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J. Biol. Chem., Vol. 277, Issue 29, 26194-26199, July 19, 2002
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From the The process of NO transfer into erythrocytes
(RBCs) is of critical biological importance because it regulates the
bioavailability and diffusional distance of endothelial-derived NO. It
has been reported that the rate of NO reaction with oxyhemoglobin (Hb) within RBCs is nearly three orders of magnitude slower than that by
equal amounts of free oxyhemoglobin. Consistent with early studies on
oxygen uptake by RBCs, the process of extracellular diffusion was
reported to explain this much lower NO uptake by RBC encapsulated Hb
(Liu, X., Miller, M. J., Joshi, M. S., Sadowska-Krowicka, H., Clark,
D. A., and Lancaster, J. R., Jr. (1998) J. Biol.
Chem. 273, 18709-18713). However, it was subsequently proposed
that the RBC membrane provides the main resistance to NO uptake rather than the process of extracellular diffusion (Vaughn, M. W., Huang, K. T., Kuo, L., and Liao, J. C. (2000) J. Biol.
Chem. 275, 2342-2348). This conclusion was based on competition
experiments that were assumed to be able to determine the rate constant
of NO uptake by RBCs without extracelluar diffusion limitation. To test
the validity of this hypothesis, we theoretically analyzed competition experiments. Here, we show that competition experiments do not eliminate the extracellular diffusion limitation. Simulation of the
competition data indicates that the main resistance to NO uptake by
RBCs is caused by extracellular diffusion in the unstirred layer
surrounding each RBC but not by the RBC membrane. This
extracellular diffusion resistance is responsible for preventing
interference of NO signaling in the endothelium without the need for
special NO uptake by intracellular hemoglobin or a unique membrane
resistance mechanism.
Nitric Oxide Uptake by Erythrocytes Is Primarily Limited by
Extracellular Diffusion Not Membrane Resistance*
§,,
Molecular and Cellular Biophysics
Laboratories, Department of Medicine, Division of Cardiology and the
Electron Paramagnetic Resonance Center, The Johns Hopkins University
School of Medicine, Baltimore, Maryland 21224 and the
¶ Departments of Physiology and Medicine, Louisiana State
University Health Sciences Center, New Orleans, Louisiana 70112
*
This work was supported by an American Heart Association
Scientist Development Grant (to X. L.) and National Institutes of Health Grants HL38324, HL63744, and HL65608 (to J. L. Z.) and DK46935
(to J. R. L.).The costs of publication of this
article were defrayed in part by the
payment of page charges. The article must therefore be hereby marked
"advertisement" in
accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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