Integrin-Mediated Adhesion in the Unicellular Holozoan Capsaspora owczarzaki

Parra-Acero, Helena; Harcet, Matija; Sánchez-Pons, Núria; Casacuberta, Elena; Brown, Nicholas; Dudin, Omaya; Ruiz‐Trillo, Iñaki

doi:10.1016/j.cub.2020.08.015

Cited by 23 publications

(19 citation statements)

References 39 publications

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“…Our study suggests that the abnormal 3D shape of coYki -/- aggregates is due to increased cell–substrate adhesion without affecting cell–cell adhesion. Capsaspora encodes an integrin adhesome ( Sebé-Pedrós et al, 2010 ), and Capsaspora cell–substrate adhesion is mediated at least in part by integrins ( Parra-Acero et al, 2020 ). Indeed, our RNA-seq data shows that two integrin-β genes (CAOG_05058 and CAOG_01283) are upregulated in coYki -/- cells, suggesting a potential contribution by integrins in this phenotype.…”

Section: Discussionmentioning

confidence: 99%

Genome editing in the unicellular holozoan Capsaspora owczarzaki suggests a premetazoan role for the Hippo pathway in multicellular morphogenesis

Phillips

Santos

Konchwala

et al. 2022

eLife

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Animal development is mediated by a surprisingly small set of canonical signaling pathways such as Wnt, Hedgehog, TGF-beta, Notch, and Hippo pathways. Although once thought to be present only in animals, recent genome sequencing has revealed components of these pathways in the closest unicellular relatives of animals. These findings raise questions about the ancestral functions of these developmental pathways and their potential role in the emergence of animal multicellularity. Here, we provide the first functional characterization of any of these developmental pathways in unicellular organisms by developing techniques for genetic manipulation in Capsaspora owczarzaki, a close unicellular relative of animals that displays aggregative multicellularity. We then use these tools to characterize the Capsaspora ortholog of the Hippo signaling nuclear effector YAP/TAZ/Yorkie (coYki), a key regulator of tissue size in animals. In contrast to what might be expected based on studies in animals, we show that coYki is dispensable for cell proliferation but regulates cytoskeletal dynamics and the three-dimensional (3D) shape of multicellular structures. We further demonstrate that the cytoskeletal abnormalities of individual coYki mutant cells underlie the abnormal 3D shape of coYki mutant aggregates. Taken together, these findings implicate an ancestral role for the Hippo pathway in cytoskeletal dynamics and multicellular morphogenesis predating the origin of animal multicellularity, which was co-opted during evolution to regulate cell proliferation.

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Section: Discussionmentioning

confidence: 99%

Genome editing in the unicellular holozoan Capsaspora owczarzaki suggests a premetazoan role for the Hippo pathway in multicellular morphogenesis

Phillips

Santos

Konchwala

et al. 2022

eLife

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show abstract

“…Our study suggests that the abnormal 3D shape of coYki -/- aggregates is due to increased cell-substrate adhesion without affecting cell-cell adhesion. Capsaspora encodes an integrin adhesome (Sebe-Pedros et al, 2010), and Capsaspora cell-substrate adhesion is mediated at least in part by integrins (Parra-Acero et al, 2020). Indeed, our RNA-seq data shows that two integrin-β genes (CAOG_05058 and CAOG_01283) are upregulated in coYki -/- cells, suggesting a potential contribution by integrins in this phenotype.…”

Section: Discussionmentioning

confidence: 99%

Genome editing in the unicellular holozoan Capsaspora owczarzaki suggests a premetazoan function for the Hippo pathway in multicellular morphogenesis

Phillips

Santos

Kanchwala

et al. 2021

Preprint

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Many genes that function in animal development are present in the close unicellular relatives of animals, but little is known regarding the premetazoan function of these genes. Here, we develop techniques for genetic manipulation in the filasterean Capsaspora owczarzaki and use these tools to characterize the Capsaspora ortholog of the Hippo signaling nuclear effector YAP/TAZ/Yorkie (coYki). In contrast to its potent oncogene activity in metazoans, we show that coYki is dispensable for cell proliferation but regulates cytoskeletal dynamics and the morphology of multicellular aggregates in Capsaspora. Our results suggest an ancestral role for the Hippo pathway in cytoskeletal regulation, which was later co-opted to regulate cell proliferation in animals.One Sentence SummaryGene disruption in a unicellular holozoan suggests an ancestral role for YAP/TAZ/Yorkie in cytoskeletal regulation and cell aggregation but not cell proliferation.

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“…Recent work in unicellular holozoans shows that they do function in adhesion to substrates. 57 Our most comprehensive comparative genomic and transcriptomic survey of Amoebozoa has revealed the presence of a full set of IMAC across the Amoebozoa. To date, this complex was believed to be Obazoa specific; our data show that these IMAC proteins predate Obazoa.…”

Section: Articlementioning

confidence: 99%

The integrin-mediated adhesive complex in the ancestor of animals, fungi, and amoebae

et al. 2021

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Integrin-Mediated Adhesion in the Unicellular Holozoan Capsaspora owczarzaki

Cited by 23 publications

References 39 publications

Genome editing in the unicellular holozoan Capsaspora owczarzaki suggests a premetazoan role for the Hippo pathway in multicellular morphogenesis

Genome editing in the unicellular holozoan Capsaspora owczarzaki suggests a premetazoan role for the Hippo pathway in multicellular morphogenesis

Genome editing in the unicellular holozoan Capsaspora owczarzaki suggests a premetazoan function for the Hippo pathway in multicellular morphogenesis

The integrin-mediated adhesive complex in the ancestor of animals, fungi, and amoebae

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