Dorsoventral patterning in the Drosophila central nervous system: The intermediate neuroblasts defective homeobox gene specifies intermediate column identity

Genes and Development

Volumn 12, Issue 22, 1998, Pages 3591-3602

  Weiss, Joseph B ^a   Von Ohlen, Tonia ^c   Mellerick, Dervla M ^d   Dressler, Gregory ^d   Doe, Chris Q ^b,c   Scott, Matthew P ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF OREGON   (United States)

^d UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

Central nervous system; Neuroectoderm; NK2; Tinman; vnd

Indexed keywords

ARTICLE; DROSOPHILA; EMBRYO; EVOLUTION; GENETIC CONSERVATION; HOMEOBOX; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NEUROECTODERM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

DROSOPHILA; HEXAPODA; INSECTA; VERTEBRATA;

EID: 0032533213     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.12.22.3591     Document Type: Article

References (58)

1. Adams, B., P. Dorfler, A. Aguzzi, Z. Kozmik, P. Urbanek, I. Maurer-Fogy, and M. Busslinger. 1992. Pax-5 encodes the transcription factor BSAP and is expressed in B lymphocytes, the developing CNS, and adult testis. Genes & Dev. 6: 1589-1607.
2. Altschul, S.F., T.L. Madden, A.A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D.J. Lipman. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
3. Angerer, L. and R. Angerer. 1992. In situ hybridization to cellular RNA with radiolabelled RNA probes. In In situ hybridization: A practical approach (ed. D.G. Wilkinson), pp. 15-32. Oxford University Press, Oxford, UK.
4. Ausubel, F.M., R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl. 1994. Current protocols in molecular biology, John Wiley & Sons, New York, NY.
5. Azpiazu, N. and M. Frasch. 1993. tinman and bagpipe: Two homeobox genes that determine cell fates in the dorsal mesoderm of Dzosophila. Genes & Dev. 7: 1325-1340.
6. Barth, K.A. and S.W. Wilson. 1995. Expression of zebrafish nk2.2 is influenced by sonic hedgehog/vertebrate hedgehog-1 and demarcates a zone of neuronal differentiation in the embryonic forebrain. Development 121: 1755-1768.
7. Bhat, K.M. 1996. The patched signaling pathway mediates repression of gooseberry allowing neuroblast specification by wingless during Drosophila neurogenesis. Development 122: 2921-2932.
8. Bhat, K.M. and P. Schedl. 1997. Requirement for engrailed and invected genes reveals novel regulatory interactions between engrailed/invected, patched, gooseberry and wingless during Drosophila neurogenesis. Development 124: 1675-1688.
9. Bier, E. 1997. Anti-neural-inhibition a conserved mechanism for neural induction. Cell 89: 681-684.
10. Bodmer, R. 1993. The gene tinman is required for specification of the heart and visceral muscles in Drosophila. Development 118: 719-729.
11. Bossing, T., G. Udolph, C.Q. Doe, and G.M. Technau. 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.
12. Brown, N.H. and F.C. Kafatos. 1988. Functional cDNA libraries from Drosophila embryos. J. Mol. Biol. 203: 425-437.
13. Campos-Ortega, J.A. 1995. Genetic mechanisms of early neurogenesis in Drosophila melanogaster. Mol. Neurobiol. 10: 75-89.
14. Campos-Ortega, J.A. and V. Hartenstein. 1997. The embryonic development of Drosophila melanogaster, 2nd ed. Springer-Verlag, Berlin, Germany.
15. Chen, C.Y. and R.J. Schwartz, 1995. Identification of novel DNA binding targets and regulatory domains of a murine tinman homeodomain factor, nkx-2.5. J. Biol. Chem. 270: 15628-15633.
16. Chu-LaGraff, Q. and C.Q. Doe. 1993. Neuroblast specification and formation regulated by wingless in the Drosophila CNS. Science 261: 1594-1597.
17. Chu-LaGraff, Q., A. Schmid, J. Leidel, G. Bronner, H. Jackle, and C.Q. Doe. 1995. huckebein specifies aspects of CNS precursor identity required for motoneuron axon pathfinding. Neuron 15: 1041-1051.
