Molecular markers for identified neuroblasts in the developing brain of Drosophila

Development

Volumn 130, Issue 16, 2003, Pages 3621-3637

  Urbach, Rolf ^a   Technau, Gerhard M ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Brain development; CNS; Drosophila; Gap genes; Molecular markers; Neuroblasts

Indexed keywords

FASCICLIN II; MOLECULAR MARKER;

ANIMAL CELL; BRAIN DEVELOPMENT; BRAIN REGION; CELL FATE; CELL POPULATION; CELL SPECIFICITY; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CRANIAL NERVE; DATA ANALYSIS; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EYE DEVELOPMENT; GENE EXPRESSION; GENETIC LINKAGE; HOMEOBOX; MARKER GENE; NERVE CORD; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NEUROECTODERM; NEUROMERE; NONHUMAN; PRIORITY JOURNAL; REVIEW; STEM CELL;

ANIMALS; BIOLOGICAL MARKERS; BRAIN; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MORPHOGENESIS; NEURONS; NUCLEAR PROTEINS; TRANS-ACTIVATORS;

ANIMALIA; CASTOR; INSECTA;

EID: 0042536462     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00533     Document Type: Review

References (81)

1. Bhat, K. M. (1999). Segment polarity genes in neuroblast formation and identity specification during Drosophila neurogenesis. BioEssays 21, 472-485.
2. Bhat, K. M., van Beers, E. H. and Bhat, P. (2000). Sloppy paired acts as the downstream target of wingless in the Drosophila CNS and interaction between sloppy paired and gooseberry inhibits sloppy paired during neurogenesis. Development 127, 655-665.
3. Bier, E., Vaessin, H., Younger-Shepherd, S., Jan, L. Y. and Jan, Y. N. (1992). deadpan, an essential pan-neural gene in Drosophila, encodes a helix- loop-helix protein similar to the hairy gene product. Genes Dev. 6, 2137-2151.
4. Bossing, T., Udolph, G., Doe, C. Q. and Technau, G. M. (1996). 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.
5. Brand, M., Jarman, A. P., Jan, L. Y. and Jan, Y. N. (1993). asense is a Drosophila neural precursor gene and is capable of initiating sense organ formation. Development 119, 1-17.
6. Broadus, J., Skeath, J. B., Spana, E. P., Bossing, T., Technau, G. M. and Doe, C. Q. (1995). New neuroblast markers and the origin of the aCC/pCC neurons in the Drosophila central nervous system. Mech. Dev. 53, 393-402.
7. Brody, T. and Odenwald, W. F. (2000). Programmed transformations in neuroblast gene expression during Drosophila CNS lineage development. Dev. Biol. 226, 34-44.
8. Brönner, G. and Jäckle, H. (1991). Control and function of terminal gap gene activity in the posterior pole region of the Drosophila embryo. Mech. Dev. 35, 205-211.
9. Cadigan, K. M., Grossniklaus, U. and Gehring, W. J. (1994a). Functional redundancy: the respective roles of the two sloppy paired genes in Drosophila segmentation. Proc. Natl. Acad. Sci. USA 91, 6324-6328.
10. Cadigan, K. M., Grossniklaus, U. and Gehring, W. J. (1994b). Localized expression of sloppy paired protein maintains the polarity of Drosophila parasegments. Genes Dev. 8, 899-913.
11. Campos-Ortega, J. A. and Hartenstein, V. (1997). The Embryonic Development of Drosophila melanogaster. Berlin, Heidelberg, New York: Springer Verlag.
12. Chiang, C., Young, K. E. and Beachy, P. A. (1995). Control of Drosophila tracheal branching by the novel homeodomain gene unplugged, a regulatory target for genes of the bithorax complex. Development 121, 3901-3912.
13. Cribbs, D. L., Pultz, M. A., Johnson, D., Mazzulla, M. and Kaufman, T. C. (1992). Structural complexity and evolutionary conservation of the Drosophila homeotic gene proboscipedia. EMBO J. 11, 1437-1449.
14. Cui, X. and Doe, C. Q. (1992). ming is expressed in neuroblast sublineages and regulates gene expression in the Drosophila central nervous system. Development 116, 943-952.
15. Cui, X. and Doe, C. Q. (1995). The role of the cell cycle and cytokinesis in regulating neuroblast sublineage gene expression in the Drosophila CNS. Development 121, 3233-3243.
16. Czerny, T., Halder, G., Kloter, U., Souabni, A., Gehring, W. J. and Busslinger, M. (1999). twin of eyeless, a second Pax-6 gene of Drosophila, acts upstream of eyeless in the control of eye development. Mol. Cell 3, 297-307.
