Transcriptional regulation of peripheral glial cell differentiation in the embryonic nervous system of drosophila

GLIA

Volumn 59, Issue 9, 2011, Pages 1264-1272

  Schmidt, Imke ^a   Franzdóttir, Sigrídur Rut ^a,c   Edenfeld, Gundula ^a,b   Rodrigues, Floriano ^a   Zierau, Ariane ^a   Klämbt, Christian ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b Goethe Gymnasium Düsseldorf ^*  (Germany)

^c UNIVERSITY OF ICELAND   (Iceland)

Author keywords

Drosophila; Glia; Jaywalker; Nejire; PNS; Tango

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; NETRIN;

ALLELE; ANIMAL EMBRYO; ARTICLE; CELL FUNCTION; CELL HETEROGENEITY; CELL MIGRATION; DROSOPHILA; EMBRYONIC STRUCTURES; GLIA CELL; HISTOLOGY; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; TRACHEA; TRANSCRIPTION REGULATION;

ANIMALS; ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR; CELL DIFFERENTIATION; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; NEUROGENESIS; NEUROGLIA; P300-CBP TRANSCRIPTION FACTORS; PERIPHERAL NERVOUS SYSTEM; RNA, MESSENGER;

EID: 79959959339     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.21123     Document Type: Article

References (102)

