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Am J Physiol Regul Integr Comp Physiol. 2018 Aug 1;315(2):R397-R407. doi: 10.1152/ajpregu.00062.2018. Epub 2018 Apr 11.

Time course of red blood cell intracellular pH recovery following short-circuiting in relation to venous transit times in rainbow trout, Oncorhynchus mykiss.

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Department of Zoology, University of British Columbia , Vancouver, BC , Canada.
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania.
Department of Chemical and Petroleum Engineering, University of Pittsburgh, Pittsburgh, Pennsylvania.
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania.
Department of Critical Care Medicine, University of Pittsburgh , Pittsburgh, Pennsylvania.
ALung Technologies, Inc. , Pittsburgh, Pennsylvania.
NEUROFARBA Department, Università degli Studi di Firenze , Florence , Italy.


Accumulating evidence is highlighting the importance of a system of enhanced hemoglobin-oxygen (Hb-O2) unloading for cardiovascular O2 transport in teleosts. Adrenergically stimulated sodium-proton exchangers (β-NHE) create H+ gradients across the red blood cell (RBC) membrane that are short-circuited in the presence of plasma-accessible carbonic anhydrase (paCA) at the tissues; the result is a large arterial-venous pH shift that greatly enhances O2 unloading from pH-sensitive Hb. However, RBC intracellular pH (pHi) must recover during venous transit (31-90 s) to enable O2 loading at the gills. The halftimes ( t1/2) and magnitudes of RBC β-adrenergic stimulation, short-circuiting with paCA and recovery of RBC pHi, were assessed in vitro, on rainbow trout whole blood, and using changes in closed-system partial pressure of O2 as a sensitive indicator for changes in RBC pHi. In addition, the recovery rate of RBC pHi was assessed in a continuous-flow apparatus that more closely mimics RBC transit through the circulation. Results indicate that: 1) the t1/2 of β-NHE short-circuiting is likely within the residence time of blood in the capillaries, 2) the t1/2 of RBC pHi recovery is 17 s and within the time of RBC venous transit, and 3) after short-circuiting, RBCs reestablish the initial H+ gradient across the membrane and can potentially undergo repeated cycles of short-circuiting and recovery. Thus, teleosts have evolved a system that greatly enhances O2 unloading from pH-sensitive Hb at the tissues, while protecting O2 loading at the gills; the resulting increase in O2 transport per unit of blood flow may enable the tremendous athletic ability of salmonids.


Bohr effect; hemoglobin; plasma-accessible carbonic anhydrase; teleost; β-NHE

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