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Enthalpic consequences of reduced chloride binding in Andean frog (Telmatobius peruvianus) hemoglobin

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Abstract

Based on the exothermic nature of heme oxygenation, the O2 affinity of hemoglobin (Hb) decreases with increasing temperature, which may be physiologically advantageous in augmenting O2 unloading from blood in warm tissues with elevated metabolic rates. This negative oxygenation enthalpy (∆H O) may, however, become maladaptive, as in cold-tolerant ungulates where it may hamper O2 unloading in cold extremities and commonly is mitigated by an ‘additional’ chloride-binding site that decreases the temperature effect by increasing the endothermic release of Cl− ions upon O2 binding. Since no previous studies have focused on the consequences of reduced Cl− binding, I report and compare the enthalpic effects of chloride ions and the allosteric effector, ATP, on Hbs of the high-altitude aquatic Andean frog Telmatobius peruvianus that lacks the α-chain chloride-binding site, and the lowland (sub-)tropical frog Xenopus laevis that has retained this site and exhibits high chloride sensitivity. In contrast to Xenopus, Telmatobius Hb exhibits high temperature sensitivity (high negative ∆H′) in the presence of Cl− ions, supporting the inverse relationship between the number of Cl−-binding sites and temperature sensitivity, and extending it to ectothermic vertebrates. The radically reduced chloride binding in Telmatobius Hb permits assessment of the enthalpy of ATP binding [(∆H′ ≈ −62 kJ (mol ATP)−1 at pH 7.0]—which contrasts sharply with previously reported increases in temperature sensitivity by ATP in toad (Bufo bufo) Hb. The high temperature sensitivity associated with decreased chloride binding and low phosphate sensitivity of Telmatobius Hb likely promotes cutaneous O2 uptake in cold, high-altitude ponds and streams.

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Abbreviations

Hb:

Hemoglobin

P 50 :

O2 tension that saturates 50 % of the Hb

n 50 :

Hill’s cooperativity coefficient at 50 % oxygenation of the Hb

ATP:

Adenosine triphosphate

DPG:

2,3-Diphosphoglycerate

IPP:

Inositol pentaphosphate

∆H′:

Apparent enthalpy of oxygenation

φ :

Bohr factor (∆log P 50/∆pH)

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Acknowledgments

I thank Kevin L. Campbell (Winnipeg) and Angela Fago (Aarhus) for critical comments, and the Faculty of Science and Technology, Aarhus University for support.

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  1. Zoophysiology, Department of Bioscience, Aarhus University, Aarhus, Denmark

    Roy E. Weber

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Correspondence to Roy E. Weber.

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Communicated by G. Heldmaier.

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Weber, R.E. Enthalpic consequences of reduced chloride binding in Andean frog (Telmatobius peruvianus) hemoglobin. J Comp Physiol B 184, 613–621 (2014). https://doi.org/10.1007/s00360-014-0823-2

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  • DOI: https://doi.org/10.1007/s00360-014-0823-2

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