Expression patterns and adaptive functional diversity of vertebrate myoglobins

Helbo, Signe; Weber, Roy E.; Fago, Angela

doi:10.1016/j.bbapap.2013.01.037

Cited by 41 publications

(40 citation statements)

References 125 publications

(196 reference statements)

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“…However, even before this study, exceptions to this ‘rule’ were suspected, including the entire class Amphibia and a few teleost species [2,5,6]. Nevertheless, such cases have been deemed extraordinary [2,5].…”

Section: Discussionmentioning

confidence: 96%

“…Myoglobin (Mb) is an oxygen-binding haemprotein of the globin family, typically expressed at high levels in aerobic striated muscle [1,2]. ‘Classic’ functions include the storage of oxygen in the intracellular compartment and the enhancement of oxygen diffusion from blood to mitochondria [1,2].…”

Section: Introductionmentioning

confidence: 99%

“…‘Classic’ functions include the storage of oxygen in the intracellular compartment and the enhancement of oxygen diffusion from blood to mitochondria [1,2]. More recently characterized functions in a range of cell-types include the regulation of intracellular nitric oxide and reactive oxygen species (reviewed in [2,3]). High Mb is positively associated with lifestyles or environments that demand efficient oxygen delivery.…”

Section: Introductionmentioning

confidence: 99%

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Cardiac myoglobin deficit has evolved repeatedly in teleost fishes

2014

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Myoglobin (Mb) is the classic vertebrate oxygen-binding protein present in aerobic striated muscles. It functions principally in oxygen delivery and provides muscle with its characteristic red colour. Members of the Antarctic icefish family (Channichthyidae) are widely thought to be extraordinary for lacking cardiac Mb expression, a fact that has been attributed to their low metabolic rate and unusual evolutionary history. Here, we report that cardiac Mb deficit, associated with pale heart colour, has evolved repeatedly during teleost evolution. This trait affects both gill- and air-breathing species from temperate to tropical habitats across a full range of salinities. Cardiac Mb deficit results from total pseudogenization in three-spined stickleback and is associated with a massive reduction in mRNA level in two species that evidently retain functional Mb. The results suggest that near or complete absence of Mb-assisted oxygen delivery to heart muscle is a common facet of teleost biodiversity, even affecting lineages with notable oxygen demands. We suggest that Mb deficit may affect how different teleost species deal with increased tissue oxygen demands arising under climate change.

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Section: Discussionmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Cardiac myoglobin deficit has evolved repeatedly in teleost fishes

2014

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“…1. higher SNO levels and higher NO formation from nitrite (FeNO) during anoxia. Deoxygenated myoglobin effectively reduces nitrite to NO (Shiva et al, 2007b;Helbo et al, 2013), but myoglobin may also be important in elevating muscle nitrite levels. We suggest that the negatively charged nitrite ion binds to positive charges on myoglobin, and that this binding increases during anoxia, because the net positive charge on myoglobin progressively increases as a result of its buffering of H + from the anoxia-induced acidosis.…”

Section: Research Articlementioning

confidence: 99%

Nitric oxide metabolites during anoxia and reoxygenation in the anoxia-tolerant vertebrate, Trachemys scripta

Frank

Hansen

Montesanti

et al. 2013

Journal of Experimental Biology

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Moderate elevations of nitrite and nitric oxide (NO) protect mammalian tissues against ischemia (anoxia)-reperfusion damage by inhibiting mitochondrial electron transport complexes and reducing the formation of reactive oxygen species (ROS) upon reoxygenation. Crucian carp appear to exploit this mechanism by upregulating nitrite and other nitrite/NO metabolites (S-nitroso and iron-nitrosyl compounds) in several tissues when exposed to anoxia. We investigated whether this is a common strategy amongst anoxiatolerant vertebrates by evaluating NO metabolites in red-eared slider turtles during long-term (9 days) anoxia and subsequent reoxygenation at low temperature, a situation naturally encountered by turtles in ice-covered ponds. We also measured glutathione in selected tissues and assessed the impact of anoxia on electrolyte status. Anoxia induced major increases in [nitrite] in the heart, pectoral muscle and red blood cells, while [nitrite] was maintained unaltered in brain and liver. Concomitantly, the concentrations of Snitroso and iron-nitrosyl compounds increased, showing that nitrite was used to produce NO and to S-nitrosate cellular molecules during anoxia. The changes were gradually reversed during reoxygenation (1 h and 24 h), testifying that the processes were reversible. The increased NO bioavailability occurred in the absence of NO synthase activity (due to global anoxia) and may involve mobilization of internal/external nitrite reservoirs. Our data support the theory that anoxic upregulation of nitrite and other NO metabolites could be a general cytoprotective strategy amongst anoxia-tolerant vertebrates. The possible mechanisms of nitrite-derived NO and S-nitrosation in protecting cells from destructive Ca 2+ influx during anoxia and in limiting ROS formation during reoxygenation are discussed.

