Morphological diversity and development of glia in Drosophila

GLIA

Volumn 59, Issue 9, 2011, Pages 1237-1252

  Hartenstein, Volker ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Development; Drosophila; Glia

Indexed keywords

ARTICLE; BRAIN CORTEX; CELL DIFFERENTIATION; CELL ENCAPSULATION; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CELL SHAPE; CELL STRUCTURE; CENTRAL NERVOUS SYSTEM; DROSOPHILA; GLIA; GLIA CELL; INSECT DEVELOPMENT; LAMELLAR BODY; NEOCORTEX; NERVE CELL; NERVE CORD; NERVE FIBER GROWTH; NERVE FUNCTION; NERVE SHEATH; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NEUROPIL; NONHUMAN; PERIKARYON; PERIPHERAL NERVE; PRIORITY JOURNAL;

ANIMALS; BRAIN; CEREBRAL CORTEX; DROSOPHILA; EMBRYO, NONMAMMALIAN; HUMANS; LARVA; NEUROGLIA; NEUROPIL; PERIPHERAL NERVES;

EID: 79959999314     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.21162     Document Type: Article

References (106)

1. Aigouy B, Lepelletier L, Giangrande A. 2008. Glial chain migration requires pioneer cells. J Neurosci 28: 11635-11641.
2. Akiyama-Oda Y, Hosoya T, Hotta Y. 1999. Asymmetric cell division of thoracic neuroblast 6-4 to bifurcate glial and neuronal lineage in Drosophila. Development 126: 1967-1974.
3. 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.
4. 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.
5. 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.
6. 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.
7. Banerjee S, Pillai AM, Paik R, Li J, Bhat MA. 2006. Axonal ensheathment and septate junction formation in the peripheral nervous system of Drosophila. J Neurosci 26: 3319-3329.
8. Baumgartner S, Littleton JT, Broadie K, Bhat MA, Harbecke R, Lengyel JA, Chiquet-Ehrismann R, Prokop A, Bellen HJ. 1996. A Drosophila neurexin is required for septate junction and blood-nerve barrier formation and function. Cell 87: 1059-1068.
9. 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.
10. Bello BC, Izergina N, Caussinus E, Reichert H. 2008. Amplification of neural stem cell proliferation by intermediate progenitor cells in Drosophila brain development. Neural Dev 19: 3-5.
11. Bernardoni R, Kammerer M, Vonesch JL, Giangrande A. 1999. Gliogenesis depends on glide/gcm through asymmetric division of neuroglioblasts. Dev Biol 216: 265-275.
12. Bery A, Cardona A, Martinez P, Hartenstein V. 2010. Structure of the central nervous system of a juvenile acoel, Symsagittifera roscoffensis. Dev Genes Evol 220: 61-76.
13. Blauth K, Banerjee S, Bhat MA. 2010. Axonal ensheathment and intercellular barrier formation in Drosophila. Int Rev Cell Mol Biol 283: 93-128.
14. Bodmer R, Carretto R, Jan YN. 1989. Neurogenesis of the peripheral nervous system in Drosophila embryos: DNA replication patterns and cell lineages. Neuron 3: 21-32.
15. Boone JQ, Doe CQ. 2008. Identification of Drosophila type II neuroblast lineages containing transit amplifying ganglion mother cells. Dev Neurobiol 68: 1185-1195.
16. Bossing T, Technau GM. 1994. The fate of the CNS midline progenitors in Drosophila as revealed by a new method for single cell labelling. Development 120: 1895-1906.
17. Bowsher JH, Nijhout HF. 2010. Partial co-option of the appendage patterning pathway in the development of abdominal appendages in the sepsid fly Themira biloba. Dev Genes Evol 219: 577-587.
18. Buchanan RL, Benzer S. 1993. Defective glia in the Drosophila brain degeneration mutant drop-dead. Neuron 10: 839-850.
19. Campbell G, Göring H, Lin T, Spana E, Andersson S, Doe CQ, Tomlinson A. 1994. RK2, a glial-specific homeodomain protein required for embryonic nerve cord condensation and viability in Drosophila. Development 120: 2957-2966.
20. Cantera R. 1993. Glial cells in adult and developing prothoracic ganglion of the hawk moth Manduca sexta. Cell Tissue Res 272: 93-108.
21. Carlson SD, Juang JL, Hilgers SL, Garment MB. 2000. Blood barriers of the insect. Annu Rev Entomol 45: 151-74.
22. 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.
23. Chotard C, Salecker I. 2007. Glial cell development and function in the Drosophila visual system. Neuron Glia Biol 3: 17-25.
