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Article ; Online: Four-Dimensional Mesoscale Liquid Model of Nucleus Resolves Chromatin's Radial Organization.

Laghmach, Rabia / Di Pierro, Michele / Potoyan, Davit A

PRX life

2024 Volume 2, Issue 1

Abstract: Recent advances chromatin capture, imaging techniques, and polymer modeling have dramatically enhanced quantitative understanding of chromosomal folding. However, the dynamism inherent in genome architectures due to physical and biochemical forces and ... ...

Abstract	Recent advances chromatin capture, imaging techniques, and polymer modeling have dramatically enhanced quantitative understanding of chromosomal folding. However, the dynamism inherent in genome architectures due to physical and biochemical forces and their impact on nuclear architecture and cellular functions remains elusive. While imaging of chromatin in four dimensions is becoming more common, there is a conspicuous lack of physics-based computational tools appropriate for revealing the forces that shape nuclear architecture and dynamics. To this end, we have developed a multiphase liquid model of the nucleus, which can resolve chromosomal territories, compartments, and nuclear lamina using a physics-based and data-informed free-energy function. The model enables rapid hypothesis-driven prototyping of nuclear dynamics in four dimensions, thereby facilitating comparison with whole nucleus imaging experiments. As an application, we model the
Language	English
Publishing date	2024-01-30
Publishing country	United States
Document type	Journal Article
ISSN	2835-8279
ISSN (online)	2835-8279
DOI	10.1103/PRXLife.2.013006
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Article ; Online: Inner workings of gene folding.

Di Pierro, Michele

Proceedings of the National Academy of Sciences of the United States of America

2019 Volume 116, Issue 11, Page(s) 4774–4775

Language	English
Publishing date	2019-02-22
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, Non-U.S. Gov't ; Comment
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.1900875116
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Article ; Online: An associative memory Hamiltonian model for DNA and nucleosomes.

Lu, Weiqi / Onuchic, José N / Di Pierro, Michele

PLoS computational biology

2023 Volume 19, Issue 3, Page(s) e1011013

Abstract: A model for DNA and nucleosomes is introduced with the goal of studying chromosomes from a single base level all the way to higher-order chromatin structures. This model, dubbed the Widely Editable Chromatin Model (WEChroM), reproduces the complex ... ...

Abstract	A model for DNA and nucleosomes is introduced with the goal of studying chromosomes from a single base level all the way to higher-order chromatin structures. This model, dubbed the Widely Editable Chromatin Model (WEChroM), reproduces the complex mechanics of the double helix including its bending persistence length and twisting persistence length, and the temperature dependence of the former. The WEChroM Hamiltonian is composed of chain connectivity, steric interactions, and associative memory terms representing all remaining interactions leading to the structure, dynamics, and mechanical characteristics of the B-DNA. Several applications of this model are discussed to demonstrate its applicability. WEChroM is used to investigate the behavior of circular DNA in the presence of positive and negative supercoiling. We show that it recapitulates the formation of plectonemes and of structural defects that relax mechanical stress. The model spontaneously manifests an asymmetric behavior with respect to positive or negative supercoiling, similar to what was previously observed in experiments. Additionally, we show that the associative memory Hamiltonian is also capable of reproducing the free energy of partial DNA unwrapping from nucleosomes. WEChroM is designed to emulate the continuously variable mechanical properties of the 10nm fiber and, by virtue of its simplicity, is ready to be scaled up to molecular systems large enough to investigate the structural ensembles of genes. WEChroM is implemented in the OpenMM simulation toolkits and is freely available for public use.
MeSH term(s)	Nucleosomes/genetics ; DNA/genetics ; DNA/chemistry ; Chromatin ; Entropy ; Computer Simulation ; Nucleic Acid Conformation
Chemical Substances	Nucleosomes ; DNA (9007-49-2) ; Chromatin
Language	English
Publishing date	2023-03-27
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, Non-U.S. Gov't
ZDB-ID	2193340-6
ISSN	1553-7358 ; 1553-734X
ISSN (online)	1553-7358
ISSN	1553-734X
DOI	10.1371/journal.pcbi.1011013
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Article ; Online: An associative memory Hamiltonian model for DNA and nucleosomes.

