Frizzled signalling controls orientation of asymmetric sense organ precursor cell divisions in Drosophila

Gho, Michel; Schweisguth, François

doi:10.1038/30265

Cited by 209 publications

(148 citation statements)

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“…Immunostaining. Dissected nota from 24-hr-APF pupae were processed as described previously (6). Primary antibodies were rat anti-Suppressor of Hairless [Su(H)] (1:500), mouse anti-Prospero (MR1a; 1:2), mouse anti-Notch (C17-9C6; 1:1000), rat anti-Ttk69 (1:300), and rabbit anti-␤-galactosidase (Cappel; 1:500).…”

Section: Methodsmentioning

confidence: 99%

“…Each pI divides asymmetrically along the anteroposterior (a-p) axis of the fly body to generate two secondary precursor cells, a posterior pIIa cell and an anterior pIIb cell (6). pIIb divides prior to pIIa, perpendicularly to the plane of the epithelium, to generate a small subepithelial glial cell, which will later migrate away from the sense organ, and a pIIIb cell (7). pIIa then divides asymmetrically, along the a-p axis to produce the shaft and socket cells.…”

mentioning

confidence: 99%

“…Finally, pIIIb divides to generate the neuron and the sheath cell. At the pI, pIIa, and pIIIb divisions, distinct fates are conferred on sister cells by the unequal activation of Notch signaling that results from the asymmetric segregation of Numb (7)(8)(9)(10). Because Numb is unequally segregated during the pIIb division, it is conceivable that Notch signaling also participates in the pIIIb͞glial cell fate decision.…”

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confidence: 99%

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Dominant-negative mutation in the β2 and β6 proteasome subunit genes affect alternative cell fate decisions in the Drosophila sense organ lineage

Schweisguth

1999

Proc. Natl. Acad. Sci. U.S.A.

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In Drosophila, dominant-negative mutations in the ␤2 and ␤6 proteasome catalytic subunit genes have been identified as dominant temperature-sensitive (DTS) mutations. At restrictive temperature, ␤2 and ␤6 DTS mutations confer lethality at the pupal stage. I investigate here the role of proteasome activity in regulating cell fate decisions in the sense organ lineage at the early pupal stage. Temperatureshift experiments in ␤2 and ␤6 DTS mutant pupae occasionally resulted in external sense organs with two sockets and no shaft. This double-socket phenotype was strongly enhanced in conditions in which Notch signaling was up-regulated. Furthermore, conditional overexpression of the ␤6 dominantnegative mutant subunit led to shaft-to-socket and to neuronto-sheath cell fate transformations, which are both usually associated with increased Notch signaling activity. Finally, expression of the ␤6 dominant-negative mutant subunit led to the stabilization of an ectopically expressed nuclear form of Notch in imaginal wing discs. This study demonstrates that mutations affecting two distinct proteasome catalytic subunits affect two alternative cell fate decisions and enhance Notch signaling activity in the sense organ lineage. These findings raise the possibility that the proteasome targets an active form of the Notch receptor for degradation in Drosophila.In eukaryotic cells, degradation of many proteins involves their covalent modification by conjugation with ubiquitin. Ubiquitinated proteins can be rapidly degraded by a large multisubunit complex called the 26S proteasome (1). This complex is present in the nucleus and in the cytosol of all cells. The 26S proteasome consists of a 20S core particle capped by two 19S regulatory complexes. The 20S proteasome is a barrel-shaped cylinder composed of four stacked rings of seven subunits each (2). The two external rings are composed of seven ␣ subunits (␣1-7), and the two inner rings comprise seven ␤ subunits (␤1-7) that catalyze the hydrolysis of polypeptide substrates.In Drosophila, the DTS7 and DTS5 dominant temperaturesensitive (DTS) mutations affect the ␤2 and ␤6 proteasome subunit genes, respectively (3, 4). DTS5 and DTS7 heterozygous flies develop perfectly at the permissive temperature (25°C), but die as undifferentiated pupae with failures in head eversion at the restrictive temperature (29°C). The DTS5 and DTS7 mutations behave genetically as antimorphic mutations, and they correspond to substitutions in residues that are conserved from flies to vertebrates (3, 4). The structure proposed for the yeast 20S proteasome indicates that ␤2 directly interacts with ␤6 in the adjacent ring (2), and it predicts that the amino acids mutated in the DTS5 and DTS7

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Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Dominant-negative mutation in the β2 and β6 proteasome subunit genes affect alternative cell fate decisions in the Drosophila sense organ lineage

Schweisguth

1999

Proc. Natl. Acad. Sci. U.S.A.