24. 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.
25. Daneman R, Barres BA. 2005. The blood-brain barrier-Lessons from moody flies. Cell 123: 9-12.
26. Dearborn RJr, Kunes S. 2004. An axon scaffold induced by retinal axons directs glia to destinations in the Drosophila optic lobe. Development 131: 2291-2303.
27. Doherty J, Logan MA, Taşdemir OE, Freeman MR. 2009. Ensheathing glia function as phagocytes in the adult Drosophila brain. J Neurosci 29: 4768-4781.
28. Dumstrei K, Wang F, Tepass U, Hartenstein V. 2003. Role of DE-cadherin in neuroblast proliferation, neural morphogenesis and axon tract formation in Drosophila larval brain development. J Neurosci 23: 3325-3335.
29. Dupont S, Thorndyke W, Thorndyke MC, Burke RD. 2009. Neural development of the brittlestar Amphiura filiformis. Dev Genes Evol 219: 159-166.
30. Edwards JS, Swales LS, Bate M. 1993. The differentiation between neuroglia and connective tissue sheath in insect ganglia revisited: The neural lamella and perineurial sheath cells are absent in a mesodermless mutant of Drosophila. J Comp Neurol 333: 301-308.
31. Edwards TN, Meinertzhagen IA. 2010. The functional organisation of glia in the adult brain of Drosophila and other insects. Prog Neurobiol 90: 471-497.
32. Fischbach KF, Hiesinger PR. 2008. Optic lobe development. Adv Exp Med Biol 628: 115-136.
33. Freeman MR, Doe CQ. 2001. Asymmetric prospero localization is required to generate mixed neuronal/glial lineages in the Drosophila CNS. Development 128: 4103-4112.
34. Freeman MR, Doherty J. 2006. Glial cell biology in Drosophila and vertebrates. Trends Neurosci 29: 82-90.
35. Fung S, Wang F, Spindler SR, Hartenstein V. 2009. Drosophila E-cadherin and its binding partner Armadillo/beta-catenin are required for axonal pathway choices in the developing larval brain. Dev Biol 332: 371-382.
36. Gho M, Bellaïche Y, Schweisguth F. 1999. Revisiting the Drosophila microchaete lineage: A novel intrinsically asymmetric cell division generates a glial cell. Development 126: 3573-3584.
37. Giangrande A, Murray MA, Palka J. 1993. Development and organization of glial cells in the peripheral nervous system of Drosophila melanogaster. Development 117: 895-904.
38. 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.
39. Grosjean Y, Grillet M, Augustin H, Ferveur JF, Featherstone DE. 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.
40. Halter DA, Urban J, Rickert C, Ner SS, Ito K, Travers AA, Technau GM, Hartenstein V. 1988. Development of the Drosophila larval sensory organs: Spatiotemporal pattern of sensory neurones, peripheral axonal pathways, and sensilla differentiation. Development 102: 869-886.
41. Hartenstein V, Ehlers U. 2000. The embryonic development of the rhabdocoel flatworm Mesostoma lingua. Dev Genes Evol 210: 399-415.
42. Hartenstein V, Nassif C, Lekven A. 1998. Embryonic development of the Drosophila brain II. The glia cells of the brain. J Comp Neurol 402: 32-48.
43. Hartenstein V, Spindler S, Pereanu W, Fung S. 2008. The development of the Drosophila larval brain. Adv Exp Med Biol 628: 1-31.
44. Hidalgo A, Learte AR, McQuilton P, Pennack J, Zhu B. 2006. Neurotrophic and gliatrophic contexts in Drosophila. Brain Behav Evol 68: 173-80.
45. 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.
46. Hoyle G. 1986. Glial cells of an insect ganglion. J Comp Neurol 246: 85-103.
47. Ito K, Urban J, Technau GM. 1994. Distribution, classification and development of Drosophila glia cells during late embryogenesis. Roux's Arch Dev Biol 204: 284-307.
48. Izergina N, Balmer J, Bello B, Reichert H. 2009. Postembryonic development of transit amplifying neuroblast lineages in the Drosophila brain. Neural Dev 4: 44.
49. Jackson FR, Haydon PG. 2008. Glial cell regulation of neurotransmission and behavior in Drosophila. Neuron Glia Biol 4: 11-17.
50. Jacobs JR. 2000. The midline glia of Drosophila: A molecular genetic model for the developmental functions of glia. Prog Neurobiol 62: 475-508.
51. 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.
