Overlapping Roles of<i>Drosophila</i>Drak and Rok Kinases in Epithelial Tissue Morphogenesis

Neubueser, Dagmar; Hipfner, David R.

doi:10.1091/mbc.e10-04-0328

Cited by 22 publications

(43 citation statements)

References 62 publications

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“…This is the case for the activation of MyoII during intercalation as germband extension proceeds (Bertet et al, 2004;Simoes Sde et al, 2010), but also during various instances of compartment boundary formation and cell sorting situations in the embryo (Monier et al, 2010) and in the wing imaginal disc (Landsberg et al, 2009). Our work reveals that in the constricting cells of the MF, Rok functions redundantly with Drak, a kinase recently shown to phosphorylate Sqh both in vitro and in vivo (Neubueser and Hipfner, 2010). It is noteworthy that previous work has shown that RhoGEF2 is not required for cell constriction in the MF (Corrigall et al, 2007;Escudero et al, 2007), suggesting that perhaps another guanine exchange factor (GEF) might function redundantly with RhoGEF2 to promote cell constriction.…”

Section: Epithelial Cell Constriction and Multicellular Pattern Formasupporting

confidence: 59%

“…Images in RЈ and RЉ were created using the Fire filter from FIJI. (Neubueser and Hipfner, 2010). Examination of retina lacking Drak function and heterozygous for rok 2 revealed instances of impaired cell constriction (Fig.…”

Section: Drak and Rok Function Redundantly During Multicellular Pattementioning

confidence: 94%

“…-w,hsflp122;Tub>w[+] (Neubueser and Hipfner, 2010) and discs were examined for defects in constriction. Drak Del (Neubueser and Hipfner, 2010) was recombined onto a rok 2 FRT19A chromosome and recombinants were tested using PCR.…”

Section: Genotypes Used In This Studymentioning

confidence: 99%

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Atonal and EGFR signalling orchestraterok- andDrak-dependent adherens junction remodelling during ommatidia morphogenesis

et al. 2012

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SUMMARYMorphogenesis of epithelial tissues relies on the interplay between cell division, differentiation and regulated changes in cell shape, intercalation and sorting. These processes are often studied individually in relatively simple epithelia that lack the complexity found during organogenesis when these processes might all coexist simultaneously. To address this issue, we are making use of the developing fly retinal neuroepithelium. Retinal morphogenesis relies on a coordinated sequence of interdependent morphogenetic events that includes apical cell constriction, localized alignment of groups of cells and ommatidia morphogenesis coupled to neurogenesis. Here, we use live imaging to document the sequence of adherens junction (AJ) remodelling events required to generate the fly ommatidium. In this context, we demonstrate that the kinases Rok and Drak function redundantly during Myosin II-dependent cell constriction, subsequent multicellular alignment and AJ remodelling. In addition, we show that early multicellular patterning characterized by cell alignment is promoted by the conserved transcription factor Atonal (Ato). Further ommatidium patterning requires the epidermal growth factor receptor (EGFR) signalling pathway, which transcriptionally governs rok-and Drakdependent AJ remodelling while also promoting neurogenesis. In conclusion, our work reveals an important role for Drak in regulating AJ remodelling during retinal morphogenesis. It also sheds new light on the interplay between Ato, EGFR-dependent transcription and AJ remodelling in a system in which neurogenesis is coupled with cell shape changes and regulated steps of cell intercalation.

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Section: Epithelial Cell Constriction and Multicellular Pattern Formasupporting

confidence: 59%

Section: Drak and Rok Function Redundantly During Multicellular Pattementioning

confidence: 94%

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Atonal and EGFR signalling orchestraterok- andDrak-dependent adherens junction remodelling during ommatidia morphogenesis

et al. 2012

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“…The combined depletion of both Par-1 and Rok almost completely abolished detachment, suggesting that the two kinases converge (directly or indirectly) on the same target (Myo-II). Epithelial morphogenesis during C. elegans embryonic elongation and Drosophila larval tissue development require multiple kinases to optimally activate Myo-II [42, 43]. Furthermore, different kinases have been shown to regulate MRLC activation at discrete locations within single migrating cells.…”

