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Myoglobin and Myoglobin Mrna in Fish Heart

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Myoglobin and Myoglobin Mrna in Fish Heart The Journal of Experimental Biology 203, 1277–1286 (2000) 1277 Printed in Great Britain © The Company of Biologists Limited 2000 JEB2492 CONCENTRATIONS OF MYOGLOBIN AND MYOGLOBIN mRNA IN HEART VENTRICLES FROM ANTARCTIC FISHES THOMAS J. MOYLAN AND BRUCE D. SIDELL* School of Marine Sciences, University of Maine, 5741 Libby Hall, Orono, ME 04469-5741, USA *Author for correspondence (e-mail: [email protected]) Accepted 9 February; published on WWW 23 March 2000 Summary We used a combined immunochemical and molecular was used to quantify mRNA in five Mb-expressing icefishes. approach to ascertain the presence and concentrations Mb mRNA was found in low but detectable amounts in of both the intracellular oxygen-binding hemoprotein Champsocephalus gunnari, one of the species lacking myoglobin (Mb) and its messenger RNA (mRNA) in 13 of detectable Mb. Mb mRNA concentrations in heart 15 known species of Antarctic channichthyid icefishes. ventricle from Mb-expressing species ranged from Mb protein is present in the hearts of eight species 0.78±0.02 to 16.22±2.17 pg Mb mRNA µg−1 total RNA). Mb of icefishes: Chionodraco rastrospinosus, Chionodraco protein and Mb mRNA are absent from the oxidative hamatus, Chionodraco myersi, Chaenodraco wilsoni, skeletal muscle of all icefishes. Steady-state concentrations Pseudochaenichthys georgianus, Cryodraco antarcticus, of Mb protein do not parallel steady-state concentrations Chionobathyscus dewitti and Neopagetopsis ionah. Five of Mb mRNA within and among icefishes, indicating that icefish species lack detectable Mb protein: Chaenocephalus the concentration of Mb protein is not determined by the aceratus, Pagetopsis macropterus, Pagetopsis maculatus, size of its mRNA pool. Champsocephalus gunnari and Dacodraco hunteri. Mb concentrations range from 0.44±0.02 to 0.71±0.08 mg Mb g−1 wet mass in heart ventricle of species Key words: myoglobin, mRNA, Antarctic fish, Channichthyidae, expressing the protein. A Mb-mRNA-specific cDNA probe Nototheniidae, heart, cardiac muscle, mRNA. Introduction Low temperatures and high oxygen solubility characterize the absence of a circulating oxygen-transport protein, many the Southern Ocean surrounding Antarctica. Mean annual investigators have characterized icefishes as also lacking the temperature in McMurdo Sound is −1.86 °C (Littlepage, 1965), 16–17 kDa intracellular oxygen-binding protein myoglobin. while the temperatures of waters surrounding the Antarctic Myoglobin is a monomeric protein containing a single Peninsula range between +0.3 °C during the austral summer to coordinated heme group that binds oxygen reversibly with a −1.1 °C during the winter months (DeWitt, 1971). Despite 1:1 molecular stoichiometry. It has an important role in the these chronically cold temperatures, coastal Antarctica storage and transport of oxygen from capillaries to supports an abundant fish fauna dominated by species of the mitochondria in oxidative muscle tissues of vertebrates (Covell perciform suborder Notothenioidei, a group that has been and Jacquez, 1987; Wittenberg and Wittenberg, 1989). While evolving since the formation of the Antarctic Circumpolar the cardiovascular alterations described above may help offset Current, between 14 and 25 million years ago (Eastman and the loss of hemoglobin, it is difficult to envisage how these Grande, 1989). features could compensate for the reported absence of Channichthyid icefishes are thought to have diverged from myoglobin in highly aerobic heart tissues (Hamoir, 1988; other notothenioid families approximately 1–3 million years Eastman, 1990). ago (Bargelloni et al., 1994). The 15 species of the Although the consensus view has been that icefishes lack Channichthyidae are unique among adult vertebrates in their myoglobin, Douglas et al. (1985) reported that myoglobin complete lack of expression of hemoglobin, a characteristic was expressed in heart tissue of two icefish species, first described in the scientific literature by Ruud (1954). These Pseudochaenichthys georgianus and Chaenocephalus fishes show profound cardiovascular modifications (large aceratus. The technical basis for this report, however, was the hearts and blood vessels, high cardiac output, increased blood detection of the formation of pyridine hemochromagen in volume) that apparently ensure adequate delivery of oxygen to crude supernatant extracts from hearts, a method that could the tissues despite the lack of circulating hemoglobin easily lead to false positive results in tissues containing high (Hemmingsen et al., 1972; Hemmingsen, 1991). In addition to concentrations of mitochondrial cytochromes. To resolve the 1278 T. J. MOYLAN AND B. D. SIDELL question of myoglobin expression in the icefishes, our