52. 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.
53. Jones BW. 2005. Transcriptional control of glial cell development in Drosophila. Dev Biol 278: 265-273.
54. 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.
55. Juang JL, Carlson SD. 1994. Analog of vertebrate anionic sites in blood-brain interface of larval Drosophila. Cell Tissue Res 277: 87-95.
56. Kaphingst K, Kunes S. 1994. Pattern formation in the visual centers of the Drosophila brain: Wingless acts via decapentaplegic to specify the dorsoventral axis. Cell 78: 437-448.
57. Kato K, Awasaki T, Ito K. 2009. Neuronal programmed cell death induces glial cell division in the adult Drosophila brain. Development 136: 51-59.
58. Klämbt C, Goodman CS. 1991. The diversity and pattern of glia during axon pathway formation in the Drosophila embryo. Glia 4: 205-213.
59. Klämbt C, Jacobs JR, Goodman CS. 1991. The midline of the Drosophila central nervous system: A model for the genetic analysis of cell fate, cell migration, and growth cone guidance. Cell 64: 801-815.
60. Kurant E, Axelrod S, Leaman D, Gaul U. 2008. Six-microns-under acts upstream of Draper in the glial phagocytosis of apoptotic neurons. Cell 133: 498-509.
61. Lane N. 1982. Insect intercellular junctions: Their structure and development. In: King RC, Akai H, editors. "Insect ultrastructure." New York: Plenum.
62. Lane NJ. 1981. Invertebrate neuroglia-junctional structure and development. J Exp Biol 95: 7-33.
63. Lane NJ, Swales LS. 1979. Intercellular junctions and the development of the blood-brain barrier in Manduca sexta. Brain Res 168: 227-245.
64. Larsen C, Shy D, Spindler S, Fung S, Younossi-Hartenstein A, Hartenstein V. 2009. Patterns of growth, axonal extension and axonal arborization of neuronal lineages in the developing Drosophila brain. Dev Biol 335: 289-304.
65. 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.
66. Magie CR, Martindale MQ. 2008. Cell-cell adhesion in the cnidaria: Insights into the evolution of tissue morphogenesis. Biol Bull 214: 218-232.
67. Mashanov VS, Zueva OR, Garcia-Arraras JE. 2010. Organization of glial cells in the adult sea cucumber central nervous system. Glia 58: 1581-1593.
68. Mashanov VS, Zueva OR, Heinzeller T, Aschauer B, Naumann WW, Grondona JM, Cifuentes M, Garcia-Arraras JE. 2009. The central nervous system of sea cucumbers (Echinodermata: Holothuroidea) shows positive immunostaining for a chordate glial secretion. Front Zool 6: 11.
69. Meinertzhagen IA, Hanson TE. 1993. The development of Drosophila, Vol. II. In: Bate CM, Martinez Arias A, editors. New York: Cold Spring Laboratory Press. pp 1363-1491.
70. Mission JP, Takahashi T, Caviness VSJr. 1991. Ontogeny of radial and other astroglial cells in murine cerebral cortex. Glia 4: 138-148.
71. Morris J, Nallur R, Ladurner P, Egger B, Rieger R, Hartenstein V. 2004. The embryonic development of the flatworm Macrostomum sp. Dev Gen Evol 214: 220-239.
72. Nakano H, Nakajima Y, Amemiya S. 2009. Nervous system development of two crinoid species, the sea lily Metacrinus rotundus and the feather star Oxycomanthus japonicus. Dev Genes Evol 219: 565-576.
73. Nambu JR, Franks RG, Hu S, Crews ST. 1990. The single-minded gene of Drosophila is required for the expression of genes important for the development of CNS midline cells. Cell 63: 63-75.
74. Nassif C, Noveen A, Hartenstein V. 1998. Embryonic development of the Drosophila brain I. The pattern of pioneer tracts. J Comp Neurol 402: 10-31.
75. Parker RJ, Auld VJ. 2004. Signaling in glial development: Differentiation migration and axon guidance. Biochem Cell Biol 82: 694-707.
76. Parker RJ, Auld VJ. 2006. Roles of glia in the Drosophila nervous system. Semin Cell Dev Biol 17: 66-77.
77. Pereanu W, Garcia L, Hartenstein V. 2006. Tracheal development in the Drosophila larval brain is guided by glial cells. Dev Biol 302: 169-180.
78. Pereanu W, Shy D, Hartenstein V. 2005. Morphogenesis and proliferation of the larval brain glia in Drosophila. Dev Biol 283: 191-203.
79. Radojcic T, Pentreath VW. 1979. Invertebrate glia. Progr Neurobiol 12: 115-179.
