The fruitless gene is required for the proper formation of axonal tracts in the embryonic central nervous system of Drosophila

Genetics

Volumn 162, Issue 4, 2002, Pages 1703-1724

  Song, Ho Juhn ^a,e   Billeter, Jean Christophe ^b,f   Reynaud, Enrique ^c,g   Carlo, Troy ^b   Spana, Eric P ^d,h   Perrimon, Norbert ^d   Goodwin, Stephen F ^b,f   Baker, Bruce S ^c   Taylor, Barbara J ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b BRANDEIS UNIVERSITY   (United States)

^c STANFORD UNIVERSITY   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e NOVARTIS PHARMA AG   (Switzerland)

^f UNIVERSITY OF GLASGOW   (United Kingdom)

^g INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

^h SYNGENTA BIOTECHNOLOGY INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CENTRAL NERVOUS SYSTEM; DROSOPHILA; EMBRYO; FEMALE; FRUITLESS GENE; GENE; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GLIA; MALE; MORPHOLOGY; NERVE FIBER; NERVE PROJECTION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; SEXUAL BEHAVIOR;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; AXONS; BASE SEQUENCE; BODY PATTERNING; CENTRAL NERVOUS SYSTEM; CHROMOSOME MAPPING; DNA, COMPLEMENTARY; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, INSECT; HETEROZYGOTE; HOMOZYGOTE; MALE; MUTATION; NERVE TISSUE PROTEINS; NEUROGLIA; NEURONS; PERIPHERAL NERVOUS SYSTEM; PHENOTYPE; PROMOTER REGIONS (GENETICS); RNA, MESSENGER; TRANSCRIPTION FACTORS;

ARACHNIDA; DROSOPHILA MELANOGASTER; HEXAPODA; INSECTA; MELANOGASTER;

EID: 0345576900     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (66)

