Mark J. Koury, MD
Dr. Koury indicated no relevant conflicts of interest.
Dupire J, Socol M, Viallat A. Full dynamics of a red blood cell in shear flow. Proc Natl Acad Sci USA . 2012;109:20808-20813.
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The main function of erythrocytes, the transporting of gasses (oxygen, carbon dioxide, and nitric oxide) involved in tissue respiration, occurs in small vessels. Shear forces on erythrocytes vary as blood flows from small arterioles through capillaries into venous sinuses. Under conditions of low and moderate shear force experienced in small vessels, the rheologic properties of human erythrocytes are largely determined by specific changes in their shape and motion. Two basic motions of erythrocytes (Figure) have previously been described as tumbling or flipping when exposed to low shear rates, and tank-treading when the shear rate and/or the viscosity of the suspending medium are increased. The membrane of a tank-treading erythrocyte has fluidity and elasticity that allows its rotation around the hemoglobin-filled cytoplasm, while the biconcave shape is maintained at moderate shear rates, and a more ellipsoid shape is assumed with higher shear rates.1 When the shear force is removed, the formerly tank-treading erythrocyte membrane reorients itself to assume the same position relative to the rim and biconcave dimples that it had prior to the initiation of tank-treading (i.e., erythrocytes have shape memory).1
In their videomicroscopy study, Dupire et al. demonstrated that at low and moderate shear rates, erythrocytes maintain their biconcave shapes with only slight long-axis distortion. With low shear rates, an erythrocyte tumbles or flips. As the shear rate is increased, the tumbling erythrocyte can undergo a transition in its orientation so that it rolls like a wheel. This tumbling-to-rolling transition requires a limited amount of membrane elasticity, but after achieving the rolling orientation, the energy expended in cell shape maintenance is minimized compared with that expended in preserving cell shape during tumbling or that expended in the membrane rotation of tank-treading. At progressively higher shear rates, the rolling erythrocytes undergo a 90-degree orientation change to a Frisbee-like spinning motion that precedes a transition to tank-treading with fluctuations of the angle of orientation in the shear plane, a process termed swinging.2
Dupire and colleagues demonstrated specific transition states as an erythrocyte goes from rolling/spinning to tank-treading and also when it makes the opposite transition from tank-treading directly to tumbling. In the former transition, focal areas of the membrane appear to remain solid as the rest of the membrane has acquired the fluid movement of tank-treading. In the transition from tank-treading to tumbling caused by decreasing shear rate, the erythrocytes have short periods in which tank-treading is interrupted by one or two flips of the erythrocyte before there is complete loss of membrane fluidity and a return to a tumbling motion.
The fascinating studies of Dupire et al. demonstrate that transitions in cell shape and motion in response to changes in shear rate may help erythrocytes adapt to the vicissitudes of transit through the various components of the microvasculature, but future experiments will be needed to verify the roles of these rheologic changes in vivo. Characterization of the rheologic properties of normal erythrocytes enhances our understanding of the pathophysiology of diseases that involve abnormalities of the erythrocyte membrane, serum viscosities, and microvessels, including sickle cell anemia, malaria, polycythemia, macroglobulinemia, vasculitis, and diabetes.;
1. Fischer TM. Shape memory of human red blood cells. Biophys J. 2004;86:3304-3313.
2. Abkarian M, Faivre M, Viallat A. Swinging of red blood cells under shear flow. Phys Rev Lett. 2007;98:188302.
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