Broad complex isoforms have unique distributions during central nervous system metamorphosis in Drosophila melanogaster

Journal of Comparative Neurology

Volumn 517, Issue 1, 2009, Pages 15-36

  Spokony, Rebecca F ^a,c   Restifo, Linda L ^a,b  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

Duplicated exons; Ecdysone cascade; Glia; Insect; Morphogenesis; Neuroblast; Neuron; Subfunctionalization

Indexed keywords

BROAD COMPLEX Z1; BROAD COMPLEX Z2; BROAD COMPLEX Z3; BROAD COMPLEX Z4; ISOPROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL INTERACTION; CELL PROLIFERATION; CELL TYPE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DNA BINDING; DROSOPHILA MELANOGASTER; EXON; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; GENE SEQUENCE; GENE SWITCHING; GENETIC SIMILARITY; HORMONAL REGULATION; LARVA; METAMORPHOSIS; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; PUPA (LIFE CYCLE STAGE);

ANIMALS; BRAIN; CELL DIFFERENTIATION; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GANGLIA, INVERTEBRATE; IMMUNOHISTOCHEMISTRY; METAMORPHOSIS, BIOLOGICAL; MICROSCOPY, CONFOCAL; NEUROGENESIS; NEUROGLIA; NEURONS; PROTEIN ISOFORMS; TIME FACTORS; TRANSCRIPTION FACTORS;

EID: 70349843230     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22119     Document Type: Article

References (101)

