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JOURNAL ARTICLES
Antagonistic activities of Suppressor of Hairless and Hairless control alternative cell fates in the Drosophila adult epidermis
F. Schweisguth, J.W. Posakony
Development 1994 120: 1433-1441;

Summary

Successive alternative cell fate choices in the imaginal disc epithelium lead to the differentiation of a relatively invariant pattern of multicellular adult sensory organs in Drosophila. We show here that the activity of Suppressor of Hairless is required for both the sensory organ precursor (SOP) versus epidermal cell fate decision, and for the trichogen (shaft) versus tormogen (socket) cell fate choice. Complete loss of Suppressor of Hairless function causes most proneural cluster cells to accumulate high levels of the achaete and Delta proteins and to adopt the SOP fate. Late or partial reduction in Suppressor of Hairless activity leads to the apparent transformation of the tormogen (socket) cell into a second trichogen (shaft) cell, producing a ‘double shaft’ phenotype. We find that overexpression of Suppressor of Hairless has the opposite phenotypic effects. SOP determination is prevented by an early excess of Suppressor of Hairless activity, while at a later stage, the trichogen (shaft) cell is transformed into a second tormogen (socket) cell, resulting in ‘double socket’ bristles. We conclude that, for two different cell fate decisions in adult sensory organ development, decreasing or increasing the level of Suppressor of Hairless function confers mutant phenotypes that closely resemble those associated with gain and loss of Hairless activity, respectively. These results, along with the intermediate SOP phenotype observed in Suppressor of Hairless; Hairless double mutant imaginal discs, suggest that the two genes act antagonistically to commit imaginal disc cells stably to alternative fates.

REFERENCES

    1. Bang A.,
    2. Hartenstein V.,
    3. Posakony J. W.
    (1991) Hairless is required for the development of adult sensory organ precursor cells in Drosophila. Development 111, 89–104
    OpenUrlAbstract
    1. Bang A.,
    2. Posakony J. W.
    (1992) The Drosophila gene Hairless encodes a novel basic protein that controls alternative cell fates in adult sensory organ development. Genes Dev 6, 1752–1769
    OpenUrlAbstract/FREE Full Text
    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. de Celis J.,
    2. Mari-Beffa M.,
    3. Garcia-Bellido A.
    (1991) Cell-autonomous role of Notch, an epidermal growth factor homologue, in sensory organ differentiation in Drosophila. Proc. Natl. Acad. Sci. USA 88, 632–636
    OpenUrlAbstract/FREE Full Text
    1. Dietrich U.,
    2. Campos-Ortega J. A.
    (1984) The expression of neurogenic loci in the imaginal epidermal cells of Drosophila melanogaster. J. Neurogenetics 1, 315–332
    OpenUrlPubMed
    1. Furukawa T.,
    2. Maruyama S.,
    3. Kawaichi M.,
    4. Honjo T.
    (1992) The Drosophila homolog of the immunoglobulin recombination signal-binding protein regulates peripheral nervous system development. Cell 69, 1191–1197
    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. Golic K.,
    2. Lindquist S.
    (1989) The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59, 499–509
    OpenUrlCrossRefPubMedWeb of Science
    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. Hartenstein V.,
    2. Posakony J. W.
    (1989) Development of adult sensilla on the wing and notum of Drosophila melanogaster. Development 107, 389–405
    OpenUrlAbstract
    1. Hartenstein V.,
    2. Posakony J. W.
    (1990) A dual function of the Notch gene in Drosophila sensillum development. Dev. Biol 142, 13–30
    OpenUrlCrossRefPubMedWeb of Science
    1. Heitzler P.,
    2. Simpson P.
    (1991) The choice of cell fate in the epidermis of Drosophila. Cell 64, 1083–1092
    OpenUrlCrossRefPubMedWeb of Science
    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. Lees A. D.,
    2. Waddington C. H.
    (1942) The development of the bristles in normal and some mutant types of Drosophila melanogaster. Proc. Roy. Soc. Ser. B 131, 87–110
    OpenUrlAbstract/FREE Full Text
    1. Maier D.,
    2. Stumm G.,
    3. Kuhn K.,
    4. Preiss A.
    (1992) Hairless, a Drosophila gene involved in neural development, encodes a novel, serine rich protein. Mech. Dev 38, 143–156
    OpenUrlCrossRefPubMedWeb of Science
    1. Mlodzik M.,
    2. Baker N. E.,
    3. Rubin G. M.
    (1990) Isolation and expression of scabrous, a gene regulating neurogenesis in Drosophila. Genes Dev 4, 1848–1861
    OpenUrlAbstract/FREE Full Text
    1. Parks A. L.,
    2. Muskavitch M. A.
    (1993) Delta function is required for bristle organ determination and morphogenesis in Drosophila. Dev. Biol 157, 484–496
    OpenUrlCrossRefPubMedWeb of Science
    1. Posakony J. W.
    (1994) Nature vs. nurture: Asymmetric cell divisions in Drosophila bristle development. Cell 76, 415–418
    OpenUrlCrossRefPubMedWeb of Science
    1. Rebay I.,
    2. Fehon R. G.,
    3. Artavanis-Tsakonas S.
    (1993) Specific truncations of Drosophila Notch define dominant activated and dominant negative forms of the receptor. Cell 74, 319–329
    OpenUrlCrossRefPubMedWeb of Science
    1. Romani S.,
    2. Campuzano S.,
    3. Macagno E. R.,
    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. Rubin G. M.,
    2. Spradling A. C.
    (1982) Genetic transformation of Drosophila with transposable element vectors. Science 218, 348–353
    OpenUrlAbstract/FREE Full Text
    1. Schweisguth F.,
    2. Posakony J. W.
    (1992) Suppressor of Hairless, the Drosophila homolog of the mouse recombination signal-binding protein gene, controls sensory organ cell fates. Cell 69, 1199–1212
    OpenUrlCrossRefPubMedWeb of Science
    1. Simpson P.
    (1990) Lateral inhibition and the development of the sensory bristles of the adult peripheral nervous system of Drosophila. Development 109, 509–519
    OpenUrlAbstract
    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. Van Doren M.,
    2. Powell P. A.,
    3. Pasternak D.,
    4. Singson A.,
    5. Posakony J. W.
    (1992) Spatial regulation of proneural gene activity: auto-and cross-activation of achaete is antagonized by extramacrochaetae. Genes Dev 6, 2592–2605
    OpenUrlAbstract/FREE Full Text
    1. Xu T.,
    2. Rubin G. M.
    (1993) Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223–1237
    OpenUrlAbstract
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JOURNAL ARTICLES
Antagonistic activities of Suppressor of Hairless and Hairless control alternative cell fates in the Drosophila adult epidermis
F. Schweisguth, J.W. Posakony
Development 1994 120: 1433-1441;
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