Plasma-accessible carbonic anhydrase at the tissue of a teleost fish may greatly enhance oxygen delivery: in vitro evidence in rainbow trout, Oncorhynchus mykiss

Rummer, Jodie L., and Brauner, Colin J. (2011) Plasma-accessible carbonic anhydrase at the tissue of a teleost fish may greatly enhance oxygen delivery: in vitro evidence in rainbow trout, Oncorhynchus mykiss. Journal of Experimental Biology, 214. pp. 2319-2328.

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Abstract

During a generalized acidosis in rainbow trout, catecholamines are released into the blood, activating red blood cell (RBC) Na+/H+ exchange (βNHE), thus protecting RBC intracellular pH (pHi) and subsequent O2 binding at the gill. Because of the presence of a Root effect (a reduction in oxygen carrying capacity of the blood with a reduction in pH), the latter could otherwise be impaired. However, plasma-accessible carbonic anhydrase (CA) at the tissues (and absence at the gills) may result in selective short-circuiting of RBC βNHE pH regulation. This would acidify the RBCs and greatly enhance O2 delivery by exploitation of the combined Bohr-Root effect, a mechanism not previously proposed. As proof-of-principle, an in vitro closed system was developed to continuously monitor extracellular pH (pHe) and O2 tension (PO2) of rainbow trout blood. In this closed system, adding CA to acidified, adrenergically stimulated RBCs short-circuited βNHE pH regulation, resulting in an increase in PO2 by >30 mmHg, depending on the starting Hb-O2 saturation and degree of initial acidification. Interestingly, in the absence of adrenergic stimulation, addition of CA still elevated PO2, albeit to a lesser extent, a response that was absent during general NHE inhibition. If plasma-accessible CA-mediated short-circuiting is operational in vivo, the combined Bohr-Root effect system unique to teleost fishes could markedly enhance tissue O2 delivery far in excess of that in vertebrates possessing a Bohr effect alone and may lead to insights about the early evolution of the Root effect.

Item ID: 33082
Item Type: Article (Research - C1)
ISSN: 1477-9145
Keywords: combined Bohr–Root effect, haemoglobin, βNHE, oxygen delivery, carbonic anhydrase, catecholamine, isoproterenol, short-circuiting
Funders: Natural Sciences and Engineering Research Council of Canada, University of British Columbia
Date Deposited: 25 Aug 2016 03:14
FoR Codes: 06 BIOLOGICAL SCIENCES > 0606 Physiology > 060603 Animal Physiology Systems @ 50%
06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060309 Phylogeny and Comparative Analysis @ 50%
SEO Codes: 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 100%
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