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Characterization of the definitive classical calpain family of vertebrates using phylogenetic, evolutionary and expression analyses.

Macqueen DJ, Wilcox AH - Open Biol (2014)

Bottom Line: We reveal that while all vertebrate classical calpains have been subject to persistent purifying selection during evolution, the degree and nature of selective pressure has often been lineage-dependent.This highlighted systematic divergence in expression across vertebrate taxa, with most classic calpain genes from fish and amphibians having more extensive tissue distribution than in amniotes.Our data suggest that classical calpain functions have frequently diverged during vertebrate evolution and challenge the ongoing value of the established system of classifying calpains by expression.

View Article: PubMed Central - PubMed

Affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK.

ABSTRACT
The calpains are a superfamily of proteases with extensive relevance to human health and welfare. Vast research attention is given to the vertebrate 'classical' subfamily, making it surprising that the evolutionary origins, distribution and relationships of these genes is poorly characterized. Consequently, there exists uncertainty about the conservation of gene family structure, function and expression that has been principally defined from work with mammals. Here, more than 200 vertebrate classical calpains were incorporated in phylogenetic analyses spanning an unprecedented range of taxa, including jawless and cartilaginous fish. We demonstrate that the common vertebrate ancestor had at least six classical calpains, including a single gene that gave rise to CAPN11, 1, 2 and 8 in the early jawed fish lineage, plus CAPN3, 9, 12, 13 and a novel calpain gene, hereafter named CAPN17. We reveal that while all vertebrate classical calpains have been subject to persistent purifying selection during evolution, the degree and nature of selective pressure has often been lineage-dependent. The tissue expression of the complete classic calpain family was assessed in representative teleost fish, amphibians, reptiles and mammals. This highlighted systematic divergence in expression across vertebrate taxa, with most classic calpain genes from fish and amphibians having more extensive tissue distribution than in amniotes. Our data suggest that classical calpain functions have frequently diverged during vertebrate evolution and challenge the ongoing value of the established system of classifying calpains by expression.

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The mRNA expression of complete classical calpain gene systems in adult tissues of four vertebrate species. (a) Zebrafish, (b) African clawed frog, (c) anole lizard, (d) pig. Data are shown in the style of a Northern dot blot, but are derived from qPCR data normalized to the expression of rps13. Phylogenetic trees indicate the relationships of the classical calpain genes. When duplicated calpain family members are present, a superscript number is provided for each copy and referred to in figure 1 and the electronic supplementary material, table S1.
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RSOB130219F5: The mRNA expression of complete classical calpain gene systems in adult tissues of four vertebrate species. (a) Zebrafish, (b) African clawed frog, (c) anole lizard, (d) pig. Data are shown in the style of a Northern dot blot, but are derived from qPCR data normalized to the expression of rps13. Phylogenetic trees indicate the relationships of the classical calpain genes. When duplicated calpain family members are present, a superscript number is provided for each copy and referred to in figure 1 and the electronic supplementary material, table S1.

Mentions: We profiled the mRNA expression of every classical calpain family member in multiple adult tissues from four vertebrate species separated by more than 300 Myr [34] (figure 5). Seven of the eight studied tissues were common across species. The data provide an unprecedented overview of classical calpain expression across vertebrate taxa. However, differences in expression may reflect ontogenic effects rather than true evolutionary divergence. Accordingly, we do not focus extensively on specific data, instead attempting to draw out broader evolutionary patterns.FigureĀ 5.


Characterization of the definitive classical calpain family of vertebrates using phylogenetic, evolutionary and expression analyses.

Macqueen DJ, Wilcox AH - Open Biol (2014)

The mRNA expression of complete classical calpain gene systems in adult tissues of four vertebrate species. (a) Zebrafish, (b) African clawed frog, (c) anole lizard, (d) pig. Data are shown in the style of a Northern dot blot, but are derived from qPCR data normalized to the expression of rps13. Phylogenetic trees indicate the relationships of the classical calpain genes. When duplicated calpain family members are present, a superscript number is provided for each copy and referred to in figure 1 and the electronic supplementary material, table S1.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4043111&req=5

RSOB130219F5: The mRNA expression of complete classical calpain gene systems in adult tissues of four vertebrate species. (a) Zebrafish, (b) African clawed frog, (c) anole lizard, (d) pig. Data are shown in the style of a Northern dot blot, but are derived from qPCR data normalized to the expression of rps13. Phylogenetic trees indicate the relationships of the classical calpain genes. When duplicated calpain family members are present, a superscript number is provided for each copy and referred to in figure 1 and the electronic supplementary material, table S1.
Mentions: We profiled the mRNA expression of every classical calpain family member in multiple adult tissues from four vertebrate species separated by more than 300 Myr [34] (figure 5). Seven of the eight studied tissues were common across species. The data provide an unprecedented overview of classical calpain expression across vertebrate taxa. However, differences in expression may reflect ontogenic effects rather than true evolutionary divergence. Accordingly, we do not focus extensively on specific data, instead attempting to draw out broader evolutionary patterns.FigureĀ 5.

Bottom Line: We reveal that while all vertebrate classical calpains have been subject to persistent purifying selection during evolution, the degree and nature of selective pressure has often been lineage-dependent.This highlighted systematic divergence in expression across vertebrate taxa, with most classic calpain genes from fish and amphibians having more extensive tissue distribution than in amniotes.Our data suggest that classical calpain functions have frequently diverged during vertebrate evolution and challenge the ongoing value of the established system of classifying calpains by expression.

View Article: PubMed Central - PubMed

Affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK.

ABSTRACT
The calpains are a superfamily of proteases with extensive relevance to human health and welfare. Vast research attention is given to the vertebrate 'classical' subfamily, making it surprising that the evolutionary origins, distribution and relationships of these genes is poorly characterized. Consequently, there exists uncertainty about the conservation of gene family structure, function and expression that has been principally defined from work with mammals. Here, more than 200 vertebrate classical calpains were incorporated in phylogenetic analyses spanning an unprecedented range of taxa, including jawless and cartilaginous fish. We demonstrate that the common vertebrate ancestor had at least six classical calpains, including a single gene that gave rise to CAPN11, 1, 2 and 8 in the early jawed fish lineage, plus CAPN3, 9, 12, 13 and a novel calpain gene, hereafter named CAPN17. We reveal that while all vertebrate classical calpains have been subject to persistent purifying selection during evolution, the degree and nature of selective pressure has often been lineage-dependent. The tissue expression of the complete classic calpain family was assessed in representative teleost fish, amphibians, reptiles and mammals. This highlighted systematic divergence in expression across vertebrate taxa, with most classic calpain genes from fish and amphibians having more extensive tissue distribution than in amniotes. Our data suggest that classical calpain functions have frequently diverged during vertebrate evolution and challenge the ongoing value of the established system of classifying calpains by expression.

Show MeSH