Myoglobin enhances cardiac performance in antarctic icefish species that express the protein

Abstract

Channichthyid icefishes of Antarctica are unique among adult vertebrates. All icefish species lack hemoglobin and red blood cells in their circulating blood. All icefishes examined to date also lack the intracellular oxygen-binding protein myoglobin (Mb) in their oxidative skeletal muscles. However, some icefish species do express Mb in their heart ventricles. It is unknown whether Mb in those species in which it is present represents an evolutionary relic or has functional significance. To address this problem, we compared mechanical performance of isolated, perfused hearts from two species of icefish in which Mb is either present (Chionodraco rastrospinosus) or is absent (Chaenocephalus aceratus). Hearts were challenged with increasing afterload (2.5-4.0 kPa) under conditions of defined basal flow (approximately 100 ml.min-1.kg-1), in both the presence and absence of 5 mM sodium nitrite, a Mb poison. Unlike hearts from C. aceratus, which were unable to maintain a constant cardiac output under pressure loading, those from C. rastrospinosus retained a constant flow up to 3.5 kPa afterload. At the upper range of power outputs, hearts of Mb-lacking C. aceratus display greater oxygen utilization than those of Mb-containing C. rastrospinosus. Poisoning of Mb significantly impaired the ability of C. rastrospinosus hearts to face pressure loading without reduction in flow, whereas those of C. aceratus were refractory to the treatment. The results strongly support a functional role for Mb in the former species.

Expression patterns and adaptive functional diversity of vertebrate myoglobins

“…Overall the results showed that perfused Mb-rich hearts were better at maintaining O 2 consumption and cardiac performance under hypoxic conditions than Mb-poor hearts [56,63]. Similar results were obtained when comparing the mechanical performance of perfused hearts from two icefish species -one expressing and one not expressing Mb protein [65]. Thus it appears that heart Mb plays a corresponding role in fish as in mammals, namely in maintaining O 2 consumption in myocytes when O 2 levels decrease.…”

Myoglobin function reassessed

“…Some species lack cardiac myoglobin as well. The mechanical performance of isolated perfused hearts from two very similar, congeneric channichthyids show little difference at normal work loads, but that of the species with myoglobin is far more able to maintain cardiac output in the face of the additional insult of increased aortic arterial pressure (Acierno et al, 1997;Sidell, 1998). Channichthyid fish without myoglobin served as a control of the effects of nitrite in an experiment demonstrating decreased cardiac function following blockade of cardiac myoglobin (Acierno et al, 1997).…”

The myoglobin gene of the Antarctic icefish, Chaenocephalus aceratus, contains a duplicated TATAAAA sequence that interferes with transcription

“…When isolated, perfused hearts from Mb-expressing and Mb-lacking icefish species are challenged with increasing afterload, hearts whose ventricles contain Mb are capable of greater pressure-work (Acierno et al, 1997). Furthermore, specific poisoning of Mb function in these preparations causes performance of Mb-expressing hearts to decrement below that of normally Mb-lacking hearts, indicating that the latter display mechanisms that partially compensate for the absence of this oxygen-binding protein.…”