Decoding Information in Cell Shape

Rangamani, Padmini; Lipshtat, Azi; Azeloglu, Evren U.; Calizo, Rhodora C.; Hu, Mufeng; Ghassemi, Saba; Hone, James; Scarlata, Suzanne; Neves, Susana R.; Iyengar, Ravi

doi:10.1016/j.cell.2013.08.026

Cited by 175 publications

(206 citation statements)

References 57 publications

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“…Despite the source of the expansion-promoting hormone and downstream gene expression being principally present within the radicle tip, the displacement of the primary site of expansion is predetermined by the developmentally defined cellular geometries of the mature embryo. Although the shapes of individual cells can encode information mediating local subcellular signaling (33), the morphogenetic future of the organ may be imprinted through the collective cell shapes and arrangements defined during its development. …”

Section: Resultsmentioning

confidence: 99%

Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo

Bassel

Stamm

Mosca

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

178

202

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Morphogenesis occurs in 3D space over time and is guided by coordinated gene expression programs. Here we use postembryonic development in Arabidopsis plants to investigate the genetic control of growth. We demonstrate that gene expression driving the production of the growth-stimulating hormone gibberellic acid and downstream growth factors is first induced within the radicle tip of the embryo. The center of cell expansion is, however, spatially displaced from the center of gene expression. Because the rapidly growing cells have very different geometry from that of those at the tip, we hypothesized that mechanical factors may contribute to this growth displacement. To this end we developed 3D finiteelement method models of growing custom-designed digital embryos at cellular resolution. We used this framework to conceptualize how cell size, shape, and topology influence tissue growth and to explore the interplay of geometrical and genetic inputs into growth distribution. Our simulations showed that mechanical constraints are sufficient to explain the disconnect between the experimentally observed spatiotemporal patterns of gene expression and early postembryonic growth. The center of cell expansion is the position where genetic and mechanical facilitators of growth converge. We have thus uncovered a mechanism whereby 3D cellular geometry helps direct where genetically specified growth takes place.computational modeling | quantification | biomechanics | plant development | seed germination C entral to developmental biology is the question of how gene expression leads to morphogenesis and the creation of form (1, 2). However, there are few studies that link genes directly with shape change in a mechanistic way (3-5). In plants, where cells do not move, nearly all shape change and morphogenesis occur through the tightly regulated control over the mechanical properties of the cell wall. Mathematical models of plant cell growth are based on the turgor-driven Lockhart model and its derivatives (6, 7) that link the rate of cell wall expansion to the stress experienced by the wall. This model fits well with the biochemistry of the cell wall, which is composed of a strong cellulose microfibril network embedded in a pectin matrix with cross-links of hemicellulose, structural proteins, and other polysaccharides (8). Stress on the cell wall from turgor pressure causes elastic expansion, which becomes plastic as remodeling enzymes rearrange the network and incorporate new material (8). Thus, the physical manifestation of growth, cell expansion, results from a balance between genetically controlled enzymatic activity and the mechanical forces experienced by the cell wall.A common simplifying assumption is that gene expression associated with cell wall modification directly specifies the rate of growth of cells. This assumption is, however, limited as growthpromoting gene expression rarely correlates well with gradients of active cell expansion (9, 10). This suggests that gene expression patterns alone are not sufficient to pr...

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Section: Resultsmentioning

confidence: 99%

Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo

Bassel

Stamm

Mosca

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

178

202

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“…4 Recent results by Rangamani et al suggest that changes in cell shape induce local gradients of receptors or signaling molecules which amplify signals during differentiation. 15 Nuclear shape may play a similar signaling role in transcription and other cellular processes. To confirm and understand such phenomena, the first step is studying how nuclear morphology changes over time.…”

Section: Introductionmentioning

confidence: 99%

Periodicity of nuclear morphology in human fibroblasts

Seaman

Meixner

Snyder

et al. 2015

Nucleus

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Motivation: Morphology of the cell nucleus has been used as a key indicator of disease state and prognosis, but typically without quantitative rigor. It is also not well understood how nuclear morphology varies with time across different genetic backgrounds in healthy cells. To help answer these questions we measured the size and shape of nuclei in cellcycle-synchronized primary human fibroblasts from 6 different individuals at 32 time points over a 75 hour period.Results: The nucleus was modeled as an ellipsoid and its dynamics analyzed. Shape and volume changed significantly over this time. Two prominent frequencies were found in the 6 individuals: a 17 hour period consistent with the cell cycle and a 26 hour period. Our findings suggest that the shape of the nucleus changes over time and thus any time-invariant shape property may provide a misleading characterization of cellular populations at different phases of the cell cycle. The proposed methodology provides a general method to analyze morphological change using multiple time points even for non-live-cell experiments.

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“…It is possible that endgrowing bacteria have evolved to take advantage of this fact. This possibility is also hinted at by observations showing that elongated cells often distribute membrane receptors accordingly, with higher densities near their tips [28]. Next I note that, from an energy consumption perspective, cell division provides no benefit in a homogeneous, flowing nutrient ensemble.…”

Section: Discussionmentioning

confidence: 91%

Shape-dependent bounds on cell growth rates

Landy¹

2014

EPL

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I consider how cell shape and environmental geometry affect the rate of nutrient capture and the consequent maximum growth rate of a cell, focusing on rod-like species like E. coli. Simple modeling immediately implies that it is the elongated profiles of such cells that allows for them to grow -as observed -at exponential rates in nutrient-rich media. Growth is strongly suppressed when nutrient capture is diffusion-limited: In three dimensions, the length is bounded by log L t 1/2 , and in lower dimensions growth is algebraic. Similar bounds are easily obtained for other cell geometries, groups of cells, etc. Fits of experimental growth curves to such bounds can be used to estimate various quantities of interest, including generalized metabolic rates.

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Decoding Information in Cell Shape

Cited by 175 publications

References 57 publications

Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo

Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo

Periodicity of nuclear morphology in human fibroblasts

Shape-dependent bounds on cell growth rates

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