Neuromancer1 and Neuromancer2 regulate cell fate specification in the developing embryonic CNS of Drosophila melanogaster

Developmental Biology

Volumn 325, Issue 1, 2009, Pages 138-150

  Leal, S M ^a   Qian, L ^b   Lacin, H ^a   Bodmer, R ^c   Skeath, J B ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GLADSTONE INSTITUTES   (United States)

^c BURNHAM INSTITUTE   (United States)

Author keywords

CNS development; Even skipped; Neuroblast lineage; Neuromancer1 2; T box transcription factors

Indexed keywords

T BOX TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NEUROMANCER1; TRANSCRIPTION FACTOR NEUROMANCER2; UNCLASSIFIED DRUG;

ARTICLE; CELL FATE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

DROSOPHILA MELANOGASTER; INVERTEBRATA; VERTEBRATA;

EID: 57849112703     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2008.10.006     Document Type: Article

References (85)

1. Adell T., and Muller W.E. Expression pattern of the Brachyury and Tbx2 homologues from the sponge Suberites domuncula. Biol. Cell 97 (2005) 641-650
2. Ahn D.G., Ruvinsky I., Oates A.C., et al. tbx20, a new vertebrate T-box gene expressed in the cranial motor neurons and developing cardiovascular structures in zebrafish. Mech. Dev. 95 (2000) 253-258
3. Alexandre C., Lecourtois M., and Vincent J. Wingless and Hedgehog pattern Drosophila denticle belts by regulating the production of short-range signals. Development 126 (1999) 689-698
4. Basson C.T., Huang T., Lin R.C., et al. Different TBX5 interactions in heart and limb defined by Holt-Oram syndrome mutations. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 2919-2924
5. Bossing T., and Brand A.H. Determination of cell fate along the anteroposterior axis of the Drosophila ventral midline. Development 133 (2006) 1001-1012
6. Bossing T., Udolph G., Doe C.Q., and Technau G.M. The embryonic central nervous system lineages of Drosophila melanogaster I. Neuroblast lineages derived from the ventral half of the neuroectoderm. Dev. Biol. 179 (1996) 41-64
7. Brand A.H., and Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118 (1993) 401-415
8. Broihier H.T., and Skeath J.B. Drosophila homeodomain protein dHb9 directs neuronal fate via crossrepressive and cell-nonautonomous mechanisms. Neuron 35 (2002) 39-50
9. Broihier H.T., Kuzin A., Zhu Y., et al. Drosophila homeodomain protein Nkx6 coordinates motoneuron subtype identity and axonogenesis. Development 131 (2004) 5233-5242
10. Brook W.J., and Cohen S.M. Antagonistic interactions between wingless and decapentaplegic responsible for dorsal-ventral pattern in the Drosophila leg. Science 273 (1996) 1373-1377
11. Brown D.D., Martz S.N., Binder O., et al. Tbx5 and Tbx20 act synergistically to control vertebrate heart morphogenesis. Development 132 (2005) 553-563
12. Buescher M., Svendsen P.C., Tio M., et al. Drosophila T box proteins break the symmetry of hedgehog-dependent activation of wingless. Curr. Biol. 14 (2004) 1694-1702
13. Buescher M., Tio M., Tear G., et al. Functions of the segment polarity genes midline and H15 in Drosophila melanogaster neurogenesis. Dev. Biol. 292 (2006) 418-429
14. Cai C.L., Zhou W., Yang L., et al. T-box genes coordinate regional rates of proliferation and regional specification during cardiogenesis. Development 132 (2005) 2475-2487
15. Cavener D.R. Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Res. 15 (1987) 1353-1361
16. Chapman D.L., and Papaioannou V.E. Three neural tubes in mouse embryos with mutations in the T-box gene. Nature 391 (1998) 695-697
17. Daniels R.W., Collins C.A., Gelfrand M.V., et al. Increased expression of the Drosophila vesicular glutamate transporter leads to excess glutamate release and a compensatory decrease in quantal content. J. Neurosci. 24 (2004) 10466-10474
18. Doe C.Q., Smouse D., and Goodman C.S. Control of neuronal fate by the Drosophila segmentation gene even-skipped. Nature 333 (1988) 376-378
