Nucleoli in epithelial cell collectives respond to tumorigenic, spatial, and mechanical cues

Jaecker, Florence Flick; Almeida, J. A. Afonso de; Krull, Carly M; Pathak, Amit

doi:10.1091/mbc.e22-02-0070

Cited by 7 publications

(4 citation statements)

References 48 publications

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“…Accordingly, we report that disruption of actin laments (F-actin) by CytoD or remodeling of the F-actin network into cortical actin by sorbitol treatment both promote the formation of a single round nucleolus in dividing cells. These results add to emerging evidence that the nucleolus is a mechanosensitive organelle in human cells [21][22][23] . Interestingly, only CytoD disrupts the linear correlation between nuclear and nucleolar sizes in proliferating ASCs, pointing to the importance of a preserved cytoskeleton for size scaling of the nucleolus.…”

Section: Discussionsupporting

confidence: 72%

“…The nucleolus governs ribosome biogenesis and de novo protein synthesis. Recent reports suggest that the nucleolus is a mechanosensitive organelle responsive to changes in extracellular matrix stiffness and intracellular tension [21][22][23] . Accordingly, defective cytoskeletal remodeling during adipogenesis is accompanied by a deregulation of translation 9,10 .…”

Section: Introductionmentioning

confidence: 99%

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Cytoskeletal remodeling defines nucleolar architecture during adipogenesis

Potolitsyna

Pickering

Germier

et al. 2023

Preprint

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Differentiation of adipose progenitor cells into mature adipocytes entails a dramatic reorganization of the cellular architecture to accommodate lipid storage into cytoplasmic lipid droplets. Lipid droplets occupy most of the adipocyte volume, compressing the nucleus beneath the plasma membrane. How this cellular remodeling affects sub-nuclear structure, including size and number of nucleoli, remains unclear. We describe the morphological remodeling of the nucleus and the nucleolus during in vitro adipogenic differentiation of primary human adipose stem cells. We find that cell cycle arrest elicits a remodeling of nucleolar structure which correlates with a decrease in protein synthesis. Strikingly, triggering cytoskeletal rearrangements mimics the nucleolar remodeling observed during adipogenesis. Our results point to nucleolar remodeling as an active, mechano-regulated mechanism during adipogenic differentiation and demonstrate a key role of the actin cytoskeleton in defining nuclear and nucleolar architecture in differentiating human adipose stem cells.

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Section: Discussionsupporting

confidence: 72%

Section: Introductionmentioning

confidence: 99%

Cytoskeletal remodeling defines nucleolar architecture during adipogenesis

Potolitsyna

Pickering

Germier

et al. 2023

Preprint

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“…Finally, the cellular context may drive the differences observed. Cancer cell nucleoli are less responsive to mechanical signaling than normal cells (Jaecker et al, 2022). Further, cancer cells are mitotic, and nucleolar stress can drive the death of individual cells.…”

Section: Pgs Control the Functions Of The Nucleolusmentioning

confidence: 99%

Prostaglandins limit nuclear actin to control nucleolar function during oogenesis

Talbot

Vormezeele²,

Kimble³

et al. 2023

Front. Cell Dev. Biol.

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Prostaglandins (PGs), locally acting lipid signals, regulate female reproduction, including oocyte development. However, the cellular mechanisms of PG action remain largely unknown. One cellular target of PG signaling is the nucleolus. Indeed, across organisms, loss of PGs results in misshapen nucleoli, and changes in nucleolar morphology are indicative of altered nucleolar function. A key role of the nucleolus is to transcribe ribosomal RNA (rRNA) to drive ribosomal biogenesis. Here we take advantage of the robust, in vivo system of Drosophila oogenesis to define the roles and downstream mechanisms whereby PGs regulate the nucleolus. We find that the altered nucleolar morphology due to PG loss is not due to reduced rRNA transcription. Instead, loss of PGs results in increased rRNA transcription and overall protein translation. PGs modulate these nucleolar functions by tightly regulating nuclear actin, which is enriched in the nucleolus. Specifically, we find that loss of PGs results in both increased nucleolar actin and changes in its form. Increasing nuclear actin, by either genetic loss of PG signaling or overexpression of nuclear targeted actin (NLS-actin), results in a round nucleolar morphology. Further, loss of PGs, overexpression of NLS-actin or loss of Exportin 6, all manipulations that increase nuclear actin levels, results in increased RNAPI-dependent transcription. Together these data reveal PGs carefully balance the level and forms of nuclear actin to control the level of nucleolar activity required for producing fertilization competent oocytes.