17. Dalton, D., Chadwick, R. and McGinnis, W. (1989). Expression and embryonic function of empty spiracles: a Drosophila homeo box gene with two patterning functions on the anterior-posterior axis of the embryo. Genes Dev. 3, 1940-1956.
18. Dick, T., Yang, X., Yeo, S. and Chia, W. (1991). Two closely linked Drosophila POU domain genes are expressed in neuroblasts and sensory elements. Proc. Natl. Acad. Sci. USA 88, 7645-7649.
19. Diederich, R. J., Merrill, V., Pultz, M. A. and Kaufman, T. C. (1989). Isolation, structure, and expression of labial, a homeotic gene of the Antennapedia-Complex involved in Drosophila head development. Genes Dev. 3, 399-414.
20. Diederich, R. J., Pattatucci, A. M. and Kaufman, T. C. (1991). Developmental and evolutionary implications of labial, Deformed and engrailed expression in the Drosophila head. Development 113, 273-281.
21. Doe, C. Q. (1992). Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila central nervous system. Development 116, 855-863.
22. Doe, C. Q. and Technau, G. M. (1993). Identification and cell lineage of individual neural precursors in the Drosophila CNS. Trends Neurosci. 16, 510-514.
23. Dormand, E. L. and Brand, A. H. (1998). Runt determines cell fates in the Drosophila embryonic CNS. Development 125, 1659-1667.
24. Finkelstein, R. and Perrimon, N. (1990). The orthodenticle gene is regulated by bicoid and torso and specifies Drosophila head development. Nature 346, 485-488.
25. Gao, Q., Wang, Y. and Finkelstein, R. (1996). Orthodenticle regulation during embryonic head development in Drosophila. Mech. Dev. 56, 3-15.
26. Garcia-Alonso, L., VanBerkum, M. F., Grenningloh, G., Schuster, C. and Goodman, C. S. (1995). Fasciclin II controls proneural gene expression in Drosophila. Proc. Natl. Acad. Sci. USA 92, 10501-10505.
27. Gergen, J. P. and Butler, B. A. (1988). Isolation of the Drosophila segmentation gene runt and analysis of its expression during embryogenesis. Genes Dev. 2, 1179-1193.
28. Gorman, M. J. and Kaufman, T. C. (1995). Genetic analysis of embryonic cis-acting regulatory elements of the Drosophila homeotic gene sex combs reduced. Genetics 140, 557-572.
29. Grenningloh, G., Rehm, E. J. and Goodman, C. S. (1991). Genetic analysis of growth cone guidance in Drosophila: Fasciclin II functions as a neuronal recognition molecule. Cell 57, 45-57.
30. Grossniklaus, U., Pearson, R. K. and Gehring, W. (1992). The Drosophila sloppy paired locus encodes two proteins involved in segmentation that show homology to mammalian transcription factors. Genes Dev. 6, 1030-1051.
31. Grossniklaus, U., Cadigan, K. M. and Gehring, W. J. (1994). Three maternal coordinate systems cooperate in the patterning of the Drosophila head. Development 120, 3155-3171.
32. Halder, G., Callaerts, P. and Gehring, W. J. (1995). Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267, 1788-1792.
33. Hama, C., Ali, Z. and Kornberg, T. B. (1990). Region-specific recombination and expression are directed by portions of the Drosophila engrailed promoter. Genes Dev. 4, 1079-1093.
34. Hartenstein, V. and Campos-Ortega, J. A. (1984). Early neurogenesis in wild-type Drosophila melanogaster. Roux's Arch. Dev. Biol. 193, 308-325.
35. Hartmann, B., Hirth, F., Walldorf, U. and Reichert, H. (2000). Expression, regulation and function of the homeobox gene empty spiracles in brain and ventral nerve cord development of Drosophila. Mech. Dev. 90, 143-153.
36. Hirth, F., Therianos, S., Loop, T., Gehring, W. J., Reichert, H. and Furukubo-Tokunaga, K. (1995). Developmental defects in brain segmentation caused by mutations of the homeobox genes orthodenticle and empty spiracles in Drosophila. Neuron 15, 769-778.
37. Hirth, F., Hartmann, B. and Reichert, H. (1998). Homeotic gene action in embryonic brain development of Drosophila. Development 125, 1579-1589.
38. Isshiki, T., Pearson, B., Holbrook, S. and Doe, C. Q. (2001). Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 106, 511-521.
39. Jagla, K., Jagla, T., Heitzler, P., Dretzen, G., Bellard, F. and Bellard, M. (1997). ladybird, a tandem of homeobox genes that maintain late wingless expression in terminal and dorsal epidermis of the Drosophila embryo. Development 124, 91-100.
