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JOURNAL ARTICLES
asense is a Drosophila neural precursor gene and is capable of initiating sense organ formation
M. Brand, A.P. Jarman, L.Y. Jan, Y.N. Jan
Development 1993 119: 1-17;

Summary

Neural precursor cells in Drosophila arise from the ectoderm in the embryo and from imaginal disc epithelia in the larva. In both cases, this process requires daughterless and the proneural genes achaete, scute and lethal-of-scute of the achaete-scute complex. These genes encode basic helix-loop-helix proteins, which are nuclear transcription factors, as does the asense gene of the achaete-scute complex. Our studies suggest that asense is a neural precursor gene, rather than a proneural gene. Unlike the proneural achaete-scute gene products, the asense RNA and protein are found in the neural precursor during its formation, but not in the proneural cluster of cells that gives rise to the neural precursor cell. Also, asense expression persists longer during neural precursor development than the proneural gene products; it is still expressed after the first division of the neural precursor. Moreover, asense is likely to be downstream of the proneural genes, because (1) asense expression is affected in proneural and neurogenic mutant backgrounds, (2) ectopic expression of asense protein with an intact DNA-binding domain bypasses the requirement for achaete and scute in the formation of imaginal sense organs. We further note that asense ectopic expression is capable of initiating the sense organ fate in cells that do not normally require the action of asense. Our studies therefore serve as a cautionary note for the inference of normal gene function based on the gain-of-function phenotype after ectopic expression.

REFERENCES

    1. Alonso M. C.,
    2. Cabrera C. V.
    (1988). The achaete-scute complex of Drosophila melanogaster comprises four homologous genes. EMBO J 7, 2585–2591
    OpenUrlPubMedWeb of Science
    1. Artavanis-Tsakonas S.
    (1988). The molecular biology of the Notch locus and the fine tuning of differentiation in Drosophila. Trends in Genetics 4, 95–100
    OpenUrlCrossRefPubMedWeb of Science
    1. Bier E.,
    2. Vaessin H.,
    3. Shepherd S.,
    4. Lee K.,
    5. McCall K.,
    6. Barbel S.,
    7. Ackerman L.,
    8. Carretto R.,
    9. Uemura T.,
    10. Grell E.,
    11. Jan L. Y.,
    12. Jan Y. N.
    (1989). Searching for pattern and mutation in the Drosophila genome with a P- lacZ vector. Genes Dev 3, 1273–1287
    OpenUrlAbstract/FREE Full Text
    1. Bier E.,
    2. Vaessin H.,
    3. Younger-Shepherd S.,
    4. Jan L. Y.,
    5. Jan Y. N.
    (1988). deadpan, an essential pan-neural gene in Drosophila, encodes a helix-loop-helix protein with a structure similar to the hairy product. Genes Dev 6, 2137–2151
    OpenUrl
    1. Blochlinger K.,
    2. Jan L. Y.,
    3. Jan Y. N.
    (1991). Transformation of sensory organ identity by ectopic expression of Cut in Drosophila. Genes Dev 5, 1124–1135
    OpenUrlAbstract/FREE Full Text
    1. Bober E.,
    2. Lyons G. E.,
    3. Braun T.,
    4. Cossu G.,
    5. Buckingham M.,
    6. Arnold H. H.
    (1991). The muscle regulatory gene, Myf-5, has a biphasic pattern of expression during early mouse development. J. Cell Biol 113, 1255–1265
    OpenUrlAbstract/FREE Full Text
    1. Boulianne G. L.,
    2. de la Concha A.,
    3. Campos-Ortega J. A.,
    4. Jan L. Y.,
    5. Jan Y. N.
    (1991). The Drosophila neurogenic gene neuralized encodes a novel protein and is expressed in precursors of larval and adult neurons. EMBO J 10, 2975–2983
