Origin and Evolution of the Self-Organizing Cytoskeleton in the Network of Eukaryotic Organelles

Jékely, Gáspár

doi:10.1101/cshperspect.a016030

Cited by 31 publications

(15 citation statements)

References 135 publications

(187 reference statements)

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“…The slow myosin is also involved in amoeboid movement [ 38 ], which probably belonged to the behavioural repertoire of early metazoan cells. In addition, we can infer that early metazoan cells formed lamellipodia and filopodia, using proteins that reorganize cortical actin filaments such as the Arp2/3 complex, the actin cross-linking protein fascin, and myosin X, a myosin with pleckstrin homology domains that associates with regions of dynamic actin [ 39 , 40 ]. Filopodia are highly dynamic structures that probably played a role in anchoring and stabilizing cells in the blastaea ( figure 2 a , b ).…”

Section: The Choanoblastaea a Sphere Of Choanoflagellate-like Cellsmentioning

confidence: 99%

Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution

Arendt

Benito‐Gutiérrez

Brunet

et al. 2015

Phil. Trans. R. Soc. B

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Prerequisite for tracing nervous system evolution is understanding of the body plan, feeding behaviour and locomotion of the first animals in which neurons evolved. Here, a comprehensive scenario is presented for the diversification of cell types in early metazoans, which enhanced feeding efficiency and led to the emergence of larger animals that were able to move. Starting from cup-shaped, gastraea-like animals with outer and inner choanoflagellate-like cells, two major innovations are discussed that set the stage for nervous system evolution. First, the invention of a mucociliary sole entailed a switch from intra- to extracellular digestion and increased the concentration of nutrients flowing into the gastric cavity. In these animals, an initial nerve net may have evolved via division of labour from mechanosensory-contractile cells in the lateral body wall, enabling coordinated movement of the growing body that involved both mucociliary creeping and changes of body shape. Second, the inner surface of the animals folded into metameric series of gastric pouches, which optimized nutrient resorption and allowed larger body sizes. The concomitant acquisition of bilateral symmetry may have allowed more directed locomotion and, with more demanding coordinative tasks, triggered the evolution of specialized nervous subsystems. Animals of this organizational state would have resembled Ediacarian fossils such as Dickinsonia and may have been close to the cnidarian–bilaterian ancestor. In the bilaterian lineage, the mucociliary sole was used mostly for creeping, or frequently lost. One possible remnant is the enigmatic Reissner's fibre in the ventral neural tube of cephalochordates and vertebrates.

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Section: The Choanoblastaea a Sphere Of Choanoflagellate-like Cellsmentioning

confidence: 99%

Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution

Arendt

Benito‐Gutiérrez

Brunet

et al. 2015

Phil. Trans. R. Soc. B

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“…The eukaryotic cytoskeleton organizes space on the cellular scale and this organization influences almost every process in the cell . The cytoskeleton refers to microfilaments and microtubules in the traditional sense, which together with the intermediate filaments form the skeleton system of nerve cells.…”

Section: Introductionmentioning

confidence: 99%

Cadmium induces actin cytoskeleton alterations and dysfunction in Neuro‐2a cells

Song

Chen

et al. 2019

Environmental Toxicology

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Cadmium (Cd) is considered a possible etiological factor in neurodegenerative diseases. However, the exact mechanism by which Cd induces neurotoxicity is not well elucidated. In this study, Neuro-2a cells were treated with 0, 10, 20, and 40 μM cadmium chloride for 24 hours to investigate the effects of Cd on the cytoskeleton of nerve cells. MTT assay and ELISA assay were used to examine cell viability and release of lactate dehydrogenase (LDH) from cells, respectively. Results showed that Cd reduced cell viability and increased the release of LDH in a dose-dependent manner (P < 0.05). The morphology of treated cell was damaged as indicated by cell collapse and dimensionality reduction. Moreover, the axonal spines and normal features of Cd-treated neurons disappeared. We checked the ultrastructure of Neuro-2a cells and found that Cd-induced swelling, membrane damage, overflow of cytoplasm contents, and cell fragmentation. Damaged mitochondria, expanded endoplasmic reticulum, and abnormal microfilaments were found in Cd-treated cells rather than in untreated cells. Compared with the control group, the relative release of glutamate in the supernatant after Cd treatment was reduced, indicating that Cd exposure could reduce the release of glutamate by inhibiting the function of nerve-2a cells. Cd decreased the mRNA and protein expression levels of cytoskeletal proteins including DBN, SYP, and TAU, which might promote cytoskeleton alterations in Cd-treated cells. In conclusion, Cd-induced actin cytoskeleton alterations and dysfunction of cultured neurons. The results of the present study provide new insights for the investigation of Cd-induced neurotoxicity.

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“…Indeed, an evolution of the actin system, and of the cytoskeleton as a whole, has taken place between uni- and multicellular organisms [95,96]. There are conspicuous differences between the migration of unicellular organisms like the rhizopode Amoeba proteus, which displays a dramatic change in shape ( ;) without obvious organizational stable polarity [97], and that of cells from animal organisms, which keep a more constant and polarized shape while migrating ().…”

Section: Why Are Unicellular Eukaryotes Polarized?mentioning

confidence: 99%

Cell polarity: having and making sense of direction—on the evolutionary significance of the primary cilium/centrosome organ in Metazoa

Bornens¹

2018

Open Biol.

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Cell-autonomous polarity in Metazoans is evolutionarily conserved. I assume that permanent polarity in unicellular eukaryotes is required for cell motion and sensory reception, integration of these two activities being an evolutionarily constrained function. Metazoans are unique in making cohesive multicellular organisms through complete cell divisions. They evolved a primary cilium/centrosome (PC/C) organ, ensuring similar functions to the basal body/flagellum of unicellular eukaryotes, but in different cells, or in the same cell at different moments. The possibility that this innovation contributed to the evolution of individuality, in being instrumental in the early specification of the germ line during development, is further discussed. Then, using the example of highly regenerative organisms like planarians, which have lost PC/C organ in dividing cells, I discuss the possibility that part of the remodelling necessary to reach a new higher-level unit of selection in multi-cellular organisms has been triggered by conflicts among individual cell polarities to reach an organismic polarity. Finally, I briefly consider organisms with a sensorimotor organ like the brain that requires exceedingly elongated polarized cells for its activity. I conclude that beyond critical consequences for embryo development, the conservation of cell-autonomous polarity in Metazoans had far-reaching implications for the evolution of individuality.

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Origin and Evolution of the Self-Organizing Cytoskeleton in the Network of Eukaryotic Organelles

Cited by 31 publications

References 135 publications

Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution

Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution

Cadmium induces actin cytoskeleton alterations and dysfunction in Neuro‐2a cells

Cell polarity: having and making sense of direction—on the evolutionary significance of the primary cilium/centrosome organ in Metazoa

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