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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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Phylogenetic tree of the teleost and human s100 gene family. A) 85 fish S100 (bony fishes in red and cartilaginous fishes in orange), 10 lamprey S100 (light-green) with human s100 genes (full set, excluding close relatives [38], light blue) and several representatives of another EF hand family, the troponins as an outgroup (black). B) Fish s100 genes from six teleost species and two cartilaginous fish (Squalus acanthias and Callorhinchus milii) are depicted. Catfish S100I [18] groups with zebrafish S100I (not shown). The Tn_S100T fragment (2nd exon, see Additional File 4) is not included for technical reasons. The colored names indicate fish s100 genes previously published. Stars indicate that the clades downstream of the node are supported by all three methods used for the phylogenetic analysis (NJ, ML and MP). The trees presented were constructed using the NJ method. Bootstrap support (total 10000 replications) is indicated at the major nodes. Scale bar indicates the number of amino acid substitution per site.
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Figure 1: Phylogenetic tree of the teleost and human s100 gene family. A) 85 fish S100 (bony fishes in red and cartilaginous fishes in orange), 10 lamprey S100 (light-green) with human s100 genes (full set, excluding close relatives [38], light blue) and several representatives of another EF hand family, the troponins as an outgroup (black). B) Fish s100 genes from six teleost species and two cartilaginous fish (Squalus acanthias and Callorhinchus milii) are depicted. Catfish S100I [18] groups with zebrafish S100I (not shown). The Tn_S100T fragment (2nd exon, see Additional File 4) is not included for technical reasons. The colored names indicate fish s100 genes previously published. Stars indicate that the clades downstream of the node are supported by all three methods used for the phylogenetic analysis (NJ, ML and MP). The trees presented were constructed using the NJ method. Bootstrap support (total 10000 replications) is indicated at the major nodes. Scale bar indicates the number of amino acid substitution per site.

Mentions: A recursive search strategy in the NCBI and Ensembl databases using the complete repertoire of human s100 genes as reference set, in combination with retrieval of automated ortholog predictions (see Methods) uncovered a total of 97 fish s100 genes. Fourteen s100 genes each were identified for zebrafish and Takifugu rubripes, and thirteen genes each for three-spined stickleback, medaka, and Tetraodon nigroviridis. In addition, fourteen s100 genes were found in EST libraries of another teleost, Salmo salar. All of these genes are novel, with the exception of one zebrafish and one Takifugu gene (see Figure 1). We believe that the result of the data mining approach used reflects the total repertoire of the s100 genes in the cases of Danio rerio, Gasterosteus aculeatus, Oryzias latipes, Tetraodon nigroviridis and Takifugu rubripes. In the case of Salmo salar several transcripts were found for each gene predicted, so that the repertoire reported here may approximate the complete S100 family present in this species.


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

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

Phylogenetic tree of the teleost and human s100 gene family. A) 85 fish S100 (bony fishes in red and cartilaginous fishes in orange), 10 lamprey S100 (light-green) with human s100 genes (full set, excluding close relatives [38], light blue) and several representatives of another EF hand family, the troponins as an outgroup (black). B) Fish s100 genes from six teleost species and two cartilaginous fish (Squalus acanthias and Callorhinchus milii) are depicted. Catfish S100I [18] groups with zebrafish S100I (not shown). The Tn_S100T fragment (2nd exon, see Additional File 4) is not included for technical reasons. The colored names indicate fish s100 genes previously published. Stars indicate that the clades downstream of the node are supported by all three methods used for the phylogenetic analysis (NJ, ML and MP). The trees presented were constructed using the NJ method. Bootstrap support (total 10000 replications) is indicated at the major nodes. Scale bar indicates the number of amino acid substitution per site.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Phylogenetic tree of the teleost and human s100 gene family. A) 85 fish S100 (bony fishes in red and cartilaginous fishes in orange), 10 lamprey S100 (light-green) with human s100 genes (full set, excluding close relatives [38], light blue) and several representatives of another EF hand family, the troponins as an outgroup (black). B) Fish s100 genes from six teleost species and two cartilaginous fish (Squalus acanthias and Callorhinchus milii) are depicted. Catfish S100I [18] groups with zebrafish S100I (not shown). The Tn_S100T fragment (2nd exon, see Additional File 4) is not included for technical reasons. The colored names indicate fish s100 genes previously published. Stars indicate that the clades downstream of the node are supported by all three methods used for the phylogenetic analysis (NJ, ML and MP). The trees presented were constructed using the NJ method. Bootstrap support (total 10000 replications) is indicated at the major nodes. Scale bar indicates the number of amino acid substitution per site.
Mentions: A recursive search strategy in the NCBI and Ensembl databases using the complete repertoire of human s100 genes as reference set, in combination with retrieval of automated ortholog predictions (see Methods) uncovered a total of 97 fish s100 genes. Fourteen s100 genes each were identified for zebrafish and Takifugu rubripes, and thirteen genes each for three-spined stickleback, medaka, and Tetraodon nigroviridis. In addition, fourteen s100 genes were found in EST libraries of another teleost, Salmo salar. All of these genes are novel, with the exception of one zebrafish and one Takifugu gene (see Figure 1). We believe that the result of the data mining approach used reflects the total repertoire of the s100 genes in the cases of Danio rerio, Gasterosteus aculeatus, Oryzias latipes, Tetraodon nigroviridis and Takifugu rubripes. In the case of Salmo salar several transcripts were found for each gene predicted, so that the repertoire reported here may approximate the complete S100 family present in this species.

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
Related in: MedlinePlus