18. Church, G.M. and W. Gilbert. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. 81: 1991-1995.
19. D'Alessio, M. and M. Frasch. 1996. msh may play a conserved role in dorsoventral patterning of the neuroectoderm and mesoderm. Mech. Dev. 58: 217-231.
20. Doe, C.Q. 1992. Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila central nervous system. Development 116: 855-863.
21. Ferguson, E.L. 1996. Conservation of dorsal-ventral patterning in arthropods and chordates. Curr. Opin. Genet. Dev. 6: 424-431.
22. Frei, E., S. Baumgartner, J.-E. Edström, and M. Noll. 1986. Cloning of the extra sex combs gene of Drosophila and its identification by P-element-mediated gene transfer. EMBO J. 4: 979-987.
23. Gruschus, J.M., D.H. Tsao, L.H. Wang, M. Nirenberg, and J.A. Ferretti. 1997. Interactions of the vnd/NK-2 homeodomain with DNA by nuclear magnetic resonance spectroscopy: Basis of binding specificity. Biochemistry 36: 5372-5380.
24. Holland, P.W. 1991. Cloning and evolutionary analysis of msh-like homeobox genes from mouse, zebrafish and ascidian. Gene 98: 253-257.
25. Isshiki, T., M. Takeichi, and A. Nose. 1997. The role of the msh homeobox gene during Drosophila neurogenesis: Implication for the dorsoventral specification of the neuroectoderm. Development 124: 3099-3109.
26. Jimenez, F., L.E. Martin-Morris, L. Velasco, H. Chu, J. Sierra, D.R. Rosen, and K. White. 1995. vnd, a gene required for early neurogenesis of Drosophila, encodes a homeodomain protein. EMBO J. 14: 3487-3495.
27. Lehmann, R. and D. Tautz. 1994. In situ hybridization to RNA. In Drosophila melanogaster: Practical uses in cell and molecular biology (ed. L.S.B. Goldstein and E.A. Fyrberg), pp. 575-598. Academic Press, San Diego, CA.
28. Liu, J., T.E. Wilson, J. Milbrandt, and M. Johnston. 1993. Identifying DNA-binding sites and analyzing DNA-binding domains using a yeast selection system. Methods: A Companion to Meth. Enzymol. 5: 125-137.
29. Mastick, G.S., R. McKay, T. Oligino, K. Donovan, and A.J. Lopez. 1995. Identification of target genes regulated by homeotic proteins in Drosophila melanogaster through genetic selection of Ultrabithorax protein-binding sites in yeast. Genetics 139: 349-363.
30. Mastick, G.S., N.M. Davis, G.L. Andrew, and S.S. Easter Jr. 1997. Pax-6 functions in boundary formation and axon guidance in the embryonic mouse forebrain. Development 124: 1985-1997.
31. Matsuzaki, M. and K. Saigo. 1996. hedgehog signaling independent of engrailed and wingless required for post-S1 neuroblast formation in Drosophila CNS. Development 122: 3567-3575.
32. Maxam, A.M. and W. Gilbert. 1980. Sequencing end-labeled DNA with base-specific chemical cleavages. Meth. Enzymol. 65: 499-560.
33. McDonald, J.A. and C.Q. Doe. 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.
34. McDonald, J.A., S. Holbrook, T. Isshiki, J. Weiss, C.Q. Doe, and D.M. Mellerick. 1998. Dorsoventral patterning in the Drosophila CNS: The vnd homeobox gene specifies ventral column identity. Genes & Dev. (this issue).
35. Mellerick, D.M. and M. Nirenberg. 1995. Dorsal-ventral patterning genes restrict NK-2 homeobox gene expression to the ventral half of the central nervous system of Drosophila embryos. Dev. Biol. 171: 306-316.
36. Pardue, M.-L. 1994. Looking at polytene chromosomes. In Drosophila melanogaster: Practical uses in cell and molecular biology (ed. L.S.B. Goldstein and E.A. Fyrberg), pp. 333-351. Academic Press, San Diego, CA.
37. Patel, N.H. 1994. Imagining neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes. In Drosophila melanogaster: Practical uses in cell and molecular biology (ed. L.S.B. Goldstein and E.A. Fyrberg), pp. 445-487. Academic Press, San Diego, CA.
