Architecture of cell–cell adhesion mediated by sidekicks

Tang, Hengjing; Chang, Haishuang; Dong, Yue; Guo, Luqiang; Shi, Xiangyi; Wu, Yih‐Min; Huang, Ying; He, Yongning

doi:10.1073/pnas.1801810115

Cited by 24 publications

(25 citation statements)

References 40 publications

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“…It is indeed required for synaptic localization in the retina (Yamagata and Sanes, 2010) and cytoskeletal organization in the kidney podocytes (Kaufman et al, 2010). Ig5, Ig6, and FNIII domains are associated with plasma membranes (Tang et al, 2018). (B) The crystal structure of Sdk1 Ig1-Ig5 homodimers (https://www.rcsb.org/3d-view/5K6W) (Goodman et al, 2016).…”

Section: Cytoplasmic Domainmentioning

confidence: 99%

“…Drosophila Sdk protein is a homophilic adhesion molecule ( Astigarraga et al, 2018 ). Vertebrate Sdk1 and Sdk2 also show homophilic binding: Sdk1 binds to Sdk1, and Sdk2 binds to Sdk2 ( Yamagata et al, 2002 ; Hayashi et al, 2005 ; Goodman et al, 2016 ; Tang et al, 2018 ). Moreover, neither exhibits heterophilic interactions with other IgSF molecules tested ( Yamagata and Sanes, 2008 , 2012 ), although biochemical assays have demonstrated weak cross-binding to other IgSFs under restricted conditions in vitro ( Visser et al, 2015 ).…”

Section: Structurementioning

confidence: 99%

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Structure and Functions of Sidekicks

Yamagata

2020

Front. Mol. Neurosci.

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Many of the immunoglobulin superfamily (IgSF) molecules play pivotal roles in cell communication. The Sidekick (Sdk) gene, first described in Drosophila, encodes the single-pass transmembrane protein, Sdk, which is one of the largest among IgSF membrane proteins. Sdk first appeared in multicellular animals during the Precambrian age and later evolved to Sdk1 and Sdk2 in vertebrates by gene duplication. In flies, a single Sdk is involved in positioning photoreceptor neurons and their axons in the visual system and is responsible for dynamically rearranging cell shapes by strictly populating tricellular adherens junctions in epithelia. In vertebrates, Sdk1 and Sdk2 are expressed by unique sets of cell types and distinctively participate in the formation and/or maintenance of neural circuits in the retina, indicating that they are determinants of synaptic specificity. These functions are mediated by specific homophilic binding of their ectodomains and by intracellular association with PDZ scaffold proteins. Recent human genetic studies as well as animal experiments implicate that Sdk genes may influence various neurodevelopmental and psychiatric disorders, such as autism spectrum disorders, attention-deficit hyperactivity disorder, addiction, and depression. The gigantic Sdk1 gene is susceptible to erratic gene rearrangements or mutations in both somatic and germ-line cells, potentially contributing to neurological disorders and some types of cancers. This review summarizes what is known about the structure and roles of Sdks.

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Section: Cytoplasmic Domainmentioning

confidence: 99%

Section: Structurementioning

confidence: 99%

Structure and Functions of Sidekicks

Yamagata

2020

Front. Mol. Neurosci.

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“…Vertebrate Sdk molecules bind the Membrane-associated guanylate kinase inverted (MAGI) protein via this conserved C-terminal motif, which is important for both renal and neuronal functions [27, 28]. Structure studies of Sdk-1 and Sdk-2 ectodomains show that they form homophilic dimers in cis - and in trans - [29, 30].…”