Weiqi Lu / José N Onuchic / Michele Di Pierro

PLoS Computational Biology, Vol 19, Iss 3, p e

2023 Volume 1011013

Abstract	A model for DNA and nucleosomes is introduced with the goal of studying chromosomes from a single base level all the way to higher-order chromatin structures. This model, dubbed the Widely Editable Chromatin Model (WEChroM), reproduces the complex mechanics of the double helix including its bending persistence length and twisting persistence length, and the temperature dependence of the former. The WEChroM Hamiltonian is composed of chain connectivity, steric interactions, and associative memory terms representing all remaining interactions leading to the structure, dynamics, and mechanical characteristics of the B-DNA. Several applications of this model are discussed to demonstrate its applicability. WEChroM is used to investigate the behavior of circular DNA in the presence of positive and negative supercoiling. We show that it recapitulates the formation of plectonemes and of structural defects that relax mechanical stress. The model spontaneously manifests an asymmetric behavior with respect to positive or negative supercoiling, similar to what was previously observed in experiments. Additionally, we show that the associative memory Hamiltonian is also capable of reproducing the free energy of partial DNA unwrapping from nucleosomes. WEChroM is designed to emulate the continuously variable mechanical properties of the 10nm fiber and, by virtue of its simplicity, is ready to be scaled up to molecular systems large enough to investigate the structural ensembles of genes. WEChroM is implemented in the OpenMM simulation toolkits and is freely available for public use.
Keywords	Biology (General) ; QH301-705.5
Subject code	612
Language	English
Publishing date	2023-03-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
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Article: A Liquid State Perspective on Dynamics of Chromatin Compartments.

Laghmach, Rabia / Di Pierro, Michele / Potoyan, Davit

Frontiers in molecular biosciences

2022 Volume 8, Page(s) 781981

Abstract: The interior of the eukaryotic cell nucleus has a crowded and heterogeneous environment packed with chromatin polymers, regulatory proteins, and RNA molecules. Chromatin polymer, assisted by epigenetic modifications, protein and RNA binders, forms multi- ... ...

Abstract	The interior of the eukaryotic cell nucleus has a crowded and heterogeneous environment packed with chromatin polymers, regulatory proteins, and RNA molecules. Chromatin polymer, assisted by epigenetic modifications, protein and RNA binders, forms multi-scale compartments which help regulate genes in response to cellular signals. Furthermore, chromatin compartments are dynamic and tend to evolve in size and composition in ways that are not fully understood. The latest super-resolution imaging experiments have revealed a much more dynamic and stochastic nature of chromatin compartments than was appreciated before. An emerging mechanism explaining chromatin compartmentalization dynamics is the phase separation of protein and nucleic acids into membraneless liquid condensates. Consequently, concepts and ideas from soft matter and polymer systems have been rapidly entering the lexicon of cell biology. In this respect, the role of computational models is crucial for establishing a rigorous and quantitative foundation for the new concepts and disentangling the complex interplay of forces that contribute to the emergent patterns of chromatin dynamics and organization. Several multi-scale models have emerged to address various aspects of chromatin dynamics, ranging from equilibrium polymer simulations, hybrid non-equilibrium simulations coupling protein binding and chromatin folding, and mesoscopic field-theoretic models. Here, we review these emerging theoretical paradigms and computational models with a particular focus on chromatin's phase separation and liquid-like properties as a basis for nuclear organization and dynamics.
Language	English
Publishing date	2022-01-13
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2814330-9
ISSN	2296-889X
ISSN	2296-889X
DOI	10.3389/fmolb.2021.781981
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Article: The Moral Foundations of Desired Cultural Tightness.

Di Santo, Daniela / Gelfand, Michele J / Baldner, Conrad / Pierro, Antonio

Frontiers in psychology

2022 Volume 13, Page(s) 739579

Abstract: People vary on their desire for strict norms, and the moral underpinnings of these differences have yet to be explored. The current research examined whether and how moral beliefs held by individuals would affect the extent to which they want their ... ...

