Ancestral roles of atypical cadherins in planar cell polarity

Maria Brooun; Alexander Klimovich; Mikhail Bashkurov; Bret J. Pearson; Robert E. Steele; Helen McNeill

doi:10.1073/pnas.1917570117

Ancestral roles of atypical cadherins in planar cell polarity

Maria Brooun, Alexander Klimovich, Mikhail Bashkurov, Bret J. Pearson, Robert E. Steele, Helen McNeill

Research output: Contribution to journal › Article › peer-review

6 Scopus citations

Abstract

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 in Hydra, a member of phylum Cnidaria a sister group of bilaterian. We found Hydra does 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.

Original language	English (US)
Pages (from-to)	19310-19320
Number of pages	11
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	117
Issue number	32
DOIs	https://doi.org/10.1073/pnas.1917570117
State	Published - Jul 29 2020
Externally published	Yes

Bibliographical note

KAUST Repository Item: Exported on 2022-06-14
Acknowledgements: We are grateful to Bert Hobmayer (University of Innsbruck) for providing the claudin-GFP transgenic Hydra and the AEP strain of H. vulgaris; Jörg Wittlieb (University of Kiel) for generating transgenic lines; Celina Juliano (University of California, Davis) and Hiroshi Shimizu (King Abdullah University of Science and Technology) for providing the AEP H. vulgaris strain; Dae-Kyum Kim (Lunenfeld-Tanenbaum Research Institute) for helping with the statistical analysis; and Brigitte Galliot (University of Geneva) for providing the FGF2 antibody. We thank anonymous reviewers for their critique and constructive suggestions. M. Brooun and H.M. were funded by the Natural Sciences and Engineering Research Council of Canada grant RGPIN-2016-06354. H.M. was supported by a Canadian Institutes of Health Research foundation grant (FDN 143319) and start up funds from Washington University School of Medicine. B.J.P. was supported by Ontario Institute for Cancer Research grant IA-026.
This publication acknowledges KAUST support, but has no KAUST affiliated authors.

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title = "Ancestral roles of atypical cadherins in planar cell polarity",

abstract = "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 in Hydra, a member of phylum Cnidaria a sister group of bilaterian. We found Hydra does 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.",

author = "Maria Brooun and Alexander Klimovich and Mikhail Bashkurov and Pearson, {Bret J.} and Steele, {Robert E.} and Helen McNeill",

note = "KAUST Repository Item: Exported on 2022-06-14 Acknowledgements: We are grateful to Bert Hobmayer (University of Innsbruck) for providing the claudin-GFP transgenic Hydra and the AEP strain of H. vulgaris; J{\"o}rg Wittlieb (University of Kiel) for generating transgenic lines; Celina Juliano (University of California, Davis) and Hiroshi Shimizu (King Abdullah University of Science and Technology) for providing the AEP H. vulgaris strain; Dae-Kyum Kim (Lunenfeld-Tanenbaum Research Institute) for helping with the statistical analysis; and Brigitte Galliot (University of Geneva) for providing the FGF2 antibody. We thank anonymous reviewers for their critique and constructive suggestions. M. Brooun and H.M. were funded by the Natural Sciences and Engineering Research Council of Canada grant RGPIN-2016-06354. H.M. was supported by a Canadian Institutes of Health Research foundation grant (FDN 143319) and start up funds from Washington University School of Medicine. B.J.P. was supported by Ontario Institute for Cancer Research grant IA-026. This publication acknowledges KAUST support, but has no KAUST affiliated authors.",

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doi = "10.1073/pnas.1917570117",

language = "English (US)",

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T1 - Ancestral roles of atypical cadherins in planar cell polarity

AU - Brooun, Maria

AU - Klimovich, Alexander

AU - Bashkurov, Mikhail

AU - Pearson, Bret J.

AU - Steele, Robert E.

AU - McNeill, Helen

N1 - KAUST Repository Item: Exported on 2022-06-14 Acknowledgements: We are grateful to Bert Hobmayer (University of Innsbruck) for providing the claudin-GFP transgenic Hydra and the AEP strain of H. vulgaris; Jörg Wittlieb (University of Kiel) for generating transgenic lines; Celina Juliano (University of California, Davis) and Hiroshi Shimizu (King Abdullah University of Science and Technology) for providing the AEP H. vulgaris strain; Dae-Kyum Kim (Lunenfeld-Tanenbaum Research Institute) for helping with the statistical analysis; and Brigitte Galliot (University of Geneva) for providing the FGF2 antibody. We thank anonymous reviewers for their critique and constructive suggestions. M. Brooun and H.M. were funded by the Natural Sciences and Engineering Research Council of Canada grant RGPIN-2016-06354. H.M. was supported by a Canadian Institutes of Health Research foundation grant (FDN 143319) and start up funds from Washington University School of Medicine. B.J.P. was supported by Ontario Institute for Cancer Research grant IA-026. This publication acknowledges KAUST support, but has no KAUST affiliated authors.

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N2 - 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 in Hydra, a member of phylum Cnidaria a sister group of bilaterian. We found Hydra does 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.

AB - 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 in Hydra, a member of phylum Cnidaria a sister group of bilaterian. We found Hydra does 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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JF - Proceedings of the National Academy of Sciences of the United States of America

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ER -

Ancestral roles of atypical cadherins in planar cell polarity

Abstract

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