Hemoglobin Heterogeneity: Embryonic Hemoglobin in the Duckling and Its Disappearance in the Adult

Borgese, Thomas A.; Bertles, John F.

doi:10.1126/science.148.3669.509

Cited by 39 publications

(9 citation statements)

References 9 publications

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“…In the common ancestor of amniote vertebrates, it may be that the ancestral α D -globin was expressed early in development, and was later recruited for expression in the mature erythrocytes of adult birds and reptiles, although the ancestral mode of embryonic expression has been retained in some avian species (Godovac-Zimmermann and Braunitzer 1984). In most birds, the α D -globin gene is expressed at lower levels than α A -globin, but the relative expression levels of the two genes vary widely among different species (Borgese and Bertles 1965;Braunitzer 1984, 1985;Hiebl et al 1986;Hiebl et al 1987;Hiebl et al 1989;Nothum, Weber et al 1989;Ikehara et al 1997).…”

Section: Discussionmentioning

confidence: 99%

“…In birds and reptiles, by contrast, the α-chains of adult hemoglobin are encoded by both the α D -and α A -globin genes. In most birds studied to date, α D -containing hemoglobin Origin Of the α D -glObin gene in the AncestOr Of tetrApOd VertebrAtes 1983 (HbD) constitutes the minor fraction of adult hemoglobin and α A -containing hemoglobin (HbA) constitutes the major fraction (Borgese and Bertles 1965;Brown and Ingram 1974;Hiebl et al 1987). Thus, unlike the case in most mammals, the mature erythrocytes of adult birds and reptiles may contain a mixture of functionally distinct hemoglobin isoforms that have different biochemical properties.…”

Section: Introductionmentioning

confidence: 99%

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The αD-Globin Gene Originated via Duplication of an Embryonic α-Like Globin Gene in the Ancestor of Tetrapod Vertebrates

Hoffmann

Storz

2007

Molecular Biology and Evolution

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Gene duplication is thought to play an important role in the co-option of existing protein functions to new physiological pathways. The globin superfamily of genes provides an excellent example of the kind of physiological versatility that can be attained through the functional and regulatory divergence of duplicated genes that encode different subunit polypeptides of the tetrameric hemoglobin protein. In contrast to prevailing views about the evolutionary history of the alpha-globin gene family, here we present phylogenetic evidence that the alpha(A)- and alpha(D)-globin genes are not the product of a single, tandem duplication of an ancestral globin gene with adult function in the common ancestor of extant birds, reptiles, and mammals. Instead, our analysis reveals that the alpha(D)-globin gene of amniote vertebrates arose via duplication of an embryonic alpha-like globin gene that predated the radiation of tetrapods. The important evolutionary implication is that the distinct biochemical properties of alpha(D)-hemoglobin (HbD) are not exclusively derived characters that can be attributed to a post-duplication process of neofunctionalization. Rather, many of the distinct biochemical properties of HbD are retained ancestral characters that reflect the fact that the alpha(D)-globin gene arose via duplication of a gene that had a larval/embryonic function. These insights into the evolutionary origin of HbD illustrate how adaptive modifications of physiological pathways may result from the retention and opportunistic co-option of ancestral protein functions.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The αD-Globin Gene Originated via Duplication of an Embryonic α-Like Globin Gene in the Ancestor of Tetrapod Vertebrates

Hoffmann

Storz

2007

Molecular Biology and Evolution

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“…This is supported by the observations that phenylhydrazine-induced anemia in adult chickens does not result in circulating erythroblasts with increased amounts of E70, and that bone marrow from anemic and normal adult chickens contains little erythroid E70, as assayed by immunofluorescence (data not shown). Precedents exist for this time course of expression of avian erythroid components: A hemoglobin variant (22,23) and certain cell surface antigens (24,25) are present in embryos but disappear within a few months of hatching; furthermnore, induced anemia does not result in their reappearance (23,25). The observed range in the amount of E70 present in different cells from a given individual (regardless of age) suggests that synthesis of E70 may be influenced by hemopoietic microenvironments or may be a function of stem cell heritage.…”

Section: Expression Of the Major Neurofilament Subunit In Chicken Erymentioning

confidence: 99%

Expression of the Major Neurofilament Subunit in Chicken Erythrocytes

Granger

Lazarides

1983

Science

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The 70,000-dalton core polypeptide of neurofilaments, thought to exist only in neurons, has been detected in chicken erythrocytes, where it coexists with vimentin and synemin as a component of the intermediate filament network. It is present in the circulating erythroid cells of embryos and young chickens but is nearly absent from the erythroid cells of adults. These findings are inconsistent with current models of intermediate filament expression, but provide another example of unexpected similarities between the nervous and hemopoietic systems.

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“…This suggests that the product of  observed in birds. In the definitive erythroid cells of adult birds, the  D -chain isoform typically constitutes the minor fraction of adult Hb and the  A -chain isoform typically constitutes the major fraction, although the relative abundance of the two isoforms is quite variable among species (Borgese and Bertles, 1965;Brown and Ingram, 1974;Hiebl et al, 1987;Ikehara et al, 1997).…”

Section: Expression Of -Chain Isohbsmentioning

confidence: 99%

Developmental regulation of hemoglobin synthesis in the green anole lizard Anolis carolinensis

Storz

Hoffmann

Opazo

et al. 2011

Journal of Experimental Biology

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SUMMARYTetrapod vertebrates possess multiple -and -like globin genes that are ontogenetically regulated, such that functionally distinct hemoglobin (Hb) isoforms are synthesized during different stages of development. The -and -like globin genes of amphibians, birds and mammals are differentially expressed during embryonic development and postnatal life, but little is known about the developmental regulation of globin gene expression in non-avian reptiles. Here we report an investigation into the developmental regulation of Hb synthesis in the green anole lizard Anolis carolinensis. We tested two hypotheses derived from comparative genomic studies of the globin gene clusters in tetrapod vertebrates. First, we tested whether the product of the Anolis  D -globin gene is incorporated into embryonic Hb, thereby performing the role that would normally be performed by the embyronic  E -globin gene (which has been deleted from the green anole genome). Second, we tested whether two 'lizard-specific' -globin paralogs have independently evolved a division of labor between an early-expressed embryonic gene and a later-expressed adult gene. Results of a proteomic analysis revealed that -and -like globin genes of the anole are differentially expressed during embryonic development. However, the same repertoire of -and -chain Hb isoforms was expressed during all stages of development and postnatal life, and the ontogenetic shifts in isoform composition were relatively subtle. In contrast to the pattern that has been documented in other tetrapod vertebrates, it appears that the developmental regulation of Hb synthesis in the green anole lizard does not involve discrete, stage-specific switches in gene activation and gene silencing.

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Hemoglobin Heterogeneity: Embryonic Hemoglobin in the Duckling and Its Disappearance in the Adult

Cited by 39 publications

References 9 publications

The αD-Globin Gene Originated via Duplication of an Embryonic α-Like Globin Gene in the Ancestor of Tetrapod Vertebrates

The αD-Globin Gene Originated via Duplication of an Embryonic α-Like Globin Gene in the Ancestor of Tetrapod Vertebrates

Expression of the Major Neurofilament Subunit in Chicken Erythrocytes

Developmental regulation of hemoglobin synthesis in the green anole lizard Anolis carolinensis

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