-B ecdysone receptor isoforms are required for larval molting and for neuron remodeling during metamorphosis. Development. 125:1998;2053-2062.
62. Lee T., Marticke S., Sung C., Robinow S., Luo L. Cell-autonomous requirement for the USP/EcR-B ecdysone receptor for mushroom body neuronal remodeling in Drosophila. Neuron. 28:2000;807-818.
63. Zheng X., Wang J., Haerry T.E., Wu A.Y., Martin J., O'Connor M.B., Lee C.H., Lee T. TGF-β signaling activates steroid hormone receptor expression during neuronal remodeling in the Drosophila brain. Cell. 112:2003;303-315 A mosaic screen for genes affecting MB neuron remodeling identified babo and dSmad2, components of the TGF-β signaling cascade. TGF-β signaling controls the spatial expression of the ecdysone receptor isoform, EcR-B1, a key regulator of ecdysone-induced dendritic pruning.
64. Schubiger M., Tomita S., Sung C., Robinow S., Truman J.W. Isoform specific control of gene activity in vivo by the Drosophila ecdysone receptor. Mech. Dev. 120:2003;909-918.
65. Jefferis GSXE, Vyas RM, Berdnik D, Ramaekers A, Stocker RF, Tanaka NK, Ito K, Luo L: Developmental origin of wiring specificity in the olfactory system of Drosophila. Development 2003 Nov 26 [Epub ahead of print].
66. Landgraf M, Jeffrey V, Fujioka M, Jaynes JB, Bate M: Embryonic origins of a motor system: Motor dendrites form a myotopic map in Drosophila. PLoS Biol 2003, 1:E41. DOI: 10.1371/journal.pbio.0000041.
67. Williams DW, Truman JW: Mechanisms of dendritic elaboration of sensory neurons in Drosophila: Insights from in vivo time lapse. J Neurosci, in press.