New tools for the analysis of glial cell biology in Drosophila

GLIA

Volumn 59, Issue 9, 2011, Pages 1377-1386

  Awasaki, Takeshi ^a,b   Lee, Tzumin ^a,b  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Drosophila; GAL4 UAS; Genetic tools; Glial cell biology; MARCM

Indexed keywords

ARTICLE; CELL FUNCTION; CELL LABELING; CELL MANIPULATION; CELL MATURATION; CELL STRUCTURE; CYTOLOGY; DROSOPHILA; GAL4 UAS SYSTEM; GENE EXPRESSION; GENE FUNCTION; GENETIC ANALYSIS; GENETIC MANIPULATION; GLIA CELL; IN VIVO STUDY; MARCM ANALYSIS; NERVOUS SYSTEM; NONHUMAN; PRIORITY JOURNAL; TRANSGENE;

ANIMALS; CELL BIOLOGY; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION; GENES, REPORTER; MOLECULAR BIOLOGY; MUTATION; NEUROGLIA; TRANSCRIPTION FACTORS; TRANSGENES; UPSTREAM STIMULATORY FACTORS;

EID: 79959927720     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.21133     Document Type: Article

References (100)

1. Altenhein B, Becker A, Busold C, Beckmann B, Hoheisel JD, Technau GM. 2006. Expression profiling of glial genes during Drosophila embryogenesis. Dev Biol 296: 545-560.
2. Awasaki T, Ito K. 2004. Engulfing action of glial cells is required for programmed axon pruning during Drosophila metamorphosis. Curr Biol 14: 668-677.
3. Awasaki T, Lai SL, Ito K, Lee T. 2008. Organization and postembryonic development of glial cells in the adult central brain of Drosophila. J Neurosci 28: 13742-13753.
4. Awasaki T, Tatsumi R, Takahashi K, Arai K, Nakanishi Y, Ueda R, Ito K. 2006. Essential role of the apoptotic cell engulfment genes draper and ced-6 in programmed axon pruning during Drosophila metamorphosis. Neuron 50: 855-867.
5. Bainton RJ, Tsai LT, Schwabe T, DeSalvo M, Gaul U, Heberlein U. 2005. Moody encodes two GPCRs that regulate cocaine behaviors and blood-brain barrier permeability in Drosophila. Cell 123: 145-156.
6. Beckervordersandforth RM, Rickert C, Altenhein B, Technau GM. 2008. Subtypes of glial cells in the Drosophila embryonic ventral nerve cord as related to lineage and gene expression. Mech Dev 125: 542-557.
7. Bellaiche Y, Gho M, Kaltschmidt JA, Brand AH, Schweisguth F. 2001. Frizzled regulates localization of cell-fate determinants and mitotic spindle rotation during asymmetric cell division. Nat Cell Biol 3: 50-57.
8. Bergmann A, Tugentman M, Shilo BZ, Steller H. 2002. Regulation of cell number by MAPK-dependent control of apoptosis: A mechanism for trophic survival signaling. Dev Cell 2: 159-170.
9. Booth GE, Kinrade EF, Hidalgo A. 2000. Glia maintain follower neuron survival during Drosophila CNS development. Development 127: 237-244.
10. Brand AH, Perrimon N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
11. Buchanan RL, Benzer S. 1993. Defective glia in the Drosophila brain degeneration mutant drop-dead. Neuron 10: 839-850.
12. Chen CH, Huang H, Ward CM, Su JT, Schaeffer LV, Guo M, Hay BA. 2007. A synthetic maternal-effect selfish genetic element drives population replacement in Drosophila. Science 316: 597-600.
13. Chen P, Nordstrom W, Gish B, Abrams JM. 1996. Grim, a novel cell death gene in Drosophila. Genes Dev 10: 1773-1782.
14. Chotard C, Leung W, Salecker I. 2005. Glial cells missing and gcm2 cell autonomously regulate both glial and neuronal development in the visual system of Drosophila. Neuron 48: 237-251.
15. Cox RT, Spradling AC. 2003. A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development 130: 1579-1590.
16. Daneman R, Barres BA. 2005. The blood-brain barrier--Lessons from moody flies. Cell 123: 9-12.
17. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, Fellner M, Gasser B, Kinsey K, Oppel S, Scheiblauer S, Couto A, Marra V, Keleman K, Dickson BJ. 2007. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448: 151-156.
18. Doe CQ. 1992. Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila central nervous system. Development 116: 855-863.
19. Doherty J, Logan MA, Tasdemir OE, Freeman MR. 2009. Ensheathing glia function as phagocytes in the adult Drosophila brain. J Neurosci 29: 4768-4781.
20. Egger B, Leemans R, Loop T, Kammermeier L, Fan Y, Radimerski T, Strahm MC, Certa U, Reichert H. 2002. Gliogenesis in Drosophila: Genome-wide analysis of downstream genes of glial cells missing in the embryonic nervous system. Development 129: 3295-3309.
21. Ewer J, Frisch B, Hamblen-Coyle MJ, Rosbash M, Hall JC. 1992. Expression of the period clock gene within different cell types in the brain of Drosophila adults and mosaic analysis of these cells' influence on circadian behavioral rhythms. J Neurosci 12: 3321-3349.
22. Fichelson P, Gho M. 2003. The glial cell undergoes apoptosis in the microchaete lineage of Drosophila. Development 130: 123-133.
23. Fortier E, Belote JM. 2000. Temperature-dependent gene silencing by an expressed inverted repeat in Drosophila. Genesis 26: 240-244.
24. Franzdottir SR, Engelen D, Yuva-Aydemir Y, Schmidt I, Aho A, Klambt C. 2009. Switch in FGF signalling initiates glial differentiation in the Drosophila eye. Nature 460: 758-761.
25. Freeman MR, Delrow J, Kim J, Johnson E, Doe CQ. 2003. Unwrapping glial biology: Gcm target genes regulating glial development, diversification, and function. Neuron 38: 567-580.
26. Golic KG. 1991. Site-specific recombination between homologous chromosomes in Drosophila. Science 252: 958-961.
27. Grether ME, Abrams JM, Agapite J, White K, Steller H. 1995. The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev 9: 1694-1708.
28. Griffiths RL, Hidalgo A. 2004. Prospero maintains the mitotic potential of glial precursors enabling them to respond to neurons. EMBO J 23: 2440-2450.
29. Grosjean Y, Grillet M, Augustin H, Ferveur JF, Featherstone DE. 2008. A glial amino-acid transporter controls synapse strength and courtship in Drosophila. Nat Neurosci 11: 54-61.
30. Halassa MM, Fellin T, Haydon PG. 2007. The tripartite synapse: Roles for gliotransmission in health and disease. Trends Mol Med 13: 54-63.
31. Haley B, Hendrix D, Trang V, Levine M. 2008. A simplified miRNA-based gene silencing method for Drosophila melanogaster. Dev Biol 321: 482-490.
32. Hebbar S, Fernandes JJ. 2010. Glial remodeling during metamorphosis influences the stabilization of motor neuron branches in Drosophila. Dev Biol 340: 344-354.
33. Hidalgo A, Booth GE. 2000. Glia dictate pioneer axon trajectories in the Drosophila embryonic CNS. Development 127: 393-402.
34. Hidalgo A, Kinrade EF, Georgiou M. 2001. The Drosophila neuregulin vein maintains glial survival during axon guidance in the CNS. Dev Cell 1: 679-690.
35. Hidalgo A, Urban J, Brand AH. 1995. Targeted ablation of glia disrupts axon tract formation in the Drosophila CNS. Development 121: 3703-3712.
36. Hosoya T, Takizawa K, Nitta K, Hotta Y. 1995. glial cells missing: A binary switch between neuronal and glial determination in Drosophila. Cell 82: 1025-1036.
37. Ito K, Awano W, Suzuki K, Hiromi Y, Yamamoto D. 1997. 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 124: 761-771.