19. Dufour H.D., Chettouh Z., Deyts C., et al. Precraniate origin of cranial motoneurons. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 8727-8732
20. Enright A.J., John B., Gaul U., Tuschl T., Sander C., and Marks D.S. MicroRNA targets in Drosophila. Genome Biol. 5 (2003) R1
21. Fong S.H., Emelyanov A., The C., and Korzh V. Wnt signaling mediated by Tbx2b regulates cell migration during the formation of the neural plate. Development 132 (2005) 3587-3596
22. Frasch M., Hoey T., Rushlow C., et al. Characterization and localization of the even-skipped protein of Drosophila. EMBO J. 16 (1987) 749-759
23. Gibson-Brown J.J., I Agulnik S., Silver L.M., and Papaioannou V.E. Expression of T-box genes Tbx2-Tbx5 during chick organogenesis. Mech. Dev. 74 (1998) 165-169
24. Grenningloh G., Rehm E.J., and Goodman C.S. Genetic analysis of growth cone guidance in Drosophila: fasciclin II functions as a neuronal recognition molecule. Cell 67 (1991) 45-57
25. Griffin K.J., Stoller J., Gibson M., Chen S., et al. A conserved role for H15-related T-box transcription factors in zebrafish and Drosophila heart formation. Dev. Biol. 218 (2000) 235-247
26. Halter D.A., Urban J., Rickert C., et al. The homeobox gene repo is required for the differentiation and maintenance of glia function in the embryonic nervous system of Drosophila melanogaster. Development 121 (1995) 317-322
27. Harrison D.A., and Perrimon N. Simple and efficient generation of marked clones in Drosophila. Curr. Biol. 3 (1993) 424-433
28. Herzig M.C., Thor S., Thomas J.B., et al. Expression and function of the LIM homeodomain protein Apterous during embryonic brain development of Drosophila. Dev. Genes Evol. 211 (2001) 545-554
29. Hortsch M., Patel N.H., Bieber A.J., et al. Drosophila neurotactin, a surface glycoprotein with homology to serine esterases, is dynamically expressed during embryogenesis. Development 110 (1990) 1327-1340
30. Isshiki T., Pearson B., Holbrook S., and Doe C.Q. Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 106 (2001) 511-521
31. Jackson F.R., Newby L.M., and Kulkarni S.J. Drosophila GABAergic systems: sequence and expression of glutamic acid decarboxylase. J. Neurochem. 54 (1990) 1068-1078
32. Jerome L.A., and Papaioannou V.E. DiGeorge syndrome phenotype in mice mutant for the T-box gene, Tbx1. Nat. Genet. 27 (2001) 286-291
33. King M., Arnold J.S., Shanske A., and Morrow B.E. T-genes and limb bud development. Am. J. Med. Genet. A 140 (2006) 1407-1413
34. Kulkarni S.J., Newby L.M., and Jackson F.R. Drosophila GABAergic systems. II. Mutational analysis of chromosomal segment 64AB, a region containing the glutamic acid decarboxylase gene. Mol. Gen. Genet. 243 (1994) 555-564
35. Kutach A.K., and Kadonaga J.T. The downstream promoter element DPE appears to be as widely used as the TATA box in Drosophila core promoters. Mol. Cell Biol. 20 (2000) 4754-4764
36. Kuzin A., Brody T., Moore A.W., and Odenwald W.F. Nerfin-1 is required for early axon guidance decisions in the developing Drosophila CNS. Dev. Biol. 277 (2005) 347-365
37. Kuzin A., Kundu M., Brody T., and Odenwald W.F. The Drosophila nerfin-1 mRNA requires multiple microRNAs to regulate its spatial and temporal translation dynamics in the developing nervous system. Dev. Biol. 310 (2007) 35-43
38. Lai Z.C., Rushton E., Bate M., and Rubin G.M. Loss of function of the Drosophila zfh-1 gene results in abnormal development of mesodermally derived tissues. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 4122-4126
39. Landgraf M., Bossing T., Technau G.M., and Bate M. The origin, location, and projections of the embryonic abdominal motorneurons of Drosophila. J. Neurosci. 17 (1997) 9642-9655
40. Landgraf M., Roy S., Prokop A., VijayRaghavan K., et al. Even-skipped determines the dorsal growth of motor axons in Drosophila. Neuron 22 (1999) 43-52
