Single cell spreading and deconstruction at liquid crystal interfaces

Biological cells are often damaged by interactions with fluid interfaces, yet the cell-scale processes that underlie their destruction have not been fully elucidated. Here we investigate whether interactions of cells at aqueous interfaces of thermotropic liquid crystals (LCs) drive changes in LC ordering, thereby generating spatiotemporal optical signatures that yield insights into the pathways by which single cells are damaged at fluid interfaces and how molecular adsorbates influence those pathways. MCF10A breast epithelial cells were sedimented onto micrometer-thick films of nematic LCs and imaged using optical microscopy. We found that the cells exhibited a lag phase on the interface (lasting seconds to an hour during which no optical response of the LC was evident) that was followed by rapid lateral displacement of the cells and the generation of complex spatiotemporal patterns in the LC. Fingering instabilities evident in the patterned optical response revealed deconstruction of cells and redistribution of cellular components driven by interfacial tension gradients. Pretreatment of the LC interface with amphiphilic adsorbates altered spreading dynamics and domain shapes, suggesting a role for Marangoni stresses in the disassembly pathway and revealing angular spatial patterns consistent with a crossover to capillary fracturing driven by interfacial elasticity. Fluorescence imaging along with control experiments with synthetic vesicles and red blood cells enabled spatiotemporal features of the LC response to epithelial cells to be associated with specific intracellular structures (nucleus, plasma membrane, and cytosol). The duration of the lag phase was also found to be influenced by cell-surface expression levels of the mucin MUC1. Overall, our findings reveal key physical processes that occur when cells interact with fluid interfaces and highlight the potential of LC interfaces to form the basis of single cell-level analyses of biophysical properties.