Single-cell mapping of neural and glial gene expression in the developing Drosophila CNS midline cells

Developmental Biology

Volumn 294, Issue 2, 2006, Pages 509-524

  Wheeler, Scott R ^a   Kearney, Joseph B ^a   Guardiola, Amaris R ^a   Crews, Stephen T ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

CNS; Drosophila; Glia; Mesectoderm; Midline cells; Neurogenesis; Neurons

Indexed keywords

ENZYME; NEUROTRANSMITTER; NEUROTRANSMITTER RECEPTOR; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CELL FATE; CELL MATURATION; CELL TYPE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DROSOPHILA; GENE EXPRESSION; GENE MAPPING; GENETIC ANALYSIS; GLIA CELL; IMAGING; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION;

EID: 33744974975     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2006.03.016     Document Type: Article

References (56)

1. Ashraf S.I., and Ip Y.T. The Snail protein family regulates neuroblast expression of inscuteable and string, genes involved in asymmetry and cell division in Drosophila. Development 128 (2001) 4757-4767
2. Bergmann A., Tugentman M., Shilo B.Z., and Steller H. Regulation of cell number by MAPK-dependent control of apoptosis: a mechanism for trophic survival signaling. Dev. Cell 2 (2002) 159-170
3. Bhat K.M. Segment polarity genes in neuroblast formation and identity specification during Drosophila neurogenesis. Bioessays 21 (1999) 472-485
4. Blackshaw S., Harpavat S., Trimarchi J., Cai L., Huang H., Kuo W.P., Weber G., Lee K., Fraioli R.E., Cho S.H., Yung R., Asch E., Ohno-Machado L., Wong W.H., and Cepko C.L. Genomic analysis of mouse retinal development. PLoS Biol. 2 (2004) E247
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., and Technau G.M. The fate of the CNS midline progenitors in Drosophila as revealed by a new method for single cell labelling. Development 120 (1994) 1895-1906
7. Budnik V., and White K. Catecholamine-containing neurons in Drosophila melanogaster: distribution and development. J. Comp. Neurol. 268 (1988) 400-413
8. Cai Y., Chia W., and Yang X. A family of snail-related zinc finger proteins regulates two distinct and parallel mechanisms that mediate Drosophila neuroblast asymmetric divisions. EMBO J. 20 (2001) 1704-1714
9. Callahan C.A., and Thomas J.B. Tau-beta-galactosidase, an axon-targeted fusion protein. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 5972-5976
10. Campos-Ortega J.A., and Hartenstein V. The Embryonic Development of Drosophila melanogaster (1997), Springer Verlag, Berlin
11. Chu-LaGraff Q., and Doe C.Q. Neuroblast specification and formation regulated by wingless in the Drosophila CNS. Science 261 (1993) 1594-1597
12. Cinar H., Keles S., and Jin Y. Expression profiling of GABAergic motor neurons in Caenorhabditis elegans. Curr. Biol. 15 (2005) 340-346
13. Crews S.T. Drosophila bHLH-PAS developmental regulatory proteins. In: Crews S.T. (Ed). PAS Proteins: Regulators and Sensors of Development and Physiology (2003), Kluwer
14. Daniels R.W., Collins C.A., Gelfand M.V., Dant J., Brooks E.S., Krantz D.E., and DiAntonio A. 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
15. Dong R., and Jacobs J.R. Origin and differentiation of supernumerary midline glia in Drosophila embryos deficient for apoptosis. Dev. Biol. 190 (1997) 165-177
16. Freeman M.R., Delrow J., Kim J., Johnson E., and Doe C.Q. Unwrapping glial biology: Gcm target genes regulating glial development, diversification, and function. Neuron 38 (2003) 567-580
17. Friggi-Grelin F., Coulom H., Meller M., Gomez D., Hirsh J., and Birman S. Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. J. Neurobiol. 54 (2003) 618-627
18. Goodman C.S. Embryonic development of identified neurons in the grasshopper. In: Spitzer N.C. (Ed). Neuronal Development (1982), Plenum 171-212
19. Gray P.A., Fu H., Luo P., Zhao Q., Yu J., Ferrari A., Tenzen T., Yuk D.I., Tsung E.F., Cai Z., Alberta J.A., Cheng L.P., Liu Y., Stenman J.M., Valerius M.T., Billings N., Kim H.A., Greenberg M.E., McMahon A.P., Rowitch D.H., Stiles C.D., and Ma Q. Mouse brain organization revealed through direct genome-scale TF expression analysis. Science 306 (2004) 2255-2257
20. Greer C.L., Grygoruk A., Patton D.E., Ley B., Romero-Calderon R., Chang H.Y., Houshyar R., Bainton R.J., Diantonio A., and Krantz D.E. A splice variant of the Drosophila vesicular monoamine transporter contains a conserved trafficking domain and functions in the storage of dopamine, serotonin, and octopamine. J. Neurobiol (2005)
21. Hummel T., Schimmelpfeng K., and Klambt C. Commissure formation in the embryonic CNS of Drosophila: I. Identification of the required gene functions. Dev. Biol. 209 (1999) 381-398
22. 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
23. Jacobs J.R. The midline glia of Drosophila: a molecular genetic model for the developmental functions of glia. Prog. Neurobiol. 62 (2000) 475-508
24. Jacobs J.R., and Goodman C.S. Embryonic development of axon pathways in the Drosophila CNS: II. Behavior of pioneer growth cones. J. Neurosci. 9 (1989) 2412-2422