41. Larroux C., Fahey B., Liubicich D., et al. Developmental expression of transcription factor genes in a desmosponge: insights into the origin of metazoan multicellularity. Evol. Dev. 8 (2006) 150-173
42. Layden M.J., Odden J.P., Schmid A., et al. Zfh1, a somatic motor neuron transcription factor, regulates axon exit from the CNS. Dev. Biol. 291 (2006) 253-263
43. Li Q.y., Newbury-Ecob R.A., Terrett J.A., et al. Holt-Oram syndrome is caused by mutations in TBX5, a member of the Brachyury (T) gene family. Nat. Genet. 15 (1997) 21-29
44. Lilly B., Zhao B., Ranganayakulu G., et al. Requirement of MADS domain transcription factor D-MEF2 for muscle formation in Drosophila. Science 267 (1995) 688-693
45. Lin D.M., and Goodman C.S. Ectopic and increased expression of Fasciclin II alters motoneuron cone guidance. Neuron 13 (1994) 507-523
46. Lundell M.J., Lee H.K., Perez E., and Chadwell L. The regulation of apoptosis by Numb/Notch signaling in the serotonin lineage of Drosophila. Development 130 (2003) 4109-4121
47. Lundgren S.E., Callahan C.A., Thor S., and Thomas J.B. Control of neuronal pathway selection by the Drosophila LIM homeodomain gene apterous. Development 121 (1995) 1769-1773
48. Mardon G., Solomon N.M., and Rubin G.M. Dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila. Development 120 (1994) 3473-3486
49. Miguel-Aliaga I., Allan D.W., and Thor S. Independent roles of the dachshund and eyes absent genes in BMP signaling, axon pathfinding and neuronal specification. Development 131 (2004) 5837-5848
50. Miskolczi-McCallum C.M., Scavetta R.J., Svendsen P.C., et al. The Drosophila melanogaster T-box genes midline and H15 are conserved regulators of heart development. Dev. Biol. 278 (2005) 459-472
51. Naiche L.A., Harrelson Z., Kelly R.G., and Papaioannou V.E. T-box genes in vertebrate development. Annu. Rev. Genet. 39 (2005) 219-239
52. Nordstrom U., Maier E., Jessell T.M., and Edlund T. An early role for WNT signaling in specifying neural patterns of Cdx and Hox gene expression and motor neuron subtype identity. PLoS Biol. 4 (2006) e252
53. Novotny T., Eiselt R., and Urban J. Hunchback is required for the specification of the early sublineage of neuroblast 7-3 in the Drosophila central nervous system. Development 129 (2002) 1027-1036
54. Nusslein-Volhard C., Wieschaus E., and Kluding H. Zygotic loci on the second chromosome. Roux Arch. Dev. Biol. 193 (1984) 267-282
55. Nusslein-Volhard C., Kluding H., and Jurgens G. Genes affecting the segmental subdivision of the Drosophila embryo. Cold Spring Harbor Symp. Quant. Biol. 50 (1985) 145-154
56. Papaioannou V.E., and Silver L.M. The T-box gene family. Bioessays 20 (1998) 9-19
57. Patel N.H. Imaging neuronal subsets and other cell types in whole mount Drosophila embryos and larvae using antibody probes. In: Goldstein L.S.B., and Fyrberg E. (Eds). Methods in Cell Biology. Drosophila melanogaster: Practical Uses in Cell Biology Vol 44 (1994), Academic Press, New York
58. Patel N.H., Kornberg T.B., and Goodman C.S. Expression of Engrailed during segmentation in grasshopper and crayfish. Development 107 (1989) 210-212
59. Plageman Jr. T.F., and Yutzey K.E. Differential expression and function of Tbx5 and Tbx20 in cardiac development. J. Biol. Chem. 279 (2004) 19026-19034
60. Poeck B., Hofbauer A., and Pflugfelder G.O. Expression of the Drosophila optomotor-blind gene transcript in neuronal and glial cells of the developing nervous system. Development 117 (1993) 1017-1029
61. Prince V.E., and Pickett F.B. Splitting pairs: the diverging fates of duplicated genes. Nat. Rev. Genet. 11 (2002) 827-837
62. Qian L., Liu J., and Bodmer R. Neuromancer TBX20-related genes (H15/midline) promote cell fate specification and morphogenesis of the Drosophila heart. Dev. Biol. 279 (2005) 509-524
63. Reim I., and Frasch M. The Dorsocross T-box genes are key components of the regulatory network controlling early cardiogenesis in Drosophila. Development 132 (2005) 4911-4925
