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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.

Author information

1
Department of Zoology, University of British Columbia , Vancouver, BC , Canada.
2
McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania.
3
Department of Chemical and Petroleum Engineering, University of Pittsburgh, Pittsburgh, Pennsylvania.
4
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania.
5
Department of Critical Care Medicine, University of Pittsburgh , Pittsburgh, Pennsylvania.
6
ALung Technologies, Inc. , Pittsburgh, Pennsylvania.
7
NEUROFARBA Department, Università degli Studi di Firenze , Florence , Italy.

Abstract

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.

KEYWORDS:

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

PMID:
29641235
PMCID:
PMC6139614
DOI:
10.1152/ajpregu.00062.2018
[Indexed for MEDLINE]
Free PMC Article

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