scholarly journals Attractive internuclear force drives the collective behavior of nuclear arrays in Drosophila embryos

2021 ◽  
Vol 17 (11) ◽  
pp. e1009605
Author(s):  
Xiaoxuan Wu ◽  
Kakit Kong ◽  
Wenlei Xiao ◽  
Feng Liu
Keyword(s):  
Force Field ◽  
Collective Behavior ◽  
Collective Motion ◽  
Standing Waves ◽  
Light Sheet ◽  
Developmental Patterns ◽  
Collective Behaviors ◽  
Light Sheet Microscopy ◽  
Anterior Posterior ◽  
Drosophila Embryos

The collective behavior of the nuclear array in Drosophila embryos during nuclear cycle (NC) 11 to NC14 is crucial in controlling cell size, establishing developmental patterns, and coordinating morphogenesis. After live imaging on Drosophila embryos with light sheet microscopy, we extract the nuclear trajectory, speed, and internuclear distance with an automatic nuclear tracing method. We find that the nuclear speed shows a period of standing waves along the anterior-posterior (AP) axis after each metaphase as the nuclei collectively migrate towards the embryo poles and partially move back. And the maximum nuclear speed dampens by 28%-45% in the second half of the standing wave. Moreover, the nuclear density is 22–42% lower in the pole region than the middle of the embryo during the interphase of NC12-NC14. To find mechanical rules controlling the collective motion and packing patterns of the nuclear array, we use a deep neural network (DNN) to learn the underlying force field from data. We apply the learned spatiotemporal attractive force field in the simulations with a particle-based model. And the simulations recapitulate nearly all the observed characteristic collective behaviors of nuclear arrays in Drosophila embryos.

scholarly journals Attractive internuclear force drives the collective behavior of nuclear arrays in Drosophila embryos

2020 ◽  
Author(s):  
Xiaoxuan Wu ◽  
Kakit Kong ◽  
Wenlei Xiao ◽  
Feng Liu
Keyword(s):  
Force Field ◽  
Standing Wave ◽  
Collective Behavior ◽  
Collective Motion ◽  
Membrane Separation ◽  
Light Sheet ◽  
Test Tube ◽  
Nuclear Density ◽  
Collective Behaviors ◽  
Light Sheet Microscopy

ABSTRACTThe emerging collective behaviors during embryogenesis play an important role in precise and reproducible morphogenesis. An important question in the study of collective behavior is what rule underlies the emerging pattern. Here we use the Drosophila embryo as a test tube to study this question. We focus on the nuclear array without membrane separation on the embryo periphery from the nuclear cycle (NC) 11 to NC14. After live imaging with light sheet microscopy, we extract the nuclear trajectory, speed, and internuclear distance with an automatic nuclear tracing method. We find that the nuclear speed shows a period of standing waves along the anterior-posterior (AP) axis after each metaphase as the nuclei collectively migrate towards the embryo poles and partially move back. And the maximum nuclear speed dampens by 38% in the second half of the standing wave. Moreover, the nuclear density is 35% higher in the middle than the pole region of the embryo during the S phase of NC11-NC14. To find mechanical rules controlling the collective motion and packing patterns of the nuclear array, we use the deep neural network (DNN) to learn the force field from data. We find two potential strong nuclear-age-dependent force fields, i.e., the repulsive or attractive force field. Simulations with the particle-based model indicate that only if the net internuclear force is attractive and increases with distance, the pseudo-synchronous mitotic wave in a nuclear array with lower nuclear density in embryo poles can drive the collective motion with the damped standing wave of the nuclear speed, and the collective nuclear motion, in turn, maintains the non-uniform nuclear density.

scholarly journals Dynamic multifactor hubs interact transiently with sites of active transcription in Drosophila embryos

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Mustafa Mir ◽  
Michael R Stadler ◽  
Stephan A Ortiz ◽  
Colleen E Hannon ◽  
Melissa M Harrison ◽  
...  
Keyword(s):  
Transcription Factors ◽  
Single Molecule ◽  
High Speed ◽  
Light Sheet ◽  
Editorial Note ◽  
Regulation Of Transcription ◽  
Light Sheet Microscopy ◽  
4D Imaging ◽  
Active Transcription ◽  
Drosophila Embryos

The regulation of transcription requires the coordination of numerous activities on DNA, yet how transcription factors mediate these activities remains poorly understood. Here, we use lattice light-sheet microscopy to integrate single-molecule and high-speed 4D imaging in developing Drosophila embryos to study the nuclear organization and interactions of the key transcription factors Zelda and Bicoid. In contrast to previous studies suggesting stable, cooperative binding, we show that both factors interact with DNA with surprisingly high off-rates. We find that both factors form dynamic subnuclear hubs, and that Bicoid binding is enriched within Zelda hubs. Remarkably, these hubs are both short lived and interact only transiently with sites of active Bicoid-dependent transcription. Based on our observations, we hypothesize that, beyond simply forming bridges between DNA and the transcription machinery, transcription factors can organize other proteins into hubs that transiently drive multiple activities at their gene targets.Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (<xref ref-type="decision-letter" rid="SA1">see decision letter</xref>).