1. Adryan B, Teichmann SA. 2007. Computational identification of site-specific transcription factors in Drosophila. Fly 1:142-145.
2. Aigouy B, Van de Bor V, Boeglin M, Giangrande A. 2004. Time-lapse and cell ablation reveal the role of cell interactions in fly glia migration and proliferation. Development 131:5127-5138.
3. Alfonso TB, Jones BW. 2002. gcm2 promotes glial cell differentiation and is required with glial cells missing for macrophage development in Drosophila. Dev Biol 248:369-383.
4. Andres AJ, Thummel CS. 1994. Methods for quantitative analysis of transcription in larvae and prepupae. In: Goldstein LSB, Fyrberg EA, editors. Drosophila melanogaster: practical uses in cell and molecular biology. San Diego: Academic Press. p 565-573.
5. Andres AJ, Fletcher JC, Karim FD, Thummel CS. 1993. Molecular analysis of the initiation of insect metamorphosis: a comparative study of Drosophila ecdysteroid-regulated transcription. Dev Biol 160:388-404.
6. Arbeitman MN, Furlong EE, Imam F, Johnson E, Null BH, Baker BS, Krasnow MA, Scott MP, Davis RW, White KP. 2002. Gene expression during the life cycle of Drosophila melanogaster. Science 297:2270-2275.
7. 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.
8. 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.
9. Bayer CA, Holley B, Fristrom JW. 1996a. A switch in Broad-Complex zinc-finger isoform expression is regulated posttranscriptionally during the metamorphosis of Drosophila imaginal discs. Dev Biol 177:1-14.
10. Bayer CA, von Kalm L, Fristrom JW. 1996b. Gene regulation in imaginal disc and salivary gland development during Drosophila metamorphosis. In: Gilbert LI, Tata JR, Atkinson BG, editors. Metamorphosis: postembryonic reprogramming of gene expression in amphibian and insect cells. San Diego: Academic Press. p 322-361.
11. Bayer CA, von Kalm L, Fristrom JW. 1997. Relationships between protein isoforms and genetic functions demonstrate functional redundancy at the Broad-Complex during Drosophila metamorphosis. Dev Biol 187: 267-282.
12. Bayer C, Zhou X, Zhou B, Riddiford LM, von Kalm L. 2003. Evolution of the Drosophila broad locus: the Manduca sexta broad Z4 isoform has biological activity in Drosophila. Dev Genes Evol 213:471-476.
13. Belyaeva ES, Aizenzon MG, Semeshin VF, Kiss I, Koczka K, Baritcheva EM, Gorelova TD, Zhimulev IF. 1980. Cytogenetic analysis of the 2B3-4 - 2B11 region of the X-chromosome of Drosophila melanogaster. I. Cytology of the region and mutant complementation groups. Chromosoma 81:281-306.
14. Belyaeva ES, Vlassova IE, Biyasheva ZM, Kakpakov VT, Richards G, Zhimulev IF. 1981. Cytogenetic analysis of the 2B3-4 - 2B11 region of the X chromosome of Drosophila melanogaster. II. Changes in 20-OH ecdysone puffing caused by genetic defects of puff 2B5. Chromosoma 84:207-219.
15. 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.
16. Brennan CA, Li TR, Bender M, Hsiung F, Moses K. 2001. Broad-complex, but not Ecdysone receptor, is required for progression of the morphogenetic furrow in the Drosophila eye. Development 128:1-11.
17. 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.
18. Carlson SD, Juang JL, Hilgers SL, Garment MB. 2000. Blood barriers of the insect. Annu Rev Entomol 45:151-174.
19. Choi YJ, Lee G, Park JH. 2006. Programmed cell death mechanisms of identifiable peptidergic neurons in Drosophila melanogaster. Development 133:2223-2232.
20. Chotard C, Salecker I. 2004. Neurons and glia: team players in axon guidance. Trends Neurosci 27:655-661.
21. 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.
22. Consoulas C, Restifo LL, Levine RB. 2002. Dendritic remodeling and growth of motoneurons during metamorphosis of Drosophila melanogaster. J Neurosci 22:4906-4917.
23. Consoulas C, Levine RB, Restifo LL. 2005. The steroid hormone-regulated gene Broad Complex is required for dendritic growth of motoneurons during metamorphosis of Drosophila. J Comp Neurol 485:321-337.
24. Crossgrove K, Bayer CA, Fristrom JW, Guild GM. 1996. The Drosophila Broad-Complex early gene directly regulates late gene transcription during the ecdysone-induced puffing cascade. Dev Biol 180:745-758.
25. Deng W-M, Bownes M. 1997. Two signalling pathways specify localised expression of the Broad-Complex in Drosophila eggshell patterning and morphogenesis. Development 124:4639-4647.
