Cell polarity in the protist-to-animal transition

Brunet, Thibaut; Booth, David S.

doi:10.1016/bs.ctdb.2023.03.001

Cited by 12 publications

(7 citation statements)

References 196 publications

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“…C. flexa was discovered in 2018 in splash pools (see glossary) on the rocky coast of the Caribbean island of Curaçao in the form of curved multicellular “sheet” colonies ( Figure 1A-D ) ( 35 ). Cells within C. flexa colonies are held together through direct collar-collar interactions, forming a concave monolayer of cells with aligned apico-basal polarity ( Figure 1B-D ) ( 35 , 36 ). C. flexa sheets display collective contractility under the control of environmental cues (including light-to-dark transitions), inverting their curvature and switching from a feeding state (relaxed form, flagella-in; Figure 1B ) to a swimming state (contracted form, flagella-out; Figure 1D ) ( 35 , 37 ).…”

Section: Resultsmentioning

confidence: 99%

Mixed clonal-aggregative multicellularity entrained by extreme salinity fluctuations in a close relative of animals

Ros-Rocher,

Reyes-Rivera,

Foroughijabbari

et al. 2024

Preprint

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Multicellularity evolved multiple times independently during eukaryotic diversification. Two distinct mechanisms underpin multicellularity: clonal development (serial cell division of a single precursor cell) and aggregation (in which independent cells assemble into a multicellular entity). Clonal and aggregative development are traditionally considered to be mutually exclusive and to result from independent acquisitions of multicellularity. Here, we show that the choanoflagellate Choanoeca flexa, a close relative of animals that forms contractile monolayers of cells (or "sheet colonies"), develops by an unconventional intermediate mechanism that we name "clonal-aggregative multicellularity". We find that C. flexa sheets can form through purely clonal processes, purely aggregative processes, or a combination of both, depending on experimental conditions. To assess the ecological relevance of these findings, we characterize the natural context of multicellular development in the native environment of C. flexa on the island of Curaçao. We show that the C. flexa life cycle is environmentally regulated by extreme salinity fluctuations in splash pools undergoing cycles of evaporation and refilling. Upon desiccation, C. flexa colonies dissociate into drought-resistant quiescent cells, which resume activity and reform multicellular sheets after rehydration. We hypothesize that clonal-aggregative development reflects selection for fast transitions into and out of multicellularity in the ephemeral context of coastal splash pools. Our findings underscore the potential of the exploration of biodiversity to reveal new fundamental biological phenomena and expand the known option space for both multicellular development and for the origin of animal multicellularity.

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Section: Resultsmentioning

confidence: 99%

Mixed clonal-aggregative multicellularity entrained by extreme salinity fluctuations in a close relative of animals

Ros-Rocher,

Reyes-Rivera,

Foroughijabbari

et al. 2024

Preprint

Self Cite

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“…Studying organelle positioning in a quantitative high throughput manner across different cell types, organisms, stimuli, microenvironmental contexts, and diseases, could also reveal quantitatively whether some organelles maintain a rather fixed position that is conserved throughout different organisms, cell types, and contexts, or may more dynamically adapt to the cellular and physiological requirement. These approaches may also lead to the characterisation of whether organelle positioning evolved with cell motility strategies and the complexity of multicellular organisms (Brunet and Booth, 2023 ; Fritz-Laylin, 2020 ) and whether cancer cells or intracellular parasites, such as the obligate intracellular parasite Toxoplasma gondii , hijack mechanisms of precise, efficient, and robust organelle positioning.…”

Section: Discussionmentioning

confidence: 99%

Principles of organelle positioning in motile and non-motile cells

Kroll,

Renkawitz

2024

EMBO Rep

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Cells are equipped with asymmetrically localised and functionally specialised components, including cytoskeletal structures and organelles. Positioning these components to specific intracellular locations in an asymmetric manner is critical for their functionality and affects processes like immune responses, tissue maintenance, muscle functionality, and neurobiology. Here, we provide an overview of strategies to actively move, position, and anchor organelles to specific locations. By conceptualizing the cytoskeletal forces and the organelle-to-cytoskeleton connectivity, we present a framework of active positioning of both membrane-enclosed and membrane-less organelles. Using this framework, we discuss how different principles of force generation and organelle anchorage are utilised by different cells, such as mesenchymal and amoeboid cells, and how the microenvironment influences the plasticity of organelle positioning. Given that motile cells face the challenge of coordinating the positioning of their content with cellular motion, we particularly focus on principles of organelle positioning during migration. In this context, we discuss novel findings on organelle positioning by anchorage-independent mechanisms and their advantages and disadvantages in motile as well as stationary cells.

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“…In animals, the predominant form of multicellular structure is epithelia, in which cells with apical-basal polarity form lateral contacts at adherens junctions, septate junctions, tight junctions, and desmosomes (Abedin and King, 2010). However, microvilli/filopodial adhesion plays important roles in dorsal closure in Drosophila (Jacinto et al, 2000), early embryo compaction in mouse (Fierro-Gonzalez et al, 2013), and other developmental processes (Brunet and Booth, 2023). Further, inter-microvillar contacts are the apparent means of adherence in the choanoflagellate C. flexa, another close unicellular relative of animals, that can exist in a sheet-like morphology with a remarkable actomyosin-dependent inverting activity (Brunet et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

The Hippo kinase cascade regulates a contractile cell behavior and cell density in a close unicellular relative of animals

Phillips

Pan

2023

Preprint

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The genomes of close unicellular relatives of animals encode orthologs of many genes that regulate animal development. However, little is known about the function of such genes in unicellular organisms or the evolutionary process by which these genes came to function in multicellular development. The Hippo pathway, which regulates cell proliferation and tissue size in animals, is present in some of the closest unicellular relatives of animals, including the amoeboid organismCapsaspora owczarzaki. We previously showed that theCapsasporaortholog of the Hippo pathway nuclear effector Yorkie/YAP/TAZ (coYki) regulates actin dynamics and the three-dimensional morphology ofCapsasporacell aggregates, but is dispensable for cell proliferation control (Phillips et al., 2022). However, the function of upstream Hippo pathway components, and whether and how they regulate coYki inCapsaspora, remained unknown. Here, we analyze the function of the upstream Hippo pathway kinases coHpo and coWts inCapsasporaby generating mutant lines for each gene. Loss of either kinase results in increased nuclear localization of coYki, indicating an ancient, premetazoan origin of this Hippo pathway regulatory mechanism. Strikingly, we find that loss of either kinase causes a contractile cell behavior and increased density of cell packing withinCapsasporaaggregates. We further show that this increased cell density is not due to differences in proliferation, but rather actomyosin-dependent changes in the multicellular architecture of aggregates. Given its well-established role in cell density-regulated proliferation in animals, the increased density of cell packing incoHpoandcoWtsmutants suggests a shared and possibly ancient and conserved function of the Hippo pathway in cell density control. Together, these results implicate cytoskeletal regulation but not proliferation as an ancestral function of the Hippo pathway and uncover a novel role for Hippo signaling in regulating cell density in a proliferation-independent manner.

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Cell polarity in the protist-to-animal transition

Cited by 12 publications

References 196 publications

Mixed clonal-aggregative multicellularity entrained by extreme salinity fluctuations in a close relative of animals

Mixed clonal-aggregative multicellularity entrained by extreme salinity fluctuations in a close relative of animals

Principles of organelle positioning in motile and non-motile cells

The Hippo kinase cascade regulates a contractile cell behavior and cell density in a close unicellular relative of animals

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