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Structural and functional diversification in the teleost S100 family of calcium-binding proteins.

Kraemer AM, Saraiva LR, Korsching SI - BMC Evol. Biol. (2008)

Bottom Line: Individual species feature distinctive subsets of thirteen to fourteen genes that result from local gene duplications and gene losses.Several S100 family members are found in jawless fish already, but none of them are clear orthologs of cartilaginous or bony fish s100 genes.Accordingly, our findings provide an excellent basis for future studies of the functions and interaction partners of s100 genes and finally their role in diseases, using the zebrafish as a model organism.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Genetics, University of Cologne, Zuelpicher Strasse 47, 50674 Cologne, Germany. a.kraemer@gmx.com

ABSTRACT

Background: Among the EF-Hand calcium-binding proteins the subgroup of S100 proteins constitute a large family with numerous and diverse functions in calcium-mediated signaling. The evolutionary origin of this family is still uncertain and most studies have examined mammalian family members.

Results: We have performed an extensive search in several teleost genomes to establish the s100 gene family in fish. We report that the teleost S100 repertoire comprises fourteen different subfamilies which show remarkable similarity across six divergent teleost species. Individual species feature distinctive subsets of thirteen to fourteen genes that result from local gene duplications and gene losses. Eight of the fourteen S100 subfamilies are unique for teleosts, while six are shared with mammalian species and three of those even with cartilaginous fish. Several S100 family members are found in jawless fish already, but none of them are clear orthologs of cartilaginous or bony fish s100 genes. All teleost s100 genes show the expected structural features and are subject to strong negative selection. Many aspects of the genomic arrangement and location of mammalian s100 genes are retained in the teleost s100 gene family, including a completely conserved intron/exon border between the two EF hands. Zebrafish s100 genes exhibit highly specific and characteristic expression patterns, showing both redundancy and divergence in their cellular expression. In larval tissue expression is often restricted to specific cell types like keratinocytes, hair cells, ionocytes and olfactory receptor neurons as demonstrated by in situ hybridization.

Conclusion: The origin of the S100 family predates at least the segregation of jawed from jawless fish and some extant family members predate the divergence of bony from cartilaginous fish. Despite a complex pattern of gene gains and losses the total repertoire size is remarkably constant between species. On the expression level the teleost S100 proteins can serve as precise markers for several different cell types. At least some of their functions may be related to those of their counterparts in mammals. Accordingly, our findings provide an excellent basis for future studies of the functions and interaction partners of s100 genes and finally their role in diseases, using the zebrafish as a model organism.

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Estimated minimal evolutionary age of S100 family members. Open rectangles represent the gene gain events in each lineage, and black boxes represent the gene loss events. Inside each box is the name of the respective gene(s). A duplication event leading to a gene pair is indicated by a common rectangle. The major phylogenetic transitions are indicated: bo/nobo, bony fish/cartilaginous fish; ac/sa, actinopterygian/sarcopterygian split; os/neo, ostariophysii/neoteleostei segregation. The maximum parsimony principle was followed for construction of this scheme, i.e. minimal gene losses and gene gains were assumed. Thus gene gains are depicted at the last possible stage before additional gains would become necessary for explanation, but may in fact have occurred earlier, accompanied by gene loss in some lineages.
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Figure 2: Estimated minimal evolutionary age of S100 family members. Open rectangles represent the gene gain events in each lineage, and black boxes represent the gene loss events. Inside each box is the name of the respective gene(s). A duplication event leading to a gene pair is indicated by a common rectangle. The major phylogenetic transitions are indicated: bo/nobo, bony fish/cartilaginous fish; ac/sa, actinopterygian/sarcopterygian split; os/neo, ostariophysii/neoteleostei segregation. The maximum parsimony principle was followed for construction of this scheme, i.e. minimal gene losses and gene gains were assumed. Thus gene gains are depicted at the last possible stage before additional gains would become necessary for explanation, but may in fact have occurred earlier, accompanied by gene loss in some lineages.

Mentions: All teleost-restricted genes that contain both a zebrafish and another teleost representative (S100I, S, T, U, V, W) should have been present at least in the most recent common ancestor (MRCA) of Neoteleostei and Ostariophysii (zebrafish lineage diverged early from the more modern neoteleosts, to which the other four species analyzed here belong, salmon takes an intermediate position, closer to the Neoteleostei than zebrafish). Thus, the partial absence of several genes, e.g. S100I in pufferfish (cf. Figure 1) suggests a partial loss of these genes in the pufferfish family (cf. Figure 2) although it cannot be ruled out with certainty that some apparent gene losses are actually caused by inadequacies of the currently available databases. Other examples for restricted loss in some teleost species concern S100Q, U, V and the gene pair S100S/T (Figure 2, cf. Figure 1B).


