The effect of the red cell membrane and a diffusion boundary layer on the rate of oxygen uptake by human erythrocytes

Huxley, Virginia H.; Kutchai, Howard

doi:10.1113/jphysiol.1981.sp013773

Cited by 68 publications

(37 citation statements)

References 25 publications

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“…A similar effect is observed for the uptake of oxygen (5)(6)(7). This reduction in the scavenging rate allows NO that is produced in the endothelial cells within the walls of blood vessels to diffuse to the smooth muscle in sufficient concentrations to activate soluble guanylate cyclase (8 -12), which would not be possible otherwise (13).…”

Section: Hemoglobin (Hb)supporting

confidence: 62%

Mechanisms of Slower Nitric Oxide Uptake by Red Blood Cells and Other Hemoglobin-containing Vesicles

Azarov

Liu

Reynolds

et al. 2011

Journal of Biological Chemistry

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Nitric oxide (NO) acts as a smooth muscle relaxation factor and plays a crucial role in maintaining vascular homeostasis. NO is scavenged rapidly by hemoglobin (Hb). However, under normal physiological conditions, the encapsulation of Hb inside red blood cells (RBCs) significantly retards NO scavenging, permitting NO to reach the smooth muscle. The rate-limiting factors (diffusion of NO to the RBC surface, through the RBC membrane or inside of the RBC) responsible for this retardation have been the subject of much debate. Knowing the relative contribution of each of these factors is important for several reasons including optimization of the development of blood substitutes where Hb is contained within phospholipid vesicles. We have thus performed experiments of NO uptake by erythrocytes and microparticles derived from erythrocytes and conducted simulations of these data as well as that of others. We have included extracellular diffusion (that is, diffusion of the NO to the membrane) and membrane permeability, in addition to intracellular diffusion of NO, in our computational models. We find that all these mechanisms may modulate NO uptake by membrane-encapsulated Hb and that extracellular diffusion is the main ratelimiting factor for phospholipid vesicles and erythrocytes. In the case of red cell microparticles, we find a major role for membrane permeability. These results are consistent with prior studies indicating that extracellular diffusion of several gas ligands is also rate-limiting for erythrocytes, with some contribution of a low membrane permeability. Hemoglobin (Hb)2 encapsulated within red blood cells scavenges NO at a significantly slower rate than hemoglobin that is freely dissolved within blood plasma (cell-free Hb) (1-4). A similar effect is observed for the uptake of oxygen (5-7). This reduction in the scavenging rate allows NO that is produced in the endothelial cells within the walls of blood vessels to diffuse to the smooth muscle in sufficient concentrations to activate soluble guanylate cyclase (8 -12), which would not be possible otherwise (13). NO thus effectively functions as a smooth muscle relaxant under normal physiological conditions. The reasons for the reduction of the rate of NO scavenging by red cell-encapsulated versus cell-free Hb have been extensively investigated and yet this remains a debated subject. The difference in the scavenging rates has been attributed to four possible factors: 1) a red blood cell (RBC)-free zone adjacent to the endothelium due to the velocity gradient in laminar flow (2-4), 2) NO uptake being rate-limited by diffusion of NO to the RBC, which contributes to the phenomenon of an unstirred layer around the RBC (1, 6, 14 -16), 3) an intrinsic, physical RBC membrane barrier to NO diffusion (14,(17)(18)(19)(20), and 4) NO uptake being rate-limited by diffusion of NO within the RBC (intracellular diffusion) (17, 21). Although there is no disagreement about the effect of the RBC-free zone along the endothelium on reducing NO reaction rates with red cell hem...

