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JOURNAL ARTICLES
Drosophila EcR-B ecdysone receptor isoforms are required for larval molting and for neuron remodeling during metamorphosis
M. Schubiger, A.A. Wade, G.E. Carney, J.W. Truman, M. Bender
Development 1998 125: 2053-2062;

Summary

During the metamorphic reorganization of the insect central nervous system, the steroid hormone 20-hydroxyecdysone induces a wide spectrum of cellular responses including neuronal proliferation, maturation, cell death and the remodeling of larval neurons into their adult forms. In Drosophila, expression of specific ecdysone receptor (EcR) isoforms has been correlated with particular responses, suggesting that different EcR isoforms may govern distinct steroid-induced responses in these cells. We have used imprecise excision of a P element to create EcR deletion mutants that remove the EcR-B promoter and therefore should lack EcR-B1 and EcR-B2 expression but retain EcR-A expression. Most of these EcR-B mutant animals show defects in larval molting, arresting at the boundaries between the three larval stages, while a smaller percentage of EcR-B mutants survive into the early stages of metamorphosis. Remodeling of larval neurons at metamorphosis begins with the pruning back of larval-specific dendrites and occurs as these cells are expressing high levels of EcR-B1 and little EcR-A. This pruning response is blocked in the EcR-B mutants despite the fact that adult-specific neurons, which normally express only EcR-A, can progress in their development. These observations support the hypothesis that different EcR isoforms control cell-type-specific responses during remodeling of the nervous system at metamorphosis.

