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1.
Nat Phys ; 19(12): 1927-1935, 2023 Dec.
Article in English | MEDLINE | ID: mdl-38831923

ABSTRACT

The cell nucleus is enveloped by a complex membrane, whose wrinkling has been implicated in disease and cellular aging. The biophysical dynamics and spectral evolution of nuclear wrinkling during multicellular development remain poorly understood due to a lack of direct quantitative measurements. Here, we characterize the onset and dynamics of nuclear wrinkling during egg development in the fruit fly when nurse cell nuclei increase in size and display stereotypical wrinkling behavior. A spectral analysis of three-dimensional high-resolution live imaging data from several hundred nuclei reveals a robust asymptotic power-law scaling of angular fluctuations consistent with renormalization and scaling predictions from a nonlinear elastic shell model. We further demonstrate that nuclear wrinkling can be reversed through osmotic shock and suppressed by microtubule disruption, providing tuneable physical and biological control parameters for probing mechanical properties of the nuclear envelope. Our findings advance the biophysical understanding of nuclear membrane fluctuations during early multicellular development.

2.
Nat Phys ; 17(12): 1391-1395, 2021 Dec.
Article in English | MEDLINE | ID: mdl-35242199

ABSTRACT

Clonal dominance arises when the descendants (clones) of one or a few founder cells contribute disproportionally to the final structure during collective growth [1-8]. In contexts such as bacterial growth, tumorigenesis, and stem cell reprogramming [2-4], this phenomenon is often attributed to pre-existing propensities for dominance, while in stem cell homeostasis, neutral drift dynamics are invoked [5,6]. The mechanistic origin of clonal dominance during development, where it is increasingly documented [1,6-8], is less understood. Here, we investigate this phenomenon in the Drosophila melanogaster follicle epithelium, a system in which the joint growth dynamics of cell lineage trees can be reconstructed. We demonstrate that clonal dominance can emerge spontaneously, in the absence of pre-existing biases, as a collective property of evolving excitable networks through coupling of divisions among connected cells. Similar mechanisms have been identified in forest fires and evolving opinion networks [9-11]; we show that the spatial coupling of excitable units explains a critical feature of the development of the organism, with implications for tissue organization and dynamics [1,12,13].

3.
Nat Phys ; 14(10): 1016-1021, 2018 Oct.
Article in English | MEDLINE | ID: mdl-30881478

ABSTRACT

Optimal packings [1, 2] of unconnected objects have been studied for centuries [3-6], but the packing principles of linked objects, such as topologically complex polymers [7, 8] or cell lineages [9, 10], are yet to be fully explored. Here, we identify and investigate a generic class of geometrically frustrated tree packing problems, arising during the initial stages of animal development when interconnected cells assemble within a convex enclosure [10]. Using a combination of 3D imaging, computational image analysis, and mathematical modelling, we study the tree packing problem in Drosophila egg chambers, where 16 germline cells are linked by cytoplasmic bridges to form a branched tree. Our imaging data reveal non-uniformly distributed tree packings, in agreement with predictions from energy-based computations. This departure from uniformity is entropic and affects cell organization during the first stages of the animal's development. Considering mathematical models of increasing complexity, we investigate spherically confined tree packing problems on convex polyhedrons [11] that generalize Platonic and Archimedean solids. Our experimental and theoretical results provide a basis for understanding the principles that govern positional ordering in linked multicellular structures, with implications for tissue organization and dynamics [12, 13].

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