Fat/Dachsous family cadherins in cell and tissue organisation

Fulford, Alexander D.; McNeill, Helen

doi:10.1016/j.ceb.2019.10.006

Cited by 49 publications

(45 citation statements)

References 84 publications

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“…We proposed that the levels of Ds activity would be graded in opposite ways in the A and the P compartment and ultimately these gradients would be read out as PCP in each of the cells ( Casal et al, 2002 ). We imagined that gradients of Ds activity would persist and this has been assumed by most ( Casal et al, 2006; Matis and Axelrod, 2013; Lawrence and Casal, 2018; Fulford and McNeill, 2019 ) and actually detected, locally, in the migrating larval epidermal cells in the pupa ( Arata et al, 2017 ). Alternatively, once the arrow of polarity has been established in each cell, a redistribution of bridges could occur and ultimately each cell would develop the same numbers and disposition of bridges and, if so, no persistent multicellular gradient in Ds amounts would be present (eg Hale et al, 2015 ).…”

Section: Discussionmentioning

confidence: 99%

Planar cell polarity in the larval epidermis ofDrosophilaand the role of microtubules

Pietra

Lawrence

et al. 2020

Preprint

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10We investigate the mechanisms of planar cell polarity (PCP) in the larval epidermis of 11 Drosophila. Measurements of the amount of Dachsous across the segment find a peak 12 located near the rear of the anterior compartment. Localisation of Dachs and 13 orientation of ectopic denticles reveal the polarity of every cell in the segment. We 14 discuss how well these findings evidence a zigzag gradient model of Dachsous activity. 15 Several groups have proposed that Dachsous and Fat fix the direction of PCP via 16 oriented microtubules that transport PCP proteins to one side of the cell. We test this 17 proposition in the larval cells and find that most microtubules grow perpendicularly 18 to the axis of PCP. We find no significant bias in the polarity of those microtubules 19 aligned close to that axis. We also reexamine published data from the pupal abdomen 20 and fail to find evidence supporting the hypothesis that microtubular orientation 21 draws the arrow of PCP. 22As cells construct embryos and organs they need access to vectorial information that 24 informs them, for example, which way to migrate, divide, extend axons or how to 25 orient protrusions. In Drosophila there are (at least) two conserved genetic systems 26 Page 2 of 32 that generate vectorial information, and here we are concerned with only one of those, 27 the Dachsous/Fat system. Dachsous (Ds) and Fat (Ft) are large atypical cadherin 28 molecules that form heterodimeric bridges from cell to cell that help build planar cell 29 polarity (PCP) in one cell and also convey polarity between cells (Ma et al., 2003; 30 Matakatsu and Blair, 2004; Casal et al., 2006; Lawrence and Casal, 2018). The 31 activity of Ft is increased and Ds is reduced when they are phosphorylated by a third 32 molecule, Four-jointed (Fj), a Golgi-based kinase (Ishikawa et al., 2008; Brittle et al., 33 2010; Simon et al., 2010). The distribution of Ds, Ft and Fj and the interaction 34 between these molecules together determine what we describe as "Ds activity", by 35 which we mean the propensity of Ds on one cell to bind to Ft in the neighbouring cell. 36 Experiments suggest that, using the disposition and orientation of Ds-Ft bridges, each 37 cell compares the Ds activity of its two neighbours and points its denticles towards the 38 neighbour with the higher Ds activity. In this way, the local slopes in a landscape of Ds 39 activity determine polarities of all the cells (Casal et al., 2002; see Lawrence and 40 Casal, 2018 for more explanation). 41 A model: the ventral epidermis of the Drosophila larva 42Each segment of the larva is divided by cell lineage into an anterior (A) and a 43 posterior (P) compartment. In the ventral epidermis, a limited region of the segment 44 makes rows of thorny denticles that are polarised in an almost invariant pattern, while 45 the larger part of each segment makes no denticles and therefore its polarity is not 46 known (Figure 1-figure supplement 1). The Ds/Ft system is alone effective in 47 48 the "core" or Stan/Fz system (Casal et ...

