The importance of the nuclear positioning of the PPARG gene for its expression during porcine in vitro adipogenesis

Stachecka, Joanna; Nowacka‐Woszuk, Joanna; Kołodziejski, Paweł; Szczerbal, Izabela

doi:10.1007/s10577-019-09604-2

Cited by 18 publications

(17 citation statements)

References 74 publications

(83 reference statements)

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“…Such behavior of OCT4 alleles can be considered evidence for a correlation between gene expression and gene positioning. This is in agreement with a report by Stachecka, Nowacka-Woszuk, Kolodziejski, and Szczerbal (2019), who demonstrated that active PPARG alleles are centrally positioned when inactive. Nevertheless, our data also demonstrated that the distance of active and inactive SOX2 alleles from the nuclear membrane did not differ significantly in both 4-and 8-cell blastomeres.…”

Section: Discussionsupporting

confidence: 94%

Pluripotency‐associated genes reposition during early embryonic developmental stages in pigs

Nguyen

Nghĩa

Lien

et al. 2020

Animal Science Journal

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We examined the allelic expression and positioning of two pluripotency‐associated genes, OCT4 and SOX2 , and two housekeeping genes, ACTB and TUBA , in 4‐ and 8‐cell porcine embryos utilizing RNA and DNA fluorescence in situ hybridization (FISH) in single blastomeres. The proportion of blastomeres expressing SOX2 bi‐allelically increased from 45% at the 4‐cell stage to 60% at the 8‐cell stage. Moreover, in 8‐cell embryos, SOX2 was expressed bi‐allelically in significantly more blastomeres than was the case for OCT4 , and this was associated with a tendency for SOX2 alleles to move toward the nuclear interior during 4‐ to 8‐cell transition. However, the radial location of OCT4 alleles did not change significantly during this transition. The locations of active and inactive alleles based on DNA and RNA FISH signals were also calculated. Inactive OCT4 alleles were located in very close proximity to the nuclear membrane, whereas active OCT4 alleles were more centrally disposed in the nucleus. Nevertheless, the nuclear location of active and inactive SOX2 alleles did not change in either 4‐ or 8‐cell blastomeres. Our RNA and DNA FISH data provide novel information on the allelic expression patterns and positioning of pluripotency‐associated genes, OCT4 and SOX2 , during embryonic genome activation in pigs.

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Section: Discussionsupporting

confidence: 94%

Pluripotency‐associated genes reposition during early embryonic developmental stages in pigs

Nguyen

Nghĩa

Lien

et al. 2020

Animal Science Journal

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“…For example, it has been previously shown that DNA is wound into chromatin territories, with specific areas corresponding to specific genes 8–10 . The localization of genes within the nucleus is not random and have been demonstrated to be related to gene activation 11,12 , suggesting the reorganization of the nucleus is a prerequisite to initiate the reprogramming to a different cell lineage 13 .…”

Section: Introductionmentioning

confidence: 99%

Correlation between Nuclear Morphology and Adipogenic Differentiation: Application of a Combined Experimental and Computational Modeling Approach

McColloch

Rabiei

Rabbani

et al. 2019

Sci Rep

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Stem cells undergo drastic morphological alterations during differentiation. While extensive studies have been performed to examine the cytoskeletal remodeling, there is a growing interest to determine the morphological, structural and functional changes of the nucleus. The current study is therefore aimed at quantifying the extent of remodeling of the nuclear morphology of human mesenchymal stem cells during biochemically-induced adipogenic differentiation. Results show the size of nuclei decreased exponentially over time as the lipid accumulation is up-regulated. Increases in the lipid accumulation appear to lag the nuclear reorganization, suggesting the nuclear deformation is a prerequisite to adipocyte maturation. Furthermore, the lamin A/C expression was increased and redistributed to the nuclear periphery along with a subsequent increase in the nuclear aspect ratio. To further assess the role of the nucleus, a nuclear morphology with a high aspect ratio was achieved using microcontact-printed substrate. The cells with an elongated nuclear shape did not efficiently undergo adipogenesis, suggesting the cellular and nuclear processes associated with stem cell differentiation at the early stage of adipogenesis cause a change in the nuclear morphology and cannot be abrogated by the morphological cues. In addition, a novel computational biomechanical model was generated to simulate the nuclear shape change during differentiation and predict the forces acting upon the nucleus. This effort led to the development of computational scaling approach to simulate the experimentally observed adipogenic differentiation processes over 15 days in less than 1.5 hours.