Structural and functional diversification in the teleost S100 family of calcium-binding proteins.

Kraemer AM, Saraiva LR, Korsching SI - BMC Evol. Biol. (2008)

Estimated minimal evolutionary age of S100 family members. Open rectangles represent the gene gain events in each lineage, and black boxes represent the gene loss events. Inside each box is the name of the respective gene(s). A duplication event leading to a gene pair is indicated by a common rectangle. The major phylogenetic transitions are indicated: bo/nobo, bony fish/cartilaginous fish; ac/sa, actinopterygian/sarcopterygian split; os/neo, ostariophysii/neoteleostei segregation. The maximum parsimony principle was followed for construction of this scheme, i.e. minimal gene losses and gene gains were assumed. Thus gene gains are depicted at the last possible stage before additional gains would become necessary for explanation, but may in fact have occurred earlier, accompanied by gene loss in some lineages.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2266712&req=5

Figure 2: Estimated minimal evolutionary age of S100 family members. Open rectangles represent the gene gain events in each lineage, and black boxes represent the gene loss events. Inside each box is the name of the respective gene(s). A duplication event leading to a gene pair is indicated by a common rectangle. The major phylogenetic transitions are indicated: bo/nobo, bony fish/cartilaginous fish; ac/sa, actinopterygian/sarcopterygian split; os/neo, ostariophysii/neoteleostei segregation. The maximum parsimony principle was followed for construction of this scheme, i.e. minimal gene losses and gene gains were assumed. Thus gene gains are depicted at the last possible stage before additional gains would become necessary for explanation, but may in fact have occurred earlier, accompanied by gene loss in some lineages.
Mentions: All teleost-restricted genes that contain both a zebrafish and another teleost representative (S100I, S, T, U, V, W) should have been present at least in the most recent common ancestor (MRCA) of Neoteleostei and Ostariophysii (zebrafish lineage diverged early from the more modern neoteleosts, to which the other four species analyzed here belong, salmon takes an intermediate position, closer to the Neoteleostei than zebrafish). Thus, the partial absence of several genes, e.g. S100I in pufferfish (cf. Figure 1) suggests a partial loss of these genes in the pufferfish family (cf. Figure 2) although it cannot be ruled out with certainty that some apparent gene losses are actually caused by inadequacies of the currently available databases. Other examples for restricted loss in some teleost species concern S100Q, U, V and the gene pair S100S/T (Figure 2, cf. Figure 1B).

Bottom Line: Individual species feature distinctive subsets of thirteen to fourteen genes that result from local gene duplications and gene losses.Several S100 family members are found in jawless fish already, but none of them are clear orthologs of cartilaginous or bony fish s100 genes.Accordingly, our findings provide an excellent basis for future studies of the functions and interaction partners of s100 genes and finally their role in diseases, using the zebrafish as a model organism.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Genetics, University of Cologne, Zuelpicher Strasse 47, 50674 Cologne, Germany. a.kraemer@gmx.com

ABSTRACT

Background: Among the EF-Hand calcium-binding proteins the subgroup of S100 proteins constitute a large family with numerous and diverse functions in calcium-mediated signaling. The evolutionary origin of this family is still uncertain and most studies have examined mammalian family members.

Results: We have performed an extensive search in several teleost genomes to establish the s100 gene family in fish. We report that the teleost S100 repertoire comprises fourteen different subfamilies which show remarkable similarity across six divergent teleost species. Individual species feature distinctive subsets of thirteen to fourteen genes that result from local gene duplications and gene losses. Eight of the fourteen S100 subfamilies are unique for teleosts, while six are shared with mammalian species and three of those even with cartilaginous fish. Several S100 family members are found in jawless fish already, but none of them are clear orthologs of cartilaginous or bony fish s100 genes. All teleost s100 genes show the expected structural features and are subject to strong negative selection. Many aspects of the genomic arrangement and location of mammalian s100 genes are retained in the teleost s100 gene family, including a completely conserved intron/exon border between the two EF hands. Zebrafish s100 genes exhibit highly specific and characteristic expression patterns, showing both redundancy and divergence in their cellular expression. In larval tissue expression is often restricted to specific cell types like keratinocytes, hair cells, ionocytes and olfactory receptor neurons as demonstrated by in situ hybridization.

Conclusion: The origin of the S100 family predates at least the segregation of jawed from jawless fish and some extant family members predate the divergence of bony from cartilaginous fish. Despite a complex pattern of gene gains and losses the total repertoire size is remarkably constant between species. On the expression level the teleost S100 proteins can serve as precise markers for several different cell types. At least some of their functions may be related to those of their counterparts in mammals. Accordingly, our findings provide an excellent basis for future studies of the functions and interaction partners of s100 genes and finally their role in diseases, using the zebrafish as a model organism.

Show MeSH