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Section: Hemoglobin (Hb)supporting

confidence: 62%

Mechanisms of Slower Nitric Oxide Uptake by Red Blood Cells and Other Hemoglobin-containing Vesicles

Azarov

Liu

Reynolds

et al. 2011

Journal of Biological Chemistry

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“…Thus, assuming that BSA does not influence the value of X, but am is decreased with increasing BSA, the relation between S and BSA concentration was evaluated by taking ks/as = k/a. The influence of added protein on the oxygenation rate has hitherto been ascribed to the reduction of convection or diffusibility across a stagnant boundary layer surrounding the RBC [2, 8,26,33]. However, in the present study, the influence of added protein on j is ascribed to the change in S, but not to the change in convection.…”

Section: Evaluation Of the K And S Values For 02 Co And Co2contrasting

confidence: 51%

“…Initially, the slowness of the oxygenation rate was ascribed to the resistance across the RBC membrane [22,27,28]. In subsequent studies [2, 8,13,14,26,33], the main cause of retardation was, however,-ascribed to the reduction in diffusibility across the stagnant boundary layer around the RBC. The solubility of C02 is about 20 times higher than that of 02, whereas the diffusion coefficient of C02 [6] is estimated to be 75°c that of 02 [5].…”

mentioning

confidence: 99%

Relationship between the transfer rate and the gap in partial pressure of gas molecules at a heterogeneous interface.

Mochizuki¹

1988

Jpn.J.Physiol

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The partial pressure of a gas corresponds to the kinetic energy per unit volume. At equilibrium, the kinetic energy in the gas phase, or the partial pressure of the gas, must be equal to that in the liquid phase. On the other hand, the number of gas molecules dissolved in a unit volume of solution is usually smaller than the number of molecules in the same volume of gas. Consequently, the kinetic energy of a gas molecule in solution must be higher than that in the gas phase. Thus, in order for the gas molecule to cross a heterogeneous interface, it must undergo a rise of fall in kinetic energy. To counter the change in energy transfer rate across the interface, a gap in partial pressure appears essential.We [18] introduced a term, transfer coefficient, to evaluate the relationship between the magnitude of the gap in partial pressure and the transfer rate across the red blood cell (RBC) membrane. The transfer coefficient (ii) was obtained by dividing the diffusion flux by the size of the gap in partial pressure. Thus, the dimensions are similar to those of permeability. However, , is concerned with the discontinuity in partial pressure at heterogeneous interface caused by the difference in kinetic energy, while permeability is related to the diffusibility within a thin layer such as is found in artificial and some biological membranes. UCHIDA et al. [31] measured the C02 diffusion rate in a thin layer of hemoglobin solution, and found that the inward and outward diffusions were equally retarded at the gas-liquid interface. NIIZEKI et al. [23,24] measured the C02 diffusion rate in the RBC under lowered convective conditions and found that the value of tj for C02, being 2.5 x 10-6 cm • s-1 • Torr-1, was identical to that for 02 [9,10,16].Oxygenation and deoxygenation reactions of hemoglobin are very fast [20] and hydration and dehydration reactions of C02 are also highly accelerated by carbonic anhydrase in RBC [23]. Thus, the rates of 02 and C02 reactions with RBC are limited by the transfer rates of these gases and HC03 -ion across the RBC interface as well as by the intracellular diffusion rate. Therefore, estimation of the i values of the RBC and alveolar membranes is a key problem for the kinetic studies in the

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“…In the acute brain slice preparation oxygen has to diffuse into the tissue due to the absence of active transport. The balance between the diffusion flow of oxygen into the tissue and amount of oxygen consumed by cells is required to keep a steady state conditions [14,15].…”

Section: Discussionmentioning

confidence: 99%

Modulation of 4-aminopyridine-induced neuronal activity and local pO2 in rat hippocampal slices by changing the flow rate of the superfusion medium

Sydorenko¹,

Комаров²,

Sushko³

et al. 2016

Fiziol Zh

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The effect of the red cell membrane and a diffusion boundary layer on the rate of oxygen uptake by human erythrocytes

Cited by 68 publications

References 25 publications

Mechanisms of Slower Nitric Oxide Uptake by Red Blood Cells and Other Hemoglobin-containing Vesicles

Mechanisms of Slower Nitric Oxide Uptake by Red Blood Cells and Other Hemoglobin-containing Vesicles

Relationship between the transfer rate and the gap in partial pressure of gas molecules at a heterogeneous interface.

Modulation of 4-aminopyridine-induced neuronal activity and local pO2 in rat hippocampal slices by changing the flow rate of the superfusion medium

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