38. Ito K, Urban J, Technau G. 1995. Distribution, classification, and development of Drosophila glial cells in the late embryonic and early larval ventral nerve cord. Dev Genes Evol 204: 284-307.
39. Jacobs JR, Goodman CS. 1989. Embryonic development of axon pathways in the Drosophila CNS. I. A glial scaffold appears before the first growth cones. J Neurosci 9: 2402-2411.
40. Jacobs JR, Hiromi Y, Patel NH, Goodman CS. 1989. Lineage, migration, and morphogenesis of longitudinal glia in the Drosophila CNS as revealed by a molecular lineage marker. Neuron 2: 1625-1631.
41. Jones BW, Fetter RD, Tear G, Goodman CS. 1995. glial cells missing: A genetic switch that controls glial versus neuronal fate. Cell 82: 1013-1023.
42. Kennerdell JR, Carthew RW. 2000. Heritable gene silencing in Drosophila using double-stranded RNA. Nat Biotechnol 18: 896-898.
43. Kidd T, Bland KS, Goodman CS. 1999. Slit is the midline repellent for the robo receptor in Drosophila. Cell 96: 785-794.
44. Kinrade EF, Brates T, Tear G, Hidalgo A. 2001. Roundabout signalling, cell contact and trophic support confine longitudinal glia and axons in the Drosophila CNS. Development 128: 207-216.
45. Kitamoto T. 2001. Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J Neurobiol 47: 81-92.
46. Kitamoto T. 2002. Conditional disruption of synaptic transmission induces male-male courtship behavior in Drosophila. Proc Natl Acad Sci USA 99: 13232-13237.
47. Klambt C, Goodman CS. 1991. The diversity and pattern of glia during axon pathway formation in the Drosophila embryo. Glia 4: 205-213.
48. Kretzschmar D, Hasan G, Sharma S, Heisenberg M, Benzer S. 1997. The swiss cheese mutant causes glial hyperwrapping and brain degeneration in Drosophila. J Neurosci 17: 7425-7432.
49. Lai SL, Lee T. 2006. Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat Neurosci 9: 703-709.
50. Lam G, Thummel CS. 2000. Inducible expression of double-stranded RNA directs specific genetic interference in Drosophila. Curr Biol 10: 957-963.
51. Learte AR, Forero MG, Hidalgo A. 2008. Gliatrophic and gliatropic roles of PVF/PVR signaling during axon guidance. Glia 56: 164-176.
52. Lee T, Luo L. 1999. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22: 451-461.
53. Lee T, Marticke S, Sung C, Robinow S, Luo L. 2000a. Cell-autonomous requirement of the USP/EcR-B ecdysone receptor for mushroom body neuronal remodeling in Drosophila. Neuron 28: 807-818.
54. Lee T, Winter C, Marticke SS, Lee A, Luo L. 2000b. Essential roles of Drosophila RhoA in the regulation of neuroblast proliferation and dendritic but not axonal morphogenesis. Neuron 25: 307-316.
55. Lin DM, Auld VJ, Goodman CS. 1995. Targeted neuronal cell ablation in the Drosophila embryo: Pathfinding by follower growth cones in the absence of pioneers. Neuron 14: 707-715.
56. Livet J. 2007. [The brain in color: Transgenic "Brainbow" mice for visualizing neuronal circuits]. Med Sci (Paris) 23: 1173-1176.
57. MacDonald JM, Beach MG, Porpiglia E, Sheehan AE, Watts RJ, Freeman MR. 2006. The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron 50: 869-881.
58. Martinek S, Young MW. 2000. Specific genetic interference with behavioral rhythms in Drosophila by expression of inverted repeats. Genetics 156: 1717-1725.
59. Mayer F, Mayer N, Chinn L, Pinsonneault RL, Kroetz D, Bainton RJ. 2009. Evolutionary conservation of vertebrate blood-brain barrier chemoprotective mechanisms in Drosophila. J Neurosci 29: 3538-3550.
60. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL. 2003. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302: 1765-1768.
61. Moffat KG, Gould JH, Smith HK, O'Kane CJ. 1992. Inducible cell ablation in Drosophila by cold-sensitive ricin A chain. Development 114: 681-687.
62. Ni JQ, Liu LP, Binari R, Hardy R, Shim HS, Cavallaro A, Booker M, Pfeiffer BD, Markstein M, Wang H, Villalta C, Laverty TR, Perkins LA, Perrimon N. 2009. A Drosophila resource of transgenic RNAi lines for neurogenetics. Genetics 182: 1089-1100.
63. Nicholson L, Singh GK, Osterwalder T, Roman GW, Davis RL, Keshishian H. 2008. Spatial and temporal control of gene expression in Drosophila using the inducible GeneSwitch GAL4 system. I. Screen for larval nervous system drivers. Genetics 178: 215-234.
64. Osterwalder T, Yoon KS, White BH, Keshishian H. 2001. A conditional tissue-specific transgene expression system using inducible GAL4. Proc Natl Acad Sci USA 98: 12596-12601.
65. Paladi M, Tepass U. 2004. Function of Rho GTPases in embryonic blood cell migration in Drosophila. J Cell Sci 117(Pt 26): 6313-6326.
66. Potter CJ, Tasic B, Russler EV, Liang L, Luo L. 2010. The Q system: A repressible binary system for transgene expression, lineage tracing, and mosaic analysis. Cell 141: 536-548.
67. Read RD, Cavenee WK, Furnari FB, Thomas JB. 2009. A drosophila model for EGFR-Ras and PI3K-dependent human glioma. PLoS Genet 5: e1000374.
68. Ritzenthaler S, Suzuki E, Chiba A. 2000. Postsynaptic filopodia in muscle cells interact with innervating motoneuron axons. Nat Neurosci 3: 1012-1017.
69. Rogulja-Ortmann A, Luer K, Seibert J, Rickert C, Technau GM. 2007. Programmed cell death in the embryonic central nervous system of Drosophila melanogaster. Development 134: 105-116.
70. Rusten TE, Lindmo K, Juhasz G, Sass M, Seglen PO, Brech A, Stenmark H. 2004. Programmed autophagy in the Drosophila fat body is induced by ecdysone through regulation of the PI3K pathway. Dev Cell 7: 179-192.
71. Schmid A, Chiba A, Doe CQ. 1999. Clonal analysis of Drosophila embryonic neuroblasts: Neural cell types, axon projections and muscle targets. Development 126: 4653-4689.
72. Schmidt H, Rickert C, Bossing T, Vef O, Urban J, Technau GM. 1997. The embryonic central nervous system lineages of Drosophila melanogaster. II. Neuroblast lineages derived from the dorsal part of the neuroectoderm. Dev Biol 189: 186-204.
73. Scholz H, Sadlowski E, Klaes A, Klambt C. 1997. Control of midline glia development in the embryonic Drosophila CNS. Mech Dev 62: 79-91.
74. Schwabe T, Bainton RJ, Fetter RD, Heberlein U, Gaul U. 2005. GPCR signaling is required for blood-brain barrier formation in drosophila. Cell 123: 133-144.
75. Sepp KJ, Auld VJ. 1999. Conversion of lacZ enhancer trap lines to GAL4 lines using targeted transposition in Drosophila melanogaster. Genetics 151: 1093-1101.
76. Sepp KJ, Auld VJ. 2003. Reciprocal interactions between neurons and glia are required for Drosophila peripheral nervous system development. J Neurosci 23: 8221-8230.
77. Sepp KJ, Schulte J, Auld VJ. 2001. Peripheral glia direct axon guidance across the CNS/PNS transition zone. Dev Biol 238: 47-63.
78. Shiga Y, Tanaka-Matakatsu M, Hayashi S. 1996. A nuclear GFP/ beta-galactosidase fusion protein as a marker for morphogenesis in living Drosophila. Dev Growth Differ 38: 99-106.
79. Shishido E, Ono N, Kojima T, Saigo K. 1997. Requirements of DFR1/Heartless, a mesoderm-specific Drosophila FGF-receptor, for the formation of heart, visceral and somatic muscles, and ensheathing of longitudinal axon tracts in CNS. Development 124: 2119-2128.
