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Composition and evolution of the vertebrate and mammalian selenoproteomes.

Mariotti M, Ridge PG, Zhang Y, Lobanov AV, Pringle TH, Guigo R, Hatfield DL, Gladyshev VN - PLoS ONE (2012)

Bottom Line: In total, we detected 45 selenoprotein subfamilies. 28 of them were found in mammals, and 41 in bony fishes.Mammalian thioredoxin reductase 1 and thioredoxin-glutathione reductase evolved from an ancestral glutaredoxin-domain containing enzyme, still present in fish.It also provides a wealth of information on these selenoproteins and their forms.

View Article: PubMed Central - PubMed

Affiliation: Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, United States of America.

ABSTRACT

Background: Selenium is an essential trace element in mammals due to its presence in proteins in the form of selenocysteine (Sec). Human genome codes for 25 Sec-containing protein genes, and mouse and rat genomes for 24.

Methodology/principal findings: We characterized the selenoproteomes of 44 sequenced vertebrates by applying gene prediction and phylogenetic reconstruction methods, supplemented with the analyses of gene structures, alternative splicing isoforms, untranslated regions, SECIS elements, and pseudogenes. In total, we detected 45 selenoprotein subfamilies. 28 of them were found in mammals, and 41 in bony fishes. We define the ancestral vertebrate (28 proteins) and mammalian (25 proteins) selenoproteomes, and describe how they evolved along lineages through gene duplication (20 events), gene loss (10 events) and replacement of Sec with cysteine (12 events). We show that an intronless selenophosphate synthetase 2 gene evolved in early mammals and replaced functionally the original multiexon gene in placental mammals, whereas both genes remain in marsupials. Mammalian thioredoxin reductase 1 and thioredoxin-glutathione reductase evolved from an ancestral glutaredoxin-domain containing enzyme, still present in fish. Selenoprotein V and GPx6 evolved specifically in placental mammals from duplications of SelW and GPx3, respectively, and GPx6 lost Sec several times independently. Bony fishes were characterized by duplications of several selenoprotein families (GPx1, GPx3, GPx4, Dio3, MsrB1, SelJ, SelO, SelT, SelU1, and SelW2). Finally, we report identification of new isoforms for several selenoproteins and describe unusually conserved selenoprotein pseudogenes.

Conclusions/significance: This analysis represents the first comprehensive survey of the vertebrate and mammal selenoproteomes, and depicts their evolution along lineages. It also provides a wealth of information on these selenoproteins and their forms.

Show MeSH
SECIS elements of SelM and SelO.Multiple sequence alignment of SelM (A) and SelO (B) SECIS elements. Critical regions are marked in red.
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pone-0033066-g006: SECIS elements of SelM and SelO.Multiple sequence alignment of SelM (A) and SelO (B) SECIS elements. Critical regions are marked in red.

Mentions: The SECIS element is present in all eukaryotic selenoprotein genes and is the fundamental signal for Sec insertion. While the overall stem-loop structure of the SECIS element is critical to its function, several especially important regions (and bases) have been identified. First, the base of the main stem has non-Watson-Crick interacting bases, known as the Quartet, or the core, including the invariant GA/GA pairs [5], [57], [58]. Next, in the apical loop, two unpaired bases are important for function, although their exact role is not known. In most cases, these two bases are AA. A comprehensive analysis of vertebrate SECIS elements showed that, as expected, almost all examined SECIS elements have the GA/GA quartet and AA in the apical loop. The exception included two selenoproteins, SelM and SelO, in which we found CC in the apical loop (Figure 6). The CC in SelM SECIS elements was only found in placental mammals, while all other vertebrates had AA. In SelO SECIS elements, the CC sequence was found in all mammals and in no other species. Thus, it appears that the CC forms of SECIS elements evolved specifically in mammals. Further analysis did not show any significant features that correlate with the presence of CC pattern.


Composition and evolution of the vertebrate and mammalian selenoproteomes.

Mariotti M, Ridge PG, Zhang Y, Lobanov AV, Pringle TH, Guigo R, Hatfield DL, Gladyshev VN - PLoS ONE (2012)

SECIS elements of SelM and SelO.Multiple sequence alignment of SelM (A) and SelO (B) SECIS elements. Critical regions are marked in red.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3316567&req=5

pone-0033066-g006: SECIS elements of SelM and SelO.Multiple sequence alignment of SelM (A) and SelO (B) SECIS elements. Critical regions are marked in red.
Mentions: The SECIS element is present in all eukaryotic selenoprotein genes and is the fundamental signal for Sec insertion. While the overall stem-loop structure of the SECIS element is critical to its function, several especially important regions (and bases) have been identified. First, the base of the main stem has non-Watson-Crick interacting bases, known as the Quartet, or the core, including the invariant GA/GA pairs [5], [57], [58]. Next, in the apical loop, two unpaired bases are important for function, although their exact role is not known. In most cases, these two bases are AA. A comprehensive analysis of vertebrate SECIS elements showed that, as expected, almost all examined SECIS elements have the GA/GA quartet and AA in the apical loop. The exception included two selenoproteins, SelM and SelO, in which we found CC in the apical loop (Figure 6). The CC in SelM SECIS elements was only found in placental mammals, while all other vertebrates had AA. In SelO SECIS elements, the CC sequence was found in all mammals and in no other species. Thus, it appears that the CC forms of SECIS elements evolved specifically in mammals. Further analysis did not show any significant features that correlate with the presence of CC pattern.

Bottom Line: In total, we detected 45 selenoprotein subfamilies. 28 of them were found in mammals, and 41 in bony fishes.Mammalian thioredoxin reductase 1 and thioredoxin-glutathione reductase evolved from an ancestral glutaredoxin-domain containing enzyme, still present in fish.It also provides a wealth of information on these selenoproteins and their forms.

View Article: PubMed Central - PubMed

Affiliation: Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, United States of America.

ABSTRACT

Background: Selenium is an essential trace element in mammals due to its presence in proteins in the form of selenocysteine (Sec). Human genome codes for 25 Sec-containing protein genes, and mouse and rat genomes for 24.

Methodology/principal findings: We characterized the selenoproteomes of 44 sequenced vertebrates by applying gene prediction and phylogenetic reconstruction methods, supplemented with the analyses of gene structures, alternative splicing isoforms, untranslated regions, SECIS elements, and pseudogenes. In total, we detected 45 selenoprotein subfamilies. 28 of them were found in mammals, and 41 in bony fishes. We define the ancestral vertebrate (28 proteins) and mammalian (25 proteins) selenoproteomes, and describe how they evolved along lineages through gene duplication (20 events), gene loss (10 events) and replacement of Sec with cysteine (12 events). We show that an intronless selenophosphate synthetase 2 gene evolved in early mammals and replaced functionally the original multiexon gene in placental mammals, whereas both genes remain in marsupials. Mammalian thioredoxin reductase 1 and thioredoxin-glutathione reductase evolved from an ancestral glutaredoxin-domain containing enzyme, still present in fish. Selenoprotein V and GPx6 evolved specifically in placental mammals from duplications of SelW and GPx3, respectively, and GPx6 lost Sec several times independently. Bony fishes were characterized by duplications of several selenoprotein families (GPx1, GPx3, GPx4, Dio3, MsrB1, SelJ, SelO, SelT, SelU1, and SelW2). Finally, we report identification of new isoforms for several selenoproteins and describe unusually conserved selenoprotein pseudogenes.

Conclusions/significance: This analysis represents the first comprehensive survey of the vertebrate and mammal selenoproteomes, and depicts their evolution along lineages. It also provides a wealth of information on these selenoproteins and their forms.

Show MeSH