Molecular Mechanisms for Drosophila Neuronetwork Formation

NeuroSignals

Volumn 13, Issue 1-2, 2004, Pages 37-49

  Furrer, Marie Pierre ^a,b   Chiba, Akira ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b B107 Chem and Life Sci Laboratory   (United States)

Author keywords

Axon; Branching; Dendrites; Drosophila; Guidance; Targeting

Indexed keywords

DENDRITE; DROSOPHILA; FUNCTIONAL ANATOMY; MOLECULAR DYNAMICS; MORPHOLOGICAL TRAIT; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NERVE GROWTH; NEUROANATOMY; NEUROMUSCULAR SYSTEM; NEUROPHYSIOLOGY; NONHUMAN; PHOTORECEPTOR; REVIEW;

ANIMALS; AXONS; DENDRITES; DROSOPHILA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; NERVE NET; NERVOUS SYSTEM PHYSIOLOGY; NEUROMUSCULAR JUNCTION; NEURONS; PHOTORECEPTORS, INVERTEBRATE;

EID: 1542316849     PISSN: 1424862X     EISSN: None     Source Type: Journal    
DOI: 10.1159/000076157     Document Type: Review

References (105)

1. Tessier-Lavigne M, Goodman CS: The molecular biology of axon guidance. Science 1996;274:1123-1133.
2. Schmid A, Chiba A, Doe CQ: Clonal analysis of Drosophila embryonic neuroblasts: Neural cell types, axon projections and muscle targets. Development 1999;126:4653-4689.
3. Landgraf M, Bossing T, Technau GM, Bate M: The origin, location, and projections of the embryonic abdominal motorneurons of Drosophila. J Neurosci 1997;17:9642-9655.
4. Seeger M, Tear G, Ferres-Marco D, Goodman CS: Mutations affecting growth cone guidance in Drosophila: Genes necessary for guidance toward or away from the midline. Neuron 1993;10:409-426.
5. Jacobs JR: The midline glia of Drosophila: A molecular genetic model for the developmental functions of glia. Prog Neurobiol 2000;62:475-508.
6. Harris R, Sabatelli LM, Seeger MA: Guidance cues at the Drosophila CNS midline: Identification and characterization of two Drosophila Netrin/UNC-6 homologs. Neuron 1996;17:217-228.
7. Kolodziej PA, Timpe LC, Mitchell KJ, Fried SR, Goodman CS, Jan LY, Jan YN: Frazzled encodes a Drosophila member of the DCC immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell 1996;87:197-204.
8. Mitchell KJ, Doyle JL, Serafini T, Kennedy TE, Tessier-Lavigne M, Goodman CS, Dickson BJ: Genetic analysis of Netrin genes in Drosophila: Netrins guide CNS commissural axons and peripheral motor axons. Neuron 1996;17:203-215.
9. Keleman K, Dickson BJ: Short- and long-range repulsion by the Drosophila Unc5 netrin receptor. Neuron 2001;32:605-617.
10. Battye R, Stevens A, Jacobs JR: Axon repulsion from the midline of the Drosophila CNS requires slit function. Development 1999;126:2475-2481.
11. Kidd T, Bland KS, Goodman CS: Slit is the midline repellent for the robo receptor in Drosophila. Cell 1999;96:785-794.
12. Simpson JH, Kidd T, Bland KS, Goodman CS: Short-range and long-range guidance by slit and its Robo receptors. Robo and Robo2 play distinct roles in midline guidance. Neuron 2000;28:753-766.
13. Rajagopalan S, Vivancos V, Nicolas E, Dickson BJ: Selecting a longitudinal pathway: Robo receptors specify the lateral position of axons in the Drosophila CNS. Cell 2000;103:1033-1045.
14. Rhee J, Mahfooz NS, Arregui C, Lilien J, Balsamo J, VanBerkum MF: Activation of the repulsive receptor Roundabout inhibits N-cadherin-mediated cell adhesion. Nat Cell Biol 2002;4:798-805.
15. Kidd T, Brose K, Mitchell KJ, Fetter RD, Tessier-Lavigne M, Goodman CS, Tear G: Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell 1998;92:205-215.
16. Keleman K, Rajagopalan S, Cleppien D, Teis D, Paiha K, Huber LA, Technau GM, Dickson BJ: Comm sorts robo to control axon guidance at the Drosophila midline. Cell 2002;110:415-427.