    OpenUrlPubMedWeb of Science
    1. Braun T.,
    2. Rudnicki M. A.,
    3. Arnold H. H.,
    4. Jaenisch R.
    (1992). Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death. Cell 71, 369–382
    OpenUrlCrossRefPubMedWeb of Science
    1. Cabrera C. V.,
    2. Martínez-Arias A.,
    3. Bate M.
    (1987). The expression of three members of the achaete-scute gene complex correlates with neuroblast segregation in Drosophila. Cell 50, 425–433
    OpenUrlCrossRefPubMedWeb of Science
    1. Cabrera C. V.
    (1990). Lateral inhibition and cell fate during neurogenesis in Drosophila: the interactions between scute, Notch and Delta. Development 109, 733–742
    OpenUrlAbstract
    1. Cabrera C. V.,
    2. Alonso M. C.
    (1991). Transcriptional activation by heterodimers of the achaete-scute and daughterless gene products of Drosophila. EMBO J 10, 2965–2973
    OpenUrlPubMedWeb of Science
    1. Cabrera C. V.
    (1992). The generation of cell diversity during early neurogenesis in Drosophila. Development 115, 893–901
    OpenUrlPubMedWeb of Science
    1. Campos-Ortega J. A.
    (1988). Cellular interactions during early neurogenesis in Drosophila melanogaster. Trends in Neurosci 11, 400–405
    OpenUrlCrossRefPubMedWeb of Science
    1. Campos-Ortega J. A.,
    2. Jan Y. N.
    (1991). Genetic and molecular basis of neurogenesis in Drosophila melanogaster. Annu. Rev. Neurosci 14, 399–420
    OpenUrlCrossRefPubMedWeb of Science
    1. Campuzano S.,
    2. Modolell J.
    (1992). Patterning of the Drosophila nervous system: the achaete-scute gene complex. Trends Genet 8, 202–208
    OpenUrlCrossRefPubMedWeb of Science
    1. Caudy M.,
    2. Vässin H.,
    3. Brand M.,
    4. Tuma R.,
    5. Jan L. Y.,
    6. Jan Y. N.
    (1988). daughterless, a gene essential for both neurogenesis and sex determination in Drosophila, has sequence similarities to myc and the achaete-scute complex. Cell 55, 1061–1067
    OpenUrlCrossRefPubMedWeb of Science
    1. Chen L.,
    2. Krause M.,
    3. Draper B.,
    4. Weintraub H.,
    5. Fire A.
    (1992). Body wall muscle formation in Caenorhabditis elegans embryos that lack the MyoD homolog hlh-1. Science 256, 240–243
    OpenUrlAbstract/FREE Full Text
    1. Cubas P.,
    2. Modolell J.
    (1992). The extramacrochaetae gene provides information for sensory organ patterning. EMBO J 11, 3385–3393
    OpenUrlPubMedWeb of Science
    1. Cubas P.,
    2. de Celis J.-F.,
    3. Campuzano S.,
    4. Modolell J.
    (1991). Proneural clusters of achaete-scute expression and the generation of sensory organs in the Drosophila imaginal wing disc. Genes Dev 5, 996–1008
    OpenUrlAbstract/FREE Full Text
    1. Dambly-Chaudiere C.,
    2. Ghysen A.
    (1987). Independent subpatterns of sense organs require independent genes of the achaete-scute complex in Drosophila larvae. Genes Dev 1, 297–306
    OpenUrlAbstract/FREE Full Text
    1. Davis R. L.,
    2. Cheng P.-F.,
    3. Lassar A. B.,
    4. Weintraub H.
    (1990). The MyoD DNA binding domain contains a recognition code for muscle-specific gene activation. Cell 60, 733–746
    OpenUrlCrossRefPubMedWeb of Science
    1. Ellis H. M.,
    2. Spann D. R.,
    3. Posakony J. W.
    (1990). extramacrochaetae, a negative regulator of sensory organ development in Drosophila, defines a new class of Helix-Loop-Helix Proteins. Cell 61, 27–38
    OpenUrlCrossRefPubMedWeb of Science
    1. García-Bellido A.
    (1979). Genetic analysis of the achaete-scute system of Drosophila melanogaster. Genetics 91, 491–.
