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Three-dimensional geometry controls division symmetry in stem cell colonies.

ABSTRACT: Proper control of division orientation and symmetry, largely determined by spindle positioning, is essential to development and homeostasis. Spindle positioning has been extensively studied in cells dividing in two-dimensional (2D) environments and in epithelial tissues, where proteins such as NuMA (also known as NUMA1) orient division along the interphase long axis of the cell. However, little is known about how cells control spindle positioning in three-dimensional (3D) environments, such as early mammalian embryos and a variety of adult tissues. Here, we use mouse embryonic stem cells (ESCs), which grow in 3D colonies, as a model to investigate division in 3D. We observe that, at the periphery of 3D colonies, ESCs display high spindle mobility and divide asymmetrically. Our data suggest that enhanced spindle movements are due to unequal distribution of the cell-cell junction protein E-cadherin between future daughter cells. Interestingly, when cells progress towards differentiation, division becomes more symmetric, with more elongated shapes in metaphase and enhanced cortical NuMA recruitment in anaphase. Altogether, this study suggests that in 3D contexts, the geometry of the cell and its contacts with neighbors control division orientation and symmetry. This article has an associated First Person interview with the first author of the paper.

SUBMITTER: Chaigne A

PROVIDER: S-EPMC8349555 | biostudies-literature | 2021 Jul

REPOSITORIES: biostudies-literature

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Three-dimensional geometry controls division symmetry in stem cell colonies.

Chaigne Agathe A Smith Matthew B MB Lopez Cavestany Rocio R Hannezo Edouard E Chalut Kevin J KJ Paluch Ewa K EK

Journal of cell science 20210729 14

Proper control of division orientation and symmetry, largely determined by spindle positioning, is essential to development and homeostasis. Spindle positioning has been extensively studied in cells dividing in two-dimensional (2D) environments and in epithelial tissues, where proteins such as NuMA (also known as NUMA1) orient division along the interphase long axis of the cell. However, little is known about how cells control spindle positioning in three-dimensional (3D) environments, such as e ...[more]

PMID: 34323278

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Project description:Cardiac tissue engineering has been working to alleviate the immense burden of cardiovascular disease for several decades. To improve cardiac tissue homogeneity and cardiomyocyte (CM) maturation, in this study, we investigated altering initial encapsulation geometry in a three-dimensional (3D) direct cardiac differentiation platform. Traditional engineered cardiac tissue production utilizes predifferentiated CMs to produce 3D cardiac tissue and often involves various cell selection and exogenous stimulation methods to promote CM maturation. Starting tissue formation directly with human induced pluripotent stem cells (hiPSCs), rather than predifferentiated CMs, simplifies the engineered cardiac tissue formation process, making it more applicable for widespread implementation and scale-up. In this study, hiPSCs were encapsulated in poly (ethylene glycol)-fibrinogen in three tissue geometries (disc-shaped microislands, squares, and rectangles) and subjected to established cardiac differentiation protocols. Resulting 3D engineered cardiac tissues (3D-ECTs) from each geometry displayed similar CM populations (∼65%) and gene expression over time. Notably, rectangular tissues displayed less tissue heterogeneity and suggested more advanced features of maturing CMs, including myofibrillar alignment and Z-line formation. In addition, rectangular tissue showed significantly higher anisotropic contractile properties compared to square and microisland tissues (MI 0.28 ± 0.03, SQ 0.35 ± 0.05, RT 0.79 ± 0.04). This study demonstrates a straightforward method for simplifying and improving 3D-ECT production without the use of exogenous mechanical or electrical pacing and has the potential to be utilized in bioprinting and drug testing applications. Impact statement Current methods for improving cardiac maturation postdifferentiation remain tedious and complex. In this study, we examined the impact of initial encapsulation geometry on improvement of three-dimensional engineered cardiac tissue (3D-ECT) production and postdifferentiation maturation for three tissue geometries, including disc-shaped microislands, squares, and rectangles. Notably, rectangular 3D-ECTs displayed less tissue heterogeneity and more advanced features of maturing cardiomyocytes, including myofibrillar alignment, Z-line formation, and anisotropic contractile properties, compared to microisland and square tissues. This study demonstrates an initial human induced pluripotent stem cell-encapsulated rectangular tissue geometry can improve cardiac maturation, rather than implementing cell selection or tedious postdifferentiation manipulation, including exogenous mechanical and/or electrical pacing.

Project description:Judging the poses, sizes, and shapes of objects accurately is necessary for organisms and machines to operate successfully in the world. Retinal images of three-dimensional objects are mapped by the rules of projective geometry and preserve the invariants of that geometry. Since Plato, it has been debated whether geometry is innate to the human brain, and Poincare and Einstein thought it worth examining whether formal geometry arises from experience with the world. We examine if humans have learned to exploit projective geometry to estimate sizes and aspects of three-dimensional shape that are related to relative lengths and aspect ratios. Numerous studies have examined size invariance as a function of physical distance, which changes scale on the retina. However, it is surprising that possible constancy or inconstancy of relative size seems not to have been investigated for object pose, which changes retinal image size differently along different axes. We show systematic underestimation of length for extents pointing toward or away from the observer, both for static objects and dynamically rotating objects. Observers do correct for projected shortening according to the optimal back-transform, obtained by inverting the projection function, but the correction is inadequate by a multiplicative factor. The clue is provided by the greater underestimation for longer objects, and the observation that they seem to be more slanted toward the observer. Adding a multiplicative factor for perceived slant in the back-transform model provides good fits to the corrections used by observers. We quantify the slant illusion with two different slant matching measurements, and use a dynamic demonstration to show that the slant illusion perceptually dominates length nonrigidity. In biological and mechanical objects, distortions of shape are manifold, and changes in aspect ratio and relative limb sizes are functionally important. Our model shows that observers try to retain invariance of these aspects of shape to three-dimensional rotation by correcting retinal image distortions due to perspective projection, but the corrections can fall short. We discuss how these results imply that humans have internalized particular aspects of projective geometry through evolution or learning, and if humans assume that images are preserving the continuity, collinearity, and convergence invariances of projective geometry, that would simply explain why illusions such as Ames' chair appear cohesive despite being a projection of disjointed elements, and thus supplement the generic viewpoint assumption.

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Three-dimensional geometry controls division symmetry in stem cell colonies.

Publications

Three-dimensional geometry controls division symmetry in stem cell colonies.

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