Dual-color on-chip light sheet microscopy of drosophila embryos

2020 ◽  
Author(s):  
Petra Paiè ◽  
Roberto Memeo ◽  
Federico Sala ◽  
Michele Castriotta ◽  
Thomas Vaccari ◽  
...  
Keyword(s):  
Light Sheet ◽  
Light Sheet Microscopy ◽  
Dual Color ◽  
On Chip ◽  
Drosophila Embryos

scholarly journals Multi-view light-sheet imaging and tracking with the MaMuT software reveals the cell lineage of a direct developing arthropod limb

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Carsten Wolff ◽  
Jean-Yves Tinevez ◽  
Tobias Pietzsch ◽  
Evangelia Stamataki ◽  
Benjamin Harich ◽  
...  
Keyword(s):  
Limb Development ◽  
Expression Patterns ◽  
Cell Lineage ◽  
Light Sheet ◽  
Limb Bud ◽  
Spatial Modulation ◽  
Spatiotemporal Resolution ◽  
Cell Behaviors ◽  
Light Sheet Microscopy ◽  
Anterior Posterior

During development, coordinated cell behaviors orchestrate tissue and organ morphogenesis. Detailed descriptions of cell lineages and behaviors provide a powerful framework to elucidate the mechanisms of morphogenesis. To study the cellular basis of limb development, we imaged transgenic fluorescently-labeled embryos from the crustacean Parhyale hawaiensis with multi-view light-sheet microscopy at high spatiotemporal resolution over several days of embryogenesis. The cell lineage of outgrowing thoracic limbs was reconstructed at single-cell resolution with new software called Massive Multi-view Tracker (MaMuT). In silico clonal analyses suggested that the early limb primordium becomes subdivided into anterior-posterior and dorsal-ventral compartments whose boundaries intersect at the distal tip of the growing limb. Limb-bud formation is associated with spatial modulation of cell proliferation, while limb elongation is also driven by preferential orientation of cell divisions along the proximal-distal growth axis. Cellular reconstructions were predictive of the expression patterns of limb development genes including the BMP morphogen Decapentaplegic.

scholarly journals Single-Molecule Imaging in Living Drosophila Embryos with Reflected Light-Sheet Microscopy

2016 ◽  
Vol 110 (4) ◽  
pp. 939-946 ◽  
Author(s):  
Ferdinand Greiss ◽  
Myrto Deligiannaki ◽  
Christophe Jung ◽  
Ulrike Gaul ◽  
Dieter Braun
Keyword(s):  
Single Molecule ◽  
Light Sheet ◽  
Single Molecule Imaging ◽  
Light Sheet Microscopy ◽  
Reflected Light ◽  
Drosophila Embryos

scholarly journals Dynamic multifactor hubs interact transiently with sites of active transcription in Drosophila embryos

2018 ◽  
Author(s):  
Mustafa Mir ◽  
Michael R. Stadler ◽  
Stephan A. Ortiz ◽  
Melissa M. Harrison ◽  
Xavier Darzacq ◽  
...  
Keyword(s):  
Transcription Factors ◽  
Single Molecule ◽  
High Speed ◽  
Nuclear Organization ◽  
Light Sheet ◽  
Regulation Of Transcription ◽  
Light Sheet Microscopy ◽  
4D Imaging ◽  
Active Transcription ◽  
Drosophila Embryos

AbstractThe regulation of transcription requires the coordination of numerous activities on DNA, yet it remains poorly understood how transcription factors facilitate these multiple functions. Here we use lattice light-sheet microscopy to integrate single-molecule and high-speed 4D imaging in developing Drosophila embryos to study the nuclear organization and interactions of the key patterning factors Zelda and Bicoid. In contrast to previous studies suggesting stable, cooperative binding, we show that both factors interact with DNA with surprisingly high off-rates. We find that both factors form dynamic subnuclear hubs, and that Bicoid binding is enriched within Zelda hubs. Remarkably, these hubs are both short lived and interact only transiently with sites of active Bicoid dependent transcription. Based on our observations we hypothesize that, beyond simply forming bridges between DNA and the transcription machinery, transcription factors can organize other proteins into hubs that transiently drive multiple activities at their gene targets.

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