Organization and postembryonic development of glial cells in the adult central brain of Drosophila

Journal of Neuroscience

Volumn 28, Issue 51, 2008, Pages 13742-13753

  Awasaki, Takeshi ^a   Lai, Sen Lin ^a,c   Ito, Kei ^b   Lee, Tzumin ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITY OF OREGON   (United States)

Author keywords

Adult brain; Cell lineage; Drosophila; Glial cells; Glial subtype; MARCM

Indexed keywords

ARTICLE; ASTROCYTE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CELL CLONE; CELL INFILTRATION; CELL LINEAGE; CELL STRUCTURE; CELL TYPE; DEVELOPMENTAL STAGE; DROSOPHILA; EMBRYO DEVELOPMENT; GLIA CELL; NEURAL STEM CELL; NEUROPIL; NONHUMAN; PERIKARYON; POSTEMBRYONIC DEVELOPMENT; PRIORITY JOURNAL; ANIMAL; ANIMAL EMBRYO; BIOSYNTHESIS; BRAIN; CELL COUNT; CELL DIFFERENTIATION; CLASSIFICATION; CYTOLOGY; GENETICS; GLIA; GROWTH, DEVELOPMENT AND AGING; LARVA; METABOLISM; NERVE CELL; PHYSIOLOGY; TRANSGENIC ANIMAL;

DIFFERENTIATION ANTIGEN; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; GCM PROTEIN, DROSOPHILA; HOMEODOMAIN PROTEIN; REPO PROTEIN, DROSOPHILA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIGENS, DIFFERENTIATION; BRAIN; CELL COUNT; CELL DIFFERENTIATION; CELL LINEAGE; CLONE CELLS; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; HOMEODOMAIN PROTEINS; LARVA; NEUROGLIA; NEURONS; NEUROPIL; TRANSCRIPTION FACTORS;

EID: 58149396831     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4844-08.2008     Document Type: Article

References (55)

