Abstract
Morphological variability in cytoskeletal organization, organelle position and cell boundaries is a common feature of cultured cells. Remarkable uniformity and reproducibility in structure can be accomplished by providing cells with defined geometric cues. Cells in tissues can also self-organize in the absence of directing extracellular cues; however the mechanical principles for such self-organization are not understood. We report that unlike horizontal shapes, the vertical shapes of the cell and nucleus in the z-dimension are uniform in cells in cultured monolayers compared to isolated cells. Apical surfaces of cells and their nuclei in monolayers were flat and heights were uniform. In contrast, isolated cells, or cells with disrupted cell-cell adhesions had nuclei with curved apical surfaces and variable heights. Isolated cells cultured within micron-sized square wells displayed flat cell and nuclear shapes similar to cells in monolayers. Local disruption of nuclear-cytoskeletal linkages resulted in spatial variation in vertical uniformity. These results suggest that competition between cell-cell pulling forces that expand and shorten the vertical cell cross-section, thereby widening and flattening the nucleus, and the resistance of the nucleus to further flattening results in uniform cell and nuclear cross-sections. Our results reveal the mechanical principles of self-organized vertical uniformity in cell monolayers.
Highlights
Morphological variability in cytoskeletal organization, organelle position and cell boundaries is a common feature of cultured cells
We report that unlike horizontal shapes, the vertical shapes of the cell and nucleus in the z-dimension are uniform in cells in cultured monolayers compared to isolated cells
Our results reveal the mechanical principles of self-organized vertical uniformity in cell monolayers
Summary
Morphological variability in cytoskeletal organization, organelle position and cell boundaries is a common feature of cultured cells. Directed self-assembly of cytoskeletal structures has been demonstrated in vitro through the patterning of adhesive extracellular matrix proteins, and has helped understand the mechanisms by which uniformity of F-actin self-assembly may emerge inside cells[12]. Cell shape control by spatially varying mechanical cues can govern the process of angiogenesis[16] While such evidence shows that directed self-assembly of cytoskeletal structures due to local variations in extracellular cues can participate in the dynamic development of complex tissues, cells can self-assemble into uniform patterns and shapes in the absence of external cues. Despite the irregularity in cell shapes and nuclear shapes in the x-y plane, the heights of the apical surfaces of the cells and the nuclei were remarkably uniform in the z- dimension This uniformity depended on intact cell-cell adhesions and an intact LINC complex. We explain the results with a simple model of competition between cell-cell pulling forces and nuclear resistance to further flattening
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