Commissure formation in the embryonic CNS of Drosophila. I. Identification of the required gene functions

Developmental Biology

Volumn 209, Issue 2, 1999, Pages 381-398

  Hummel, Thomas ^a   Schimmelpfeng, Kristina ^a   Klämbt, Christian ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MESYLIC ACID ETHYL ESTER; NETRIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR POSTERIOR AXIS; ARTICLE; BRAIN COMMISSURE; CELL SPECIFICITY; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO POLARITY; GENE DISRUPTION; GENE FUNCTION; GLIA CELL; GROWTH CONE; MUTAGENESIS; NERVE FIBER GROWTH; NERVE TRACT; NEUROMERE; NONHUMAN; PRIORITY JOURNAL; VENTRAL ROOT;

ANIMALIA; DROSOPHILA; HEXAPODA;

EID: 0033562664     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1999.9235     Document Type: Article

References (80)

1. Ackerman S. L., Kozak L. P., Przyborski S. A., Rund L. A., Boyer B. B., Knowles B. B. The mouse rostral cerebellar malformation gene encodes an UNC 5 like protein. Nature. 386:1997;838-842.
2. Bossing T., Technau G. M. The fate of the CNS midline progenitors in Drosophia as revealed by a new method for single cell labeling. Development. 120:1994;1895-1906.
3. Bossing T., Udolph G., Doe C. Q., Technau G. M. The embryonic central nervous system lineages ofDrosophila melanogaster. Dev. Biol. 179:1996;41-64.
4. Chan S. S., Zheng H., Su M. W., Wilk R., Killeen M. T., Hedgecock E. M., Culotti J. G. UNC-40, a C. elegans homolog of DCC (Deleted in Colorectal Cancer), is required in motile cells responding to UNC-6 netrin cues. Cell. 87:1996;187-195.
5. Crews S. T., Thomas J. B., Goodman C. S. The Drosophila single-minded gene encodes a nuclear protein with sequence similarity to the per gene product. Cell. 52:1988;143-151.
6. Dormand E. L., Brand A. Runt determines cell fates in the Drosophila embryonic CNS. Development. 125:1998;1659-1667.
7. Driever W., Stemple D., Schier A., Solnica-Krezel L. Zebrafish: Genetic tools for studying vertebrate development. Trends Genet. 10:1994;152-159.
8. Dye C. A., Lee J. K., Atkinson R. C., Brewster R., Han P. L., Bellen H. J. The Drosophila sanpodo gene controls sibling cell fate and encodes a tropomodulin homolog, an actin/tropomyosin associated protein. Development. 125:1998;1845-1856.
9. Elkins T., Zinn K., McAllister L., Hoffmann F. M., Goodman C. S. Genetic analysis of aDrosophila. Cell. 60:1990;565-575.
10. Ericson J., Morton S., Kawakami A., Roelink H., Jessell T. M. Two critical periods of Sonic Hedgehog signaling required for the specification of motor neuron identity. Cell. 87:1996;661-673.
11. Escherich K. Zur Entwicklung des Nervensystems der Musciden, mit besonderer Berücksichtigung des sog Mittelstranges. Z. Wissensch. Zool. LXXI:1902;525-549.
12. Fazeli A., Dickinson S. L., Hermiston M. L., Tighe R. V., Steen R. G., Small C. G., Stoeckli E. T., Keino-Masu K., Masu M., Rayburn H., Simons J., Bronson R. T., Grodon J. I., Tessier-Lavigne M., Weinberg R. A. Phenotype of mice lacking functional Deleted in colorectal cancer (Dcc) gene. Nature. 386:1997;796-804.
13. Finkelstein R., Smouse D., Capaci T. M., Spradling A. C., Perrimon N. The orthodenticle gene encodes a novel homeodomain protein involved in the development of the Drosophila nervous system and ocellar visual structures. Genes Dev. 4:1990;1516-1527.
14. Foe V. E. Mitotic domains reveal early commitment of cells in Drosophila embryos. Development. 107:1989;1-22.
15. Fujita C. S., Zipursky S. L, Benzer S., Ferrus A., Shotwell S. L. Monoclonal antibodies against the Drosophila nervous system. Proc. Natl. Acad. Sci. USA. 79:1982;59-69.
16. Gertler F. B., Bennett R. L., M. J. C., Hoffmann F. M. Drosophila. Cell. 58:1989;103-113.