1. Akimaru H, Chen Y, Dai P, Hou DX, Nonaka M, Smolik SM, Armstrong S, Goodman RH, Ishii S. 1997a. Drosophila CBP is a co-activator of cubitus interruptus in hedgehog signalling. Nature 386: 735-738.
2. Akimaru H, Hou DX, Ishii S. 1997b. Drosophila CBP is required for dorsal-dependent twist gene expression. Nat Genet 17: 211-214.
3. Akiyama Y, Hosoya T, Poole AM, Hotta Y. 1996. The gcm-motif: A novel DNA-binding motif conserved in Drosophila and mammals. Proc Natl Acad Sci USA 93: 14912-14916.
4. Alarcon JM, Malleret G, Touzani K, Vronskaya S, Ishii S, Kandel ER, Barco A. 2004. Chromatin acetylation, memory, and LTP are impaired in CBP+/- mice: A model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 42: 947-959.
5. 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.
6. Arany Z, Sellers WR, Livingston DM, Eckner R. 1994. E1A-associated p300 and CREB-associated CBP belong to a conserved family of coactivators. Cell 77: 799-800.
7. Auld VJ, Fetter RD, Broadie K, Goodman CS. 1995. Gliotactin, a novel transmembrane protein on peripheral glia, is required to form the blood-nerve barrier in Drosophila. Cell 81: 757-767.
8. Awasaki T, Lai S-L, Ito K, Lee T. 2008. Organization and postembryonic development of glial cells in the adult central brain of Drosophila. J Neurosci 28: 13742-13753.
9. Badenhorst P. 2001. Tramtrack controls glial number and identity in the Drosophila embryonic CNS. Development 128: 4093-4101.
10. 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.
11. Berger C, Renner S, Luer K, Technau GM. 2007. The commonly used marker ELAV is transiently expressed in neuroblasts and glial cells in the Drosophila embryonic CNS. Dev Dyn 236: 3562-3568.
12. Bernardoni R, Vivancos V, Giangrande A. 1997. glide/gcm is expressed and required in the scavenger cell lineage. Dev Biol 191: 118-130.
13. 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.
14. Bossing T, Technau GM, Doe CQ. 1996a. huckebein is required for glial development and axon pathfinding in the neuroblast 1-1 and neuroblast 2-2 lineages in the Drosophila central nervous system. Mech Dev 55: 53-64.
15. Bossing T, Udolph G, Doe CQ, Technau GM. 1996b. The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm. Dev Biol 179: 41-64.
16. Campbell G, Goring 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.
17. Campos-Ortega JA. 1993. Early neurogenesis in Drosophila melanogaster. In: Bate CM, Martinez-Arias A, editors. Development of Drosophila: Cold Spring Harbor: Laboratory Press. pp 1091-1129.
18. 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.
19. Chrivia JC, Kwok RP, Lamb N, Hagiwara M, Montminy MR, Goodman RH. 1993. Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365: 855-859.
20. Crews ST. 1998. Control of cell lineage-specific development and transcription by bHLH-PAS proteins. Genes Dev 12: 607-620.
21. Das C, Lucia MS, Hansen KC, Tyler JK. 2009. CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature 459: 113-117.
22. De Graeve F, Jagla T, Daponte JP, Rickert C, Dastugue B, Urban J, Jagla K. 2004. The ladybird homeobox genes are essential for the specification of a subpopulation of neural cells. Dev Biol 270: 122-134.
23. De Iaco R, Soustelle L, Kammerer M, Sorrentino S, Jacques C, Giangrande A. 2006. Huckebein-mediated autoregulation of Glide/Gcm triggers glia specification. EMBO J 25: 244-254.
24. Dickson BJ. 2002. Molecular mechanisms of axon guidance. Science 298: 1959-1964.
25. Doronkin S, Djagaeva I, Nagle ME, Reiter LT, Seagroves TN. 2010. Dose-dependent modulation of HIF-1α/sima controls the rate of cell migration and invasion in Drosophila ovary border cells. Oncogene 29: 1123-1134.
26. Edenfeld G, Altenhein B, Zierau A, Cleppien D, Krukkert K, Technau G, Klambt C. 2007. Notch and Numb are required for normal migration of peripheral glia in Drosophila. Dev Biol 301: 27-37.
27. Edenfeld G, Volohonsky G, Krukkert K, Naffin E, Lammel U, Grimm A, Engelen D, Reuveny A, Volk T, Klambt C. 2006. The splicing factor crooked neck associates with the RNA-binding protein how to control glial cell maturation in Drosophila. Neuron 52: 969-980.