    OpenUrlAbstract/FREE Full Text
    1. García-Bellido A.,
    2. Santamaria P.
    (1978). Developmental analysis of the achaete-scute system of Drosophila melanogaster. Genetics 88, 469–486
    OpenUrlAbstract/FREE Full Text
    1. Garrell J.,
    2. Modolell J.
    (1990). The Drosophila extramacrochaetae locus, and antagonist of proneural genes that, like these genes, encodes a Helix-Loop-Helix protein. Cell 61, 39–48
    OpenUrlCrossRefPubMedWeb of Science
    1. Ghysen A.,
    2. Dambly-Chaudiere C.
    (1989). Genesis of the Drosophila peripheral nervous system. Trends Genet 5, 251–255
    OpenUrlCrossRefPubMedWeb of Science
    1. Ghysen A.,
    2. O'Kane C.
    (1989). Neural enhancer-like elements as specific cell markers in Drosophila. Development 105, 35–52
    OpenUrlAbstract
    1. Hartenstein A. Y.,
    2. Rugendorff A.,
    3. Tepass U.,
    4. Hartenstein V.
    (1992). The function of the neurogenic genes during epithelial development in the Drosophila embryo. Development 116, 1203–1220
    OpenUrlAbstract/FREE Full Text
    1. Hemsley A. N.,
    2. Arnheim N.,
    3. Toney M. D.,
    4. Cortopassi G.,
    5. Galas D. J.
    (1989). A simple method for site directed mutagenesis using the polymerase chain reaction. Nucleic Acids Res 17, 6545–6551
    OpenUrlAbstract/FREE Full Text
    1. Huang F.,
    2. Dambly-Chaudiere C.,
    3. Ghysen A.
    (1991). The emergence of sense organs in the wing disc of Drosophila. Development 111, 1087–1095
    OpenUrlAbstract/FREE Full Text
    1. Jarman A. P.,
    2. Brand M.,
    3. Jan L. Y.,
    4. Jan Y. N.
    (1993). The regulation and function of the helix-loop-helix gene, asense, in Drosophila neural precursors. Development 119, 19–29
    OpenUrlAbstract
    1. Jimenez F.,
    2. Campos-Ortega J. A.
    (1987). Genes in subdivision 1B of the Drosophila melanogaster X-chromosome and their influence on neural development. J. Neurogen 4, 179–.
    OpenUrlPubMedWeb of Science
    1. Jimenez F.,
    2. Campos-Ortega J. A.
    (1990). Defective neuroblast commitment in mutants of the achaete scute complex and adjacent genes of D. melanogaster. Neuron 5, 81–89
    OpenUrlCrossRefPubMedWeb of Science
    1. Murre C.,
    2. Schonleber-McCaw P.,
    3. Vaessin H.,
    4. Caudy M.,
    5. Jan L. Y.,
    6. Jan Y. N.,
    7. Cabrera C. V.,
    8. Buskin J. N.,
    9. Hauschka S. D.,
    10. Lassar A. B.,
    11. Weintraub H.,
    12. Baltimore D.
    (1989). Interactions between heterologous Helix-Loop-Helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58, 537–544