26. Deschenes-Furry J, Perrone-Bizzozero N, Jasmin BJ. 2006. The RNAbinding protein HuD: a regulator of neuronal differentiation, maintenance and plasticity. Bioessays 28:822-833.
27. DiBello PR, Withers DA, Bayer CA, Fristrom JW, Guild GM. 1991. The Drosophila Broad-Complex encodes a family of related, zinc finger-containing proteins. Genetics 129:385-397.
28. Dumstrei K, Wang F, Nassif C, Hartenstein V. 2003. Early development of the Drosophila brain: V. Pattern of postembryonic neuronal lineages expressing DE-cadherin. J Comp Neurol 455:451-462.
29. Emery IF, Bedian V, Guild GM. 1994. Differential expression of Broad-Complex transcription factors may forecast distinct developmental tissue fates during Drosophila metamorphosis. Development 120: 3275-3287.
30. Halter D, Urban J, Rickert C, Ner S, Ito K, Travers A, Technau G. 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.
31. Hartenstein V, Spindler S, Pereanu W, Fung S. 2008. The development of the Drosophila larval brain. Adv Exp Med Biol 628:1-31.
32. Hodgetts RB, Clark WC, O'Keefe SL, Schouls M, Crossgrove K, Guild GM, von Kalm L. 1995. Hormonal induction of Dopa decarboxylase in the epidermis of Drosophila is mediated by the Broad-Complex. Development 121:3913-3922.
33. Hoekstra HE, Coyne JA. 2007. The locus of evolution: evo devo and the genetics of adaptation. Evolution 61:995-1016.
34. Hofbauer A, Campos-Ortega JA. 1990. Proliferation pattern and early differentiation of the optic lobes in Drosophila melanogaster. Roux's Arch Dev Biol 198:264-274.
35. Hoopfer ED, Penton A, Watts RJ, Luo L. 2008. Genomic analysis of Drosophila neuronal remodeling: a role for the RNA-binding protein Boule as a negative regulator of axon pruning. J Neurosci 28:6092-6103.
36. Huang Z, Kunes S. 1996. Hedgehog, transmitted along retinal axons, triggers neurogenesis in the developing visual centers of the Drosophila brain. Cell 86:411-422.
37. Huang Z, Shilo B-Z, Kunes S. 1998. A retinal axon fascicle uses Spitz, an EGF receptor ligand, to construct a synaptic cartridge in the brain of Drosophila. Cell 95:693-703.
38. Huet F, Ruiz C, Richards G. 1993. Puffs and PCR: the in vivo dynamics of early gene expression during ecdysone responses in Drosophila. Development 118:613-627.
39. Ito K, Hotta Y. 1992. Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster. Dev Biol 149:134-148.
40. Jacobs JR. 2000. The midline glia of Drosophila: a molecular genetic model for the developmental functions of glia. Prog Neurobiol 62:475-508.
41. Karim FD, Thummel CS. 1992. Temporal coordination of regulatory gene expression by the steroid hormone ecdysone. EMBO J 11:4083-4093.
42. Karim FD, Guild GM, Thummel CS. 1993. The Drosophila Broad-Complex plays a key role in controlling ecdysone-regulated gene expression at the onset of metamorphosis. Development 118:977-988.
43. Kiss I, Bencze G, Fekete E, Fodor A, Gausz J, Maroy P, Szabad J, Szidonya J. 1976. Isolation and characterization of X-linked lethal mutants affecting differentiation of the imaginal discs in Drosophila melanogaster. Theoret Appl Genet 48:217-226.
44. Kiss I, Beaton AH, Tardiff J, Fristrom D, Fristrom JW. 1988. Interactions and developmental effects of mutations in the Broad-Complex of Drosophila melanogaster. Genetics 118:247-259.
45. Koushika SP, Soller M, White K. 2000. The neuron-enriched splicing pattern of Drosophila erect wing is dependent on the presence of ELAV protein. Mol Cell Biol 20:1836-1845.
46. Kraft R, Levine RB, Restifo LL. 1998. The steroid hormone 20- hydroxyecdysone enhances neurite growth of Drosophila mushroom body neurons isolated during metamorphosis. J Neurosci 18:8886-8899.
47. Kraft R, Escobar MM, Narro ML, Kurtis JL, Efrat A, Barnard K, Restifo LL. 2006. Phenotypes of Drosophila brain neurons in primary culture reveal a role for fascin in neurite shape and trajectory. J Neurosci 26:8734-8747.
48. Kucharova-Mahmood S, Raska I, Mechler BM, Farkas R. 2002. Temporal regulation of Drosophila salivary gland degeneration by the Broad- Complex transcription factors. J Struct Biol 140:67-78.
49. Laissue PP, Reiter C, Hiesinger PR, Halter S, Fischbach KF, Stocker RF. 1999. Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J Comp Neurol 405:543-552.