28. Edenfeld G. 2004. Die Entwicklung der periphen Gliazellen von Drosophila melanogaster. Dissertation Universität Münster.
29. Edwards TN, Meinertzhagen IA. 2010. The functional organisation of glia in the adult brain of Drosophila and other insects. Prog Neurobiol 90: 471-497.
30. 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.
31. 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.
32. Ghysen A, Dambly-Chaudiere CEA, Jan LY, Jan YN. 1986. Sensory neurons and peripheral pathways in Drosophila embryos. Roux's Arch Dev Biol 195: 281-289.
33. Giesen K, Hummel T, Stollewerk A, Harrison S, Travers A, Klambt C. 1997. Glial development in the Drosophila CNS requires concomitant activation of glial and repression of neuronal differentiation genes. Development 124: 2307-2316.
34. Granderath S, Bunse I, Klambt C. 2000. gcm and pointed synergistically control glial transcription of the Drosophila gene loco. Mech Dev 91: 197-208.
35. Granderath S, Klämbt C. In press. Genetic analysis of gliogenesis in Drosophila. In: Jessen K, Richardson W, editors. Glial cell development. Oxford: Oxford University Press.
36. Granderath S, Stollewerk A, Greig S, Goodman CS, O'Kane CJ, Klambt C. 1999. loco encodes an RGS protein required for Drosophila glial differentiation. Development 126: 1781-1791.
37. Griffiths RL, Hidalgo A. 2004. Prospero maintains the mitotic potential of glial precursors enabling them to respond to neurons. EMBO J 23: 2440-2450.
38. 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.
39. Hiromi Y, Kuroiwa A, Gehring WJ. 1985. Control elements of the Drosophila segmentation gene fushi tarazu. Cell 43(3, Pt 2): 603- 613.
40. Ho MS-c, Chen H, Chen M, Jacques C, Giangrande A, Chien C-T. 2009. Gcm protein degradation suppresses proliferation of glial progenitors. Proc Natl Acad Sci USA 106: 6778-6783.
41. 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.
42. Hummel T, Schimmelpfeng K, Klambt C. 1999. Commissure formation in the embryonic CNS of Drosophila. Dev Biol 209: 381-398.
43. Isaac DD, Andrew DJ. 1996. Tubulogenesis in Drosophila: A requirement for the trachealess gene product. Genes Dev 10: 103-117.
44. Ito K, Urban J, Technau GM. 1995. Distribution, classification, and development of Drosophila glial cells in the late embryonic and early larval ventral nerve cord. Roux's Arch Dev Biol 204: 284-307.
45. 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.
46. Janknecht R, Hunter T. 1996. Transcription. A growing coactivator network. Nature 383: 22-23.
47. 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.
48. Kee BL, Arias J, Montminy MR. 1996. Adaptor-mediated recruitment of RNA polymerase II to a signal-dependent activator. J Biol Chem 271: 2373-2375.
49. Klaes A, Menne T, Stollewerk A, Scholz H, Klambt C. 1994. The Ets transcription factors encoded by the Drosophila gene pointed direct glial cell differentiation in the embryonic CNS. Cell 78: 149-160.
50. Klambt C. 1993. The Drosophila gene pointed encodes two ETS-like proteins which are involved in the development of the midline glial cells. Development 117: 163-176.
51. Klambt C, Goodman CS. 1991. The diversity and pattern of glia during axon pathway formation in the Drosophila embryo. Glia 4: 205-213.
52. Klambt 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.
53. Kumar JP, Jamal T, Doetsch A, Turner FR, Duffy JB. 2004. CREB binding protein functions during successive stages of eye development in Drosophila. Genetics 168: 877-893.
54. Laczko R, Szauter KM, Jansen MK, Hollosi P, Muranyi M, Molnar J, Fong KS, Hinek A, Csiszar K. 2007. Active lysyl oxidase (LOX) correlates with focal adhesion kinase (FAK)/paxillin activation and migration in invasive astrocytes. Neuropathol Appl Neurobiol 33: 631-643.
55. Landgraf M, Sanchez-Soriano N, Technau GM, Urban J, Prokop A. 2003. Charting the Drosophila neuropile: A strategy for the standardised characterisation of genetically amenable neurites. Dev Biol 260: 207-225.