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“…Myoglobin (Mb) plays a key role in the transport and storage of oxygen in muscle cells (Helbo et al 2013). It maintains the level of oxidative phosphorylation required for achieving muscular work under long-term oxygen deficiency.…”

Section: Introductionmentioning

confidence: 99%

Seasonal oxidative capacity of skeletal muscles in hibernating Daurian ground squirrels (Spermophilus dauricus)

et al. 2015

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We investigated the mechanism of high oxidative capacity of skeletal muscles in hibernating Daurian ground squirrels (Spermophilus dauricus Brandt, 1843). Myoglobin (Mb) levels, as well as citrate synthase and lactate dehydrogenase (LDH) activities, were measured by spectrophotometry. Mb content in the soleus (SOL) muscle lasted from the beginning of hibernation to spring. Mb content in SOL was 87% higher in the hibernating group than in the summer group. Mb content in the extensor digitorum longus (EDL) muscle stayed at similar levels during the different periods of the year. Citrate synthase activity in SOL was 30% higher in the hibernating group than in the summer group. Meanwhile, citrate synthase activity in EDL did not change during hibernation. LDH activity in SOL was not different between the hibernating group and the summer active group, whereas LDH activity in EDL increased significantly (up to 11%) in the 2 days arousal after hibernation group compared with the hibernating group. We conclude that high oxidative capacity is provided by increased oxygen storage capacity of slow-twitch muscle fibers rather than from fast-twitch muscle fibers in hibernating animals. Résumé :Nous avons examiné le mécanisme qui sous-tend la capacité oxydative élevée des muscles squelettiques chez des spermophiles de Daourie (Spermophilus dauricus Brandt, 1843) hibernants. Les teneurs en myoglobine (Mb), ainsi que les activités de la citrate-synthase et de la lactate-déshydrogénase (LDH) ont été mesurées par spectrophotométrie. Les teneurs en Mb dans le muscle soléaire (SOL) persistaient du début de l'hibernation jusqu'au printemps. Les teneurs en Mb dans le SOL étaient de 87 % plus grandes dans le groupe hibernant que dans le groupe d'été. La Mb dans le muscle long extenseur du doigt (EDL) se maintenait à des teneurs semblables durant toutes les saisons de l'année. L'activité de la citrate-synthase dans le SOL était de 30 % plus grande dans le groupe hibernant que dans le groupe estival, alors que dans l'EDL, elle ne changeait pas durant l'hibernation. Il n'y avait pas de différence sur le plan de l'activité de la LDH dans le SOL entre le groupe hibernant et le groupe estival, alors que dans l'EDL, l'activité de la LDH augmentait de manière significative (jusqu'à 11 %) dans le groupe observé 2 jours après le réveil suivant l'hibernation par rapport au groupe hibernant. Nous concluons que la capacité oxydative élevée chez les animaux hibernants est assurée par une capacité de stockage d'oxygène accrue dans les fibres musculaires à contraction lente plutôt que par les fibres musculaires à contraction rapide. [Traduit par la Rédaction]

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Expression patterns and adaptive functional diversity of vertebrate myoglobins

Cited by 41 publications

References 125 publications

Cardiac myoglobin deficit has evolved repeatedly in teleost fishes

Cardiac myoglobin deficit has evolved repeatedly in teleost fishes

Nitric oxide metabolites during anoxia and reoxygenation in the anoxia-tolerant vertebrate, Trachemys scripta

Seasonal oxidative capacity of skeletal muscles in hibernating Daurian ground squirrels (Spermophilus dauricus)

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