1. ANAND, A., A. VILLELLA, L. C. RYNER, T. CARLO, S. F. GOODWIN et al., 2001 Molecular genetic dissection of the sex-specific and vital functions of the Drosophila melanogaster sex determination gene fruitless. Genetics 158: 1569-1595.
2. BAINBRIDGE, S. P., and M. BOWNES, 1981 Staging the metamorphosis of Drosophila melanogaster. J. Embryol. Exp. Morphol. 66: 57-80.
3. BAYER, C. A., L. VON KALM and J. W. FRISTROM, 1997 Relationships between protein isoforms and genetic functions demonstrate functional redundancy at the Broad-Complex during Drosophila metamorphosis. Dev. Biol. 187: 267-282.
4. BRAND, A. H., and N. PERRIMON, 1993 Targeted gene expression as a means of altering cell fate and generating dominant phenotypes. Development 118: 401-415.
5. BROADUS, J., and C. Q. DOE, 1995 Evolution of neuroblast identity: seven-up and prospero expression reveal homologous and divergent neuroblast fates in Drosophila and Schistocerca. Development 121: 3989-3996.
6. BROADUS, J., J. B. SKEATH, E. P. SPANA, T. BOSSING, G. TECHNAU et al., 1995 New neuroblast markers and the origin of the aCC/pCC neurons in the Drosophila central nervous system. Mech. Dev. 53: 393-402.
7. BROSE, K., and M. TESSIER-LAVIGNE, 2000 Slit proteins: key regulators of axon guidance, axonal branching, and cell migration. Curr. Opin. Neurobiol. 10: 95-102.
8. CAMPBELL, G., H. GÖRING, T. LIN, E. SPANA, S. ANDERSSON et al., 1994 RK2, a glial-specific homeodomain protein required for embryonic nerve cord condensation and viability in Drosophila. Development 120: 2957-2966.
9. CAMPOS-ORTEGA, J. A., and V. HARTENSTEIN, 1997 The Embryonic Development of Drosophila melanogaster. Ed. 2. Springer-Verlag, New York.
10. CASTRILLON, D. H., P. GONZY, S. ALEXANDER, R. RAWSON, C. G. EBERHART et al., 1993 Toward a molecular genetic analysis of spermatogenesis in Drosophila melanogaster: characterization of male-sterile mutants generated by single P-element mutagenesis. Genetics 135: 489-505.
11. DIBELLO, P. R., D. A. WITHERS, C. A. BAYER, J. W. FRISTROM and G. M. GUILD, 1991 The Drosophila Broad-Complex encodes a family of related proteins containing zinc fingers. Genetics 129: 385-397.
12. FLYBASE, 1999 The FlyBase database of the Drosophila genome projects and community literature. Nucleic Acids Res. 27: 85-88 (http://flybase.bio.indiana.edu/).
13. FREEMAN, M., C. KLÄABT, C. S. GOODMAN and G. M. RUBIN, 1992 The argos gene encodes a diffusible factor that regulates cell fate decision in the Drosophila eye. Cell 69: 963-975.
14. FUJITA, S. C., S. L. ZIPURSKY, S. BENZER, A. FERRUS and S. W. SHOTWELL, 1982 Monoclonal antibodies against the Drosophila nervous system. Proc. Natl. Acad. Sci. USA 79: 7929-7933.
15. GIESEN, K., T. HUMMEL, A. STOLLEWERK, S. HARRISON, A. TRAVERS et al., 1997 Glial development in the Drosophila CNS requires concomitant activation of glial and repression of neuronal differentiation genes. Development 124: 2307-2316.
16. GINIGER, E., K. TIETJE, L. Y. JAN and Y. N. JAN, 1994 lola encodes a putative transcription factor required for axon growth and guidance in Drosophila. Development 120: 1385-1398.
17. GOODMAN, C. S., 1996 Mechanisms and molecules that control growth cone guidance. Annu. Rev. Neurosci. 19: 341-377.
18. GOODMAN, C. S., and C. Q. DOE, 1993 Embryonic development of the Drosophila central nerve system, pp. 1131-1206 in Development of Drosophila melanogaster, edited by M. BATE and A. MARTINEZ-ARIAS, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
19. GOODWIN, S. F., B. J. TAYLOR, A. VILLELLA, M. Foss, L. C. RYNER et al., 2000 Aberrant splicing and altered spatial expression patterns in fruitless mutants of Drosophila melanogaster. Genetics 154: 725-745.
20. GRANDERATH, S., and C. KLÄMBT, 1999 Glia development in the embryonic CNS of Drosophila. Curr. Opin. Neurobiol. 9: 531-536.
21. GRENNINGLOH, C., E. J. REHM and C. S. GOODMAN, 1991 Genetic analysis of growth cone guidance in Drosophila: fasciclin II functions as a neuronal recognition molecule. Cell 67: 45-57.
22. GUTHRIE, S., 1999 Axon guidance: starting and stopping with slit. Curr. Biol. 9: R432-R435.