towards deciphering the molecular basis for the unusual pattern laboratory has recently used more definitive immunochemical of myoglobin expression. These measurements also permitted and molecular techniques to establish that myoglobin is us to evaluate any correlation between pools of myoglobin expressed in heart ventricles of some icefish species while mRNA and the concentration of myoglobin protein in the heart being completely absent from the same tissue in others (Sidell ventricle of notothenioid species. et al., 1997). Furthermore, the disparate positions of myoglobin non-expressers within the phylogeny of icefishes suggested that multiple independent mutational events led to the loss of Materials and methods myoglobin expression during the evolution of the family. The Animal and tissue collection establishment of discretely different mutational mechanisms Chionodraco rastrospinosus, Pseudochaenichthys among these myoglobin non-expressers has corroborated this georgianus, Chaenodraco wilsoni, Chaenocephalus aceratus, conclusion (Small et al., 1998). The seemingly random pattern Champsocephalus gunnari, Gobionotothen gibberifrons, of loss of myoglobin among icefish species appeared to suggest Trematomus newnesi and Notothenia coriiceps were collected that the protein may not be of functional significance at the by 18 foot otter trawl net deployed from the R/V Polar Duke severely cold body temperature of Antarctic icefishes, thus while fishing off the Antarctic Peninsula in Dallman Bay near relaxing all selective pressure on the retention of its expression Astrolabe Needle (64°10′S, 62°35′W) in March–May 1993 and and/or structure. 1996. Fish were transported live to the US Antarctic research The provocative suggestion that myoglobin may not station, Palmer Station, and maintained there in running function at the body temperature of Antarctic fishes led our seawater tanks (−1.5 to +1.0 °C). Animals were killed by a laboratory and collaborators to examine the functional sharp blow to the head followed by severing the spinal cord characteristics of oxygen-binding by myoglobin from these immediately posterior to the head. The heart ventricle and animals and its potential physiological role in those Antarctic pectoral adductor profundus tissues were rapidly dissected on icefishes that do express the protein. Using stopped-flow a chilled stage, weighed and frozen in liquid nitrogen prior to kinetics measurements, we found that myoglobins from both storage at −80 °C. Antarctic and temperate-zone teleost fishes show more rapid Tissues from Pagetopsis macropterus, Pagetopsis binding and release of oxygen at cold temperature than those maculatus, Dacodraco hunteri, Chionodraco myersi and from mammals (Cashon et al., 1997). These results indicate Cryodraco antarcticus were generously provided by Dr A. that fish myoglobins, including those from Antarctic species, DeVries (University of Illinois) and were collected in possess alterations in protein structure/sequence that increase McMurdo Sound, Antarctica. Drs R. Acierno and G. di Prisco the speed of binding and release of oxygen at low (Italian National Antarctic Program) kindly supplied samples temperatures. Additional experiments with isolated, perfused of Chionodraco hamatus, collected in the vicinity of Terra hearts from two icefishes, one lacking (Chaenocephalus Nova Bay, Antarctica. Dr T. Iwami (Tokyo Kasei Gakuin aceratus) and one containing (Chionodraco rastrospinosus) University, Japan) supplied Chionobathyscus dewitti and myoglobin protein, demonstrated that hearts possessing Neopagetopsis ionah collected in the Weddell Sea. Tissues myoglobin were capable of greater mechanical performance were dissected and maintained frozen (liquid nitrogen, dry ice than those lacking it (Acierno et al., 1997). Both lines of or −80 °C storage) until use. evidence strongly indicate that myoglobin is functional at the normal body temperature of icefish and that it does play a Purification of myoglobin standard physiological role in the delivery of oxygen to working To determine myoglobin concentrations in icefishes, a muscle. These conclusions make the observation that myoglobin standard was purified from the related nototheniid myoglobin is absent from oxidative skeletal muscle of all species Notothenia coriiceps. Frozen Notothenia coriiceps notothenioid fishes examined to date even more perplexing heart ventricle (2.4 g) was weighed and homogenized [40 % in the light of the highly aerobic metabolism of this tissue (w/v)] in filtered 100 mmol l−1 potassium phosphate buffer, (Sidell et al., 1987). pH 7.8, with a glass tissue grinder (Tenbroeck). The The confirmation of extremely variable expression of homogenate was centrifuged at 23 000 g for 30 min at 4 °C. The myoglobin in the notothenioid suborder (Fig. 1) is therefore at resulting supernatant was collected
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