17. Giebel B. Genetische und molekulargenetische Untersuchungen zur Neurogenese von Drosophila melanogaster unter Verwendung des GAL4-Systems. 1996;Universität zu KölnInstitut für Entwicklungsbiologie, Cologne.
18. Giesen K., Hummel T., Stollewerk A., Harrison S., Travers A., Klämbt C. Glial development in theDrosophila. Development. 124:1997;2307-2311.
19. Giniger E., Tietje K., Jan L. Y., Jan Y. N. lola encodes a putative transcription factor required for axon growth and guidance in Drosophila. Development. 120:1994;1385-1398.
20. Goodman C. S., Doe C. Q. Embryonic development of the Drosophila central nervous system. Development of Drosophila. 1993;Cold Spring Harbor Laboratory Press, Cold Spring Harbor. p. 1131-1206.
21. Goodman C. S., Shatz C. J. Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell. 72:1993;77-82.
22. Hamelin M., Zhou Y., Su M. W., Scott I. M., Culotti J. G. Expression of the unc-5 guidance receptor in the touch neurons of C. elegans steers their axons dorsally. Nature. 364:1993;327-330.
23. Harris R., Sabatelli L. M., Seeger M. A. Guidance cues at the Drosophila midline: Identification and characterization of two Drosophila netrin/unc6 homologs. Neuron. 17:1996;217-228.
24. Hedgecock E. M., Culotti J. G., Hall D. H. the unc-5, unc-6 and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neruon. 4:1990;61-85.
25. Hedgecock E. M., Culotti J. G., Thomsn J. N., Perkins L. A. Axonal guidance mutants ofCaenorhabditis elegans. Dev. Biol. 111:1985;158-170.
26. Hooper J. E., Scott M. P. The Drosophila patched gene encodes a putative membrane protein required for segmental patterning. Cell. 59:1989;751-765.
27. Hu S., Sonnenfeld M., Stahl S., Crews S. T. Midline fasciclin: A Drosophila fasciclin I related membrane protein localized to the CNS midline cells and trachea. J. Neurobiol. 35:1998;77-93.
28. Hummel T., Schimmelpfeng K., Klämbt C. Fast and efficient egg collection and antibody staining from large numbers ofDrosophila. Dev. Genes Evol. 207:1997;131-135.
29. Hummel T., Schmimmelpfeng K., Klämbt C. Commissure formation in the embryonic CNS ofDrosophila. Development. 126:1999;771-779.
30. Hynes M., Porter J. A., Chiang C., Chang D., Tessier-Lavigne M., Beachy P. A., Rosenthal A. Induction of midbrain dopaminergic neurons by Sonic hedgehog. Neuron. 15:1995;35-44.
31. Jacobs J. R., goodman C. S. Embryonic development of axon pathways in the Drosophila CNS. I. A glial scaffold appears before the first growth cones. J. Neurosci. 9:1989;2402-2411.
32. Jürgens G., Wieschaus E., Nüsslein-Volhard C., Kluding H. Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. II. Zygotic loci on the third chromosome. Roux's Arch. Dev. Biol. 193:1984;283-295.
33. Keino-Msu K., Masu M., Hinck L., Leonardo E. D., Chan S. S., Culotti J. G., Tessier-Lavigne M. Deleted in Colorectal Cancer (DCC) encodes a netrin receptor. Cell. 87:1996;175-185.
34. Kennedy T. E., Serafini T., de la Torre J. R., Tessier-Lavigne M. Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell. 78:1994;425-435.
35. Kidd T., Brose K., Mitchell K. J., Fetter R. D., Tessier-Lavigne M., Goodman C. S., Tear G. Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell. 92:1998a;205-215.
36. Kidd T., Russell C., Goodman C. S., Tear G. Dosage sensitive and complementary functions of roundabout and commissureless control axon crossing of the CNS midline. Neuron. 20:1998b;25-33.
37. Kim S. H., Crews S. T. Influence of Drosophila ventral epidermal development by the CNS midline cells and spitz class genes. Development. 118:1993;893-901.
38. Klämbt C. The Drosophila gene pointed encodes two ets like proteins, which are involved in the development of the midline glial cells. Development. 117:1993;163-176.
39. Klämbt C., Jacobs R. J., Goodman C. S. The midline of the Drosophila CNS: Model and genetic analysis of cell lineage, cell migration, development of commissural axon pathways. Cell. 64:1991;801-815.
