Adaptable interaction between aquaporin‐1 and band 3 reveals a potential role of water channel in blood CO₂transport

Abstract

Human CO respiration requires rapid conversion between CO and HCO Carbonic anhydrase II facilitates this reversible reaction inside red blood cells, and band 3 [anion exchanger 1 (AE1)] provides a passage for HCO flux across the cell membrane. These 2 proteins are core components of the CO transport metabolon. Intracellular HO is necessary for CO/HCO conversion. However, abundantly expressed aquaporin 1 (AQP1) in erythrocytes is thought not to be part of band 3 complexes or the CO transport metabolon. To solve this conundrum, we used Förster resonance energy transfer (FRET) measured by fluorescence lifetime imaging (FLIM-FRET) and identified interaction between aquaporin-1 and band 3 at a distance of 8 nm, within the range of dipole-dipole interaction. Notably, their interaction was adaptable to membrane tonicity changes. This suggests that the function of AQP1 in tonicity response could be coupled or correlated to its function in band 3-mediated CO/HCO exchange. By demonstrating AQP1 as a mobile component of the CO transport metabolon, our results uncover a potential role of water channel in blood CO transport and respiration.-Hsu, K., Lee, T.-Y., Periasamy, A., Kao, F.-J., Li, L.-T., Lin, C.-Y., Lin, H.-J., Lin, M. Adaptable interaction between aquaporin-1 and band 3 reveals a potential role of water channel in blood CO transport.

Natural Antioxidants Beneficial Effects on Anion Exchange through Band 3 Protein in Human Erythrocytes

“…Importantly, interaction between B3p and AQP1 was adaptable to changes in membrane tonicity, which suggests that AQP1 involvement in response to tonicity could be associated with its function in B3p-mediated exchange. For this reason, AQP1 seems to be critically implicated in blood CO 2 transport and, in turn, respiration [16]. Their primary function is to allow tissue oxygenation and CO 2 elimination, but erythrocytes, flowing in the blood stream, make tissue oxygenation effective due to their biconcave shape, which corresponds to a greater area available for gas exchange and, notably, lets them adapt to the narrow capillaries.…”

Proposed Dynamics of CDB3 Activation in Human Erythrocytes by Nifedipine Studied with Scanning Flow Cytometry

“…The estimated rate of HCO 3 − /Cl − exchange by erythrocytes of blood passed through the human lung corresponds to the rate of oxygen consumption of a human body . The importance of this theme is supported by known publications . For example, it was reported that in the case of hypoxia the amount of active CDB3 per erythrocyte of asphyxiated neonates was decreased in comparison with healthy newborns.…”

“…Most (> 90%) of the carbon dioxide inside and outside erythrocytes in blood is converted to anions HCO 3 − (the enzyme carbonic anhydrase accelerates this reaction) ( (55). The importance of this theme is supported by known publications (8,(56)(57)(58)(59)(60)(61). For example, it was reported (57) that in the case of hypoxia the amount of active CDB3 per erythrocyte of asphyxiated neonates was decreased in comparison with healthy newborns.…”

Exploring the Potential Roles of Band 3 and Aquaporin-1 in Blood CO2 Transport–Inspired by Comparative Studies of Glycophorin B-A-B Hybrid Protein GP.Mur

“…Though their interaction is more obvious in GP.Mur RBCs, AQP1-band 3 interaction also exists in RBCs lacking GP.Mur. Importantly, this AQP1-band 3 interaction could be dissipated by hypotonic conditioning (e.g., by diluting the physiological buffer HBSS with water to ∼250 mOsm/Kg) ( Hsu et al, 2017 ). This osmotically sensitive interaction between AQP1 and band 3 conceivably allows erythrocytes to sense and respond to hemodynamic shear stress, as well as changes of erythrocyte volume and shape during circulation.…”

“…Conceivably, membrane-bound, mobile AQP1 and cytosolic CAII may preferentially interact with one or more types of the band 3 complexes, resulting in structurally and functionally differentiable complexes on the erythrocyte membrane. Very likely the population of cytoskeleton-independent band 3 preferentially interacts with AQP1, as the protein-protein interaction between AQP1 and band 3 was measured by FLIM-FRET using inside-out vesicles (IOVs) from erythrocyte membrane that were depleted of much spectrin cytoskeleton and non-integral membrane-bound proteins ( Hsu et al, 2017 ). Additionally, as AQP1-band 3 interaction is adaptable to osmotic changes ( Hsu et al, 2017 ), it is possible that the interaction between CAII and band 3 could also be transitory and sensitive to osmotic or hemodynamic shear stresses ( Lazaro et al, 2014 ).…”