Abstract
Nuclear migration is a general term for the movement of the nucleus towards a specific site in the cell. These movements are involved in a number of fundamental biological processes, such as fertilization, cell division, and embryonic development. Despite of its importance, the mechanism of nuclear migration is still poorly understood in mammalian cells. In order to shed light on the mechanical processes underlying nuclear movements, we adapted a micro-patterning based assay. C6 rat and U87 human glioma cells seeded on fibronectin patterns - thereby forced into a bipolar morphology - displayed oscillatory movements of the nucleus or the whole cell, respectively. We found that both the actomyosin system and microtubules are involved in the nuclear/cellular movements of both cell lines, but their contributions are cell-/migration-type specific. Dynein activity was necessary for nuclear migration of C6 cells but active myosin-II was dispensable. On the other hand, coupled nuclear and cellular movements of U87 cells were driven by actomyosin contraction. We explain these cell-line dependent effects by the intrinsic differences in the overall mechanical tension due to the various cytoskeletal elements inside the cell. Our observations showed that the movements of the nucleus and the centrosome are strongly correlated and display large variation, indicating a tight but flexible coupling between them. The data also indicate that the forces responsible for nuclear movements are not acting directly via the centrosome. Based on our observations, we propose a new model for nuclear oscillations in C6 cells in which dynein and microtubule dynamics are the main drivers of nuclear movements. This mechanism is similar to the meiotic nuclear oscillations of Schizosaccharomyces pombe and may be evolutionary conserved.
Highlights
The nucleus is an organelle of central importance in eukaryotic cells
In U87 cells, blebbistatin and cytochalasin D strongly reduced the speed of oscillating cells, and increased the period lengths, the amplitude of oscillations remained close to that of the control cells (Table S1). These results show that C6 and U87 cells are different in their oscillatory properties, as nuclear oscillations of C6 cells are slower, but have higher period lengths and half-peak amplitudes than the coupled nuclear and cellular oscillations of U87 cells (Table S1)
In accordance with previous data [43], perturbing microtubule dynamics interfered with nuclear movements in C6 cells
Summary
The nucleus is an organelle of central importance in eukaryotic cells. Establishment of a specific position of the nucleus within the cell contributes to key biological processes [1]. Nuclear movements have been described throughout eukaryotes, their actual functions show remarkable variations. The migration of the nucleus to the bud neck in Saccharomyces cerevisiae is required for the proper distribution of the genetic material to the daughter cell [2,3]. During Schizosaccharomyces pombe meiosis, the nucleus performs oscillatory movements [4], which facilitate the recombination of meiotic chromosomes [5]. Further observations in Caenorhabditis elegans [6] and Drosophila melanogaster [7,8] embryos have revealed the importance of nuclear migration processes in the development of metazoan organisms
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