Literature DB >> 31378311

Self-Similar Dynamics of Nuclear Packing in the Early Drosophila Embryo.

Sayantan Dutta1, Nareg J-V Djabrayan2, Salvatore Torquato3, Stanislav Y Shvartsman4, Matej Krajnc5.   

Abstract

Embryonic development starts with cleavages, a rapid sequence of reductive divisions that result in an exponential increase of cell number without changing the overall size of the embryo. In Drosophila, the final four rounds of cleavages occur at the surface of the embryo and give rise to ∼6000 nuclei under a common plasma membrane. We use live imaging to study the dynamics of this process and to characterize the emergent nuclear packing in this system. We show that the characteristic length scale of the internuclear interaction scales with the density, which allows the densifying embryo to sustain the level of structural order at progressively smaller length scales. This is different from nonliving materials, which typically undergo disorder-order transition upon compression. To explain this dynamics, we use a particle-based model that accounts for density-dependent nuclear interactions and synchronous divisions. We reproduce the pair statistics of the disordered packings observed in embryos and recover the scaling relation between the characteristic length scale and the density both in real and reciprocal space. This result reveals how the embryo can robustly preserve the nuclear-packing structure while being densified. In addition to providing quantitative description of self-similar dynamics of nuclear packings, this model generates dynamic meshes for the computational analysis of pattern formation and tissue morphogenesis.
Copyright © 2019 Biophysical Society. Published by Elsevier Inc. All rights reserved.

Entities:  

Year:  2019        PMID: 31378311      PMCID: PMC6712419          DOI: 10.1016/j.bpj.2019.07.009

Source DB:  PubMed          Journal:  Biophys J        ISSN: 0006-3495            Impact factor:   4.033


  37 in total

1.  Stripe phases from isotropic repulsive interactions.

Authors:  Gianpietro Malescio; Giuseppe Pellicane
Journal:  Nat Mater       Date:  2003-02       Impact factor: 43.841

2.  A force balance model of early spindle pole separation in Drosophila embryos.

Authors:  E N Cytrynbaum; J M Scholey; A Mogilner
Journal:  Biophys J       Date:  2003-02       Impact factor: 4.033

3.  Fluidization of tissues by cell division and apoptosis.

Authors:  Jonas Ranft; Markus Basan; Jens Elgeti; Jean-François Joanny; Jacques Prost; Frank Jülicher
Journal:  Proc Natl Acad Sci U S A       Date:  2010-11-15       Impact factor: 11.205

4.  Dynamic ordering of nuclei in syncytial embryos: a quantitative analysis of the role of cytoskeletal networks.

Authors:  Takuma Kanesaki; Carina M Edwards; Ulrich S Schwarz; Jörg Grosshans
Journal:  Integr Biol (Camb)       Date:  2011-10-14       Impact factor: 2.192

5.  Early spindle assembly in Drosophila embryos: role of a force balance involving cytoskeletal dynamics and nuclear mechanics.

Authors:  E N Cytrynbaum; P Sommi; I Brust-Mascher; J M Scholey; A Mogilner
Journal:  Mol Biol Cell       Date:  2005-08-03       Impact factor: 4.138

6.  Large-scale simulations of the two-dimensional melting of hard disks.

Authors:  C H Mak
Journal:  Phys Rev E Stat Nonlin Soft Matter Phys       Date:  2006-06-07

7.  Robust algorithm to generate a diverse class of dense disordered and ordered sphere packings via linear programming.

Authors:  S Torquato; Y Jiao
Journal:  Phys Rev E Stat Nonlin Soft Matter Phys       Date:  2010-12-10

8.  Dynamics of the Dorsal morphogen gradient.

Authors:  Jitendra S Kanodia; Richa Rikhy; Yoosik Kim; Viktor K Lund; Robert DeLotto; Jennifer Lippincott-Schwartz; Stanislav Y Shvartsman
Journal:  Proc Natl Acad Sci U S A       Date:  2009-12-08       Impact factor: 11.205

9.  A compartmental model for the bicoid gradient.

Authors:  Michail E Kavousanakis; Jitendra S Kanodia; Yoosik Kim; Ioannis G Kevrekidis; Stanislav Y Shvartsman
Journal:  Dev Biol       Date:  2010-05-24       Impact factor: 3.582

10.  Canalization of gene expression in the Drosophila blastoderm by gap gene cross regulation.

Authors:  Svetlana Surkova; Alexander V Spirov; Vitaly V Gursky; Hilde Janssens; Ah-Ram Kim; Ovidiu Radulescu; Carlos E Vanario-Alonso; David H Sharp; Maria Samsonova; John Reinitz
Journal:  PLoS Biol       Date:  2009-03-10       Impact factor: 8.029

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  5 in total

1.  Temporal integration of inductive cues on the way to gastrulation.

Authors:  Sarah McFann; Sayantan Dutta; Jared E Toettcher; Stanislav Y Shvartsman
Journal:  Proc Natl Acad Sci U S A       Date:  2021-06-08       Impact factor: 11.205

2.  Excess dNTPs Trigger Oscillatory Surface Flow in the Early Drosophila Embryo.

Authors:  Sayantan Dutta; Nareg J-V Djabrayan; Celia M Smits; Clarence W Rowley; Stanislav Y Shvartsman
Journal:  Biophys J       Date:  2020-03-29       Impact factor: 4.033

3.  Nuclear speed and cycle length co-vary with local density during syncytial blastoderm formation in a cricket.

Authors:  Seth Donoughe; Jordan Hoffmann; Taro Nakamura; Chris H Rycroft; Cassandra G Extavour
Journal:  Nat Commun       Date:  2022-07-06       Impact factor: 17.694

4.  Reverse-engineering forces responsible for dynamic clustering and spreading of multiple nuclei in developing muscle cells.

Authors:  Angelika Manhart; Mafalda Azevedo; Mary Baylies; Alex Mogilner
Journal:  Mol Biol Cell       Date:  2020-03-04       Impact factor: 4.138

5.  Attractive internuclear force drives the collective behavior of nuclear arrays in Drosophila embryos.

Authors:  Xiaoxuan Wu; Kakit Kong; Wenlei Xiao; Feng Liu
Journal:  PLoS Comput Biol       Date:  2021-11-19       Impact factor: 4.475

  5 in total

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