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“…The repositioning of genes from the nuclear lamina during many differentiation processes is a well-known mechanism of transcriptional activation 58 , 59 . Our previous experiments have shown the relocation of adipogenic genes from the nuclear periphery during differentiation 6 , 8 , 23 , but further studies are needed to elucidate if the decrease in lamin plays a direct role in this reorganization.…”

Section: Discussionmentioning

confidence: 96%

“…The differentiation of progenitor cells into adipocytes is accompanied not only by characteristic changes in cell morphology (resulting in round lipid-laden cells with a rim of cytoplasm and a flattened peripherally located nucleus), but also in nuclear organization 3 , 4 . This includes changes in nucleus shape and size, reduction of lamin A/C expression, reorganization of the chromocenter, and repositioning of chromosomes and genes 4 – 8 . Moreover, higher-order chromatin organization and chromatin interactions have recently emerged as important regulators of gene expression during adipogenesis 9 – 11 .…”

Section: Introductionmentioning

confidence: 99%

“…Nuclear lamins play a role in gene regulation, since most genes in lamina-associated domains (LADs) are repressed or expressed at very low level 22 . Many examples of the genes encoding key transcription factors of adipogenesis being repositioned from the nuclear periphery to the nuclear center have been described during adipogenesis 6 , 8 , 23 .…”

Section: Introductionmentioning

confidence: 99%

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Alteration of active and repressive histone marks during adipogenic differentiation of porcine mesenchymal stem cells

Stachecka

Kołodziejski

Noak

et al. 2021

Sci Rep

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A characteristic spatial distribution of the main chromatin fractions is observed in most mammalian cell nuclei, with euchromatin localized in the interior and heterochromatin at the nuclear periphery. It has been shown that interactions of heterochromatin with the nuclear lamina are necessary to establish this conventional architecture. Adipocytes are specific cells in which a reduction in lamin A/C expression is observed. We hypothesize that the loss of lamin A/C during adipogenic differentiation of mesenchymal stem cells (MSCs) may be associated with the reorganization of the main classes of chromatin in the nucleus. Thus, in this study, we examine the abundance and nuclear distribution of selected heterochromatin (H3K9me3, H3K27me3 and H4K20me3) and euchromatin (H4K8ac, H3K4me3 and H3K9ac) histone marks during in vitro adipogenesis, using the pig as a model organism. We found that not only did the expression of lamin A/C decrease in our differentiation system, but so did the expression of lamin B receptor (LBR). The level of two heterochromatin marks, H3K27me3 and H4K20me3, increased during differentiation, while no changes were observed for H3K9me3. The levels of two euchromatin histone marks, H4K8ac and H3K9ac, were significantly higher in adipocytes than in undifferentiated cells, while the level of H3K4me3 did not change significantly. The spatial distribution of all the examined histone marks altered during in vitro adipogenesis. H3K27me3 and H4K20me3 moved towards the nuclear periphery and H3K9me3 localized preferentially in the intermediate part of adipocyte nuclei. The euchromatin marks H3K9ac and H3K4me3 preferentially occupied the peripheral part of the adipocyte nuclei, while H4K8ac was more evenly distributed in the nuclei of undifferentiated and differentiated cells. Analysis of the nuclear distribution of repetitive sequences has shown their clustering and relocalization toward nuclear periphery during differentiation. Our study shows that dynamic changes in the abundance and nuclear distribution of active and repressive histone marks take place during adipocyte differentiation. Nuclear reorganization of heterochromatin histone marks may allow the maintenance of the nuclear morphology of the adipocytes, in which reduced expression of lamin A/C and LBR is observed.

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The importance of the nuclear positioning of the PPARG gene for its expression during porcine in vitro adipogenesis

Cited by 18 publications

References 74 publications

Pluripotency‐associated genes reposition during early embryonic developmental stages in pigs

Pluripotency‐associated genes reposition during early embryonic developmental stages in pigs

Correlation between Nuclear Morphology and Adipogenic Differentiation: Application of a Combined Experimental and Computational Modeling Approach

Alteration of active and repressive histone marks during adipogenic differentiation of porcine mesenchymal stem cells

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