17. Myat A, Henry P, McCabe V, Flintoft L, Rotin D, Tear G: Drosophila Nedd4, a ubiquitin ligase, is recruited by Commissureless to control cell surface levels of the roundabout receptor. Neuron 2002;35:447-459.
18. Georgiou M, Tear G: Commissureless is required both in commissural neurones and midline cells for axon guidance across the midline. Development 2002;129:2947-2956.
19. Brand AH, Perrimon N: Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993;118:401-415.
20. Cash S, Chiba A, Keshishian H: Alternate neuromuscular target selection following the loss of single muscle fibers in Drosophila. J Neurosci 1992;12:2051-2064.
21. Bossing T, Technau GM: The fate of the CNS midline progenitors in Drosophila as revealed by a new method for single cell labelling. Development 1994;120:1895-1906.
22. Wolf BD, Chiba A: Axon pathfinding proceeds normally despite disrupted growth cone decisions at CNS midline. Development 2000;127:2001-2009.
23. Furrer MP, Kim S, Wolf B, Chiba A: Robo and Frazzled/DCC mediate dendritic guidance at the CNS midline. Nat Neurosci 2003;6:223-230.
24. Stein E, Tessier-Lavigne M: Hierarchical organization of guidance receptors: Silencing of netrin attraction by slit through a Robo/DCC receptor complex. Science 2001;291:1928-1938.
25. Lin DM, Fetter RD, Kopczynski C, Grenningloh G, Goodman CS: Genetic analysis of Fasciclin II in Drosophila: Defasciculation, refasciculation, and altered fasciculation. Neuron 1994;13:1055-1069.
26. Prokop A, Uhler J, Roote J, Bate M: The kakapo mutation affects terminal arborization and central dendritic sprouting of Drosophila motorneurons. J Cell Biol 1998;143:1283-1294.
27. Zlatic M, Landgraf M, Bate M: Genetic specification of axonal arbors: Atonal regulates robo3 to position terminal branches in the Drosophila nervous system. Neuron 2003;37:41-51.
28. Simpson JH, Bland KS, Fetter RD, Goodman CS: Short-range and long-range guidance by Slit and its Robo receptors: A combinatorial code of Robo receptors controls lateral position. Cell 2000;103:1019-1032.
29. Rajagopalan S, Nicolas E, Vivancos V, Berger J, Dickson BJ: Crossing the midline: Roles and regulation of Robo receptors. Neuron 2000;28:767-777.
30. Merritt DJ, Whitington PM: Central projections of sensory neurons in the Drosophila embryo correlate with sensory modality, soma position, and proneural gene function. J Neurosci 1995;15:1755-1767.
31. Whitford KL, Marillat V, Stein E, Goodman CS, Tessier-Lavigne M, Chedotal A, Ghosh A: Regulation of cortical dendrite development by Slit-Robo interactions. Neuron 2002;33:47-61.
32. Hausser M, Spruston N, Stuart GJ: Diversity and dynamics of dendritic signaling. Science 2000;290:739-744.
33. Koch C, Segev I: The role of single neurons in information processing. Nat Neurosci 2000;3(suppl):1171-1177.
34. Golic KG, Lindquist S: The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 1989;59:499-509.
35. Lee T, Luo L: Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 1999;22:451-461.
36. Bastmeyer M, O'Leary DD: Dynamics of target recognition by interstitial axon branching along developing cortical axons. J Neurosci 1996;16:1450-1459.
37. Matheson SF, Levine RB: Steroid hormone enhancement of neurite outgrowth in identified insect motor neurons involves specific effects on growth cone form and function. J Neurobiol 1999;38:27-45.
38. Yang MY, Armstrong JD, Vilinsky I, Strausfeld NJ, Kaiser K: Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron 1995;15:45-54.
39. Ito K, Suzuki K, Estes P, Ramaswami M, Yamamoto D, Strausfeld NJ: The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn Mem 1998;5:52-77.
