Cell polarity signalling at the birth of multicellularity: What can we learn from the first animals

Wright, Bree A.; Kvansakul, Marc; Schierwater, Bernd; Humbert, Patrick O.

doi:10.3389/fcell.2022.1024489

Cited by 7 publications

(4 citation statements)

References 243 publications

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“…S2G). By focusing on a subset of genes important for flagellar formation (POC1, IFT122, IFT52) ( 59 , 60 ), cellular signalling (Gα, Gβ, PKAc-α) ( 61–63 ), cell adhesion (Talin, β-Catenin, Vinculin, Grancalcin) ( 64–67 ), and transcriptional regulation during animal development (Brachyury, CBP/p300, Piwi, Rbl1, P53, RunX) ( 55 , 68–70 ), we can observe comparable patterns of gene expression between C. perkinsii and basal animals. In certain cases, this expression exhibits conserved temporal patterns across most lineages (Fig.…”

Section: Resultsmentioning

confidence: 99%

A multicellular developmental program in a close animal relative

Olivetta,

Bhickta,

Chiaruttini

et al. 2024

Preprint

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All animals develop from a single-celled zygote into a complex multicellular organism through a series of precisely orchestrated processes. Despite the remarkable conservation of early embryogenesis across animals, the evolutionary origins of this process remain elusive. By combining time-resolved imaging and transcriptomic profiling, we show that single cells of the ichthyosporean Chromosphaera perkinsii - a close relative that diverged from animals approximately 1 billion years ago - undergo symmetry breaking and develop through cleavage divisions to produce a prolonged multicellular colony with distinct co-existing cell types. Our findings about the autonomous developmental program of C. perkinsii, hint that such animal-like multicellular development is either much older than previously thought or evolved convergently in ichthyosporeans.

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Section: Resultsmentioning

confidence: 99%

A multicellular developmental program in a close animal relative

Olivetta,

Bhickta,

Chiaruttini

et al. 2024

Preprint

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“…It is currently unclear whether this or other conserved mechanisms dictate the defects due to elevated temperature. Assuming that such general principles may exist, we will need to explore temperature dependent defects at the cellular level, with the focus on conserved cellular processes, such as cellular signaling 33,34 , metabolism through mitochondria 35,36 , cell polarity pathways 37,38 , regulation of membrane trafficking 39 , regulation of cell cycle 40 , and cytoskeletal dynamics 41,42 .…”

Section: Discussionmentioning

confidence: 99%

Elevated temperature fatally disrupts nuclear divisions in the earlyDrosophilaembryo

Kale,

Agarwal,

Diaz-Larrosa

et al. 2023

Preprint

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Temperature fluctuations can challenge animal survival, especially in embryos of animals that can't actively regulate their body temperature. Previous work in insects suggests that spatial gradients and temporal variations in temperature can affect embryonic development in a region-specific manner. Yet, it is unclear if elevated temperature produces developmental defects, and if so, how the disruption may manifest. Here we use early embryonic development of the fruit fly Drosophila melanogaster as a model to address consequences of elevated temperature on fly embryonic development. We identified the syncytial blastoderm stage as a critical time window as being particularly sensitive to elevated temperature. During the syncytial blastoderm stage involves 4 rounds of meta-synchronous nuclear divisions at the embryo cortex, followed by cellularization to form the cellular blastoderm. Live imaging these processes at elevated temperature revealed an increase in mitotic failures and a loss of cortical nuclei, both, during syncytial- and cellular-blastoderm stage. Additionally, embryos developing at elevated temperature show a local crowding of nuclei and an increase in asynchrony between the nuclear cycles in the middle vs anterior/posterior poles. Interestingly, nuclear crowding and nuclear cycle asynchrony cooperatively amplify the frequency of mitotic failures, leading to holes in the blastoderm epithelium. Strikingly, the exposure to elevated temperature during this developmental stage also increased embryonic lethality. We propose that the loss of nuclei results in a loss of patterning information and the abrogation of proper embryonic development. We identified genes that regulate mitosis, especially the ones mediating the interaction between microtubules and F-actin, and functionally tested their capacity to rescue the embryonic lethality. Our results expose a vulnerability at elevated temperatures in the interaction between cortical actin and microtubules, which leads to mitotic failures, and can be potentially rescued by modulating the expression of just a few factors. We propose that the expression levels of the corresponding genes could be used as indicators to predict fitness effects on insect populations that are exposed to increasing temperature variations.

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“…Pals1 belongs to a group of evolutionarily conserved polarity complex proteins which are asymmetrically localized within polarized cells such as epithelial cells. [96][97][98][99] As apical progenitors possess neuroepithelial characteristics, polarity proteins are critical determining factors for apicobasal polarity. Apical polarity complex proteins are concentrated at the end-feet apical to adherens junctions (Figure 5).…”

Section: Polarity Complex Gene Imbalance Is Implicated In Entosismentioning

confidence: 99%

Entosis implicates a new role for P53 in microcephaly pathogenesis, beyond apoptosis

Sterling,

Cho,

Kim

2024

BioEssays

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Entosis, a form of cell cannibalism, is a newly discovered pathogenic mechanism leading to the development of small brains, termed microcephaly, in which P53 activation was found to play a major role. Microcephaly with entosis, found in Pals1 mutant mice, displays P53 activation that promotes entosis and apoptotic cell death. This previously unappreciated pathogenic mechanism represents a novel cellular dynamic in dividing cortical progenitors which is responsible for cell loss. To date, various recent models of microcephaly have bolstered the importance of P53 activation in cell death leading to microcephaly. P53 activation caused by mitotic delay or DNA damage manifests apoptotic cell death which can be suppressed by P53 removal in these animal models. Such genetic studies attest P53 activation as quality control meant to eliminate genomically unfit cells with minimal involvement in the actual function of microcephaly associated genes. In this review, we summarize the known role of P53 activation in a variety of microcephaly models and introduce a novel mechanism wherein entotic cell cannibalism in neural progenitors is triggered by P53 activation.

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Cell polarity signalling at the birth of multicellularity: What can we learn from the first animals

Cited by 7 publications

References 243 publications

A multicellular developmental program in a close animal relative

A multicellular developmental program in a close animal relative

Elevated temperature fatally disrupts nuclear divisions in the earlyDrosophilaembryo

Entosis implicates a new role for P53 in microcephaly pathogenesis, beyond apoptosis

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