38. Raz, E. and B.Z. Shilo. 1993. Establishment of ventral cell fates in the Drosophila embryonic ectoderm requires DER, the EGF receptor homolog. Genes & Dev. 7: 1937-1948.
39. Rutledge, B.J., K. Zhang, E. Bier, Y.N. Jan, and N. Perrimon. 1992. The Drosophila spitz gene encodes a putative EGF-like growth factor involved in dorsal-ventral axis formation and neurogenesis. Genes & Dev. 6: 1503-1517.
40. Rusch, J. and M. Levine. 1996. Threshold responses to the dorsal regulatory gradient and the subdivision of primary tissue territories in the Drosophila embryo. Curr. Opin. Genet. Dev. 6: 416-423.
41. Ryan, G., V. Steele-Perkins, J.F. Morris, F.J.R. Rauscher, and G.R. Dressler. 1995. Repression of Pax-2 by WT1 during normal kidney development. Development 121: 867-875.
42. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular cloning: A laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
43. Schmidt, H., C. Rickert, T. Bossing, O. Vef, J. Urban, and G.M. Technau. 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.
44. Schweitzer, R., M. Shaharabany, R. Seger, and B.Z. Shilo. 1995. Secreted Spitz triggers the DER signaling pathway and is a limiting component in embryonic ventral ectoderm determination. Genes & Dev. 9: 1518-1529.
45. Schweitzer, R. and B.Z. Shilo. 1997. A thousand and one roles for the Drosophila EGF receptor. Trends Genet. 13: 191-196.
46. Skeath, J.B. and S.B. Carroll. 1992. Regulation of proneural gene expression and cell fate during neuroblast segregation in the Drosophila embryo. Development 114: 939-946.
47. _. 1994. The achaete-scute complex: Generation of cellular pattern and fate within the Drosophila nervous system. FASEB J. 8: 714-721.
48. Skeath, J.B., G.F. Panganiban, and S.B. Carroll. 1994. The ventral nervous system defective gene controls proneural gene expression at two distinct steps during neuroblast formation in Drosophila. Development 120: 1517-1524.
49. Skeath, J.B., Y. Zhang, R. Holmgren, S.B. Carroll, and C.Q. Doe. 1995. Specification of neuroblast identity in the Drosophila embryonic central nervous system by gooseberry-distal. Nature 376: 427-430.
50. Srinivasan, S., C.-Y. Peng, S. Nair, J.B. Skeath, E.P. Spana, and C.Q. Doe. 1998. Biochemical analysis of Prospero protein during asymmetric cell division: Cortical Prospero is highly phosphorylated relative to neclear Prospero. Dev. Biol. (in press).
51. Szucsik, J.C., D.P. Witte, H. Li, S.K. Pixley, K.M. Small, and S.S. Potter. 1997. Altered forebrain and hindbrain development in mice mutant for the Gsh2 homeobox gene. Dev. Biol. 191: 230-242.
52. Tamkun, J.W., R. Deuring, M.P. Scott, M. Kissinger, A.M. Pattatucci, T.C. Kaufman, and J.A. Kennison. 1992. brahma: A regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 68: 561-572.
53. Valerius, M.T., H. Li, J.L. Stock, M. Weinstein, S. Kaur, G. Singh, and S.S. Potter. 1995. Gsh1: A novel murine homeobox gene expressed in the central nervous system. Dev. Dyn. 203: 337-351.
54. Wang, W., X. Chen, H. Xu, and T. Lufkin. 1996. Msx3: A novel murine homolog of the Drosophila msh homeobox gene restricted to the dorsal embryonic central nervous system. Mech. Dev. 58: 203-215.
55. White, K., N.L. DeCelles, and T.C. Enlow. 1983. Genetic and developmental analysis of the locus vnd in Drosophila melanogaster. Genetics 104: 433-448.
56. Yang, X., S. Bahri, T. Klein, and W. Chia. 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.
57. Yang, X., S. Yeo, T. Dick, and W. Chia. 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.
58. Zhang, Y., A. Ungar, C. Fresquez, and R. Holmgren. 1994. Ectopic expression of either the Drosophila gooseberry-distal or proximal gene causes alterations of cell fate in the epidermis and central nervous system. Development 120: 1151-1161.