40. Kolodziej P. A., Jan L. Y., Jan Y. N. Mutations that affect the length, fasciculation, or ventral orientation of specific sensory axons in the Drosophila embryo. Neuron. 15:1995;273-286.
41. Kolodziej P. A., Timpe L. C., Mitchell K. J., Fried S. R., Goodman C. S., Jan L. Y., Jan Y. N. frazzled encodes a Drosophila member of the DCC immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell. 87:1996;197-204.
42. Lee J. J., von Kessler D. P., Parks S., Beachy P. A. Secretion and localized transcription suggest a role in positional signalling for products of the segmentations gene hedgehog. Cell. 71:1992;33-50.
43. Leonardo E. D., Hinck L., Masu M., Keino-Masu K., Ackerman S. L., Tessier-Lavigne M. Vertebrate homologues of C. elegans UNC5 are candidate netrin receptors. Nature. 386:1997;833-838.
44. Lewis E. B., Bacher F. Method of feeding ethylmethane sulfonate (EMS) toDrosophila. Drosophila Inf. Serv. 43:1968;193.
45. Lüer K., Urban J., Klämbt C., Technau G. M. Induction of identified mesodermal cells by CNS midline progenitors inDrosophila. Development. 124:1997;2681-2690.
46. Martin K. A., Poeck B., Roth H., Ebens A. J., Ballard L. C., Zipursky S. L. Mutations disrupting neuronal connectivity in the Drosophila visual system. Neuron. 14:1995;229-240.
47. Martín-Bermudo M. D., Carmena A., Jim e F. Neurogenic genes control gene expression at the transcriptional level in early neurogenesis and in mesectoderm specification. Development. 121:1995;219-224.
48. Martinez Arias A. Development and patterning of the larval epidermis ofDrosophila. Bate M., Martinez Arias A. The Development ofDrosophila melanogaster. 1993;517-608 Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
49. Mayer U., Nüsslein-Volhard C. A group of genes required for pattern formation in the ventral ectoderm of the Drosophila embryo. Genes Dev. 2:1988;1496-1511.
50. Mayer U., Torres R. A., Berleth T., Mis e S., Jürgens G. Mutations affecting body organization in theArabidopsis. Nature. 353:1991;402-407.
51. McAllister L., Goodman C. S., Zinn K. Dynamic expression of the cell adhesion molecule fasciclin I during embryonic development in Drosophila. Development. 115:1992;267-276.
52. Menne T. V., Klämbt C. The formation of commissures in the Drosophila CNS depends on the midline cells and on the Notch gene. Development. 120:1994;123-133.
53. Menne T. V., Luer K., Technau G. M., Klambt C. CNS midline cells in Drosophila induce the differentiation of lateral neural cells. Development. 124:1997;4949-4958.
54. Mitchell K. J., Doyle J. L., Serafini T., Kennedy T. E., Tessier-Lavigne M., Goodman C. S., Dickson B. J. Genetic analysis of netrin genes in Drosophila: Netrins guide CNS commissural axons and peripheral motor axons. Neuron. 17:1996;203-215.
55. Mullins M. C., Nüsslein-Volhard C. Mutational approaches to studying embryonic pattern formation in the zebrafish. Curr. Opin. Genet. Dev. 3:1993;648-654.
56. Munsterberg A. E., Lassar A. B. Combinatorial signals from the neural tube, floor plate and notochord induce myogenic bHLH gene expression in the somite. Development. 121:1995;651-660.
57. Nakano Y., Guerrero I., Hidalgo A., Taylor A., Whittle J. R., Ingham P. W. A protein with several possible membrane-spanning domains encoded by the Drosophila segment polarity gene patched. Nature. 341:1989;508-513.
58. Nambu J. R., Franks R. G., Hu S., Crews S. T. The single-minded gene of Drosophila is required for the expression of genes important for the development of CNS midline cells. Cell. 63:1990;63-75.
59. Nambu J. R., Lewis J. O., Wharton K. A., Crews S. T. The Drosophila single-minded gene encodes a helix-loop-helix protein that acts as a master regulator of midline development. Cell. 67:1991;1157-1167.