23. HALTER, D. A., J. URBAN, C. RICKERT, S. S. NER, K. ITO et al., 1995 The homeobox gene repo is required for the differentiation and maintaince of glia function in the embryonic nervous system of Drosophila melanogaster. Development 121: 317-332.
24. HEINRICHS, V., L. C. RYNER and B. S. BAKER, 1998 Regulation of sex-specific selection of fruitless 5′ splice sites by transformer and transformer-2. Mol. Cell. Biol. 18: 450-458.
25. HIDALGO, A., and G. E. BOOTH, 2000 Glia dictate pioneer axon trajectories in the Drosophila embryonic CNS. Development 127: 393-402.
26. HIDALGO, A., and A. H. BRAND, 1997 Targeted neuronal ablation: the role of pioneer neurons in guidance and fasciculation in the CNS of Drosophila. Development 124: 3253-3262.
27. HOSOYA, T., K. TAKIZAWA, K. NITTA and Y. HOTTA, 1995 glial cells missing: a binary switch between neuronal and glial determination in Drosophila. Cell 82: 1025-1036.
28. HUMMEL, T., K. SCHIMMELPFENG and C. KLÄMBT, 1999 Commissure formation in the embryonic CNS of Drosophila. II. Function of the different midline cells. Development 126: 771-779.
29. HUMMEL, T., K. KRUKKERT, J. ROOS, G. DAVIS and C. KLÄMBT, 2000 Drosophila futsch/22C10 is a MAP1B-like protein required for dendritic and axonal development. Neuron 26: 357-370.
30. ITO, H., K. FUJITANI, K. USUI, K. SHIMIZU-NISHIKAWA, S. TANAKA et al., 1996 Sexual orientation in Drosophila is altered by the satori mutation in the sex determination gene fruitless that encodes a Zinc finger protein with a BTB domain. Proc. Natl. Acad. Sci. USA 93: 9687-9692.
31. JACOBS, J. R., 2000 The midline glia of Drosophila: a molecular genetic model for the developmental function of glia. Prog. Neurobiol. 62: 475-508.
32. JONES, B. W., R. J. FETTER, G. TEAR and C. S. GOODMAN, 1995 glial cells missing: a genetic switch that controls glial versus neuronal fate. Cell 82: 1013-1023.
33. KLAES, A., T. MENNE, A. STOLLEWERK, H. SCHOLZ and C. KLÄMBT, 1994 The Ets transcription factors encoded by the Drosophila gene pointed direct glial cell differentiation in the embryonic CNS. Cell 78: 149-160.
34. KLÄMBT, C., 1993 The Drosophila gene pointed encodes two ETS-like proteins, which are involved in the development of the midline glial cells. Development 117: 163-176.
35. KRUEGER, N. X., D. VAN VACTOR, H. I. WAN, W. M. GELBART, C. S. GOODMAN et al., 1996 The transmembrane tyrosine phosphatase DLAR controls motor axon guidance in Drosophila. Cell 84: 611-622.
36. LEE, G., and J. C. HALL, 2001 Abnormalities of male-specific FRU protein and serotonin expression in the central nervons nervous system of fruitless mutants in Drosophila. J. Neurosci. 21: 513-526.
37. LEE, G., M. FOSS, S. F. GOODWIN, T. CARLO, B. J. TAYLOR et al., 2000 Spatial, temporal, and sexually dimorphic expression patterns of the fruitless gene in the Drosophila central nervous system. J. Neurobiol. 43: 404-426.
38. LEE, G., A. VILLELLA, B. J. TAYLOR and J. C. HALL, 2001 New reproductive anomalies in fruitless-mutant Drosophila males: extreme lengthening of mating durations and infertility correlated with defective serotonergic innervation of reproductive organs. J. Neurobiol. 47: 121-149.
39. LIN, D. M., and C. S. GOODMAN, 1994 Ectopic and increased expression of Fasciclin II alters motoneuron growth cone guidance. Neuron 13: 507-523.
40. LIN, D. M., R. D. FETTER, C. KOPCZYNSKI, G. GRENNINGLOH and C. S. GOODMAN, 1994 Genetic analysis of Fasciclin II in Drosophila: defasciculation, refasciculation, and altered fasciculation. Neuron 13: 1055-1069.
41. O'NEILL, E. M., I. REBAY, R. TIJAN and G. M. RUBIN, 1994 The activities of two Ets-related transcription factors requred for Drosophila eye development are modulated by the Ras/MAPK pathway. Cell 78: 137-147.
42. PATEL, N. H., 1994 Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes, pp. 445-487 in Drosophila melanogaster: Practical Uses in Cell and Molecular Biology, edited by L. S. B. GOLDSTEIN and E. A. FRYBERG. Academic Press, San Diego.
