Nuclear actin and myosin in chromatin regulation and maintenance of genome integrity

Venit, Tomáš; Mahmood, Syed Raza; Endara-Coll, Martin; Percipalle, Piergiorgio

doi:10.1016/bs.ircmb.2020.05.001

Cited by 16 publications

(38 citation statements)

References 181 publications

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“…Although, nuclear motor proteins have a number of roles in genome function ( Venit et al, 2020 ), it appears that at least one of the roles NM1β plays in young proliferating cells, whereby chromosomes and genes respond to stimuli to be relocated to new non-random active locations is not functional in old cells. The nuclear distribution of NM1β is considerably different in senescent cells when compared to young proliferating cells, so a further possible biomarker candidate?…”

Section: Discussionmentioning

confidence: 99%

Interphase Chromosomes in Replicative Senescence: Chromosome Positioning as a Senescence Biomarker and the Lack of Nuclear Motor-Driven Chromosome Repositioning in Senescent Cells

Mehta

Riyahi

Pereira

et al. 2021

Front. Cell Dev. Biol.

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This study demonstrates, and confirms, that chromosome territory positioning is altered in primary senescent human dermal fibroblasts (HDFs). The chromosome territory positioning pattern is very similar to that found in HDFs made quiescent either by serum starvation or confluence; but not completely. A few chromosomes are found in different locations. One chromosome in particular stands out, chromosome 10, which is located in an intermediate location in young proliferating HDFs, but is found at the nuclear periphery in quiescent cells and in an opposing location of the nuclear interior in senescent HDFs. We have previously demonstrated that individual chromosome territories can be actively and rapidly relocated, with 15 min, after removal of serum from the culture media. These chromosome relocations require nuclear motor activity through the presence of nuclear myosin 1β (NM1β). We now also demonstrate rapid chromosome movement in HDFs after heat-shock at 42°C. Others have shown that heat shock genes are actively relocated using nuclear motor protein activity via actin or NM1β (Khanna et al., 2014; Pradhan et al., 2020). However, this current study reveals, that in senescent HDFs, chromosomes can no longer be relocated to expected nuclear locations upon these two types of stimuli. This coincides with a entirely different organisation and distribution of NM1β within senescent HDFs.

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Section: Discussionmentioning

confidence: 99%

Interphase Chromosomes in Replicative Senescence: Chromosome Positioning as a Senescence Biomarker and the Lack of Nuclear Motor-Driven Chromosome Repositioning in Senescent Cells

Mehta

Riyahi

Pereira

et al. 2021

Front. Cell Dev. Biol.

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“…An actomyosin-based cytoskeleton using ATP energy plays a role in heterochromatin segregation and the organization of specific heterochromatin compartments: β-actin deficient cells exhibit changes in the spatial organization of H3K9Me3/HP1α—positive heterochromatin [ 109 ]. At the same time, one of the primary functions of the elastic nuclear actomyosin network is to maintain a chromatin landscape compatible with transcription [ 109 , 110 , 111 ]. How are these two functions coupled through the putative nuclear heterochromatin network?…”

Section: Flexible Heterochromatin Transcription Regulation and Related Mechanobiology Of The Actomyosin Networkmentioning

confidence: 99%

Heterochromatin Networks: Topology, Dynamics, and Function (a Working Hypothesis)

Ērenpreisa

Krigerts

Salmiņa

et al. 2021

Cells

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Open systems can only exist by self-organization as pulsing structures exchanging matter and energy with the outer world. This review is an attempt to reveal the organizational principles of the heterochromatin supra-intra-chromosomal network in terms of nonlinear thermodynamics. The accessibility of the linear information of the genetic code is regulated by constitutive heterochromatin (CHR) creating the positional information in a system of coordinates. These features include scale-free splitting-fusing of CHR with the boundary constraints of the nucleolus and nuclear envelope. The analysis of both the literature and our own data suggests a radial-concentric network as the main structural organization principle of CHR regulating transcriptional pulsing. The dynamic CHR network is likely created together with nucleolus-associated chromatin domains, while the alveoli of this network, including springy splicing speckles, are the pulsing transcription hubs. CHR contributes to this regulation due to the silencing position variegation effect, stickiness, and flexible rigidity determined by the positioning of nucleosomes. The whole system acts in concert with the elastic nuclear actomyosin network which also emerges by self-organization during the transcriptional pulsing process. We hypothesize that the the transcriptional pulsing, in turn, adjusts its frequency/amplitudes specified by topologically associating domains to the replication timing code that determines epigenetic differentiation memory.

