Oxygen Supply from the Bird's Eye Perspective

Institute of Zoology and Zoological Museum, University of Hamburg, D-20146 Hamburg, Germany.
Journal of Biological Chemistry (Impact Factor: 4.57). 05/2011; 286(30):26507-15. DOI: 10.1074/jbc.M111.224634
Source: PubMed


The visual process in the vertebrate eye requires high amounts of metabolic energy and thus oxygen. Oxygen supply of the avian
retina is a challenging task because birds have large eyes, thick retinae, and high metabolic rates but neither deep retinal
nor superficial capillaries. Respiratory proteins such as myoglobin may enhance oxygen supply to certain tissues, and thus
the mammalian retina harbors high amounts of neuroglobin. Globin E (GbE) was recently identified as an eye-specific globin
of chicken (Gallus gallus). Orthologous GbE genes were found in zebra finch and turkey genomes but appear to be absent in non-avian vertebrate classes. Analyses of globin
phylogeny and gene synteny showed an ancient origin of GbE but did not help to assign it to any specific globin type. We show
that the photoreceptor cells of the chicken retina have a high level of GbE protein, which accumulates to ∼10 μm in the total eye. Quantitative real-time RT-PCR revealed an ∼50,000-fold higher level of GbE mRNA in the eye than in the
brain. Spectroscopic analysis and ligand binding kinetics of recombinant chicken GbE reveal a penta-coordinated globin with
an oxygen affinity of P50 = 5.8 torrs at 25 °C and 15 torrs at 41 °C. Together these data suggest that GbE helps to sustain oxygen supply to the avian

