Dachsous-Dependent Asymmetric Localization of Spiny-Legs Determines Planar Cell Polarity Orientation in Drosophila

Ayukawa, Tomonori; Akiyama, Morito; Mummery-Widmer, Jennifer L.; Stoeger, Thomas; Sasaki, Junko; Knoblich, Juergen A.; Senoo, Haruki; Sasaki, Takehiko; Yamazaki, Masakazu

doi:10.1016/j.celrep.2014.06.009

Cited by 65 publications

(143 citation statements)

References 60 publications

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“…Once initial polarity has been set up through the Ds/Ft pathway, this is further relayed to and/or amplified by the core pathway. Notably, a similar two-step mechanism has also been proposed for the wing (Hogan et al, 2011;Ma et al, 2003;Yang et al, 2002) and could apply to other tissues (Olofsson et al, 2014;Ayukawa et al, 2014).…”

Section: Discussionmentioning

confidence: 92%

“…Current studies suggest that the two pathways can interact in different ways, depending on the cell context, with Ds gradient direction and core module polarization oriented either parallel or anti-parallel (Zeidler et al, 2000;Casal et al, 2002;Ma et al, 2003;Matakatsu and Blair, 2004;Rogulja et al, 2008). Notably, it has been proposed that the global system provides a directionality cue that is then used by the core system to align the polarity of each cell with that of their neighbors (Hogan et al, 2011;Ma et al, 2003;Olofsson et al, 2014;Ayukawa et al, 2014).…”

Section: Introductionmentioning

confidence: 97%

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The Atypical Cadherin Dachsous Controls Left-Right Asymmetry in Drosophila

et al. 2015

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Left-right (LR) asymmetry is essential for organ development and function in metazoans, but how initial LR cue is relayed to tissues still remains unclear. Here, we propose a mechanism by which the Drosophila LR determinant Myosin ID (MyoID) transfers LR information to neighboring cells through the planar cell polarity (PCP) atypical cadherin Dachsous (Ds). Molecular interaction between MyoID and Ds in a specific LR organizer controls dextral cell polarity of adjoining hindgut progenitors and is required for organ looping in adults. Loss of Ds blocks hindgut tissue polarization and looping, indicating that Ds is a crucial factor for both LR cue transmission and asymmetric morphogenesis. We further show that the Ds/Fat and Frizzled PCP pathways are required for the spreading of LR asymmetry throughout the hindgut progenitor tissue. These results identify a direct functional coupling between the LR determinant MyoID and PCP, essential for non-autonomous propagation of early LR asymmetry.

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Section: Discussionmentioning

confidence: 92%

Section: Introductionmentioning

confidence: 97%

The Atypical Cadherin Dachsous Controls Left-Right Asymmetry in Drosophila

et al. 2015

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“…We refer the reader to related results in the following in-press report (Ayukawa et al, 2014). In addition to finding a function for the Pk-Sple isoform ratio in orienting the response to the Ft/Ds/Fj signal, the authors suggest a mechanism in which the unique N-terminal portion of Sple is coupled to Ds localization through interaction with Dachs.…”

Section: Note Added In Proofmentioning

confidence: 99%

Prickle/spiny-legs isoforms control the polarity of the apical microtubule network in planar cell polarity

Olofsson¹,

Sharp²,

Matis³

et al. 2014

Journal of Cell Science

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Microtubules (MTs) are substrates upon which plus-and minus-end directed motors control the directional movement of cargos that are essential for generating cell polarity. Although centrosomal MTs are organized with plus-ends away from the MT organizing center, the regulation of non-centrosomal MT polarity is poorly understood. Increasing evidence supports the model that directional information for planar polarization is derived from the alignment of a parallel apical network of MTs and the directional MT-dependent trafficking of downstream signaling components. The Fat/Dachsous/Fourjointed (Ft/Ds/Fj) signaling system contributes to orienting those MTs. In addition to previously defined functions in promoting asymmetric subcellular localization of 'core' planar cell polarity (PCP) proteins, we find that alternative Prickle (Pk-Sple) protein isoforms control the polarity of this MT network. This function allows the isoforms of Pk-Sple to differentially determine the direction in which asymmetry is established and therefore, ultimately, the direction of tissue polarity. Oppositely oriented signals that are encoded by oppositely oriented Fj and Ds gradients produce the same polarity outcome in different tissues or compartments, and the tissue-specific activity of alternative Pk-Sple protein isoforms has been observed to rectify the interpretation of opposite upstream directional signals. The control of MT polarity, and thus the directionality of apical vesicle traffic, by Pk-Sple provides a mechanism for this rectification.

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“…ft is expressed in a relatively uniform pattern throughout the eye disc, whereas ds is expressed in a gradient with highest levels at the poles. Mutations in the Fat/Ds system cause strong PCP defects throughout the entire disc (Yang et al, 2002;Rawls et al, 2002;Simon, 2004;Brittle et al, 2012;Thomas and Strutt, 2012;Sharma and McNeill, 2013;Ayukawa et al, 2014). By contrast, the eyes of homozygous loss-of-function fj mutant alleles are characterized by relatively weak PCP defects (Zeidler et al, 1999).…”

Section: Introductionmentioning

confidence: 99%

Extramacrochaetae functions in dorsal-ventral patterning ofDrosophilaimaginal discs

Spratford

Kumar

2015

Development

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One of the seminal events in the history of a tissue is the establishment of the anterior-posterior, dorsal-ventral (D/V) and proximal-distal axes. Axis formation is important for the regional specification of a tissue and allows cells along the different axes to obtain directional and positional information. Within the Drosophila retina, D/V axis formation is essential to ensure that each unit eye first adopts the proper chiral form and then rotates precisely 90°in the correct direction. These two steps are important because the photoreceptor array must be correctly aligned with the neurons of the optic lobe. Defects in chirality and/or ommatidial rotation will lead to disorganization of the photoreceptor array, misalignment of retinal and optic lobe neurons, and loss of visual acuity. Loss of the helixloop-helix protein Extramacrochaetae (Emc) leads to defects in both ommatidial chirality and rotation. Here, we describe a new role for emc in eye development in patterning the D/V axis. We show that the juxtaposition of dorsal and ventral fated tissue in the eye leads to an enrichment of emc expression at the D/V midline. emc expression at the midline can be eliminated when D/V patterning is disrupted and can be induced in situations in which ectopic boundaries are artificially generated. We also show that emc functions downstream of Notch signaling to maintain the expression of four-jointed along the midline.

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Dachsous-Dependent Asymmetric Localization of Spiny-Legs Determines Planar Cell Polarity Orientation in Drosophila

Cited by 65 publications

References 60 publications

The Atypical Cadherin Dachsous Controls Left-Right Asymmetry in Drosophila

The Atypical Cadherin Dachsous Controls Left-Right Asymmetry in Drosophila

Prickle/spiny-legs isoforms control the polarity of the apical microtubule network in planar cell polarity

Extramacrochaetae functions in dorsal-ventral patterning ofDrosophilaimaginal discs

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