25. Jia X.X., and Siegler M.V. Midline lineages in grasshopper produce neuronal siblings with asymmetric expression of Engrailed. Development 129 (2002) 5181-5193
26. Kambadur R., Koizumi K., Stivers C., Nagle J., Poole S.J., and Odenwald W.F. Regulation of POU genes by castor and hunchback establishes layered compartments in the Drosophila CNS. Genes Dev. 12 (1998) 246-260
27. Kearney J.B., Wheeler S.R., Estes P., Parente B., and Crews S.T. Gene expression profiling of the developing Drosophila CNS midline cells. Dev. Biol. 275 (2004) 473-492
28. Klämbt C., Jacobs J.R., and Goodman C.S. 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 (1991) 801-815
29. Kosman D., Small S., and Reinitz J. Rapid preparation of a panel of polyclonal antibodies to Drosophila segmentation proteins. Dev. Genes Evol. 208 (1998) 290-294
30. 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
31. Landgraf M., Sanchez-Soriano N., Technau G.M., Urban J., and Prokop A. Charting the Drosophila neuropile: a strategy for the standardised characterisation of genetically amenable neurites. Dev. Biol. 260 (2003) 207-225
32. 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
33. Mesce K.A., DeLorme A.W., Brelje T.C., and Klukas K.A. Dopamine-synthesizing neurons include the putative H-cell homologue in the moth Manduca sexta. J. Comp. Neurol. 430 (2001) 501-517
34. Miguel-Aliaga I., and Thor S. Segment-specific prevention of pioneer neuron apoptosis by cell-autonomous, postmitotic Hox gene activity. Development 131 (2004) 6093-6105
35. Nambu J.R., Lewis J.L., Wharton K.A., and Crews S.T. The Drosophila single-minded gene encodes a helix-loop-helix protein which acts as a master regulator of CNS midline development. Cell 67 (1991) 1157-1167
36. Neckameyer W.S., and White K. Drosophila tyrosine hydroxylase is encoded by the pale locus. J. Neurogenet. 8 (1993) 189-199
37. Nusslein-Volhard C., and Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature 287 (1980) 795-801
38. O'Connor-Giles K.M., and Skeath J.B. Numb inhibits membrane localization of Sanpodo, a four-pass transmembrane protein, to promote asymmetric divisions in Drosophila. Dev. Cell 5 (2003) 231-243
39. Patel N.H., Marin-Blanco E., Coleman K.G., Poole S.J., Ellis M.C., Kornberg T.B., and Goodman C.S. Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58 (1989) 955-968
40. Patel N.H., Schafer B., Goodman C.S., and Holmgren R. The role of segment polarity genes during Drosophila neurogenesis. Genes Dev. 3 (1989) 890-904
41. Pearson B.J., and Doe C.Q. Specification of temporal identity in the developing nervous system. Annu. Rev. Cell Dev. Biol. 20 (2004) 619-647
42. Plautz J.D., Kaneko M., Hall J.C., and Kay S.A. Independent photoreceptive circadian clocks throughout Drosophila. Science 278 (1997) 1632-1635
43. Reeves N., and Posakony J.W. Genetic programs activated by proneural proteins in the developing Drosophila PNS. Dev. Cell 8 (2005) 413-425
44. Renn S.C., Park J.H., Rosbash M., Hall J.C., and Taghert P.H. A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99 (1999) 791-802
45. Robinow S., and White K. Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. J. Neurobiol. 22 (1991) 443-461
46. Schmid A., Chiba A., and Doe C.Q. Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development 126 (1999) 4653-4689
47. Siegler M.V., and Jia X.X. Engrailed negatively regulates the expression of cell adhesion molecules connectin and neuroglian in embryonic Drosophila nervous system. Neuron 22 (1999) 265-276
48. Sink H., and Whitington P.M. Location and connectivity of abdominal motoneurons in the embryo and larva of Drosophila melanogaster. J. Neurobiol. 22 (1991) 298-311
49. Skeath J.B., and Thor S. Genetic control of Drosophila nerve cord development. Curr. Opin. Neurobiol. 13 (2003) 8-15
50. Skeath J.B., Zhang Y., Holmgren R., Carroll S.B., and Doe C.Q. Specification of neuroblast identity in the Drosophila embryonic central nervous system by gooseberry-distal. Nature 376 (1995) 427-430
51. Spana E.P., and Doe C.Q. The prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila. Development 121 (1995) 3187-3195
52. Spana E.P., Kopczynski C., Goodman C.S., and Doe C.Q. Asymmetric localization of numb autonomously determines sibling neuron identity in the Drosophila CNS. Development 121 (1995) 3489-3494
53. Stapleton M., Liao G., Brokstein P., Hong L., Carninci P., Shiraki T., Hayashizaki Y., Champe M., Pacleb J., Wan K., Yu C., Carlson J., George R., Celniker S., and Rubin G.M. The Drosophila gene collection: identification of putative full-length cDNAs for 70% of D. melanogaster genes. Genome Res. 12 (2002) 1294-1300
54. Ward M.P., Mosher J.T., and Crews S.T. Regulation of Drosophila bHLH-PAS protein cellular localization during embryogenesis. Development 125 (1998) 1599-1608
55. Wenick A.S., and Hobert O. Genomic cis-regulatory architecture and trans-acting regulators of a single interneuron-specific gene battery in C. elegans. Dev. Cell 6 (2004) 757-770
56. Xiao H., Hrdlicka L.A., and Nambu J.R. Alternate function of the single-minded and rhomboid genes in development of the Drosophila ventral neuroectoderm. Mech. Dev. 58 (1996) 65-74