Abstract
Neural precursor cells differentiate into several cell types that display distinct functions. However, little is known about how cell surface mechanics vary during the differentiation process. Here, by precisely measuring membrane tension and bending modulus, we map their variations and correlate them with changes in neural precursor cell morphology along their distinct differentiation fates. Both cells maintained in culture as neural precursors as well as those plated in neurobasal medium reveal a decrease in membrane tension over the first hours of culture followed by stabilization, with no change in bending modulus. During astrocyte differentiation, membrane tension initially decreases and then increases after 72 h, accompanied by consolidation of glial fibrillary acidic protein expression and striking actin reorganization, while bending modulus increases following observed alterations. For oligodendrocytes, the changes in membrane tension are less abrupt over the first hours, but their values subsequently decrease, correlating with a shift from oligodendrocyte marker O4 to myelin basic protein expressions and a remarkable actin reorganization, while bending modulus remains constant. Oligodendrocytes at later differentiation stages show membrane vesicles with similar membrane tension but higher bending modulus as compared to the cell surface. Altogether, our results display an entire spectrum of how membrane elastic properties are varying, thus contributing to a better understanding of neural differentiation from a mechanobiological perspective.
Highlights
The surface of all mammalian cells is composed of the plasma membrane cushioned underneath by a cortical actomyosin cytoskeleton
Aiming to characterize the cell membrane” (CM) elastic properties of NPCs over the course of their distinct differentiation fates, and to compare the results with those found for cells maintained with stem capacity, either as neurospheres or as isolated NPCs, optical tweezers (OT)-based tether extraction experiments were performed for each cell type over periods of 2–240 h in culture
The results show that these variations are correlated with striking morphological phenotype changes that occur with NPCs
Summary
The surface of all mammalian cells is composed of the plasma membrane cushioned underneath by a cortical actomyosin cytoskeleton. Membrane tether pulling assays using optical tweezers (OT) [6,7] or atomic force microscopy (AFM) [8,9] have been used to extract nanotubes or tethers from CMs in order to determine these properties By measuring both the equilibrium force and tether radius, the cell membrane surface tension (CMT - σe f f ) and cell membrane bending modulus (CMBM - κe f f ) have been determined for different cell types [7,10,11,12,13,14,15]. CMT and CMBM result from joint contributions of cytoskeleton architecture, membrane composition and membrane-cytoskeleton attachment [14] These elastic properties ( CMT), as well as their changes, have been characterized as important regulators of cellular behaviors, especially regarding shape changes and force production [14,16]. It has been shown [13] that membrane elastic properties are correlated to cell function
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