40. Strausfeld NJ, Hansen L, Li Y, Gomez RS, Ito K: Evolution, discovery, and interpretations of arthropod mushroom bodies. Learn Mem 1998;5:11-37.
41. Davis RL: Physiology and biochemistry of Drosophila learning mutants. Physiol Rev 1996;76:299-317.
42. Heisenberg M: What do the mushroom bodies do for the insect brain? An introduction. Learn Mem 1998;5:1-10.
43. Ito K, Awano W, Suzuki K, Hiromi Y, Yamamoto D: The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. Development 1997;124:761-771.
44. Lee T, Lee A, Luo L: Development of the Drosophila mushroom bodies: Sequential generation of three distinct types of neurons from a neuroblast. Development 1999;126:4065-4076.
45. Crittenden JR, Skoulakis EM, Han KA, Kalderon D, Davis RL: Tripartite mushroom body architecture revealed by antigenic markers. Learn Mem 1998;5:38-51.
46. Noveen A, Daniel A, Hartenstein V: Early development of the Drosophila mushroom body: The roles of eyeless and dachshund. Development 2000;127:3475-3488.
47. Truman JW, Bate M: Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev Biol 1988;125:145-157.
48. Ito K, Hotta Y: Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster. Dev Biol 1992;149:134-148.
49. Kurusu M, Awasaki T, Masuda-Nakagawa LM, Kawauchi H, Ito K, Furukubo-Tokunaga K: Embryonic and larval development of the Drosophila mushroom bodies: Concentric layer subdivisions and the role of fasciclin II. Development 2002;129:409-419.
50. Watts RJ, Hoopfer ED, Luo L: Axon pruning during Drosophila metamorphosis: Evidence for local degeneration and requirement of the ubiquitin-proteasome system. Neuron 2003;38:871-885.
51. Wang J, Zugates CT, Liang IH, Lee CH, Lee T: Drosophila Dscam is required for divergent segregation of sister branches and suppresses ectopic bifurcation of axons. Neuron 2002;33:559-571.
52. Schmucker D, Clemens JC, Shu H, Worby CA, Xiao J, Muda M, Dixon JE, Zipursky SL: Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 2000;101:671-684.
53. Hummel T, Vasconcelos ML, Clemens JC, Fishilevich Y, Vosshall LB, Zipursky SL: Axonal targeting of olfactory receptor neurons in Drosophila is controlled by Dscam. Neuron 2003;37:221-231.
54. Ng J, Nardine T, Harms M, Tzu J, Goldstein A, Sun Y, Dietzl G, Dickson BJ, Luo L: Rac GTPases control axon growth, guidance and branching. Nature 2002;416:442-447.
55. Truman JW: Metamorphosis of the central nervous system of Drosophila. J Neurobiol 1990;21:1072-1084.
56. Tissot M, Stocker RF: Metamorphosis in Drosophila and other insects: The fate of neurons throughout the stages. Prog Neurobiol 2000;62:89-111.
57. Bender M, Imam FB, Talbot WS, Ganetzky B, Hogness DS: Drosophila ecdysone receptor mutations reveal functional differences among receptor isoforms. Cell 1997;91:777-788.
58. Truman JW, Talbot WS, Fahrbach SE, Hogness DS: Ecdysone receptor expression in the CNS correlates with stage-specific responses to ecdysteroids during Drosophila and Manduca development. Development 1994;120:219-234.
59. Lee T, Marticke S, Sung C, Robinow S, Luo L: Cell-autonomous requirement of the USP/EcR-B ecdysone receptor for mushroom body neuronal remodeling in Drosophila. Neuron 2000;28:807-818.
60. Brummel T, Abdollah S, Haerry TE, Shimell MJ, Merriam J, Raftery L, Wrana JL, O'Connor MB: The Drosophila activin receptor baboon signals through dSmad2 and controls cell proliferation but not patterning during larval development. Genes Dev 1999;13:98-111.
61. Newfeld SJ, Wisotzkey RG, Kumar S: Molecular evolution of a developmental pathway: Phylogenetic analyses of transforming growth factor-beta family ligands, receptors and Smad signal transducers. Genetics 1999;152:783-795.
