The rich inner life of the cell nucleus: dynamic organization, active flows, and emergent rheology
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REVIEW
The rich inner life of the cell nucleus: dynamic organization, active flows, and emergent rheology Alexandra Zidovska1 Received: 24 August 2020 / Revised: 3 September 2020 / Accepted: 14 September 2020 / Published online: 16 October 2020 © The Author(s) 2020
Abstract The cell nucleus stores the genetic material essential for life, and provides the environment for transcription, maintenance, and replication of the genome. Moreover, the nucleoplasm is filled with subnuclear bodies such as nucleoli that are responsible for other vital functions. Overall, the nucleus presents a highly heterogeneous and dynamic environment with diverse functionality. Here, we propose that its biophysical complexity can be organized around three inter-related and interactive facets: heterogeneity, activity, and rheology. Most nuclear constituents are sites of active, ATP-dependent processes and are thus inherently dynamic: The genome undergoes constant rearrangement, the nuclear envelope flickers and fluctuates, nucleoli migrate and coalesce, and many of these events are mediated by nucleoplasmic flows and interactions. And yet there is spatiotemporal organization in terms of hierarchical structure of the genome, its coherently moving regions and membrane-less compartmentalization via phase-separated nucleoplasmic constituents. Moreover, the non-equilibrium or activity-driven nature of the nucleus gives rise to emergent rheology and material properties that impact all cellular processes via the central dogma of molecular biology. New biophysical insights into the cell nucleus can come from appreciating this rich inner life. Keywords Cell nucleus · Chromatin dynamics · Nuclear compartmentalization · Active matter · Rheology
Introduction The cell nucleus is arguably one of the most important organelles in eukaryotic cell, housing the genome that contains the genetic blueprint for the entire cell (Alberts et al. 2014). The genetic information is stored in the DNA molecule, which lies at the core of the central dogma of molecular biology (Crick 1958, 1970). DNA is transcribed into RNA, which becomes translated into proteins. The first step of gene expression, transcription, occurs in the cell nucleus assisted by the intricate interplay of molecular machinery that acts on chromatin, the functional form of DNA inside cells (Van Holde 2012; Alberts et al. 2014). In addition, many other DNA transactions occur inside the nucleus such as genome replication prior to cell division or DNA repair to maintain genome integrity. These processes are ATP-dependent and their molecular Alexandra Zidovska
[email protected] 1
Center for Soft Matter Research, Department of Physics, New York University, New York, NY, USA
machinery requires direct access to the DNA molecule, leading to a persistent dynamic rearrangement of the genome. While the biochemistry of these processes has been studied in great detail (Van Holde 2012; Alberts et al. 2014), their biophysical mechanisms and implications are far from understood (H¨ubner and Spector 2010;
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