60. Nüsslein-Volhard C., Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature. 287:1980;795-801.
61. Nüsslein-Volhard C., Wieschaus E., Kluding H. Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. I. Zygotic loci on the second chromosome. Roux's Arch. Dev. Biol. 193:1984;267-282.
62. Ohshiro T., Saigo K. Transcriptional regulation of breathless FGF receptor gene by binding of TRACHEALESS/dARNT heterodimers to three central midline elements in Drosophila developing trachea. Development. 124:1997;3975-3986.
63. Patel N. H., Schafer B., Goodman C. S., Holmgren R. The role of segment polarity genes during Drosophila neurogenesis. Genes Dev. 3:1989;890-904.
64. Pourquie O., Fan C. M., Coltey M., Hirsinger E., Watanabe Y., Breant C., Francis-West P., Brickell P., Tessier-Lavigne M., Le Douarin N. M. Lateral and axial signals involved in avian somite patterning: A role for BMP4. Cell. 84:1996;461-471.
65. Roelink H., Porter J. A., Chiang C., Tanabe Y., Chang D. T., Beachy P. A., Jessell T. M. Floor plate and motor neuron induction by different concentrations of the amino terminal cleavage product of sonic hedgehog autoproteolysis. Cell. 81:1995;445-455.
66. Salzberg E., D'Evelyn D., Schultze K., Lee J.-K., Strumpf D., Tsai L., Bellen H. J. Mutations affecting the pattern of the PNS in Drosophila reveal novel aspects of neuronal development. Neuron. 13:1994;269-287.
67. Schmidt H., Rickert C., Bossing T., Vef O., Urban J., Technau G. M. 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.
68. Schmucker D., jackle H., Gaul U. Genetic analysis of the larval optic nerve projection in Drosophila. Development. 124:1997;937-948.
69. Schoenwolf G. C., Smith J. L. Mechanisms of neurulation: Traditional view point and recent advances. Development. 109:1990;243-270.
70. Seeger M., Tear G., Ferres-Marca D., Goodman C. S. Mutations affecting growth cone guidance in Drosophila: Genes necessary for guidance towards or away from the midline. Neuron. 10:1993;409-426.
71. Serafini T., Kennedy T. E., Galko M. J., Mirzayan C., Jessell T. M., Tessier-Lavigne M. The netrins define a family of axon outgrowth promoting proteins homologous to C. elegans UNC 6. Cell. 78:1994;409-424.
72. Sonnenfeld M., Ward M., Nystrom G., Mosher J., Stahl S., Crews S. The Drosophila tango gene encodes a bHLH PAS protein that is orthologous to mammalian Arnt and controls CNS midline and tracheal development. Development. 124:1997;4571-4582.
73. Sonnenfeld M. J., Jacobs J. R. Mesectodermal cell fate analysis inDrosophila. Mech. Dev. 46:1994;3-13.
74. Sonnenfeld M. J., Jacobs J. R. Apoptosis of the midline glia during Drosophila embryogenesis: A correlation with axon contact. Development. 121:1995;569-578.
75. Stollewerk A., Klämbt C. The midline glial cells are required for compartmentalisation of axon commissures in the embryonic CNS ofDrosophila. Dev. Genes Evol. 207:1997;401-409.
76. Tear G., Harris R., Sutaria S., Kilomanski K., Goodman C. S., Seeger M. A. commissureless controls growth cone guidance across the CNS midline in Drosophila and encodes a novel membrane protein. Neuron. 16:1996;501-514.
77. Tessier-Lavigne M., Goodman C. S. The molecular biology of axon guidance. Science. 274:1996;1123-1133.
78. van Vactor D., Sink H., Fambrough D., Tsoo R., Goodman C. S. Genes that control neuromuscular specificity in Drosophila. Cell. 73:1993;1137-1153.
79. Wieschaus E., Nüsslein-Volhard C., Jürgens G. Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. III Zygotic loci on the X-chromosme and the fourth chromosome. Roux's Arch. Dev. Biol. 193:1984;283-295.
80. Yamada T., Pfaff S. L., Edlund T., Jessell T. M. Control of cell pattern in the neural tube: Motor neuron induction by diffusible factors from notochord and floor plate. Cell. 73:1993;673-686.