43. PATEL, N. H., E. MARTIN-BLANCO, K. G. COLEMAN, S. J. POOLE, M. C. ELLIS et al., 1989 Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58: 955-968.
44. RESTIFO, L. L., and W. HAUGLUM, 1998 Parallel molecular genetic pathways operate during CNS metamorphosis in Drosophila. Mol. Cell. Neurosci. 11: 134-148.
45. RESTIFO, L. L., and V. K. MERRILL, 1994 Two Drosophila regulatory genes, deformed and the Broad-Complex, share common functions in development of adult GNS, head, and salivary, glands. Dev. Biol. 162: 465-485.
46. ROBERTSON, H. M., C. R. PRESTON, R. W. PHILLIS, D. M. JOHNSON-SCHLITZ, W. K. BENZ et al., 1988 A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118: 461-470.
47. RUBIN, G. M., and A. C. SPRADLING, 1982 Genetic transformation of Drosophila with transposable element vectors. Science 218: 348-353.
48. RUBIN, J., and D. VAN VACTOR, 2000 New Roundabouts send axons into the Fas lane. Neuron 28: 637-640.
49. RYNER, L. C., S. F. GOODWIN, D. H. CASTRILLON, A. ANAND, A. VIL-LELLA et al., 1996 Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87: 1079-1089.
50. SANDSTROM, D. J., C. A. BAYER, J. W. FRISTROM and L. L. RESTIFO, 1997 Broad-Complex transcription factors regulate muscle attachment in Drosophila. Dev. Biol. 181: 168-185.
51. SCHOLZ, H., E. SADLOWSKI, A. KLAES and C. KLÄMBT, 1997 Control of midline glia development in the embryonic Drosophila CNS. Mech. Dev. 64: 137-151.
52. SEEGER, M., G. TEAR, D. FERRES-MARCO and C. S. GOODMAN, 1993 Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance towards or away from the midline. Neuron 10: 409-426.
53. SMITH, D. B., 1993 Purification of glutathione-S-transferase fusion proteins. Methods Mol. Cell. Biol. 4: 220-229,
54. SPANA, E. P., and C. Q. DOE, 1995 The prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosphila. Development 121: 3187-3195.
55. SPANA, E. P., and C. Q. DOE, 1996 Numbantagonizes Notch signaling to specify sibling neuron cell fates. Neuron 17: 21-26.
56. SPANA, E. P., C. KOPCZYNSKI, C. S. GOODMAN and C. Q. DOE, 1995 Asymmetric localization of numb autonomously determines sibling neuron identity in the Drosophila GNS. Development 121: 3489-3494.
57. SPRADLING, A. C., D. STERN, A. BEATON, E. J. RHEM, T. LAVERTY et al., 1999 The Berkeley Drosophila Genome Project gene disruption project: single P-element insertions mutating 25% of vital Drosophila genes. Genetics 153: 135-177.
58. SUN, Q., S. BAHRI, A. SCHMID, W. CHIA and K. ZINN, 2000 Receptor tyrosine phosphatases regulate axon guidance across the midline of the Drosophila embryo. Development 127: 801-812.
59. TEAR, G., 1999 Neuronal guidance. A genetic perspective. Trends Genet. 15: 113-118.
60. THOMAS, J. B., 1998 Axon guidance: crossing the midline. Curr. Biol. 8: R102-R104.
61. USUI-AOKI, K., H. ITO, UI-TEI, K. TAKAHASHI, T. LUKACSOVICH et al., 2000 Formation of the male-specific muscle in female Drosophila by ectopic fruitless expression. Nat. Cell Biol. 2: 500-506.
62. VAN ROESSEL, P., and A. H. BRAND, 2000 GAL4-mediated ectopic gene expression in Drosophila, pp 439-447 in Drosophila Protocols, edited by W. SULLIVAN, M. ASHBURNER and R. S. HAWLEY. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
63. VILLELLA, A., D. A. GAILEY, B. BERWALD, S. OHSHIMA, P. T. BARNES et al., 1997 Extended reproductive roles of the fruitless gene in Drosophila melanogaster revealed by behavioral analysis of new fru mutants. Genetics 147: 1107-1130.
64. XIONG, W.-C., H. OKANO, N. H. PATEL, J. A. BLENDY and C. MONTELL, 1994 repo encodes a glial-specific homeodomain protein required in the Drosophila nervous system. Genes Dev. 8: 981-994.
65. YEO, S. L., A. LLOYD, K. KOZAK, A. DINH, T. DICK et al., 1995 On the functional overlap between two Drosophila POU homeodomain genes and the cell fate specification of a CNS neural precursor. Genes Dev. 9: 1223-1236.
66. ZOLLMAN, S., D. GODT, G. G. PRIVE, J. L. COUDERC and F. A. LASKI, 1994 The BTB domain, found primarily in zinc finger proteins, defines an evolutionarily conserved family that includes several developmentally regulated genes in Drosophila. Proc. Natl. Acad. Sci. USA 91: 10717-10721.