1. Awad TA, Truman JW (1997) Postembryonic development of the midline glia in the CNS of Drosophila: proliferation, programmed cell death, and endocrine regulation. Dev Biol 187:283-297.
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, 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.
4. 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.
5. 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.
6. Booth GE, Kinrade EF, Hidalgo A (2000) Glia maintain follower neuron survival during Drosophila CNS development. Development 127:237-244.
7. Buchanan RL, Benzer S (1993) Defective glia in the Drosophila brain degeneration mutant drop-dead. Neuron 10:839-850.
8. Cantera R (1993) Glial cells in adult and developing prothoracic ganglion of the hawk moth Manduca sexta. Cell Tissue Res 272:93-108.
9. Carlson SD, Saint Marie RL (1990) Structure and function of insect glia. Annu Rev Entomol 35:597-621.
10. 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.
11. Colonques J, Ceron J, Tejedor FJ (2007) Segregation of postembryonic neuronal and glial lineages inferred from a mosaic analysis of the Drosophila larval brain. Mech Dev 124:327-340.
12. 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.
13. Griffiths RL, Hidalgo A (2004) Prospero maintains the mitotic potential of glial precursors enabling them to respond to neurons. EMBO J 23:2440-2450.
14. 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.
15. Halassa MM, Fellin T, Haydon PG (2007) The tripartite synapse: roles for gliotransmission in health and disease. Trends Mol Med 13:54-63.
16. Halter DA, Urban J, Rickert C, Ner SS, Ito K, Travers AA, Technau GM (1995) The homeobox gene repo is required for the differentiation and maintenance of glia function in the embryonic nervous system of Drosophila melanogaster. Development 121:317-332.
17. Hayashi S, Ito K, Sado Y, Taniguchi M, Akimoto A, Takeuchi H, Aigaki T, Matsuzaki F, Nakagoshi H, Tanimura T, Ueda R, Uemura T, Yoshihara M, Goto S (2002) GETDB, a database compiling expression patterns and molecular locations of a collection of Gal4 enhancer traps. Genesis 34:58-61.
18. Hidalgo A, Booth GE (2000) Glia dictate pioneer axon trajectories in the Drosophila embryonic CNS. Development 127:393-402.
19. 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.
20. Hoopfer ED, McLaughlin T, Watts RJ, Schuldiner O, O'Leary DD, Luo L (2006) Wlds protection distinguishes axon degeneration following injury from naturally occurring developmental pruning. Neuron 50:883-895.
21. 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.
22. Ito K, Awasaki T (2008) Clonal unit architecture of the adult fly brain. In: Brain development in Drosophila melanogaster (Technau GM, ed), pp 137-158. Austin: Landes Bioscience.
23. 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.
24. Ito K, Okada R, Tanaka NK, Awasaki T (2003) Cautionary observations on preparing and interpreting brain images using molecular biology-based staining techniques. Microsc Res Tech 62:170-186.
25. Jones BW (2001) Glial cell development in the Drosophila embryo. Bioessays 23:877-887.
26. 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.
27. Kammerer M, Giangrande A (2001) Glide2, a second glial promoting factor in Drosophila melanogaster. EMBO J 20:4664-4673.
28. Kanai Y (1997) Family of neutral and acidic amino acid transporters: molecular biology, physiology and medical implications. Curr Opin Cell Biol 9:565-572.
29. Kidd T, Bland KS, Goodman CS (1999) Slit is the midline repellent for the robo receptor in Drosophila. Cell 96:785-794.
30. 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.
31. Lai SL, Lee T (2006) Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat Neurosci 9:703-709.
32. Lee T, Luo L (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:451-461.
33. Lemke G (2001) Glial control of neuronal development. Annu Rev Neurosci 24:87-105.
34. 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.
35. Meyer MR, Reddy GR, Edwards JS (1987) Immunological probes reveal spatial and developmental diversity in insect neuroglia. J Neurosci 7:512-521.
36. Oland LA, Marrero HG, Burger I (1999) Glial cells in the developing and adult olfactory lobe of the moth Manduca sexta. Cell Tissue Res 297:527-545.
37. Parker RJ, Auld VJ (2006) Roles of glia in the Drosophila nervous system. Semin Cell Dev Biol 17:66-77.
38. Pfrieger FW, Barres BA (1995) What the fly's glia tell the fly's brain. Cell 83:671-674.
39. Rival T, Soustelle L, Strambi C, Besson MT, Iché M, Birman S (2004) Decreasing glutamate buffering capacity triggers oxidative stress and neuropil degeneration in the Drosophila brain. Curr Biol 14:599-605.
40. 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.
41. 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.
42. 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.
43. Sepp KJ, Schulte J, Auld VJ (2001) Peripheral glia direct axon guidance across the CNS/PNS transition zone. Dev Biol 238:47-63.
44. Sohal RS, Sharma SP, Couch EF (1972) Fine structure of the neural sheath, glia and neurons in the brain of the housefly, Musca domestica. Z Zellforsch Mikrosk Anat 135:449-459.
45. Soustelle L, Giangrande A (2007) Novel gcm-dependent lineages in the postembryonic nervous system of Drosophila melanogaster. Dev Dyn 236:2101-2108.
46. Stork T, Engelen D, Krudewig A, Silies M, Bainton RJ, Klämbt C (2008) Organization and function of the blood-brain barrier in Drosophila. J Neurosci 28:587-597.
47. Strausfeld NJ (1976) Insect brain. New York: Springer.
48. Suh J, Jackson FR (2007) Drosophila ebony activity is required in glia for the circadian regulation of locomotor activity. Neuron 55:435-447.
49. Takahashi M, Billups B, Rossi D, Sarantis M, Hamann M, Attwell D (1997) The role of glutamate transporters in glutamate homeostasis in the brain. J Exp Biol 200:401-409.
50. Villegas SN, Poletta FA, Carri NG (2003) GLIA: A reassessment based on novel data on the developing and mature central nervous system. Cell Biol Int 27:599-609.
51. Vincent S, Vonesch JL, Giangrande A (1996) Glide directs glial fate commitment and cell fate switch between neurones and glia. Development 122:131-139.
52. Watts RJ, Schuldiner O, Perrino J, Larsen C, Luo L (2004) Glia engulf degenerating axons during developmental axon pruning. Curr Biol 14:678-684.
53. Wong AM, Wang JW, Axel R (2002) Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109:229-241.
54. Xiong WC, Montell C (1995) Defective glia induce neuronal apoptosis in the repo visual system of Drosophila. Neuron 14:581-590.
55. 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.