50. Lane NJ, Swales LS. 1978. Changes in the blood-brain barrier of the central nervous system in the blowfly during development, with special reference to the formation and disaggregation of gap and tight junctions. I. Larval development. Dev Biol 62:389-414.
51. Lee BP, Jones BW. 2005. Transcriptional regulation of the Drosophila glial gene repo. Mech Dev 122:849-862.
52. Lee T, Marticke S, Sung C, Robinow S, Luo L. 2000. Cell-autonomous requirement of the USP/EcR-B ecdysone receptor for mushroom body neuronal remodeling in Drosophila. Neuron 28:807-818.
53. Li TR, White KP. 2003. Tissue-specific gene expression and ecdysone-regulated genomic networks in Drosophila. Dev Cell 5:59-72.
54. Lisbin MJ, Qiu J, White K. 2001. The neuron-specific RNA-binding protein ELAV regulates neuroglian alternative splicing in neurons and binds directly to its pre-mRNA. Genes Dev 15:2546-2561.
55. Liu E, Restifo LL. 1998. Identification of a Broad Complex-regulated enhancer in the developing visual system of Drosophila. J Neurobiol 34:253-270.
56. Lorincz A, Nusser Z. 2008. Specificity of immunoreactions: the importance of testing specificity in each method. J Neurosci 28:9083-9086.
57. Maurange C, Gould AP. 2005. Brainy but not too brainy: starting and stopping neuroblast divisions in Drosophila. Trends Neurosci 28:30-36.
58. Maurange C, Cheng L, Gould AP. 2008. Temporal transcription factors and their targets schedule the end of neural proliferation in Drosophila. Cell 133:891-902.
59. Meinertzhagen IA, Hanson TE. 1993. The development of the optic lobe. In: Bate M, Martinez Arias A, editors. The development of Drosophila melanogaster. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. p 1363-1491.
60. Mugat B, Brodu V, Kejzlarova-Lepesant J, Antoniewski C, Bayer CA, Fristrom JW, Lepesant JA. 2000. Dynamic expression of Broad- Complex isoforms mediates temporal control of an ecdysteroid target gene at the onset of Drosophila metamorphosis. Dev Biol 227:104-117.
61. Mutch SA, Fujimoto BS, Kuyper CL, Kuo JS, Bajjalieh SM, Chiu DT. 2007. Deconvolving single-molecule intensity distributions for quantitative microscopy measurements. Biophys J 92:2926-2943.
62. Ohta T. 2003. Evolution by gene duplication revisited: differentiation of regulatory elements versus proteins. Genetica 118:209-216.
63. Oland LA, Tolbert LP. 2003. Key interactions between neurons and glial cells during neural development in insects. Annu Rev Entomol 48:89-110.
64. Parker RJ, Auld VJ. 2006. Roles of glia in the Drosophila nervous system. Semin Cell Dev Biol 17:66-77.
65. Pawley J. 2000. The 39 steps: a cautionary tale of quantitative 3-D fluorescence microscopy. Biotechniques 28:884-886, 888.
66. Pereanu W, Shy D, Hartenstein V. 2005. Morphogenesis and proliferation of the larval brain glia in Drosophila. Dev Biol 283:191-203.
67. Prokop A, Technau GM. 1994. BrdU incorporation reveals DNA replication in non dividing glial cells in the larval abdominal CNS of Drosophila. Roux's Arch Dev Biol 204:54-61.
68. Restifo LL, Hauglum W. 1998. Parallel molecular genetic pathways operate during CNS metamorphosis in Drosophila. Mol Cell Neurosci 11:134-148.
69. Restifo LL, Merrill VKL. 1994. Two Drosophila regulatory genes, Deformed and the Broad-Complex, share common functions in development of adult CNS, head, and salivary glands. Dev Biol 162:465-485.
70. Restifo LL, White K. 1991. Mutations in a steroid hormone-regulated gene disrupt the metamorphosis of the central nervous system in Drosophila. Dev Biol 148:174-194.
71. Restifo LL, White K. 1992. Mutations in a steroid hormone-regulated gene disrupt the metamorphosis of internal tissues in Drosophila: salivary glands, muscle, and gut. Roux's Arch Dev Biol 201:221-234.
72. Restifo LL, Wilson TG. 1998. A juvenile hormone agonist reveals distinct developmental pathways mediated by ecdysone-inducible Broad Complex transcription factors. Dev Genet 22:141-159.
73. Restifo LL, Estes PS, DelloRusso C. 1995. Genetics of ecdysteroid-regulated central nervous system metamorphosis in Drosophila. Eur J Entomol 92:169-187.
74. Riddiford LM. 1993. Hormones and Drosophila development. In: Bate M, Martinez Arias A, editors. The development of Drosophila melanogaster. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. p 899-939.
75. Robinow S, White K. 1988. The locus elav of Drosophila melanogaster is expressed in neurons at all developmental stages. Dev Biol 126:294-303.