REFERENCES

    1. Atkins J. F.,
    2. Weiss R. B.,
    3. Gesteland R. F.
    (1990). Ribosome gymnastics—degree of difficulty 9.5, style 10.0. Cell 62, 413–423
    OpenUrlCrossRefPubMedWeb of Science
    1. Bender M.,
    2. Imam F. B.,
    3. Talbot W. S.,
    4. Ganetzky B. S.,
    5. Hogness D. S.
    (1997) Drosophila ecdysone receptor mutations reveal functional differences among receptor isoforms. Cell 91, 777–788
    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. Carretta R.,
    9. Uemura T.,
    10. Grell E.,
    11. Jan L.,
    12. Jan Y.
    (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. Brand A. H.,
    2. Perrimon N.
    (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415
    OpenUrlAbstract
    1. Fletcher J. C.,
    2. Burtis K. C.,
    3. Hogness D. S.,
    4. Thummel C. S.
    (1995) The Drosophila E74 gene is required for metamorphosis and plays a role inthe polytene chromosome puffing response to ecdysone. Development 121, 1455–1465
    OpenUrlAbstract
    1. Ito K.,
    2. Sass H.,
    3. Urban J.,
    4. Hofbauer A.,
    5. Schneuly S.
    (1997) Gal4-responsive UAS-tau as a tool for studying the anatomy and development of the Drosophila central nervous system. Cell Tissue Res 290, 1–10
    OpenUrlCrossRefPubMedWeb of Science
    1. Jiang C.,
    2. Baehrecke E. H.,
    3. Thummel C. S.
    (1997) Steroid regulated programmed cell death during Drosophila metamorphosis. Development 124, 4673–4683
    OpenUrlAbstract
    1. Kastner P.,
    2. Mark M.,
    3. Chambon P.
    (1995) Non-steroid nuclear receptors: What are genetic studies telling us about their role in real life?. Cell 83, 859–869
    OpenUrlCrossRefPubMedWeb of Science
    1. Kastner P.,
    2. Mark M.,
    3. Ghyselinck N.,
    4. Krezel W.,
    5. Dupe V.,
    6. Grondona J. M.,
    7. Chambon P.
    (1997) Genetic evidence that the retinoid signal is transduced by heterodimeric RXR/RAR functional units during mouse development. Development 124, 313–326
    OpenUrlAbstract
    1. Koelle M. R.,
    2. Talbot W. S.,
    3. Segraves W. A.,
    4. Bender M. T.,
    5. Cherbas P.,
    6. Hogness D. S.
    (1991) The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell 67, 59–77
    OpenUrlCrossRefPubMedWeb of Science
    1. Levine R. B.,
    2. Weeks J. C.
    (1996) Cell culture approaches to understanding the action of steroid hormones on the insect nervous system. Dev.)(Neurosci 18, 73–86
    OpenUrlPubMedWeb of Science
    1. Lundquist T.,
    2. Nassel D. R.
    (1990) Substance P-like, FMRFamide-like and gastrin/cholecystokinin-like immunoreactive neurons in the thoracico-abdominal ganglia of the flies Drosophila and Calliphora. J.)(Comp. Neurol 294, 161–178
    OpenUrlCrossRefPubMedWeb of Science
    1. Masinovsky B.,
    2. Kempf S. C.,
    3. Callaway J. C.,
    4. Willows A. O.
    (1988) Monoclonal antibodies to the molluscan small cardioactive)(peptide SCPB: Immunolabeling of neurons in diverse invertebrates. J.)(Comp. Neurol 273, 500–512
    OpenUrlCrossRefPubMedWeb of Science
    1. O'Hare K.,
    2. Rubin G.
    (1983) Structures of P transposable elements and their sites of insertion and excision in the Drosophila melanogaster genome. Cell 34, 25–35
    OpenUrlCrossRefPubMedWeb of Science
    1. Oro A. E.,
    2. McKeown M.,
    3. Evans R. M.
    (1992) The Drosophila retinoid X receptor homolog ultraspiracle functions in both female reproduction and eye morphogenesis. Development 115, 449–462
    OpenUrlAbstract
    1. Perrimon N.,
    2. Engstrom L.,
    3. Mahowald A. P.
    (1985) Developmental genetics of the 2C-D region of the Drosophila X chromosome. Genetics 111, 23–41
    OpenUrlAbstract/FREE Full Text
    1. Robertson H. M.,
    2. Preston C. R.,
    3. Phillis R. W.,
    4. Johnson-Schlitz D. M.,
    5. Benz W. K.,
    6. Engels W. R.
    (1988) A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118, 461–470
    OpenUrlAbstract/FREE Full Text
    1. Robinow S.,
    2. Talbot W. S.,
    3. Hogness D. S.,
    4. Truman J. W.
    (1993) Programmed cell death in the Drosophila CNS is ecdysone-regulated and coupled with a specific ecdysone receptor isoform. Development 119, 1251–1259
    OpenUrlAbstract
    1. Schneider L. E.,
    2. Sun E. T.,
    3. Garland D. J.,
    4. Taghert P. H.
    (1993) An immunocytochemical study of the FMRFamide neuropeptide gene products in Drosophila. J.)(Comp. Neurol 337, 446–460
    OpenUrlCrossRefPubMedWeb of Science
    1. Taghert P. H.,
    2. Schneider L. E.
    (1990) Inter-specific comparison of a Drosophila gene encoding FMRFamide-related neuropeptides. J. Neurosci 10, 1929–1942
    OpenUrlAbstract
    1. Talbot W. S.,
    2. Swyryd E. A.,
    3. Hogness D. S.
    (1993) Drosophila tissues with different metamorphic responses to ecdysone express different ecdysone receptor isoforms. Cell 73, 1323–1337
    OpenUrlCrossRefPubMedWeb of Science
    1. Thomas H. E.,
    2. Stunnenberg H. G.,
    3. Stewart A. F.
    (1993) Heterodimerization of the Drosophila ecdysone receptor with retinoid X receptor and ultraspiracle. Nature 362, 471–475
    OpenUrlCrossRefPubMedWeb of Science
    1. Torok T.,
    2. Tick G.,
    3. Alvarado M.,
    4. Kiss I.
    (1993) P-lacW insertional mutagenesis on the second chromosome of Drosophila melanogaster: Isolation of lethals with different o)(vergrowth phenotypes. Genetics 135, 71–80
    OpenUrlAbstract/FREE Full Text
    1. Truman J. W.
    (1990) Metamorphosis of the central nervous system in Drosophila. J.)(Neurobiol 21, 1072–1084
    OpenUrlCrossRefPubMedWeb of Science
    1. Truman J. W.,
    2. Talbot W. S.,
    3. Fahrbach S. E.,
    4. Hogness D. S.
    (1994) Ecdysone receptor expression in the CNS correlates with stage-specific responses to ecdysteroids during Drosophila and Manduca development. Development 120, 219–234
    OpenUrlAbstract
    1. Weeks J.
    (1987) Time course of hormonal independence for developmental events in neurons and other cell types during insect metamorphosis. Dev. Biol 124, 163–176
    OpenUrlCrossRefPubMedWeb of Science
    1. Weeks J. C.,
    2. Truman J. W.
    (1985) Independent steroid control of the fates of motoneurons and their muscles during insect metamorphosis. J. Neurosci 5, 2290–2300
    OpenUrlAbstract
    1. White K.,
    2. Hurteau T.,
    3. Punsal P.
    (1986) Neuropeptide-FMRFamide-like immunoreactivity in Drosophila: Development and distribution. J. Comp. Neurol 247, 430–438
    OpenUrlCrossRefPubMedWeb of Science
    1. Yao T.-P.,
    2. Forman B. M.,
    3. Jlang Z.,
    4. Cherbas L.,
    5. Chen J.-D.,
    6. McKeown M.,
    7. Cherbas P.,
    8. Evans R. M.
    (1993) Functional ecdysone receptor is the product of EcR and Ultraspiracle genes. Nature 366, 476–479
    OpenUrlCrossRefPubMedWeb of Science
    1. Yao T. P.,
    2. Segraves W. A.,
    3. Oro A. E.,
    4. McKeown M.,
    5. Evans R. M.
    (1992) Drosophila ultraspiracle modulates ecdysone receptor function via heterodimer formation. Cell 71, 63–72
    OpenUrlCrossRefPubMedWeb of Science
    1. Zipursky S. L.,
    2. Venkatesh T. R.,
    3. Teplow D. B.,
    4. Benzer S.
    (1984) Neuronal development in the Drosophila retina: monoclonal antibodies as molecular probes. Cell 36, 15–26
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
Drosophila EcR-B ecdysone receptor isoforms are required for larval molting and for neuron remodeling during metamorphosis
M. Schubiger, A.A. Wade, G.E. Carney, J.W. Truman, M. Bender
Development 1998 125: 2053-2062;
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