64. Reim I., Mohler J.P., and Frasch M. Tbx20-related genes, mid and H15, are required for tinman expression, proper patterning, and normal differentiation of cardioblasts in Drosophila. Mech. Dev. 122 (2005) 1056-1069
65. Schmidt H., Rickert C., Bossing T., et al. The embryonic central nervous system lineages of Drosophila melanogaster II. Neuroblast lineages derived from the dorsal part of the neuroectoderm. Dev. Biol. 189 (1997) 186-204
66. Schmid A., Chiba A., and Doe C.Q. Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections, and muscle targets. Development 128 (1999) 4653-4689
67. Seeger M., Tear G., Ferres-Marco D., and Goodman C.S. Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward or away from the midline. Neuron 10 (1993) 409-426
68. Showell C., Binder O., and Conlon F.L. T-box genes in early embryogenesis. Dev. Dyn. 229 (2004) 201-218
69. Showell C., Christine K.S., Mandel E.M., and Conlon F.L. Developmental expression patterns of Tbx1, Tbx2, Tbx5, and Tbx20 in Xenopus tropicalis. Dev. Dyn. 235 (2006) 1623-1630
70. Singer J.B., Harbecke R., Kusch T., et al. Drosophila brachyenteron regulates gene activity and morphogenesis in the gut. Development 122 (1996) 3707-3718
71. Singh M.K., Christoffels V.M., Dias J.M., et al. Tbx20 is essential for cardiac chamber differentiation and repression of Tbx2. Development 132 (2005) 2697-2707
72. Sink H., and Whitington P.M. Pathfinding in the central nervous system and periphery by identified embryonic Drosophila motor neurons. Development 112 (1991) 307-316
73. Skeath J.B., and Doe C.Q. Sanpodo and Notch act in opposition to Numb to distinguish sibling fates in the Drosophila CNS. Development 125 (1998) 1857-1865
74. Song M.R., Shirasaki R., Cai C.L., et al. T-box transcription factor Tbx20 regulates a genetic program for cranial motor neuron cell body migration. Development 133 (2006) 4945-4955
75. Stark A., Brennecke J., Russell R.B., and Cohen S.M. Identification of Drosophila MicroRNA targets. PLoS Biol. 1 3 (2003) E60 Epub
76. Stennard F.A., and Harvey R.P. T-box transcription factors and their roles in regulatory hierarchies in the developing heart. Development 132 (2005) 4897-4910
77. Stennard F.A., Costa M.W., Elliot D.A., et al. Cardiac T-box factor Tbx20 directly interacts with Nkx2-5, GATA4, and GATA5 in regulation of gene expression in the developing heart. Dev. Biol. 262 (2003) 206-224
78. Stennard F.A., Costa M.W., Lai D., et al. Murine T-box transcription factor Tbx20 acts as a repressor during heart development, and is essential for adult integrity, function, and adaptation. Development 132 (2005) 2451-2462
79. Szeto D.P., Griffin K.J., and Kimelman D. Hrt is required for cardiovascular development in zebrafish. Development 129 (2002) 5093-5101
80. Taghert P.H., and Goodman C.S. Cell determination and differentiation of identified serotonin-immunoreactive neurons in the grasshopper embryo. J. Neurosci. 4 (1984) 989-1000
81. Takeuchi J.K., Mileikovskaia M., Koshiba-Takeuchi K., et al. Tbx20 dose-dependently regulates transcription factor networks required for mouse heart and motoneuron development. Development 132 (2005) 2463-2474
82. Tautz D., and Pfeifle C. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98 (1989) 81-85
83. Walters J.W., Muñoz C., Paaby A.B., and Dinardo S. Serrate-Notch signaling defines the scope of the initial denticle field by modulating EGFR activation. Dev. Biol. 286 (2005) 415-426
84. Woollard A. Gene duplications and genetic redundancy in C. elegans (June 25, 2005), WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.2.1, http://www.wormbook.org.
85. Woollard A., and Hodgkin J. The Caenorhabditis elegans fate-determining gene mab9 encodes a T-box protein required to pattern the posterior hindgut. Gene Dev. 14 (2000) 596-603