DOI: 10.1242/dev.120.6.1433. Antagonistic activities of Suppressor of Hairless and Hairless control alternative cell fates in the Drosophila adult epidermis

Antagonistic activities of Suppressor of Hairless and Hairless control alternative cell fates in the Drosophila adult epidermis

10.1242/dev.120.6.1433

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT 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 Suppres-sor of Hairless has the opposite phenotypic effects. SOP determination is prevented by an early excess of Suppres-sor 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 Sup-pressor 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.

Bibliography

Schweisguth, F., & Posakony, J. W. (1994). Antagonistic activities of Suppressor of Hairless and Hairless control alternative cell fates in the Drosophila adult epidermis. Development, 120(6), 1433â1441.

Authors 2

François Schweisguth (first)
James W. Posakony (additional)

References 30 Referenced 124

10.1093/genetics/101.3-4.447 / Genetics / The genetics of a small autosomal region of Drosophila melanogaster containing the structural gene for alcohol dehydrogenase. III. Hypomorphic and hypermorphic mutations affecting the expression of Hairless by Ashburner (1982)
10.1242/dev.111.1.89 / Development / Hairless is required for the development of adult sensory organ precursor cells in Drosophila by Bang (1991)
10.1101/gad.6.9.1752 / Genes Dev. / The Drosophila gene Hairless encodes a novel basic protein that controls alternative cell fates in adult sensory organ development by Bang (1992)
10.1101/gad.5.6.996 / Genes Dev. / Proneural clusters of achaete-scute expression and the generation of sensory organs in the Drosophila imaginal wing disc by Cubas (1991)
10.1073/pnas.88.2.632 / Proc. Natl. Acad. Sci. USA / Cell-autonomous role of Notch, an epidermal growth factor homologue, in sensory organ differentiation in Drosophila by de Celis (1991)
10.3109/01677068409107094 / J. Neurogenetics / The expression of neurogenic loci in the imaginal epidermal cells of Drosophila melanogaster by Dietrich (1984)
10.1016/0092-8674(92)90640-X / Cell / The Drosophila homolog of the immunoglobulin recombination signal-binding protein regulates peripheral nervous system development by Furukawa (1992)
10.1242/dev.105.1.35 / Development / Neural enhancer-like elements as specific cell markers in Drosophila by Ghysen (1989)
10.1016/0092-8674(89)90033-0 / Cell / The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome by Golic (1989)
10.1242/dev.116.4.1203 / Development / The function of the neurogenic genes during epithelial development in the Drosophila embryo by Hartenstein (1992)
10.1007/BF00188752 / Roux’s Arch. Dev. Biol. / Studying Drosophila embryogenesis with P-lacZ enhancer trap lines by Hartenstein (1992)
10.1242/dev.107.2.389 / Development / Development of adult sensilla on the wing and notum of Drosophila melanogaster by Hartenstein (1989)
10.1016/0012-1606(90)90147-B / Dev. Biol. / A dual function of the Notch gene in Drosophila sensillum development by Hartenstein (1990)
10.1016/0092-8674(91)90263-X / Cell / The choice of cell fate in the epidermis of Drosophila by Heitzler (1991)
10.1242/dev.111.4.1087 / Development / The emergence of sense organs in the wing disc of Drosophila by Huang (1991)
{'key': '2024121723215785200_DEVELOP_120_6_1433C16', 'first-page': '87', 'article-title': 'The development of the bristles in normal and some mutant types of Drosophila melanogaster', 'volume': '131', 'author': 'Lees', 'year': '1942', 'journal-title': 'Proc. Roy. Soc. Ser. B'} / Proc. Roy. Soc. Ser. B / The development of the bristles in normal and some mutant types of Drosophila melanogaster by Lees (1942)
{'volume-title': 'The Genome of Drosophila melanogaster', 'year': '1992', 'author': 'Lindsley', 'key': '2024121723215785200_DEVELOP_120_6_1433C17'} / The Genome of Drosophila melanogaster by Lindsley (1992)
10.1016/0925-4773(92)90006-6 / Mech. Dev. / Hairless, a Drosophila gene involved in neural development, encodes a novel, serine rich protein by Maier (1992)
10.1101/gad.4.11.1848 / Genes Dev. / Isolation and expression of scabrous, a gene regulating neurogenesis in Drosophila by Mlodzik (1990)
10.1006/dbio.1993.1151 / Dev. Biol. / Delta function is required for bristle organ determination and morphogenesis in Drosophila by Parks (1993)
10.1016/0092-8674(94)90105-8 / Cell / Nature vs. nurture: Asymmetric cell divisions in Drosophila bristle development by Posakony (1994)
10.1016/0092-8674(93)90423-N / Cell / Specific truncations of Drosophila Notch define dominant activated and dominant negative forms of the receptor by Rebay (1993)
10.1101/gad.3.7.997 / Genes Dev. / Expression of achaete and scute genes in Drosophila imaginal discs and their function in sensory organ development by Romani (1989)
10.1126/science.6289436 / Science / Genetic transformation of Drosophila with transposable element vectors by Rubin (1982)
10.1016/0092-8674(92)90641-O / Cell / Suppressor of Hairless, the Drosophila homolog of the mouse recombination signal-binding protein gene, controls sensory organ cell fates by Schweisguth (1992)
10.1242/dev.109.3.509 / Development / Lateral inhibition and the development of the sensory bristles of the adult peripheral nervous system of Drosophila by Simpson (1990)
10.1101/gad.5.6.984 / Genes Dev. / Regulation of achaete-scute gene expression and sensory organ pattern formation in the Drosophila wing by Skeath (1991)
10.1101/gad.6.12b.2592 / Genes Dev. / Spatial regulation of proneural gene activity: auto- and cross-activation of achaete is antagonized by extramacrochaetae by Van Doren (1992)
10.3109/01677068509102325 / J. Neurogenetics / Genetic interactions in early neurogenesis of Drosophila melanogaster by Vässin (1985)
10.1242/dev.117.4.1223 / Development / Analysis of genetic mosaics in developing and adult Drosophila tissues by Xu (1993)

Dates

Type	When
Created	4 years, 4 months ago (April 23, 2021, 2:45 p.m.)
Deposited	8 months, 2 weeks ago (Dec. 17, 2024, 6:22 p.m.)
Indexed	8 months, 2 weeks ago (Dec. 18, 2024, 12:39 a.m.)
Issued	31 years, 3 months ago (June 1, 1994)
Published	31 years, 3 months ago (June 1, 1994)
Published Online	31 years, 3 months ago (June 1, 1994)
Published Print	31 years, 3 months ago (June 1, 1994)

Funders 0

None

BibTeX

@article{Schweisguth_1994, title={Antagonistic activities of Suppressor of Hairless and Hairless control alternative cell fates in the Drosophila adult epidermis}, volume={120}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.120.6.1433}, DOI={10.1242/dev.120.6.1433}, number={6}, journal={Development}, publisher={The Company of Biologists}, author={Schweisguth, François and Posakony, James W.}, year={1994}, month=jun, pages={1433–1441} }

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