80. Sonnenfeld MJ, Jacobs JR. 1995. Apoptosis of the midline glia during Drosophila embryogenesis: A correlation with axon contact. Development 121: 569-578.
81. Spindler SR, Ortiz I, Fung S, Takashima S, Hartenstein V. 2009. Drosophila cortex and neuropile glia influence secondary axon tract growth, pathfinding, and fasciculation in the developing larval brain. Dev Biol 334: 355-368.
82. Stemerdink C, Jacobs JR. 1997. Argos and Spitz group genes function to regulate midline glial cell number in Drosophila embryos. Development 124: 3787-3796.
83. Struhl G, Basler K. 1993. Organizing activity of wingless protein in Drosophila. Cell 72: 527-540.
84. Suh J, Jackson FR. 2007. Drosophila ebony activity is required in glia for the circadian regulation of locomotor activity. Neuron 55: 435-447.
85. Sweeney NT, Brenman JE, Jan YN, Gao FB. 2006. The coiled-coil protein shrub controls neuronal morphogenesis in Drosophila. Curr Biol 16: 1006-1011.
86. Sweeney ST, Broadie K, Keane J, Niemann H, O'Kane CJ. 1995. Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14: 341-351.
87. Urbach R, Technau GM. 2003. Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development 130: 3621-3637.
88. Vincent S, Vonesch JL, Giangrande A. 1996. Glide directs glial fate commitment and cell fate switch between neurones and glia. Development 122: 131-139.
89. Waddell S, Armstrong JD, Kitamoto T, Kaiser K, Quinn WG. 2000. The amnesiac gene product is expressed in two neurons in the Drosophila brain that are critical for memory. Cell 103: 805-813.
90. Wang J, Ma X, Yang JS, Zheng X, Zugates CT, Lee CH, Lee T. 2004. Transmembrane/juxtamembrane domain-dependent Dscam distribution and function during mushroom body neuronal morphogenesis. Neuron 43: 663-672.
91. White K, Tahaoglu E, Steller H. 1996. Cell killing by the Drosophila gene reaper. Science 271: 805-807.
92. Witte HT, Jeibmann A, Klambt C, Paulus W. 2009. Modeling glioma growth and invasion in Drosophila melanogaster. Neoplasia 11: 882-888.
93. Wong AM, Wang JW, Axel R. 2002. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109: 229-241.
94. Xiong WC, Okano H, Patel NH, Blendy JA, Montell C. 1994. repo encodes a glial-specific homeo domain protein required in the Drosophila nervous system. Genes Dev 8: 981-994.
95. Xu T, Rubin GM. 1993. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117: 1223-1237.
96. Yu HH, Chen CH, Shi L, Huang Y, Lee T. 2009. Twin-spot MARCM to reveal the developmental origin and identity of neurons. Nat Neurosci 12: 947-953.
97. Zheng X, Wang J, Haerry TE, Wu AY, Martin J, O'Connor MB, Lee CH, Lee T. 2003. TGF-beta signaling activates steroid hormone receptor expression during neuronal remodeling in the Drosophila brain. Cell 112: 303-315.
98. Zheng Y, Wildonger J, Ye B, Zhang Y, Kita A, Younger SH, Zimmerman S, Jan LY, Jan YN. 2008. Dynein is required for polarized dendritic transport and uniform microtubule orientation in axons. Nat Cell Biol 10: 1172-1180.
99. Zhu S, Lin S, Kao CF, Awasaki T, Chiang AS, Lee T. 2006. Gradients of the Drosophila Chinmo BTB-zinc finger protein govern neuronal temporal identity. Cell 127: 409-422.
100. Ziegenfuss JS, Biswas R, Avery MA, Hong K, Sheehan AE, Yeung YG, Stanley ER, Freeman MR. 2008. Draper-dependent glial phagocytic activity is mediated by Src and Syk family kinase signalling. Nature 453: 935-939.