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“…Third, in both processes, these Fz-dependent localizations do not critically contribute to the final polarized structures, because loss of Fz (or other core group proteins) only leads to randomization in the positioning of the (usually) single-hair focus or Numb complex (Fig. 6 Center) (10,11,37). Thus, there appear to be two semiindependent mechanisms: (i) the polarization of the core group PCP proteins, which instructs (ii) the position of the self-assembling complexes.…”

Section: Both Fz and Dfz2 Appear Able To Act As Exchange Factors Formentioning

confidence: 99%

“…When the Frizzled (Fz) receptor is removed from these cells, each is still largely capable of polarizing and secreting a hair from a unique position, but the coordination is lost; the hairs are no longer uniformly arranged (10). Similarly, in fz mutants, the SOPs still polarize and divide asymmetrically; it is the correct orientation of the asymmetry that is lost (11). By inference, then, the axis of polarization of SOPs and cells of PCP are regulated by extracellular information transduced through the Fz receptor.…”

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confidence: 99%

Dual roles for the trimeric G protein Go in asymmetric cell division in Drosophila

Katanaev

Tomlinson

2006

Proc. Natl. Acad. Sci. U.S.A.

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During asymmetric division, a cell polarizes and differentially distributes components to its opposite ends. The subsequent division differentially segregates the two component pools to the daughters, which thereby inherit different developmental directives. In Drosophila sensory organ precursor cells, the localization of Numb protein to the cell's anterior cortex is a key patterning event and is achieved by the combined action of many proteins, including Pins, which itself is localized anteriorly. Here, a role is described for the trimeric G protein Go in the anterior localization of Numb and daughter cell fate specification. Go is shown to interact with Pins. In addition to a role in recruiting Numb to an asymmetric location in the cell's cortex, Go transduces a signal from the Frizzled receptor that directs the position in which the complex forms. Thus, Go likely integrates the signaling that directs the formation of the complex with the signaling that directs where the complex forms.Frizzled ͉ cell polarization ͉ signal transduction

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Centriole positioning in epithelial cells and its intimate relationship with planar cell polarity

2016

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Planar cell polarity (PCP)-signaling and associated tissue polarization are evolutionarily conserved. A well documented feature of PCP-signaling in vertebrates is its link to centriole/cilia positioning, although the relationship of PCP and ciliogenesis is still debated. A recent report in Drosophila established that Frizzled (Fz)-PCP core signaling has an instructive input to polarized centriole positioning in non-ciliated Drosophila wing epithelia as a PCP read-out. Here, we review the impact of this observation in the context of recent descriptions of the relationship(s) of core Fz-PCP signaling and cilia/centriole positioning in epithelial and non-epithelial cells. All existing data are consistent with a model where Fz-PCP signaling functions upstream of centriole/cilia positioning, independent of ciliogenesis. The combined data sets indicate that the Fz-Dsh PCP complex is instructive for centriole/ciliary positioning via an actin-based mechanism. Thereby, centriole/cilia/centrosome positioning can be considered an evolutionarily conserved readout and common downstream effect of PCP-signaling from flies to mammals.

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Frizzled signalling controls orientation of asymmetric sense organ precursor cell divisions in Drosophila

Cited by 209 publications

References 21 publications

Dominant-negative mutation in the β2 and β6 proteasome subunit genes affect alternative cell fate decisions in the Drosophila sense organ lineage

Dominant-negative mutation in the β2 and β6 proteasome subunit genes affect alternative cell fate decisions in the Drosophila sense organ lineage

Dual roles for the trimeric G protein Go in asymmetric cell division in Drosophila

Centriole positioning in epithelial cells and its intimate relationship with planar cell polarity

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