80. Ragone G, Van De Bor V, Sorrentino S, Kammerer M, Galy A, Schenck A, Bernardoni R, Miller AA, Roy N, Giangrande A. 2003. Transcriptional regulation of glial cell specification. Dev Biol 255: 138-150.
81. Ramachandra NB, Gates R, Ladurner P, Jacobs D, Hartenstein V. 2002. Neurogenesis in the primitive bilaterian Neochildia I. Normal development and isolation of genes controlling neural fate. Dev Genes Evol 212: 55-69.
82. Reddy GV, Rodrigues V. 1999. A glial cell arises from an additional division within the mechanosensory lineage during development of the microchaete on the Drosophila notum. Development 126: 4617-4622.
83. Saint Marie RL, Carlson SD, Chi C. 1984. The glial cells of insects. In: King RC, Akai H, editors. Insect ultrastructure. New York: Plenum.
84. 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.
85. Silies M, Yuva-Aydemir Y, Franzdóttir SR, Klämbt C. 2010. The eye imaginal disc as a model to study the coordination of neuronal and glial development. Fly (Austin) 4: 71-79.
86. Simon AF, Boquet I, Synguélakis M, Préat T. 1998. The Drosophila putative kinase linotte (derailed) prevents central brain axons from converging on a newly described interhemispheric ring. Mech Dev 76: 45-55.
87. Sonnenfeld MJ, Jacobs JR. 1995. Macrophages and glia participate in the removal of apoptotic neurons from the Drosophila embryonic nervous system. J Comp Neurol 359: 644-652.
88. Spindler SR, Hartenstein V. 2010 The Drosophila neural lineages: A model system to study brain development and circuitry. Dev Genes Evol 220: 1-10.
89. 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.
90. 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.
91. Tepass U, Hartenstein V. 1994. Differentiation of intercellular junctions in the Drosophila embryo. Dev Biol 161: 563-596.
92. Tepass U, Tanentzapf G, Ward R, Fehon R. 2001. Epithelial cell polarity and cell junctions in Drosophila. Annu Rev Genet 35: 747-784.
93. Udolph G, Prokop A, Bossing T, Technau GM. 1993. A common precursor for glia and neurons in the embryonic CNS of Drosophila gives rise to segment-specific lineage variants. Development 118: 765-775.
94. Udolph G, Rath P, Chia W. 2001. A requirement for Notch in the genesis of a subset of glial cells in the Drosophila embryonic central nervous system which arise through asymmetric divisions. Development 128: 1457-1466.
95. Urbach R, Technau GM. 2003. Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development 130: 3621-3637.
96. Vincent S, Vonesch JL, Giangrande A. 1996. Glide directs glial fate commitment and cell fate switch between neurones and glia. Development 122: 131-139.
97. von Hilchen CM, Beckervordersandforth RM, Rickert C, Technau GM, Altenhein B. 2008. Identity, origin, and migration of peripheral glial cells in the Drosophila embryo. Mech Dev 125: 337-352.
98. Wu VM, Schulte J, Hirschi A, Tepass U, Beitel GJ. 2004. Sinuous is a Drosophila claudin required for septate junction organization and epithelial tube size control. J Cell Biol 164: 313-323.
99. 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.
100. Younossi-Hartenstein A, Ehlers U, Hartenstein V. 2000. Embryonic development of the nervous system of the rhabdocoel flatworm Mesostoma lingua (Abildgaard, 1789). J Comp Neurol 416: 461-476.
101. Younossi-Hartenstein A, Hartenstein V. 1997. Pattern, time of birth and morphogenesis of sensillum precursors in Drosophila. Micr Res Tech 39: 479-491.
102. Younossi-Hartenstein A, Hartenstein V. 2000. The embryonic development of the polyclad flatworm Imgogine mcgrathi. Dev Genes Evol 210: 383-398.
103. Younossi-Hartenstein A, Jones M, Hartenstein V. 2001. The embryonic development of the nervous system of the temnocephalid flatworm Craspedella pedum. J Comp Neurol 434: 56-68.
104. Younossi-Hartenstein A, Nassif C, Hartenstein V. 1996. Early neurogenesis of the Drosophila brain. J Comp Neurol 370: 313-329.
105. Younossi-Hartenstein A, Shy D, Hartenstein V. 2006. The embryonic formation of the Drosophila brain neuropile. J Comp Neurol 497: 981-998.
106. 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.