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“…A nucleolus is a dynamic organelle, the structure of which refl ects the processes related to the biogenesis of ribosomes. Its sizes and components change depending on the activity of the cell and the stage of the mitotic cycle (Jaecker et al, 2022;Cmarko et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Investigation of some nucleoli traits in interphase leukocytes of two rabbit breeds and their hybrid

Dsitsiuk,

Boiko,

Honchar

et al. 2024

Agric. sci. pract.

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Aim. The aim was to study the differences in three traits of nucleoli in interphase leukocytes of two rab- bit breeds and a hybrid thereof. Methods. Doe rabbits, 4-month -old, from Ukrainian breed Poltavske Sriblo (n = 30), Californian (n = 25), and their hybrid (n = 21) were used in the experiment. The nucleoli in intact blood leukocytes were stained using silver staining according to Howell and Black (1980). Stained cells were observed, and their nucleoli counted in light microscopy at 10×100 oil immersion magnification. 200 leukocytes from each animal were analyzed. The activity of nucleoli was evaluated by the following parameters: the aver- age number of nucleoli in the nucleus (nNO), the total area of nucleoli in the nucleus (ΣSNO, mcm 2), the share of nucleolus area in the lymphocyte nucleus area (shΣS NO, %). Statistical analysis was conducted using the STATISTICA software package (2020). Results. The average number of nucleoli per cell varied from – 1.70 ± 0.08 in Californian rabbits to 5.90 ± 0.29 in hybrid animals. A statistically significant difference (p < 0.05) was found between the experimental groups of purebred and hybrid rabbits. The variation coefficient for the index of the average number of nucleoli per cell was on the average level of variability: 20.58 % for the rabbits of Poltavske sriblo breed, 19.50 % for Californian rabbits, and 16.49 % for hybrid ones. The total area of nucleoli in the cells of all the investigated animals varied from 5 μm2 in one Californian rabbit to 12 μm2 in animals of hybrid origin. The share of the nucleolus area in the nucleus area for rabbits of Poltavske sriblo, Californian, and hybrid breeds was 26.10 ± 1.80 %, 24.30 ± 1.62 and 29.40 ± 2.50, respectively. Conclusions. Polymorphism was observed for three nucleolar parameters after silver staining of interphase leukocytes of rabbits of Poltavske sriblo, Californian breed and their hybrid. This concerned 1) the average number of nucleoli (p < 0.05); 2) the total area of nucleoli (p < 0.05); 3) the average share of the nucleolar area in the nucleus area (p < 0.05). The results of our comparative analysis of the investigated nucleolar activity parameters suggest a higher activity of nucleoli in the animals of hybrid origin. In the future, the results of such studies may be used to assess the potential ability of animals to implement productive traits.

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Nucleoli in epithelial cell collectives respond to tumorigenic, spatial, and mechanical cues

Abstract: Leader epithelial cells develop nucleoli of bigger size and in higher numbers compared to follower cells. Stiff matrices and cancer cells further enhance this nucleolar mechano-response in epithelial colonies.

Cited by 7 publications

References 48 publications

Cytoskeletal remodeling defines nucleolar architecture during adipogenesis

Cytoskeletal remodeling defines nucleolar architecture during adipogenesis

Prostaglandins limit nuclear actin to control nucleolar function during oogenesis

Investigation of some nucleoli traits in interphase leukocytes of two rabbit breeds and their hybrid

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