Abstract	People vary on their desire for strict norms, and the moral underpinnings of these differences have yet to be explored. The current research examined whether and how moral beliefs held by individuals would affect the extent to which they want their country to be tight (i.e., having strict social norms) or loose (i.e., having more permissive social norms). In particular, the effects of the "binding" and "individualizing" foundations, which are moral beliefs focused on the importance of groups and individuals, respectively, were examined. We hypothesized that the binding foundations could predict people's desire for cultural tightness. We also hypothesized that the perception that one's society is threatened may drive this effect. Three studies were conducted using both cross-sectional (Studies 1 and 3) and two-wave (Study 2) designs. Demographic variables and participants' political orientation effects were controlled. In Study 1, only the binding foundations significantly predicted higher desired tightness. In Study 2, binding foundations predicted desired tightness measured at follow-up. In Study 3, the positive effect of perceived threat on desired tightness
Language	English
Publishing date	2022-04-19
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2563826-9
ISSN	1664-1078
ISSN	1664-1078
DOI	10.3389/fpsyg.2022.739579
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Article ; Online: Shaping the genome via lengthwise compaction, phase separation, and lamina adhesion.

Brahmachari, Sumitabha / Contessoto, Vinícius G / Di Pierro, Michele / Onuchic, José N

Nucleic acids research

2022 Volume 50, Issue 8, Page(s) 4258–4271

Abstract: The link between genomic structure and biological function is yet to be consolidated, it is, however, clear that physical manipulation of the genome, driven by the activity of a variety of proteins, is a crucial step. To understand the consequences of ... ...

Abstract	The link between genomic structure and biological function is yet to be consolidated, it is, however, clear that physical manipulation of the genome, driven by the activity of a variety of proteins, is a crucial step. To understand the consequences of the physical forces underlying genome organization, we build a coarse-grained polymer model of the genome, featuring three fundamentally distinct classes of interactions: lengthwise compaction, i.e., compaction of chromosomes along its contour, self-adhesion among epigenetically similar genomic segments, and adhesion of chromosome segments to the nuclear envelope or lamina. We postulate that these three types of interactions sufficiently represent the concerted action of the different proteins organizing the genome architecture and show that an interplay among these interactions can recapitulate the architectural variants observed across the tree of life. The model elucidates how an interplay of forces arising from the three classes of genomic interactions can drive drastic, yet predictable, changes in the global genome architecture, and makes testable predictions. We posit that precise control over these interactions in vivo is key to the regulation of genome architecture.
MeSH term(s)	Chromosomes/chemistry ; Chromosomes/metabolism ; Genome ; Genomics ; Nuclear Envelope ; Nuclear Lamina/chemistry ; Nuclear Lamina/metabolism ; Nuclear Proteins/chemistry ; Nuclear Proteins/metabolism
Chemical Substances	Nuclear Proteins
Language	English
Publishing date	2022-04-14
Publishing country	England
Document type	Journal Article
ZDB-ID	186809-3
ISSN	1362-4962 ; 1362-4954 ; 0301-5610 ; 0305-1048
ISSN (online)	1362-4962 ; 1362-4954
ISSN	0301-5610 ; 0305-1048
DOI	10.1093/nar/gkac231
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Article ; Online: A Liquid State Perspective on Dynamics of Chromatin Compartments

Rabia Laghmach / Michele Di Pierro / Davit Potoyan

Frontiers in Molecular Biosciences, Vol

2022 Volume 8

Abstract	The interior of the eukaryotic cell nucleus has a crowded and heterogeneous environment packed with chromatin polymers, regulatory proteins, and RNA molecules. Chromatin polymer, assisted by epigenetic modifications, protein and RNA binders, forms multi-scale compartments which help regulate genes in response to cellular signals. Furthermore, chromatin compartments are dynamic and tend to evolve in size and composition in ways that are not fully understood. The latest super-resolution imaging experiments have revealed a much more dynamic and stochastic nature of chromatin compartments than was appreciated before. An emerging mechanism explaining chromatin compartmentalization dynamics is the phase separation of protein and nucleic acids into membraneless liquid condensates. Consequently, concepts and ideas from soft matter and polymer systems have been rapidly entering the lexicon of cell biology. In this respect, the role of computational models is crucial for establishing a rigorous and quantitative foundation for the new concepts and disentangling the complex interplay of forces that contribute to the emergent patterns of chromatin dynamics and organization. Several multi-scale models have emerged to address various aspects of chromatin dynamics, ranging from equilibrium polymer simulations, hybrid non-equilibrium simulations coupling protein binding and chromatin folding, and mesoscopic field-theoretic models. Here, we review these emerging theoretical paradigms and computational models with a particular focus on chromatin’s phase separation and liquid-like properties as a basis for nuclear organization and dynamics.
Keywords	chromatin ; liquid-liquid phase separation ; heterochromatin ; euchromatin ; nuclear organization ; lamin ; Biology (General) ; QH301-705.5
Subject code	612
Language	English
Publishing date	2022-01-01T00:00:00Z
Publisher	Frontiers Media S.A.
Document type	Article ; Online
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Article ; Online: The interplay of chromatin phase separation and lamina interactions in nuclear organization.