62. Chen Y, Riese MJ, Killinger MA, Hoffmann FM: A genetic screen for modifiers of Drosophila decapentaplegic signaling identifies mutations in punt, Mothers against dpp and the BMP-7 homologue, 60A. Development 1998;125:1759-1768.
63. Aberle H, Haghighi AP, Fetter RD, McCabe BD, Magalhaes TR, Goodman CS: Wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 2002;33:545-558.
64. Marques G, Bao H, Haerry TE, Shimell MJ, Duchek P, Zhang B, O'Connor MB: The Drosophila BMP type II receptor Wishful Thinking regulates neuromuscular synapse morphology and function. Neuron 2002;33:529-543.
65. Zheng X, Wang J, Haerry TE, Wu AY, Martin J, O'Connor MB, Lee CH, Lee T: TGF-beta signaling activates steroid hormone receptor expression during neuronal remodeling in the Drosophila brain. Cell 2003;112:303-315.
66. Das P, Inoue H, Baker JC, Beppu H, Kawabata M, Harland RM, Miyazono K, Padgett RW: Drosophila dSmad2 and Atr-I transmit activin/TGFbeta signals. Genes Cells 1999;4:123-134.
67. Jan YN, Jan LY: HLH proteins, fly neurogenesis, and vertebrate myogenesis. Cell 1993;75:827-830.
68. Bodmer R, Jan YN: Morphological differentiation of the embryonic peripheral neurons in Drosophila. Rouxs Arch Dev Biol 1987;196:69-77.
69. Bodmer R, Carretto R, Jan YN: Neurogenesis of the peripheral nervous system in Drosophila embryos: DNA replication patterns and cell lineages. Neuron 1989;3:21-32.
70. Brewster R, Bodmer R: Origin and specification of type II sensory neurons in Drosophila. Development 1995;121:2923-2936.
71. Bodmer R, Barbel S, Sheperd S, Jack JW, Jan LY, Jan YN: Transformation of sensory organs by mutations of the cut locus of D. melanogaster. Cell 1987;51:293-307.
72. Gao FB, Brenman JE, Jan LY, Jan YN: Genes regulating dendritic outgrowth, branching, and routing in Drosophila. Genes Dev 1999;13:2549-2561.
73. Grueber WB, Jan LY, Jan YN: Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development 2002;129:2867-2878.
74. Blochlinger K, Bodmer R, Jan LY, Jan YN: Patterns of expression of cut, a protein required for external sensory organ development in wild-type and cut mutant Drosophila embryos. Genes Dev 1990;4:1322-1331.
75. Grueber WB, Jan LY, Jan YN: Different levels of the homeodomain protein cut regulate distinct dendrite branching patterns of Drosophila multidendritic neurons. Cell 2003;112:805-818.
76. Blochlinger K, Jan LY, Jan YN: Postembryonic patterns of expression of cut, a locus regulating sensory organ identity in Drosophila. Development 1993;117:441-450.
77. Moore AW, Jan LY, Jan YN: hamlet, a binary genetic switch between single- and multiple-dendrite neuron morphology. Science 2002;297:1355-1358.
78. Brenman JE, Gao FB, Jan LY, Jan YN: Sequoia, a tramtrack-related zinc finger protein, functions as a pan-neural regulator for dendrite and axon morphogenesis in Drosophila. Dev Cell 2001;1:667-677.
79. Usui T, Shima Y, Shimada Y, Hirano S, Burgess RW, Schwarz TL, Takeichi M, Uemura T: Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 1999;98:585-595.
80. Gao FB, Kohwi M, Brenman JE, Jan LY, Jan YN: Control of dendritic field formation in Drosophila: The roles of flamingo and competition between homologous neurons. Neuron 2000;28:91-101.
81. Sweeney NT, Li W, Gao FB: Genetic manipulation of single neurons in vivo reveals specific roles of flamingo in neuronal morphogenesis. Dev Biol 2002;247:76-88.
82. Reuter JE, Nardine TM, Penton A, Billuart P, Scott EK, Usui T, Uemura T, Luo L: A mosaic genetic screen for genes necessary for Drosophila mushroom body neuronal morphogenesis. Development 2003;130:1203-1213.