56. Lavista-Llanos S, Centanin L, Irisarri M, Russo DM, Gleadle JM, Bocca SN, Muzzopappa M, Ratcliffe PJ, Wappner P. 2002. Control of the hypoxic response in Drosophila melanogaster by the basic helix-loop-helix PAS protein similar. Mol Cell Biol 22: 6842-6853.
57. Lee BP, Jones BW. 2005. Transcriptional regulation of the Drosophila glial gene repo. Mech Dev 122: 849-862.
58. Mahr A, Aberle H. 2006. The expression pattern of the Drosophila vesicular glutamate transporter: A marker protein for motoneurons and glutamatergic centers in the brain. Gene Expr Patterns 6: 299-309.
59. Marek KW, Ng N, Fetter R, Smolik S, Goodman CS, Davis GW. 2000. A genetic analysis of synaptic development: Pre- and postsynaptic dCBP control transmitter release at the Drosophila NMJ. Neuron 25: 537-547.
60. Merritt DJ, Whitington PM. 1995. Central projections of sensory neurons in the Drosophila embryo correlate with sensory modality, soma position, and proneural gene function. J Neurosci 15(3, Pt 1): 1755-1767.
61. Mondal S, Ivanchuk SM, Rutka JT, Boulianne GL. 2007. Sloppy paired 1/2 regulate glial cell fates by inhibiting Gcm Function. Glia 55: 282-293.
62. Mortimer NT, Moberg KH. 2009. Regulation of Drosophila embryonic tracheogenesis by dVHL and hypoxia. Dev Biol 329: 294-305.
63. Nelson HB, Laughon A. 1993. Drosophila glial architecture and development: Analysis using a collection of new cell-specific markers. Roux's Arch Dev Biol 202: 341-354.
64. Ogryzko VV, Schiltz RL, Russanova V, Howard BH, Nakatani Y. 1996. The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell 87: 953-959.
65. Ohayon D, Pattyn A, Venteo S, Valmier J, Carroll P, Garces A. 2009. Zfh1 promotes survival of a peripheral glia subtype by antagonizing a Jun N-terminal kinase-dependent apoptotic pathway. EMBO J 28: 3228-3243.
66. Ohshiro T, Saigo K. 1997. Transcriptional regulation of breathless FGF receptor gene by binding of TRACHEALESS/dARNT heterodimers to three central midline elements in Drosophila developing trachea. Development 124: 3975-3986.
67. Park KS, Moon SI, Kim SH, Jeon SH. 2009. Ectopic Repo suppresses expression of castor gene in Drosophila central nervous system. Biochem Biophys Res Commun 388: 187-192.
68. Petrij F, Giles RH, Dauwerse HG, Saris JJ, Hennekam RC, Masuno M, Tommerup N, van Ommen GJ, Goodman RH, Peters DJ, Breuning MH. 1995. Rubinstein-Taybi syndrome caused by mutations in the transcriptional co-activator CBP. Nature 376: 348-351.
69. Poeck B, Fischer S, Gunning D, Zipursky SL, Salecker I. 2001. Glial cells mediate target layer selection of retinal axons in the developing visual system of Drosophila. Neuron 29: 99-113.
70. Rowitch DH. 2004. Glial specification in the vertebrate neural tube. Nat Rev Neurosci 5: 409-419.
71. Salzberg A, D'Evelyn D, Schulze KL, Lee JK, Strumpf D, Tsai L, Bellen HJ. 1994. Mutations affecting the pattern of the PNS in Drosophila reveal novel aspects of neuronal development. Neuron 13: 269-287.
72. Salzberg A, Golden K, Bodmer R, Bellen HJ. 1996. Gutfeeling, a Drosophila gene encoding an antizyme-like protein, is required for late differentiation of neurons and muscles. Genetics 144: 183-196.
73. 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.
74. 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.
75. Schreiber J, Sock E, Wegner M. 1997. The regulator of early gliogenesis glial cells missing is a transcription factor with a novel type of DNA-binding domain. Proc Natl Acad Sci USA 94: 4739-4744.
76. Sen A, Reddy GV, Rodrigues V. 2003. Combinatorial expression of Prospero, Seven-up, and Elav identifies progenitor cell types during sense-organ differentiation in the Drosophila antenna. Dev Biol 254: 79-92.
77. Sen A, Shetty C, Jhaveri D, Rodrigues V. 2005. Distinct types of glial cells populate the Drosophila antenna. BMC Dev Biol 5: 25.
78. Sepp KJ, Auld VJ. 1999. Conversion of lacZ enhancer trap lines to GAL4 lines using targeted transposition in Drosophila melanogaster. Genetics 151: 1093-1101.
