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Molecular evolution and functional divergence of the Ca(2+) sensor protein in store-operated Ca(2+) entry: stromal interaction molecule.

Cai X - PLoS ONE (2007)

Bottom Line: Human STIMs and invertebrate STIM share several functionally important protein domains, but diverge significantly in the C-terminus.STIMs were subsequently subjected to one round of gene duplication as early as in the Euteleostomi lineage in vertebrates, with a second round of fish-specific gene duplication.After duplication, STIM-1 and STIM-2 molecules appeared to have undergone purifying selection indicating strong evolutionary constraints within each group.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell Biology, Duke University Medical Center, Durham, North Carolina, United States of America. xinjiang.cai@duke.edu

ABSTRACT
Receptor-mediated Ca(2+) signaling in many non-excitable cells initially induces Ca(2+) release from intracellular Ca(2+) stores, followed by Ca(2+) influx across the plasma membrane. Recent findings have suggested that stromal interaction molecules (STIMs) function as the Ca(2+) sensor to detect changes of Ca(2+) content in the intracellular Ca(2+) stores. Human STIMs and invertebrate STIM share several functionally important protein domains, but diverge significantly in the C-terminus. To better understand the evolutionary significance of STIM activity, phylogenetic analysis of the STIM protein family was conducted after extensive database searching. Results from phylogeny and sequence analysis revealed early adaptation of the C-terminal divergent domains in Urochordata, before the expansion of STIMs in Vertebrata. STIMs were subsequently subjected to one round of gene duplication as early as in the Euteleostomi lineage in vertebrates, with a second round of fish-specific gene duplication. After duplication, STIM-1 and STIM-2 molecules appeared to have undergone purifying selection indicating strong evolutionary constraints within each group. Furthermore, sequence analysis of the EF-hand Ca(2+) binding domain and the SAM domain, together with functional divergence studies, identified critical regions/residues likely underlying functional changes, and provided evidence for the hypothesis that STIM-1 and STIM-2 might have developed distinct functional properties after duplication.

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Evolution of the protein domains in the STIM protein family.Schematic representations of protein domains of representative STIM molecules based on phylogeny of bilaterian animals [51]. The proline-rich domain and the lysine-rich domain of STIM molecules, which are absent in worms, insects and sea urchin, first appeared in Urochordata, as shown in C. intestinalis. Duplication of STIM molecules speculated to have occurred after Cephalochordata/Urochordata divergence is indicated with “?”. Fish-specific duplication of STIMs (Fig. 1) is not illustrated here. C, C-terminus; K-rich, lysine-rich domain; N, N-terminus; P-rich, proline-rich domain; TMS, transmembrane segment.
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pone-0000609-g002: Evolution of the protein domains in the STIM protein family.Schematic representations of protein domains of representative STIM molecules based on phylogeny of bilaterian animals [51]. The proline-rich domain and the lysine-rich domain of STIM molecules, which are absent in worms, insects and sea urchin, first appeared in Urochordata, as shown in C. intestinalis. Duplication of STIM molecules speculated to have occurred after Cephalochordata/Urochordata divergence is indicated with “?”. Fish-specific duplication of STIMs (Fig. 1) is not illustrated here. C, C-terminus; K-rich, lysine-rich domain; N, N-terminus; P-rich, proline-rich domain; TMS, transmembrane segment.

Mentions: Here, by extensive database searching, 40 nonredundant STIM sequences were identified from 22 species analyzed in this study (Table S1 in Supplementary Information), including sequences from Echinodermata Strongylocentrotus purpuratus, Urochordata Ciona intestinalis, and several nonmammalian Vertebrata species. Phylogenetic trees constructed with maximum likelihood (Fig. 1), maximum parsimony, and neighbor-joining methods as well as weighted neighbor-joining analysis (data not shown) were compared to infer the congruent phylogeny. The identical overall tree topologies generated from these different molecular phylogenetic approaches indicated consistent and reliable results for evolutionary relationships of the STIM protein family. Homologues of STIM-1 and -2 are present as early as in bony fishes (Takifugu rubripes, Tetraodon nigroviridis, Danio rerio), while C. intestinalis and S. purpuratus appear to contain only one copy of STIM molecule in each genome (Figs. 1 and 2, and Table S1). C. intestinalis has been shown to comprise single copies of many vertebrate gene families [20], [23] likely arising from hypothesized large-scale genome duplications in vertebrates diverging from Urochordata and Cephalochordata [24]. Thus, gene duplication of the STIM family appeared to have occurred as early as in Euteleostomi lineage to give rise to the two major STIM branches in vertebrates. Orai molecules also underwent a round of gene duplication at the early stage of vertebrates [3]. Duplication of STIM and Orai proteins, and possibly, other subunits, might have evolved to fit the adaptation of SOC entry into more advanced vertebrate physiology.