Section: Introductionmentioning

confidence: 99%

The tricellular vertex-specific adhesion molecule Sidekick facilitates polarised cell intercalation during Drosophila axis extension

et al. 2019

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In epithelia, tricellular vertices are emerging as important sites for the regulation of epithelial integrity and function. Compared to bicellular contacts, however, much less is known. In particular, resident proteins at tricellular vertices were identified only at occluding junctions, with none known at adherens junctions (AJs). In a previous study, we discovered that in Drosophila embryos, the adhesion molecule Sidekick (Sdk), well-known in invertebrates and vertebrates for its role in the visual system, localises at tricellular vertices at the level of AJs. Here, we survey a wide range of Drosophila epithelia and establish that Sdk is a resident protein at tricellular AJs (tAJs), the first of its kind. Clonal analysis showed that two cells, rather than three cells, contributing Sdk are sufficient for tAJ localisation. Super-resolution imaging using structured illumination reveals that Sdk proteins form string-like structures at vertices. Postulating that Sdk may have a role in epithelia where AJs are actively remodelled, we analysed the phenotype of sdk null mutant embryos during Drosophila axis extension using quantitative methods. We find that apical cell shapes are abnormal in sdk mutants, suggesting a defect in tissue remodelling during convergence and extension. Moreover, adhesion at apical vertices is compromised in rearranging cells, with apical tears in the cortex forming and persisting throughout axis extension, especially at the centres of rosettes. Finally, we show that polarised cell intercalation is decreased in sdk mutants. Mathematical modelling of the cell behaviours supports the notion that the T1 transitions of polarised cell intercalation are delayed in sdk mutants, in particular in rosettes. We propose that this delay, in combination with a change in the mechanical properties of the converging and extending tissue, causes the abnormal apical cell shapes in sdk mutant embryos.

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“…They are homophilic adhesion molecules (Yamagata et al, 2002; Hayashi et al, 2005; Yamagata and Sanes, 2008). Structural studies have shown that the immunoglobulin domains mediate homophilic adhesion, and defined critical residues required for adhesion per se and for homophilic specificity (Goodman et al, 2016; Tang et al, 2018). Their PDZ-binding motif binds scaffolding proteins of the MAGI family, an interaction that contributes to their concentration at synaptic sites (Yamagata and Sanes, 2010).…”

Section: Introductionmentioning

confidence: 99%

Expression and Roles of the Immunoglobulin Superfamily Recognition Molecule Sidekick1 in Mouse Retina

Yamagata

Sanes

2019

Front. Mol. Neurosci.

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Processes of >100 types of interneurons (bipolar and amacrine cells) and projection neurons (retinal ganglion cells, RGCs) form specific and stereotyped patterns of connections in the inner plexiform layer (IPL) of the mouse retina. Four closely related homophilic immunoglobulin superfamily recognition molecules (Sidekick [Sdk] 1, Sdk 2, Dscam, and DscamL1) have been shown to play roles in patterning neuronal arbors and connections in chick retina, and all but Sdk1 have been shown to play related roles in mice. Here, we compare patterns of Sdk1 and Sdk2 expression in mouse retina and use genetic methods to assess roles of Sdk1. In adult retina, 3 neuronal types express sdk1 but not sdk2 at detectable levels, 5 express sdk2 but not sdk1 and 3 express both. Patterns of gene expression and protein localization at or near synapses are established during the first postnatal week. Dendrites of amacrine cells and RGCs that express sdk1 but not sdk2 arborize in the same narrow stratum in the center of the IPL. In the absence of Sdk1, this laminar restriction is degraded. Overexpression of sdk1 in developing cells that normally express sdk2 reorients their dendrites to resemble those of endogenously Sdk1-positive cells, indicating that Sdk1 plays an instructive role in patterning the IPL. Sdk1 fails to affect arbors when introduced after they are mature, suggesting that it is required to form but not maintain laminar restrictions. The effect of ectopically expressed sdk1 requires the presence of endogenous Sdk1, suggesting that the effect requires homophilic interactions among Sdk1-positive neurites. Together with previous results on Sdk2, Dscam, DscamL1, as well as the related Contactins, our results support the idea that an elaborate immunoglobulin superfamily code plays a prominent role in establishing neural circuits in the retina by means of tightly regulated cell type-specific expression and homophilically restricted intercellular interactions.

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Architecture of cell–cell adhesion mediated by sidekicks

Cited by 24 publications

References 40 publications

Structure and Functions of Sidekicks

Structure and Functions of Sidekicks

The tricellular vertex-specific adhesion molecule Sidekick facilitates polarised cell intercalation during Drosophila axis extension

Expression and Roles of the Immunoglobulin Superfamily Recognition Molecule Sidekick1 in Mouse Retina

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