Section: Discussionmentioning

confidence: 99%

Par-1 Controls Myosin-II Activity through Myosin Phosphatase to Regulate Border Cell Migration

et al. 2012

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Summary Background Localized actomyosin contraction couples with actin polymerization and cell-matrix adhesion to regulate cell protrusions and retract trailing edges of migrating cells. While many cells migrate in collective groups during tissue morphogenesis, mechanisms that coordinate actomyosin dynamics in collective cell migration are poorly understood. Migration of Drosophila border cells, a genetically tractable model for collective cell migration, requires non-muscle myosin-II (Myo-II). How Myo-II specifically controls border cell migration and how Myo-II is itself regulated is largely unknown. Results We show that Myo-II regulates two essential features of border cell migration: 1) initial detachment of the border cell cluster from the follicular epithelium and 2) the dynamics of cellular protrusions. We further demonstrate that the cell polarity protein Par-1 (MARK), a serine-threonine kinase, regulates the localization and activation of Myo-II in border cells. Par-1 binds to myosin phosphatase and phosphorylates it at a known inactivating site. Par-1 thus promotes phosphorylated Myosin Regulatory Light Chain (MRLC), thereby increasing Myo-II activity. Furthermore, Par-1 localizes to and increases active Myo-II at the cluster rear to promote detachment; in the absence of Par-1, spatially distinct active Myo-II is lost. Conclusions We identify a critical new role for Par-1 kinase: spatiotemporal regulation of Myo-II activity within the border cell cluster through localized inhibition of myosin phosphatase. Polarity proteins such as Par-1, which intrinsically localize, can thus directly modulate the actomyosin dynamics required for border cell detachment and migration. Such a link between polarity proteins and cytoskeletal dynamics may also occur in other collective cell migrations.

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“…In recent years, there is much research on the molecular basis for the polarity in epithelial cells [53-58] as well as their intercellular junctions [44,55,57,59-61]. Tyler [62] concludes that epithelial cells appear first in the Eumetazoan blastula and are a prominent feature in subsequent adult tissues.…”

Section: Discussionmentioning

confidence: 99%

The ultrastructure of book lung development in the bark scorpion Centruroides gracilis (Scorpiones: Buthidae)

Farley

2011

Front Zool

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BackgroundNear the end of the nineteenth century the hypothesis was presented for the homology of book lungs in arachnids and book gills in the horseshoe crab. Early studies with the light microscope showed that book gill lamellae are formed by outgrowth and possibly some invagination (infolding) of hypodermis (epithelium) from the posterior surface of opisthosomal limb buds. Scorpion book lungs are formed near the bilateral sites of earlier limb buds. Hypodermal invaginations in the ventral opisthosoma result in spiracles and sac-like cavities (atria). In early histological sections of embryo book lungs, widening of the atrial entrance of some lamellae (air channels, air sacs, saccules) was interpreted as an indication of invagination as hypothesized for book gill lamellae. The hypodermal infolding was thought to produce the many rows of lamellar precursor cells anterior to the atrium. The ultrastructure of scorpion book lung development is compared herein with earlier investigations of book gill formation.ResultsIn scorpion embryos, there is ingression (inward migration) of atrial hypodermal cells rather than invagination or infolding of the atrial hypodermal layer. The ingressing cells proliferate and align in rows anterior to the atrium. Their apical-basal polarity results in primordial air channels among double rows of cells. The cuticular walls of the air channels are produced by secretion from the apical surfaces of the aligned cells. Since the precursor cells are in rows, their secreted product is also in rows (i.e., primordial air channels, saccules). For each double row of cells, their opposed basal surfaces are gradually separated by a hemolymph channel of increasing width.ConclusionsThe results from this and earlier studies show there are differences and similarities in the formation of book lung and book gill lamellae. The homology hypothesis for these respiratory organs is thus supported or not supported depending on which developmental features are emphasized. For both organs, when the epithelial cells are in position, their apical-basal polarity results in alternate page-like channels of hemolymph and air or water with outward directed hemolymph saccules for book gills and inward directed air saccules for book lungs.

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Overlapping Roles ofDrosophilaDrak and Rok Kinases in Epithelial Tissue Morphogenesis

Cited by 22 publications

References 62 publications

Atonal and EGFR signalling orchestraterok- andDrak-dependent adherens junction remodelling during ommatidia morphogenesis

Atonal and EGFR signalling orchestraterok- andDrak-dependent adherens junction remodelling during ommatidia morphogenesis

Par-1 Controls Myosin-II Activity through Myosin Phosphatase to Regulate Border Cell Migration

The ultrastructure of book lung development in the bark scorpion Centruroides gracilis (Scorpiones: Buthidae)

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