Molecular evolution and functional divergence of the Ca(2+) sensor protein in store-operated Ca(2+) entry: stromal interaction molecule.

Cai X - PLoS ONE (2007)

Evolution of the protein domains in the STIM protein family.Schematic representations of protein domains of representative STIM molecules based on phylogeny of bilaterian animals [51]. The proline-rich domain and the lysine-rich domain of STIM molecules, which are absent in worms, insects and sea urchin, first appeared in Urochordata, as shown in C. intestinalis. Duplication of STIM molecules speculated to have occurred after Cephalochordata/Urochordata divergence is indicated with “?”. Fish-specific duplication of STIMs (Fig. 1) is not illustrated here. C, C-terminus; K-rich, lysine-rich domain; N, N-terminus; P-rich, proline-rich domain; TMS, transmembrane segment.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC1904252&req=5

pone-0000609-g002: Evolution of the protein domains in the STIM protein family.Schematic representations of protein domains of representative STIM molecules based on phylogeny of bilaterian animals [51]. The proline-rich domain and the lysine-rich domain of STIM molecules, which are absent in worms, insects and sea urchin, first appeared in Urochordata, as shown in C. intestinalis. Duplication of STIM molecules speculated to have occurred after Cephalochordata/Urochordata divergence is indicated with “?”. Fish-specific duplication of STIMs (Fig. 1) is not illustrated here. C, C-terminus; K-rich, lysine-rich domain; N, N-terminus; P-rich, proline-rich domain; TMS, transmembrane segment.
Mentions: Here, by extensive database searching, 40 nonredundant STIM sequences were identified from 22 species analyzed in this study (Table S1 in Supplementary Information), including sequences from Echinodermata Strongylocentrotus purpuratus, Urochordata Ciona intestinalis, and several nonmammalian Vertebrata species. Phylogenetic trees constructed with maximum likelihood (Fig. 1), maximum parsimony, and neighbor-joining methods as well as weighted neighbor-joining analysis (data not shown) were compared to infer the congruent phylogeny. The identical overall tree topologies generated from these different molecular phylogenetic approaches indicated consistent and reliable results for evolutionary relationships of the STIM protein family. Homologues of STIM-1 and -2 are present as early as in bony fishes (Takifugu rubripes, Tetraodon nigroviridis, Danio rerio), while C. intestinalis and S. purpuratus appear to contain only one copy of STIM molecule in each genome (Figs. 1 and 2, and Table S1). C. intestinalis has been shown to comprise single copies of many vertebrate gene families [20], [23] likely arising from hypothesized large-scale genome duplications in vertebrates diverging from Urochordata and Cephalochordata [24]. Thus, gene duplication of the STIM family appeared to have occurred as early as in Euteleostomi lineage to give rise to the two major STIM branches in vertebrates. Orai molecules also underwent a round of gene duplication at the early stage of vertebrates [3]. Duplication of STIM and Orai proteins, and possibly, other subunits, might have evolved to fit the adaptation of SOC entry into more advanced vertebrate physiology.

Bottom Line: Human STIMs and invertebrate STIM share several functionally important protein domains, but diverge significantly in the C-terminus.STIMs were subsequently subjected to one round of gene duplication as early as in the Euteleostomi lineage in vertebrates, with a second round of fish-specific gene duplication.After duplication, STIM-1 and STIM-2 molecules appeared to have undergone purifying selection indicating strong evolutionary constraints within each group.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell Biology, Duke University Medical Center, Durham, North Carolina, United States of America. xinjiang.cai@duke.edu

ABSTRACT
Receptor-mediated Ca(2+) signaling in many non-excitable cells initially induces Ca(2+) release from intracellular Ca(2+) stores, followed by Ca(2+) influx across the plasma membrane. Recent findings have suggested that stromal interaction molecules (STIMs) function as the Ca(2+) sensor to detect changes of Ca(2+) content in the intracellular Ca(2+) stores. Human STIMs and invertebrate STIM share several functionally important protein domains, but diverge significantly in the C-terminus. To better understand the evolutionary significance of STIM activity, phylogenetic analysis of the STIM protein family was conducted after extensive database searching. Results from phylogeny and sequence analysis revealed early adaptation of the C-terminal divergent domains in Urochordata, before the expansion of STIMs in Vertebrata. STIMs were subsequently subjected to one round of gene duplication as early as in the Euteleostomi lineage in vertebrates, with a second round of fish-specific gene duplication. After duplication, STIM-1 and STIM-2 molecules appeared to have undergone purifying selection indicating strong evolutionary constraints within each group. Furthermore, sequence analysis of the EF-hand Ca(2+) binding domain and the SAM domain, together with functional divergence studies, identified critical regions/residues likely underlying functional changes, and provided evidence for the hypothesis that STIM-1 and STIM-2 might have developed distinct functional properties after duplication.

Show MeSH