40. Jagla, K., Stanceva, I., Dretzen, G., Bellard, F. and Bellard, M. (1994). A distinct class of homeodomain proteins is encoded by two sequentially expressed Drosophila genes from the 93D/E cluster. Nucleic Acids Res. 22, 1202-1207.
41. Jimenez, F. and Campos-Ortega, J. A. (1990). Defective neuroblast commitment in mutants of the achaete-scute complex and adjacent genes of Drosophila melanogaster. Neuron 5, 81-89.
42. Jürgens, G. and Hartenstein, V. (1993). The terminal regions of the body pattern. In The Development of Drosophila melanogaster (ed. C. M. Bate and A. Martinez-Arias), pp. 687-746. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
43. Kambadur, R., Koizumi, K., Stivers, C., Nagle, J., Poole, S. J. and Odenwald, W. F. (1998). Regulation of POU genes by castor and hunchback establishes layered compartments in the Drosophila CNS. Genes Dev. 12, 246-260.
44. Kammermeier, L., Leemans, R., Hirth, F., Flister, S., Wenger, U., Walldorf, U., Gehring, W. J. and Reichert, H. (2001). Differential expression and function of the Drosophila Pax6 genes eyeless and twin of eyeless in embryonic central nervous system development. Mech. Dev. 103, 71-78.
45. Kania, M. A., Bonner, A. S., Duffy, J. B. and Gergen, J. P. (1990). The Drosophila segmentation gene runt encodes a novel nuclear regulatory protein that is also expressed in the developing nervous system. Genes Dev. 4, 1701-1713.
46. Kurusu, M., Nagao, T., Walldorf, U., Flister, S., Gehring, W. J. and Furukubo-Tokunaga, K. (2000). Genetic control of development of the mushroom bodies, the associative learning centers in the Drosophila brain, by the eyeless, twin of eyeless, and dachshund genes. Proc. Natl. Acad. Sci. USA 97, 2140-2144.
47. Mahaffey, J. W., Diederich, R. J. and Kaufman, T. C. (1989). Novel patterns of homeotic protein accumulation in the head of the Drosophila embryo. Development 105, 167-174.
48. Mardon, G., Solomon, N. M. and Rubin, G. M. (1994). dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila. Development 120, 3473-3486.
49. Martini, S. R., Roman, G., Meuser, S., Mardon, G. and Davis, R. L. (2000). The retinal determination gene, dachshund, is required for mushroom body cell differentiation. Development 127, 2663-2672.
50. McDonald, J. A. and Doe, C. Q. (1997). Establishing neuroblast-specific gene expression in the Drosophila CNS: huckebein is activated by Wingless and Hedgehog and repressed by Engrailed and Gooseberry. Development 124, 1079-1087.
51. Mellerick, D. M., Kassis, J. A., Zhang, S. D. and Odenwald, W. F. (1992). castor encodes a novel zinc finger protein required for the development of a subset of CNS neurons in Drosophila. Neuron 9, 789-803.
52. Mlodzik, M., Hiromi, Y., Weber, U., Goodman, C. S. and Rubin, G. M. (1990). The Drosophila seven-up gene, a member of the steroid receptor gene superfamily, controls photoreceptor cell fates. Cell 60, 211-224.
53. Nassif, C., Noveen, A. and Hartenstein, V. (1998). Embryonic development of the Drosophila brain. I. Pattern of pioneer tracts. J. Comp. Neurol. 402, 10-31.
54. Noveen, A., Daniel, A. and Hartenstein, V. (2000). Early development of the Drosophila mushroom body: the roles of eyeless and dachshund. Development 127, 3475-3488.
55. Patel, N. H. (1994). Imaging neuronal subsets and other cell types in whole mount Drosophila embryos and larvae using antibody probes. In Methods in Cell Biology. Drosophila melanogaster: Practical Uses in Cell Biology, Vol. 44 (ed. L. S. B. Goldstein and E. Fyrberg), pp. 445-487. New York: Academic Press.
56. Patel, N. H., Martin-Blanco, E., Coleman, K. G., Poole, S. J., Ellis, M. C., Kornberg, T. B. and Goodman, C. S. (1989). Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58, 955-968.
57. Plickert, G., Gajewski, M., Gehrke, G., Gausepohl, H., Schlossherr, J. and Ibrahim, H. (1997). Automated in situ detection (AISD) of biomolecules. Dev. Genes Evol. 207, 362-367.
58. Prokop, A. and Technau, G. M. (1994). Early tagma-specific commitment of Drosophila CNS progenitor NB1-1. Development 120, 2567-2578.
59. Pultz, M. A., Diederich, R. J., Cribbs, D. L. and Kaufman, T. C. (1988). The proboscipedia locus of the Antennapedia complex: a molecular and genetic analysis. Genes Dev. 2, 901-920.