76. Robinow S, White K. 1991. Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. J Neurobiol 22:443-461.
77. Sandstrom DJ, Bayer CA, Fristrom JW, Restifo LL. 1997. Broad-Complex transcription factors regulate thoracic muscle attachment in Drosophila. Dev Biol 181:168-185.
78. Saper CB, Sawchenko PE. 2003. Magic peptides, magic antibodies: guidelines for appropriate controls for immunohistochemistry. J Comp Neurol 465:161-163.
79. Selleck SB, Steller H. 1991. The influence of retinal innervation on neurogenesis in the first optic ganglion of Drosophila. Neuron 6:83-99.
80. Simon A, 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.
81. 4-6 motifs important for ewg splicing regulation. Mol Cell Biol 25:7580-7591.
82. Spokony RF, Restifo LL. 2007. Anciently duplicated Broad Complex exons have distinct temporal functions during tissue morphogenesis. Dev Genes Evol 217:499-513.
83. Strigini M, Cantera R, Morin X, Bastiani MJ, Bate M, Karagogeos D. 2006. The IgLON protein Lachesin is required for the blood-brain barrier in Drosophila. Mol Cell Neurosci 32:91-101.
84. Tissot M, Stocker RF. 2000. Metamorphosis in Drosophila and other insects: the fate of neurons throughout the stages. Prog Neurobiol 62:89-111.
85. Truman JW, Bate M. 1988. Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev Biol 125:145-157.
86. Urbach R, Technau GM. 2004. Neuroblast formation and patterning during early brain development in Drosophila. Bioessays 26:739-751.
87. von Kalm L, Crossgrove K, Von Seggern D, Guild GM, Beckendorf SK. 1994. The Broad-Complex directly controls a tissue-specific response to the steroid hormone ecdysone at the onset of Drosophila metamorphosis. EMBO J 13:3505-3516.
88. Wagh DA, Rasse TM, Asan E, Hofbauer A, Schwenkert I, Durrbeck H, Buchner S, Dabauvalle MC, Schmidt M, Qin G, Wichmann C, Kittel R, Sigrist SJ, Buchner E. 2006. Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49:833-844.
89. Ward EJ, Berg CA. 2004. Juxtaposition between two cell types is necessary for dorsal appendage tube formation. Mech Dev 122:241-255.
90. White K, Kankel DR. 1978. Patterns of cell division and cell movement in the formation of the imaginal nervous system in Drosophila melanogaster. Dev Biol 65:296-321.
91. White KP, Rifkin SA, Hurban P, Hogness DS. 1999. Microarray analysis of Drosophila development during metamorphosis. Science 286:2179-2184.
92. Williams DW, Truman JW. 2005. Remodeling dendrites during insect metamorphosis. J Neurobiol 64:24-33.
93. Wilson TG, Yerushalmi Y, Donnell DM, Restifo LL. 2006. Interaction between hormonal signaling pathways in Drosophila melanogaster as revealed by genetic interaction between Methoprene-tolerant and Broad-Complex. Genetics 172:253-264.
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. Yannoni YM, White K. 1999. Domains necessary for Drosophila ELAV nuclear localization: function requires nuclear ELAV. J Cell Sci 112: 4501-4512.
96. Yao TP, Segraves WA, Oro AE, McKeown M, Evans RM. 1992. Drosophila ultraspiracle modulates ecdysone receptor function via heterodimer formation. Cell 71:63-72.
97. Yoshida S, Soustelle L, Giangrande A, Umetsu D, Murakami S, Yasugi T, Awasaki T, Ito K, Sato M, Tabata T. 2005. DPP signaling controls development of the lamina glia required for retinal axon targeting in the visual system of Drosophila. Development 132:4587-4598.
98. Yuasa Y, Okabe M, Yoshikawa S, Tabuchi K, Xiong W-C, Hiromi Y, Okana H. 2003. Drosophila homeodomain protein REPO controls glial differentiation by cooperating with ETS and BTB transcription factors. Development 130:2419-2428.
99. Zhou X, Riddiford LM. 2002. Broad specifies pupal development and mediates the 'status quo' action of juvenile hormone on the pupal-adult transformation in Drosophila and Manduca. Development 129: 2259-2269.
100. Zhou X, Zhou B, Truman JW, Riddiford LM. 2004. Overexpression of broad: a new insight into its role in the Drosophila prothoracic gland cells. J Exp Biol 207:1151-1161.
101. Zollman S, Godt D, Privé GG, Couderc J-L, Laski FA. 1994. The BTB domain, found primarily in zinc-finger proteins, defines an evolutionarily conserved family that includes several developmentally regulated genes in Drosophila. Proc Natl Acad Sci U S A 91:10717-10721.