    OpenUrlCrossRefPubMedWeb of Science
    1. Olsen E. N.
    (1990). MyoD family: a paradigm for development?. Genes Dev 4, 1454–1461
    OpenUrlFREE Full Text
    1. Ott M. O.,
    2. Bober E.,
    3. Lyons G.,
    4. Arnold H. H.,
    5. Buckingham M.
    (1991). Early expression of the myogenic regulatory gene, Myf-5, in precursor cells of skeletal muscle in the mouse embryo. Development 11, 1097–1107
    OpenUrl
    1. Rodríguez I.,
    2. Hernandez R.,
    3. Modolell J.,
    4. Ruiz-Gomez M.
    (1990). Competence to develop sensory organs is temporally and spatially regulated in Drosophila epidermal primordia. EMBO J 9, 3583–3592
    OpenUrlPubMedWeb of Science
    1. Romani S.,
    2. Campuzano S.,
    3. Modolell J.
    (1987). The achaete-scute complex is expressed in neurogenic regions of Drosophila embryos. EMBO J 6, 2085–2092
    OpenUrlPubMedWeb of Science
    1. Romani S.,
    2. Campuzano S.,
    3. Macagno E.,
    4. Modolell J.
    (1989). Expression of achaete and scute genes in Drosophila imaginal discs and their function in sensory organ development. Genes Dev 3, 997–1007
    OpenUrlAbstract/FREE Full Text
    1. Rudnicki M. A.,
    2. Braun T.,
    3. Hinuma S.,
    4. Jaenisch R.
    (1992). Inactivation of MyoD leads to upregulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell 71, 383–390
    OpenUrlCrossRefPubMedWeb of Science
    1. Ruiz-Gomez M.,
    2. Ghysen A.
    (1993). The expression and role of a proneural gene, achaete, in the development of the larval nervous system of Drosophila. EMBO J 12, 1121–1130
    OpenUrlPubMedWeb of Science
    1. Sassoon D.,
    2. Lyons G.,
    3. Wright W. E.,
    4. Lin V.,
    5. Weintraub H.
    (1989). Expression of two myogenic regulatory factors myogenin and MyoD1 during mouse embryogenesis. Nature 341, 303–307
    OpenUrlCrossRefPubMed
    1. Simpson P.
    (1990). Notch and the choice of cell fate in Drosophila neuroepithelium. Trends in Genetics 6, 343–345
    OpenUrlCrossRefPubMed
    1. Skeath J. B.,
    2. Carroll S. B.
    (1991). Regulation of achaete-scute gene expression and sensory organ pattern formation in the Drosophila wing. Genes Dev 5, 984–995
    OpenUrlAbstract/FREE Full Text
    1. Tautz D.,
    2. 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
    OpenUrlCrossRefPubMedWeb of Science
    1. Truman J. W.,
    2. Bate M.
    (1988). Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev. Biol 125, 145–157
    OpenUrlCrossRefPubMedWeb of Science
    1. Vaessin H.,
    2. Grell E.,
    3. Wolff E.,
    4. Bier E.,
    5. Jan L. Y.,
    6. Jan Y. N.
    (1992). prospero is expressed in neuronal precursors and encodes a nuclear protein that is involved in the control of axonal outgrowth in Drosophila. Cell 67, 941–953
    OpenUrl
    1. Van Doren M.,
    2. Powell P. A.,
    3. Pasgernak D.,
    4. Posakony J. W.
    (1992). Spatial patterning of proneural clusters in the Drosophila wing imaginal disc: auto-and cross-regulation of achaete is antagonized by extramacrochaetae. Genes Dev 6, 2592–.
    OpenUrlAbstract/FREE Full Text
    1. Weintraub H.,
    2. Davis R.,
    3. Tapscott S.,
    4. Thayer M.,
    5. Krause M.,
    6. Benezra R.,
    7. Blackwell T.,
    8. Turner D.,
    9. Rupp R.,
    10. Hollenberg S.
    (1991). The MyoD gene family: nodal point during the specification of the muscle cell lineage. Science 251, 761–766
    OpenUrlAbstract/FREE Full Text
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JOURNAL ARTICLES
asense is a Drosophila neural precursor gene and is capable of initiating sense organ formation
M. Brand, A.P. Jarman, L.Y. Jan, Y.N. Jan
Development 1993 119: 1-17;
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