DOI: 10.1242/dev.124.19.3727. Wingless signaling generates pattern through two distinct mechanisms

Wingless signaling generates pattern through two distinct mechanisms

10.1242/dev.124.19.3727

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT wingless (wg) and its vertebrate homologues, the Wnt genes, play critical roles in the generation of embryonic pattern. In the developing Drosophila epidermis, wg is expressed in a single row of cells in each segment, but it influences cell identities in all rows of epidermal cells in the 10- to 12-cell-wide segment. Wg signaling promotes specification of two distinct aspects of the wild-type intrasegmental pattern: the diversity of denticle types present in the anterior denticle belt and the smooth or naked cuticle constituting the posterior surface of the segment. We have manipulated the expression of wild-type and mutant wg transgenes to explore the mechanism by which a single secreted signaling molecule can promote these distinctly different cell fates. We present evidence consistent with the idea that naked cuticle cell fate is specified by a cellular pathway distinct from the denticle diversity-generating pathway. Since these pathways are differentially activated by mutant Wg ligands, we propose that at least two discrete classes of receptor for Wg may exist, each transducing a different cellular response. We also find that broad Wg protein distribution across many cell diameters is required for the generation of denticle diversity, suggesting that intercellular transport of the Wg protein is an essential feature of pattern formation within the epidermal epithelium. Finally, we demonstrate that an 85 amino acid region not conserved in vertebrate Wnts is dispensable for Wg function and we discuss structural features of the Wingless protein required for its distinct biological activities.

Bibliography

Hays, R., Gibori, G. B., & Bejsovec, A. (1997). Wingless signaling generates pattern through two distinct mechanisms. Development, 124(19), 3727â3736.

Authors 3

Rebecca Hays (first)
Gil B. Gibori (additional)
Amy Bejsovec (additional)

References 32 Referenced 55

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10.1242/dev.113.2.471 / Development / Roles of wingless in patterning the larval epidermis of Drosophila by Bejsovec (1991)
10.1016/S1064-2722(08)60056-0 / Advances in Developmental Biochemistry / The wingless/Wnt-1 signaling pathway – new insights into the cellular mechanisms of signal transduction by Bejsovec (1996)
10.1242/dev.119.2.501 / Development / Segment polarity gene interactions modulate epidermal patterning in Drosophila embryos by Bejsovec (1993)
10.1093/genetics/139.1.309 / Genetics / Signaling activities of the Drosophila wingless gene are separately mutable and appear to be transduced at the cell surface by Bejsovec (1995)
10.1038/382225a0 / Nature / A new member of the frizzled family from Drosophila functions as a Wingless receptor by Bhanot (1996)
10.1242/dev.118.2.401 / Development / Targeted gene expression as a means of altering cell fates and generating dominant phenotypes by Brand (1993)
10.1038/385829a0 / Nature / pangolin encodes a Lef-1 homolog that acts downstream of Armadillo to transduce the Wingless signal by Brunner (1997)
10.1006/dbio.1995.1219 / Dev. Biol / Expression of the Drosophila gooseberry locus defines a subset of neuroblast lineages in the central nervous system by Buenzow (1995)
10.1016/0092-8674(85)90012-1 / Cell / Development of the embryonic pattern in D. melanogaster as revealed by the accumulation of the nuclear engrailed protein by DiNardo (1985)
10.1038/332604a0 / Nature / Two-tiered regulation of spatially patterned engrailed gene expression during Drosophilia embryogenesis by DiNardo (1988)
10.1038/360347a0 / Nature / Drosophila wingless generates cell type diversity among engrailed expressing cells by Dougan (1992)
10.1016/0092-8674(89)90033-0 / Cell / The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome by Golic (1989)
10.1038/352404a0 / Nature / Multiple modes of engrailed regulation in the progression towards cell fate determination by Heemskerk (1991)
10.1038/372461a0 / Nature / Distinct pathways for autocrine and paracrine wg signaling in Drosophila embryos by Hooper (1994)
10.1242/dev.122.12.4095 / Development / tCompartments, wingless and engrailed: patterning the ventral epidermis of Drosophila embryos by Lawrence (1996)
10.1002/j.1460-2075.1993.tb06139.x / EMBO J / Role of the gooseberry gene in Drosophila embryos: maintenance of wingless expression by a wingless-gooseberry autoregulatory loop by Li (1993)
10.1242/dev.103.1.157 / Development / Role of the segment polarity genes in the definition and maintenance of cell states in the Drosophila embryo by Martinez Arias (1988)
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{'key': '2025021405021033400_DEVELOP_124_19_3727C30', 'first-page': '160', 'article-title': 'Optical clean and permanent whole mount preparation for phase-contrast microscopy of cuticular structures of insect larvae', 'volume': '52', 'author': 'van der Meer', 'year': '1977', 'journal-title': 'Dros. Inf. Serv'} / Dros. Inf. Serv / Optical clean and permanent whole mount preparation for phase-contrast microscopy of cuticular structures of insect larvae by van der Meer (1977)
10.1006/dbio.1995.1243 / Dev. Biol / Evidence for engrailed-independent wingless autoregulation in Drosophila by Yoffe (1995)
10.1016/S0092-8674(00)81991-1 / Cell / Direct and long-range action of a wingless morphogen gradient by Zecca (1996)

Dates

Type	When
Created	4 years, 4 months ago (April 23, 2021, 3:20 p.m.)
Deposited	6 months, 2 weeks ago (Feb. 14, 2025, 12:02 a.m.)
Indexed	6 months, 2 weeks ago (Feb. 15, 2025, 12:05 a.m.)
Issued	27 years, 11 months ago (Oct. 1, 1997)
Published	27 years, 11 months ago (Oct. 1, 1997)
Published Online	27 years, 11 months ago (Oct. 1, 1997)
Published Print	27 years, 11 months ago (Oct. 1, 1997)

Funders 0

None

BibTeX

@article{Hays_1997, title={Wingless signaling generates pattern through two distinct mechanisms}, volume={124}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.124.19.3727}, DOI={10.1242/dev.124.19.3727}, number={19}, journal={Development}, publisher={The Company of Biologists}, author={Hays, Rebecca and Gibori, Gil B. and Bejsovec, Amy}, year={1997}, month=oct, pages={3727–3736} }

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