79. Shandala T, Takizawa K, Saint R. 2003. The dead ringer/retained transcriptional regulatory gene is required for positioning of the longitudinal glia in the Drosophila embryonic CNS. Development 130: 1505-1513.
80. Shiga Y, Tanaka-Matakatsu M, Hayashi S. 1996. A nuclear GFP/b-galactosidase fusion protein as a marker for morphogenesis in living Drosophila. Dev Growth Differentiation 38: 99-106.
81. Silies M, Yuva Y, Engelen D, Aho A, Stork T, Klambt C. 2007. Glial cell migration in the eye disc. J Neurosci 27: 13130-13139.
82. Silies M, Yuva-Aydemir Y, Franzdottir 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.
83. Sink H, Whitington PM. 1991. Location and connectivity of abdominal motoneurons in the embryo and larva of Drosophila melanogaster. J Neurobiol 22: 298-311.
84. Sonnenfeld M, Ward M, Nystrom G, Mosher J, Stahl S, Crews S. 1997. The Drosophila tango gene encodes a bHLH-PAS protein that is orthologous to mammalian Arnt and controls CNS midline and tracheal development. Development 124: 4571-4582.
85. Soustelle L, Giangrande A. 2007. Glial differentiation and the Gcm pathway. Neuron Glia Biol 3: 5-16.
86. Soustelle L, Roy N, Ragone G, Giangrande A. 2008. Control of gcm RNA stability is necessary for proper glial cell fate acquisition. Mol Cell Neurosci 37: 657-662.
87. Stacey SM, Muraro NI, Peco E, Labbe A, Thomas GB, Baines RA, van Meyel DJ. 2010. Drosophila glial glutamate transporter Eaat1 is regulated by fringe-mediated notch signaling and is essential for larval locomotion. J Neurosci 30: 14446-14457.
88. Stork T, Engelen D, Krudewig A, Silies M, Bainton RJ, Klambt C. 2008. Organization and function of the blood-brain barrier in Drosophila. J Neurosci 28: 587-597.
89. Stork T, Thomas S, Rodrigues F, Silies M, Naffin E, Wenderdel S, Klambt C. 2009. Drosophila Neurexin IV stabilizes neuron-glia interactions at the CNS midline by binding to Wrapper. Development 136: 1251-1261.
90. Takizawa K, Hotta Y. 2001. Pathfinding analysis in a glia-less gcm mutant in Drosophila. Dev Genes Evol 211: 30-36.
91. Thomas GB, van Meyel DJ. 2007. The glycosyltransferase Fringe promotes Delta-Notch signaling between neurons and glia, and is required for subtype-specific glial gene expression. Development 134: 591-600.
92. Vincent S, Vonesch JL, Giangrande A. 1996. Glide directs glial fate commitment and cell fate switch between neurones and glia. Development 122: 131-139.
93. 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.
94. von Hilchen CM, Hein I, Technau GM, Altenhein B. 2010. Netrins guide migration of distinct glial cells in the Drosophila embryo. Development 137: 1251-1262.
95. Wang J, Weaver IC, Gauthier-Fisher A, Wang H, He L, Yeomans J, Wondisford F, Kaplan DR, Miller FD. 2010. CBP histone acetyltransferase activity regulates embryonic neural differentiation in the normal and Rubinstein-Taybi syndrome brain. Dev Cell 18: 114-125.
96. Ward MP, Mosher JT, Crews ST. 1998. Regulation of bHLH-PAS protein subcellular localization during Drosophila embryogenesis. Development 125: 1599-1608.
97. Wilk R, Weizman I, Shilo BZ. 1996. Trachealess encodes a bHLH-PAS protein that is an inducer of tracheal cell fates in Drosophila. Genes Dev 10: 93-102.
98. Woodhoo A, Sommer L. 2008. Development of the Schwann cell lineage: From the neural crest to the myelinated nerve. Glia 56: 1481-1490.
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. Yang Z, Edenberg HJ, Davis RL. 2005. Isolation of mRNA from specific tissues of Drosophila by mRNA tagging. Nucleic Acids Res 33: e148.
101. Younossi-Hartenstein A, Hartenstein V. 1993. The role of the tracheae and musculature during pathfinding of Drosophila embryonic sensory axons. Dev Biol 158: 430-447.
102. Yuasa Y, Okabe M, Yoshikawa S, Tabuchi K, Xiong WC, Hiromi Y, Okano H. 2003. Drosophila homeodomain protein REPO controls glial differentiation by cooperating with ETS, BTB transcription factors. Development 130: 2419-2428.