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Section: Discussionmentioning

confidence: 99%

Planar cell polarity in the larval epidermis ofDrosophilaand the role of microtubules

Pietra

Lawrence

et al. 2020

Preprint

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“…These polarised events occur in the SOX9 progenitors before the establishment of the perichondrium and onset of matrix expansion and are controlled by one of two Planar Cell Polarity (PCP) pathways: the DCHS1-FAT4-PCP and Wnt-PCP pathways. The definition of PCP is the co-ordinated collective cell polarity or cell behaviours within a plane of tissue [159][160][161] . Both of these PCP pathways co-ordinate the collective orientation of the chondrogenic progenitors by generation of patterned molecular asymmetries within each cell to provide a tissue polarity.…”

Section: Planar Cell Polarity Shaping Of the Early Condensationmentioning

confidence: 99%

Making and shaping endochondral and intramembranous bones

Galea

Zein

Allen

et al. 2020

Developmental Dynamics

106

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Skeletal elements have a diverse range of shapes and sizes specialized to their various roles including protecting internal organs, locomotion, feeding, hearing, and vocalization. The precise positioning, size, and shape of skeletal elements is therefore critical for their function. During embryonic development, bone forms by endochondral or intramembranous ossification and can arise from the paraxial and lateral plate mesoderm or neural crest. This review describes inductive mechanisms to position and pattern bones within the developing embryo, compares and contrasts the intrinsic vs extrinsic mechanisms of endochondral and intramembranous skeletal development, and details known cellular processes that precisely determine skeletal shape and size. Key cellular mechanisms are employed at distinct stages of ossification, many of which occur in response to mechanical cues (eg, joint formation) or preempting future load‐bearing requirements. Rapid shape changes occur during cellular condensation and template establishment. Specialized cellular behaviors, such as chondrocyte hypertrophy in endochondral bone and secondary cartilage on intramembranous bones, also dramatically change template shape. Once ossification is complete, bone shape undergoes functional adaptation through (re)modeling. We also highlight how alterations in these cellular processes contribute to evolutionary change and how differences in the embryonic origin of bones can influence postnatal bone repair.

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“…Fat and Ds interact via extracellular cadherin domains, and use their intracellular domains to transduce planar polarity signals, as well as to control proliferation via the Hippo pathway and to mediate metabolic control (reviewed in refs. 2 and 3 ). In addition, a closely related family of Fat-like cadherins, similar in their extracellular domains but with a distinct intracellular domain, can planar polarize cells and influence actin and microtubule dynamics ( 4 – 8 ).…”

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confidence: 99%

Ancestral roles of atypical cadherins in planar cell polarity

Brooun

Klimovich

Bashkurov

et al. 2020

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

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Fat, Fat-like, and Dachsous family cadherins are giant proteins that regulate planar cell polarity (PCP) and cell adhesion in bilaterians. Their evolutionary origin can be traced back to prebilaterian species, but their ancestral function(s) are unknown. We identified Fat-like and Dachsous cadherins inHydra, a member of phylum Cnidaria a sister group of bilaterian. We foundHydradoes not possess a true Fat homolog, but has homologs of Fat-like (HyFatl) and Dachsous (HyDs) that localize at the apical membrane of ectodermal epithelial cells and are planar polarized perpendicular to the oral–aboral axis of the animal. Using a knockdown approach we found that HyFatl is involved in local cell alignment and cell–cell adhesion, and that reduction of HyFatl leads to defects in tissue organization in the body column. Overexpression and knockdown experiments indicate that the intracellular domain (ICD) of HyFatl affects actin organization through proline-rich repeats. Thus, planar polarization of Fat-like and Dachsous cadherins has ancient, prebilaterian origins, and Fat-like cadherins have ancient roles in cell adhesion, spindle orientation, and tissue organization.

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Fat/Dachsous family cadherins in cell and tissue organisation

Cited by 49 publications

References 84 publications

Planar cell polarity in the larval epidermis ofDrosophilaand the role of microtubules

Planar cell polarity in the larval epidermis ofDrosophilaand the role of microtubules

Making and shaping endochondral and intramembranous bones

Ancestral roles of atypical cadherins in planar cell polarity

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