60. Quiring, R., Walldorf, U., Kloter, U. and Gehring, W. J. (1994). Homology of the eyeless gene of Drosophila to the small eye gene in mice and aniridia in humans. Science 265, 785-789.
61. Reichert, H. (2002). Conserved genetic mechanisms for embryonic brain patterning. Int. J. Dev. Biol. 46, 81-87.
62. Rogers, B. T. and Kaufman, T. C. (1996). Structure of the insect head as revealed by the EN protein pattern in developing embryos. Development 122, 3419-3432.
63. Rudolph, K. M., Liaw, G. J., Daniel, A., Green, P., Courey, A. J., Hartenstein, V. and Lengyel, J. A. (1997). Complex regulatory region mediating tailless expression in early embryonic patterning and brain development. Development 124, 4297-4308.
64. Schmidt, H., Rickert, C., Bossing, T., Vef, O., Urban, J. and Technau, G. M. (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.
65. Schmidt-Ott, U., Gonzalez-Gaitan, M., Jäckle, H. and Technau, G. M. (1994). Number, identity, and sequence of the Drosophila head segments as revealed by neural elements and their deletion patterns in mutants. Proc. Natl. Acad. Sci. USA 91, 8363-8367.
66. Schmucker, D., Jäckle, H. and Gaul, U. (1997). Genetic analysis of the larval optic nerve projection in Drosophila. Development 124, 937-948.
67. Shen, W. and Mardon, G. (1997). Ectopic eye development in Drosophila induced by directed dachshund expression. Development 124, 45-52.
68. Skeath, J. B. (1999). At the nexus between pattern formation and cell-type specification: the generation of individual neuroblast fates in the Drosophila embryonic central nervous system. BioEssays 21, 922-931.
69. Tautz, D., Lehmann, R., Schnürch, H., Schuh, R., Seifert, E., Kienlin, A., Jones, K. and Jäckle, H. (1987). Finger protein of novel structure encoded by hunchback, a second member of the gap class of Drosophila segmentation genes. Nature 327, 383-389
70. Tautz, D. and Pfeifle, C. (1989). 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, 81-85.
71. Udolph, G., Prokop, A., Bossing, T. and Technau, G. M. (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.
72. Udolph, G., Lüer, K., Bossing, T. and Technau, G. M. (1995). Commitment of CNS progenitors along the dorsoventral axis of Drosophila neuroectoderm. Science 269, 1278-1281.
73. Urbach, R., Schnabel, R. and Technau, G. M. (2003). The pattern of neuroblast formation, mitotic domains and proneural gene expression during early brain development in Drosophila. Development 130, 3589-3606.
74. Urbach, R. and Technau, G. M. (2003). Segment polarity and D/V patterning gene expression reveals segmental organization of the Drosophila brain. Development 130, 3607-3620.
75. Walldorf, U. and Gehring, W. J. (1992). empty spiracles, a gap gene containing a homeobox involved in Drosophila head development. EMBO J. 11, 2247-2259.
76. Weigel, D., Jürgens, G., Klingler, M. and Jäckle, H. (1990). Two gap genes mediate maternal terminal pattern information in Drosophila. Science 248, 495-498.
77. Wieschaus, E., Perrimon, N. and Finkelstein, R. (1992). orthodenticle activity is required for the development of medial structures in the larval and adult epidermis of Drosophila. Development 115, 801-811.
78. Yang, X., Yeo, S., Dick, T. and Chia, W. (1993). The role of a Drosophila POU homeo domain gene in the specification of neural precursor cell identity in the developing embryonic central nervous system. Genes Dev. 7, 504-516.
79. Yang, X., Bahri, S., Klein, T. and Chia, W. (1997). Klumpfuss, a putative Drosophila zinc finger transcription factor, acts to differentiate between the identities of two secondary precursor cells within one neuroblast lineage. Genes Dev. 11, 1396-1408.
80. Yeo, S. L., Lloyd, A., Kozak, K., Dinh, A., Dick, T., Yang, X., Skonju, S. and Chia, W. (1995). On the functional overlap between two Drosophila POU homeo domain genes and the cell fate specification of a CNS neural precursor. Genes Dev. 9, 1223-1236.
81. Younossi-Hartenstein, A., Green, P., Liaw, G. J., Rudolph, K., Lengyel, J. and Hartenstein, V. (1997). Control of early neurogenesis of the Drosophila brain by the head gap genes tll, otd, ems, and btd. Dev. Biol. 182, 270-283.