Laghmach, Rabia / Di Pierro, Michele / Potoyan, Davit A

Biophysical journal

2021 Volume 120, Issue 22, Page(s) 5005–5017

Abstract: The genetic material of eukaryotes is segregated into transcriptionally active euchromatin and silent heterochromatin compartments. The spatial arrangement of chromatin compartments evolves over the course of cellular life in a process that remains ... ...

Abstract	The genetic material of eukaryotes is segregated into transcriptionally active euchromatin and silent heterochromatin compartments. The spatial arrangement of chromatin compartments evolves over the course of cellular life in a process that remains poorly understood. The latest nuclear imaging experiments reveal a number of dynamical signatures of chromatin that are reminiscent of active multiphase liquids. This includes the observations of viscoelastic response, coherent motions, Ostwald ripening, and coalescence of chromatin compartments. There is also growing evidence that liquid-liquid phase separation of protein and nucleic acid components is the underlying mechanism for the dynamical behavior of chromatin. To dissect the organizational and dynamical implications of chromatin's liquid behavior, we have devised a phenomenological field-theoretic model of the nucleus as a multiphase condensate of liquid chromatin types. Employing the liquid chromatin model of the Drosophila nucleus, we have carried out an extensive set of simulations with an objective to shed light on the dynamics and chromatin patterning observed in the latest nuclear imaging experiments. Our simulations reveal the emergence of experimentally detected mesoscale chromatin channels and spheroidal droplets which arise from the dynamic interplay of chromatin type to type interactions and intermingling of chromosomal territories. We also quantitatively reproduce coherent motions of chromatin domains observed in displacement correlation spectroscopy measurements which are explained within the framework of our model by phase separation of chromatin types operating within constrained intrachromosomal and interchromosomal boundaries. Finally, we illuminate the role of heterochromatin-lamina interactions in the nuclear organization by showing that these interactions enhance the mobility of euchromatin and indirectly introduce correlated motions of heterochromatin droplets.
MeSH term(s)	Animals ; Cell Nucleus ; Chromatin ; Drosophila ; Euchromatin ; Heterochromatin
Chemical Substances	Chromatin ; Euchromatin ; Heterochromatin
Language	English
Publishing date	2021-10-13
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	218078-9
ISSN	1542-0086 ; 0006-3495
ISSN (online)	1542-0086
ISSN	0006-3495
DOI	10.1016/j.bpj.2021.10.012
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Article ; Online: Interphase chromosomes of the Aedes aegypti mosquito are liquid crystalline and can sense mechanical cues.

Contessoto, Vinícius G / Dudchenko, Olga / Aiden, Erez Lieberman / Wolynes, Peter G / Onuchic, José N / Di Pierro, Michele

Nature communications

2023 Volume 14, Issue 1, Page(s) 326

Abstract: We use data-driven physical simulations to study the three-dimensional architecture of the Aedes aegypti genome. Hi-C maps exhibit both a broad diagonal and compartmentalization with telomeres and centromeres clustering together. Physical modeling ... ...

Abstract	We use data-driven physical simulations to study the three-dimensional architecture of the Aedes aegypti genome. Hi-C maps exhibit both a broad diagonal and compartmentalization with telomeres and centromeres clustering together. Physical modeling reveals that these observations correspond to an ensemble of 3D chromosomal structures that are folded over and partially condensed. Clustering of the centromeres and telomeres near the nuclear lamina appears to be a necessary condition for the formation of the observed structures. Further analysis of the mechanical properties of the genome reveals that the chromosomes of Aedes aegypti, by virtue of their atypical structural organization, are highly sensitive to the deformation of the nuclei. This last finding provides a possible physical mechanism linking mechanical cues to gene regulation.
MeSH term(s)	Animals ; Aedes/genetics ; Cues ; Telomere/genetics ; Chromosome Structures ; Interphase
Language	English
Publishing date	2023-01-19
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-023-35909-2
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