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    • "5H and I). Studies of zebrafish and Xenopus documented predominant expression of GbX in the nervous system (Fuchs et al. 2006; Blank, Wollberg, et al. 2011). However, those studies did not examine gene expression in the gonads, which suggests that the main "
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    ABSTRACT: Comparative analyses of vertebrate genomes continue to uncover a surprising diversity of genes in the globin gene superfamily, some of which have very restricted phyletic distributions despite their antiquity. Genomic analysis of the globin gene repertoire of cartilaginous fish (Chondrichthyes) should be especially informative about the duplicative origins and ancestral functions of vertebrate globins, as divergence between Chondrichthyes and bony vertebrates represents the most basal split within the jawed vertebrates. Here we report a comparative genomic analysis of the vertebrate globin gene family that includes the complete globin gene repertoire of the elephant shark (Callorhinchus milii). Using genomic sequence data from representatives of all major vertebrate classes, integrated analyses of conserved synteny and phylogenetic relationships revealed that the last common ancestor of vertebrates possessed a repertoire of at least seven globin genes: single copies of androglobin and neuroglobin, four paralogous copies of globin X, and the single-copy progenitor of the entire set of vertebrate-specific globins. Combined with expression data, the genomic inventory of elephant shark globins yielded four especially surprising findings: (i) there is no trace of the neuroglobin gene (a highly conserved gene that is present in all other jawed vertebrates that have been examined to date), (ii) myoglobin is highly expressed in heart, but not in skeletal muscle (reflecting a possible ancestral condition in vertebrates with single-circuit circulatory systems), (iii) elephant shark possesses two highly divergent globin X paralogs, one of which is preferentially expressed in gonads, and (iv) elephant shark possesses two structurally distinct α-globin paralogs, one of which is preferentially expressed in the brain. Expression profiles of elephant shark globin genes reveal distinct specializations of function relative to orthologs in bony vertebrates and suggest hypotheses about ancestral functions of vertebrate globins. © The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail:
    Full-text · Article · Mar 2015 · Molecular Biology and Evolution
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    • "This is especially true for the eye-specific globin E gene (GbE) which is only transcribed in the eye of adult birds (Table 2). Thus, the protein is suggested to be involved in the oxygen supply of this metabolically highly active tissue (Blank et al. 2011a). "
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    ABSTRACT: In many multicellular organisms, oxygen is transported by respiratory proteins, which are globins in vertebrates, between respiratory organs and tissues. In jawed vertebrates, eight globins are known which are expressed in a highly tissue-specific manner. Until now, hemoglobin (Hb) had been agreed to be the only globin expressed in vertebrate erythrocytes. Here, we investigate for the first time the mRNA expression of globin genes in nucleated and anucleated erythrocytes of model vertebrate species by quantitative real-time reverse transcription PCR (qRT-PCR). Surprisingly, we found transcripts of the whole gnathostome globin superfamily in RBCs. The mRNA expression levels varied among species, with Hb being by far the dominant globin. Only in stickleback, a globin previously thought to be neuron-specific, neuroglobin, had higher mRNA expression. We furthermore show that in birds transcripts of globin E, which was earlier reported to be transcribed only in the eye, are also present in RBCs. Even in anucleated RBCs of mammals, we found transcripts of myoglobin, neuroglobin, and cytoglobin. Our findings add new aspects to the current knowledge on the expression of globins in vertebrate tissues. However, whether or not the mRNA expression of these globin genes has any functional significance in RBCs has to be investigated in future studies. © 2015 The Authors. Physiological Reports published by Wiley Periodicals, Inc. on behalf of the American Physiological Society and The Physiological Society.
    Full-text · Article · Feb 2015
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    • "Changes in the size and membership composition of the a-and b-globin gene families may produce changes in the developmental regulation of Hb synthesis and may therefore constrain or potentiate functional divergence between Hb isoforms that incorporate the products of paralogous globin genes (Berenbrink et al. 2005; Berenbrink 2007; Opazo et al. 2008a, 2008b; Runck et al. 2009; Hoffmann, Storz, et al. 2010; Storz, Hoffmann, et al. 2011; Storz, Opazo, et al. 2011; Grispo et al. 2012; Damsgaard et al. 2013; Opazo et al. 2013; Storz et al. 2013). Indeed, over a deeper timescale of animal evolution, the co-option and functional divergence of more ancient members of the globin gene superfamily have played a well-documented role in evolutionary innovation (Hoffmann, Opazo, et al. 2010; Blank et al. 2011; Hoffmann, Opazo, Hoogewijs, et al. 2012; Hoffmann, Opazo, Storz, 2012; Hoogewijs et al. 2012; Schwarze and Burmester 2013; Schwarze et al. 2014). All gnathostome taxa that have been examined to date express structurally and functionally distinct Hb isoforms during different stages of prenatal development (Hardison 2001), and some tetrapod groups coexpress different Hb isoforms during postnatal life. "
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    ABSTRACT: The apparent stasis in the evolution of avian chromosomes suggests that birds may have experienced relatively low rates of gene gain and loss in multigene families. To investigate this possibility and to explore the phenotypic consequences of variation in gene copy number, we examined evolutionary changes in the families of genes that encode the α- and β-type subunits of hemoglobin (Hb), the tetrameric α2β2 protein responsible for blood-O2 transport. A comparative genomic analysis of 52 bird species revealed that the size and membership composition of the α- and β-globin gene families have remained remarkably constant during ~100 million years of avian evolution. Most interspecific variation in gene content is attributable to multiple independent inactivations of the α(D)-globin gene, which encodes the α-chain subunit of a functionally distinct Hb isoform (HbD) that is expressed in both embryonic and definitive erythrocytes. Due to consistent differences in O2-binding properties between HbD and the major adult-expressed Hb isoform, HbA (which incorporates products of the α(A)-globin gene), recurrent losses of α(D)-globin contribute to among-species variation in blood-O2 affinity. Analysis of HbA/HbD expression levels in the red blood cells of 122 bird species revealed high variability among lineages and strong phylogenetic signal. In comparison with the homologous gene clusters in mammals, the low retention rate for lineage-specific gene duplicates in the avian globin gene clusters suggests that the developmental regulation of Hb synthesis in birds may be more highly conserved, with orthologous genes having similar stage-specific expression profiles and similar functional properties in disparate taxa. © The Author(s) 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
    Full-text · Article · Dec 2014 · Molecular Biology and Evolution
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