Mechanics of neutrophil phagocytosis: behavior of the cortical tension

Abstract

The mechanical implementation of phagocytosis requires a well-coordinated deployment of cytoplasm and membrane during the creation of a phagosome. We follow the time course of this process in initially round passive neutrophils presented with antibody-coated beads of radii 1.1 to 5.5 μm. In particular, we monitor the cortical tension as the apparent cellular surface area increases due to cell-driven deformations induced by phagocytosis. The behavior of the tension is then compared with conditions of similar area expansion caused by externally imposed deformations during cell aspiration into a micropipette. Whereas the resting tension remains low for an area expansion of up to only 30% during aspiration, it remains low even after an area expansion of up to 80% in phagocytosis. This is probably the result of membrane insertion from inner stores by exocytosis. We further find that the onset of viscous tension, proportional to the rate of area expansion and caused by the unfurling of plasma membrane wrinkles, is significantly delayed in phagocytosis compared with aspiration. We propose that this is the result of phagocytosis-triggered enzymatic activity that releases spare plasma membrane normally sequestered by velcro-like bonds in a reservoir of surface folds and villi.

Ca2+ and calpain control membrane expansion during rapid cell spreading of neutrophils

“…The membrane expansion accompanying this cell shape change occurred without the insertion of new membrane, and thus probably results from unfurling of wrinkled plasma membrane Hallett and Dewitt, 2007). This is also suggested from biophysical measurement (Herant et al, 2005) and the manipulation of neutrophil membrane tension (Houk et al, 2012). The cell spreading and membrane expansion depended on activation of the Ca 2+ -activated protease, calpain.…”

Frustrated Phagocytic Spreading of J774A-1 Macrophages Ends in Myosin II-Dependent Contraction

“…Above a minimum threshold, the steady-state (elastic) tension increases roughly linearly with the apparent surface area. The threshold is (A À A 0 )/ A 0 ¼ 0.12 for passive J77A.1 macrophages and 0.26 for neutrophils (17,19). Below the threshold, tension remains low and relatively constant (17).…”

“…Moreover, membrane tension has been shown to play a role in phagocytosis-related signaling (20,21). In an extensive effort to mechanically characterize and model phagocytosis, Herant and co-workers (19) argued that membrane cortical tension (which includes both the plasma membrane tension and the tension within the cytoskeletal cortex) can be thought of as being the sum of two components: an elastic component g el , which represents the steady-state elastic buildup of tension within the membrane and cortex, and a viscous component g vis , which accounts for the phagocytes' ability to relieve tension through the unfurling of membrane microfolds and exocytosis. As phagocytosis progresses, the cell's apparent surface area increases, causing elastic tension to rise.…”

“…Below the threshold, tension remains low and relatively constant (17). For cells undergoing phagocytosis, the threshold is higher, rising to 0.80 for neutrophils and 1.5 (250%) for J774A.1 (18,19). During traditional phagocytosis, J774A.1 cells have been reported to increase their apparent surface area by up to 500-600% before they are no longer able to take up more/larger particles (17).…”

A physical model for the size-dependent cellular uptake of nanoparticles modified with cationic surfactants

“…In this equation, γ 0 is the baseline surface tension when the cell is spherical, k el is the elastic expansion modulus, and A 0 is the surface area before the cell deformation. 29 If w ad denotes the adhesion strength induced by driven forces (eg, the electrostatic interaction), and A ad denotes the contact area, the adhesion energy can be expressed as:…”