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“…In eukaryotic cells, they have been implicated in chromatin and transcription regulation and more recently there is evidence for their involvement in chromosomal movements, and functional architecture of the genome (Visa and Percipalle, 2010;Miyamoto and Gurdon, 2013;Percipalle, 2013;Kelpsch and Tootle, 2018). These nuclear actin-based mechanisms appear to impact on key cellular processes such as DNA repair and nuclear reprograming during differentiation (Venit et al, 2020b;Xie et al, 2020) by leveraging on regulated actin dynamics (Plessner and Grosse, 2019) (Figure 5). In hematopoietic cells, WASp family members are in the nucleus and can have activity both dependent and independent on their capacity to induce Arp2/3 mediated actin polymerization.…”

Section: Nuclear Actin In Transcription Chromatin Remodeling and Nuclear Reprogrammingmentioning

confidence: 99%

“…These tools were critical in visualizing nuclear actin dynamics in living cells and to manipulate its levels to distinguish the function of nuclear and cytoplasmic actin. Actin dynamics has been suggested to be important for transcription and transcriptional reprogramming, as actin polymerizationdefective mutants inhibit RNA Polymerase (Pol) I transcription (Ye et al, 2008) and several regulators of actin polymerization have been found to be essential for proper assembly and processing of the transcription machinery (Venit et al, 2020b). For example, transcriptional reactivation of the pluripotency gene Oct4 is dependent on the WASp family member WAVE1 and polymeric actin (Miyamoto et al, 2011;Miyamoto and Gurdon, 2013).…”

Section: Actin and The Wasp Family Proteins In The Nucleusmentioning

confidence: 99%

“…The role of mechanosensing in immune cells is emerging as a critical signal transduction pathway and strengthens the evidence for the pivotal role of rapid cytoskeletal dynamics in immune cell functions. Moreover, the development of new tools for visualizing actin in the nucleus together with high throughput genomics data reveal that monomeric and filamentous actin exist in the nucleus and have distinct functions (Venit et al, 2020b) reviving the discussion on the form and function of nuclear actin. Many of the actin regulators described in the cytoplasm have been identified in the nucleus and like actin and nuclear myosin, a major function is through interactions with the RNA polymerase machinery.…”

Section: Perspectivementioning

confidence: 99%

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Journey to the Center of the Cell: Cytoplasmic and Nuclear Actin in Immune Cell Functions

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Saeed

Venit

et al. 2021

Front. Cell Dev. Biol.

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Actin cytoskeletal dynamics drive cellular shape changes, linking numerous cell functions to physiological and pathological cues. Mutations in actin regulators that are differentially expressed or enriched in immune cells cause severe human diseases known as primary immunodeficiencies underscoring the importance of efficienct actin remodeling in immune cell homeostasis. Here we discuss recent findings on how immune cells sense the mechanical properties of their environement. Moreover, while the organization and biochemical regulation of cytoplasmic actin have been extensively studied, nuclear actin reorganization is a rapidly emerging field that has only begun to be explored in immune cells. Based on the critical and multifaceted contributions of cytoplasmic actin in immune cell functionality, nuclear actin regulation is anticipated to have a large impact on our understanding of immune cell development and functionality.

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Nuclear actin and myosin in chromatin regulation and maintenance of genome integrity

Cited by 16 publications

References 181 publications

Interphase Chromosomes in Replicative Senescence: Chromosome Positioning as a Senescence Biomarker and the Lack of Nuclear Motor-Driven Chromosome Repositioning in Senescent Cells

Interphase Chromosomes in Replicative Senescence: Chromosome Positioning as a Senescence Biomarker and the Lack of Nuclear Motor-Driven Chromosome Repositioning in Senescent Cells

Heterochromatin Networks: Topology, Dynamics, and Function (a Working Hypothesis)

Journey to the Center of the Cell: Cytoplasmic and Nuclear Actin in Immune Cell Functions

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