The adherens junction–associated LIM domain protein Smallish regulates epithelial morphogenesis

Beati, Hamze; Peek, Irina; Hordowska, Paulina; Honemann‐Capito, Mona; Glashauser, Jade; Renschler, Fabian A.; Kakanj, Parisa; Ramrath, Andreas; Leptin, Maria; Luschnig, Stefan; Wiesner, Silke; Wodarz, Andreas

doi:10.1083/jcb.201610098

Cited by 21 publications

(34 citation statements)

References 58 publications

(92 reference statements)

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“…Notably, in the germband, Bazooka polarity depends on Rho-associated kinase that shows complementary localization at anteroposterior cell borders ( Simões et al, 2010 ). In the same tissue, Bazooka localization also requires the LIM-domain protein Smallish ( Beati et al, 2018 ), but does not seem to depend on core PCP proteins ( Simões et al, 2010 ; Zallen and Wieschaus, 2004 ). Nevertheless, in the fly eye epithelium Bazooka is planar polarized under the control of the core PCP protein Stan/Flamingo ( Aigouy and Le Bivic, 2016 ).…”

Section: Discussionmentioning

confidence: 97%

“…The conserved scaffold Par3/Pard3 plays a central role in this complex by interacting with multiple proteins and regulating cell polarity, adhesion, asymmetric cell division and migratory behavior in many tissues ( Afonso and Henrique, 2006 ; Bryant et al, 2010 ; Ebnet et al, 2001 ; Goldstein and Macara, 2007 ; Tawk et al, 2007 ). Bazooka/Par3 and its associated proteins have been functionally linked to PCP in specific Drosophila tissues ( Beati et al, 2018 ; Blankenship et al, 2006 ; Djiane et al, 2005 ; Harris and Peifer, 2007 ; Simões et al, 2010 ; Wasserscheid et al, 2007 ; Zallen and Wieschaus, 2004 ). Additionally, the effects of core PCP components on Par3 localization have been demonstrated in fly photoreceptor cells and sensor organ progenitors ( Aigouy and Le Bivic, 2016 ; Banerjee et al, 2017 ; Bellaïche et al, 2004 ; Besson et al, 2015 ).…”

Section: Introductionmentioning

confidence: 99%

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Par3 interacts with Prickle3 to generate apical PCP complexes in the vertebrate neural plate

Chuykin

Ossipova

Sokol

2018

eLife

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Vertebrate neural tube formation depends on the coordinated orientation of cells in the tissue known as planar cell polarity (PCP). In the Xenopus neural plate, PCP is marked by the enrichment of the conserved proteins Prickle3 and Vangl2 at anterior cell boundaries. Here we show that the apical determinant Par3 is also planar polarized in the neuroepithelium, suggesting a role for Par3 in PCP. Consistent with this hypothesis, interference with Par3 activity inhibited asymmetric distribution of PCP junctional complexes and caused neural tube defects. Importantly, Par3 physically associated with Prickle3 and promoted its apical localization, whereas overexpression of a Prickle3-binding Par3 fragment disrupted PCP in the neural plate. We also adapted proximity biotinylation assay for use in Xenopus embryos and show that Par3 functions by enhancing the formation of the anterior apical PCP complex. These findings describe a mechanistic link between the apical localization of PCP components and morphogenetic movements underlying neurulation.

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Section: Discussionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

Par3 interacts with Prickle3 to generate apical PCP complexes in the vertebrate neural plate

Chuykin

Ossipova

Sokol

2018

eLife

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“…Both proteins regulating adherens junctions, e.g. Smash (Beati et al 2018) , as well as adherence proteins forming adherens junctions can be planar polarized, e.g. Bazooka, Ecadherins (Simões et al 2010; Tamada, Farrell, and Zallen 2017; Levayer and Lecuit 2013; Warrington, Strutt, and Strutt 2013; Benoit Aigouy and Le Bivic 2016 .…”

Section: (3) Cell -Cell Adhesion Depends On the Orientation Of Polaritymentioning

confidence: 99%

Theoretical Tool Bridging Cell Polarities with Development of Robust Morphologies

Nissen

Rønhild

Trusina

et al. 2018

Preprint

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Despite continual renewal and damages, a multicellular organism is able to maintain its complex morphology. How is this stability compatible with the complexity and diversity of living forms? Looking for answers at protein level may be limiting as diverging protein sequences can result in similar morphologies. Inspired by the progressive role of apicalbasal and planar cell polarity in development, we propose that stability, complexity, and diversity are emergent properties in populations of proliferating polarized cells. We support our hypothesis by a theoretical approach, developed to effectively capture both types of polar cell adhesions. When applied to specific cases of development -gastrulation and the origins of folds and tubes -our theory makes experimentally testable predictions pointing to the strength of polar adhesion, initial and boundary orientation of cell polarities, and the rate of cell proliferation to be major determinants of morphological diversity and stability.

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“…Cells adhere to each other by membrane proteins assembled in adherens junctions just below the apical surface. Both proteins regulating adherens junctions, for example Smash ( Beati et al, 2018 ), as well as adherence proteins forming adherens junctions can be planar polarized, for example Bazooka, E-cadherins ( Simões et al, 2010 ; Tamada et al, 2017 ; Levayer and Lecuit, 2013 ; Warrington et al, 2013 ; Aigouy and Le Bivic, 2016 ). These indirectly support our assumption of anisotropic, planar polarized adhesion.…”

Section: Introductionmentioning

confidence: 99%

“…However, the symmetry in polarities is appealing for its simplicity and is indirectly supported by the following experimental observations: First, cells can acquire PCP without AB polarity present ( Baer et al, 2009 ; Zorn and Wells, 2009 ). Second, proteins required for AB polarity can be planar-polarized ( Warrington et al, 2013 ; Aigouy and Le Bivic, 2016 ; Beati et al, 2018 ; Choi and Sokol, 2009 ; Dollar et al, 2005 ; Kaplan and Tolwinski, 2010 ). Third, changes in cell shapes during invagination (e.g.…”

Section: Introductionmentioning

confidence: 99%

Theoretical tool bridging cell polarities with development of robust morphologies

Nissen

Rønhild

Trusina

et al. 2018

eLife

View full text Add to dashboard Cite

Despite continual renewal and damages, a multicellular organism is able to maintain its complex morphology. How is this stability compatible with the complexity and diversity of living forms? Looking for answers at protein level may be limiting as diverging protein sequences can result in similar morphologies. Inspired by the progressive role of apical-basal and planar cell polarity in development, we propose that stability, complexity, and diversity are emergent properties in populations of proliferating polarized cells. We support our hypothesis by a theoretical approach, developed to effectively capture both types of polar cell adhesions. When applied to specific cases of development – gastrulation and the origins of folds and tubes – our theoretical tool suggests experimentally testable predictions pointing to the strength of polar adhesion, restricted directions of cell polarities, and the rate of cell proliferation to be major determinants of morphological diversity and stability.

show abstract

The adherens junction–associated LIM domain protein Smallish regulates epithelial morphogenesis

Cited by 21 publications

References 58 publications

Par3 interacts with Prickle3 to generate apical PCP complexes in the vertebrate neural plate

Par3 interacts with Prickle3 to generate apical PCP complexes in the vertebrate neural plate

Theoretical Tool Bridging Cell Polarities with Development of Robust Morphologies

Theoretical tool bridging cell polarities with development of robust morphologies

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