83. Li W, Gao FB: Actin filament-stabilizing protein tropomyosin regulates the size of dendritic fields. J Neurosci 2003;23:6171-6175.
84. Cooper JA: Actin dynamics: Tropomyosin provides stability. Curr Biol 2002;12:R523-R525.
85. Clandinin TR, Zipursky SL: Afferent growth cone interactions control synaptic specificity in the Drosophila visual system. Neuron 2000;28:427-436.
86. Huang Z, Kunes S: Hedgehog, transmitted along retinal axons, triggers neurogenesis in the developing visual centers of the Drosophila brain. Cell 1996;86:411-422.
87. Newsome TP, Asling B, Dickson BJ: Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 2000;127:851-860.
88. Stowers RS, Schwarz TL: A genetic method for generating Drosophila eyes composed exclusively of mitotic clones of a single genotype. Genetics 1999;152:1631-1639.
89. Senti K, Keleman K, Eisenhaber F, Dickson BJ: Brakeless is required for lamina targeting of R1-R6 axons in the Drosophila visual system. Development 2000;127:2291-2301.
90. Rao Y, Pang P, Ruan W, Gunning D, Zipursky SL: Brakeless is required for photoreceptor growth-cone targeting in Drosophila. Proc Natl Acad Sci USA 2000;97:5966-5971.
91. Kaminker JS, Canon J, Salecker I, Banerjee U: Control of photoreceptor axon target choice by transcriptional repression of Runt. Nat Neurosci 2002;5:746-750.
92. Garrity PA, Lee CH, Salecker I, Robertson HC, Desai CJ, Zinn K, Zipursky SL: Retinal axon target selection in Drosophila is regulated by a receptor protein tyrosine phosphatase. Neuron 1999;22:707-717.
93. Desai CJ, Gindhart JG Jr, Goldstein LS, Zinn K: Receptor tyrosine phosphatases are required for motor axon guidance in the Drosophila embryo. Cell 1996;84:599-609.
94. Desai CJ, Krueger NX, Saito H, Zinn K: Competition and cooperation among receptor tyrosine phosphatases control motoneuron growth cone guidance in Drosophila. Development 1997;124:1941-1952.
95. Maurel-Zaffran C, Suzuki T, Gahmon G, Treisman JE, Dickson BJ: Cell-autonomous and -nonautonomous functions of LAR in R7 photoreceptor axon targeting. Neuron 2001;32:225-235.
96. Clandinin TR, Lee CH, Herman T, Lee RC, Yang AY, Ovasapyan S, Zipursky SL: Drosophila LAR regulates R1-R6 and R7 target specificity in the visual system. Neuron 2001;32:237-248.
97. Lee CH, Herman T, Clandinin TR, Lee R, Zipursky SL: N-Cadherin regulates target specificity in the Drosophila visual system. Neuron 2001;30:437-450.
98. Lee RC, Clandinin TR, Lee CH, Chen PL, Meinertzhagen IA, Zipursky SL: The protocadherin Flamingo is required for axon target selection in the Drosophila visual system. Nat Neurosci 2003;6:557-563.
99. Senti KA, Usui T, Boucke K, Greber U, Uemura T, Dickson BJ: Flamingo regulates r8 axonaxon and axon-target interactions in the Drosophila visual system. Curr Biol 2003;13:828-832.
100. Keshishian H, Chiba A: Neuromuscular development in Drosophila: Insights from single neurons and single genes. Trends Neurosci 1993;16:278-283.
101. Nose A, Van Vactor D, Auld V, Goodman CS: Development of neuromuscular specificity in Drosophila. Cold Spring Harb Symp Quant Biol 1992;57:441-449.
102. Chiba A: Early development of the Drosophila neuromuscular junction: A model for studying neuronal networks in development. Int Rev Neurobiol 1999;43:1-24.
103. Gramates LS, Budnik V: Assembly and maturation of the Drosophila larval neuromuscular junction. Int Rev Neurobiol 1999;43:93-117.
104. Lennon J, McCartney P: All you need is love. Parlophone 1967;R5620.
105. Mendel G: Versuche über Pflanzen-Hybriden. Verhandlungen des naturforschenden Vereins, 1865.