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Evolutionary genomics reveals lineage-specific gene loss and rapid evolution of a sperm-specific ion channel complex: CatSpers and CatSperbeta.

Cai X, Clapham DE - PLoS ONE (2008)

Bottom Line: The development of the CatSper channel complex with four CatSpers and CatSperbeta originated as early as primitive metazoans such as the Cnidarian Nematostella vectensis.The CatSper channel complex underwent rapid evolution and functional divergence, while distinct evolutionary constraints appear to have acted on different domains and specific sites of the four CatSper genes.These results reveal unique evolutionary characteristics of sperm-specific Ca2+ channels and their adaptation to sperm biology through metazoan evolution.

View Article: PubMed Central - PubMed

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

ABSTRACT
The mammalian CatSper ion channel family consists of four sperm-specific voltage-gated Ca2+ channels that are crucial for sperm hyperactivation and male fertility. All four CatSper subunits are believed to assemble into a heteromultimeric channel complex, together with an auxiliary subunit, CatSperbeta. Here, we report a comprehensive comparative genomics study and evolutionary analysis of CatSpers and CatSperbeta, with important correlation to physiological significance of molecular evolution of the CatSper channel complex. The development of the CatSper channel complex with four CatSpers and CatSperbeta originated as early as primitive metazoans such as the Cnidarian Nematostella vectensis. Comparative genomics revealed extensive lineage-specific gene loss of all four CatSpers and CatSperbeta through metazoan evolution, especially in vertebrates. The CatSper channel complex underwent rapid evolution and functional divergence, while distinct evolutionary constraints appear to have acted on different domains and specific sites of the four CatSper genes. These results reveal unique evolutionary characteristics of sperm-specific Ca2+ channels and their adaptation to sperm biology through metazoan evolution.

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Conservation of the putative pore domain of CatSpers from invertebrate and vertebrate species.The putative pore regions of CatSpers from selected species, corresponding to amino acids 210–239 of human CatSper3 (GenBank Accession No., NP_821138.1), were aligned and manually edited to improve alignments. Invertebrate CatSpers are indicated with white rectangular bars and vertebrate CatSpers with gray rectangular bars. The key aspartate residue of CatSpers is overlined with an asterisk symbol. For abbreviations, please refer to the Fig. 1 legend.
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pone-0003569-g002: Conservation of the putative pore domain of CatSpers from invertebrate and vertebrate species.The putative pore regions of CatSpers from selected species, corresponding to amino acids 210–239 of human CatSper3 (GenBank Accession No., NP_821138.1), were aligned and manually edited to improve alignments. Invertebrate CatSpers are indicated with white rectangular bars and vertebrate CatSpers with gray rectangular bars. The key aspartate residue of CatSpers is overlined with an asterisk symbol. For abbreviations, please refer to the Fig. 1 legend.

Mentions: The transmembrane segments (TMS) and the putative pore region of human and mouse CatSpers are highly conserved [17]. Sequence alignment of CatSper sequences identified in this study showed similar observations across invertebrate and vertebrate species (Fig. 2). The key aspartate residue of CatSpers, presumably corresponding to the highly conserved glutamate residues (or occasionally aspartate residues) in the pore loop regions that underlie Ca2+ selectivity in many CaV channels [46], is absolutely conserved (Fig. 2).


Evolutionary genomics reveals lineage-specific gene loss and rapid evolution of a sperm-specific ion channel complex: CatSpers and CatSperbeta.

Cai X, Clapham DE - PLoS ONE (2008)

Conservation of the putative pore domain of CatSpers from invertebrate and vertebrate species.The putative pore regions of CatSpers from selected species, corresponding to amino acids 210–239 of human CatSper3 (GenBank Accession No., NP_821138.1), were aligned and manually edited to improve alignments. Invertebrate CatSpers are indicated with white rectangular bars and vertebrate CatSpers with gray rectangular bars. The key aspartate residue of CatSpers is overlined with an asterisk symbol. For abbreviations, please refer to the Fig. 1 legend.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2572835&req=5

pone-0003569-g002: Conservation of the putative pore domain of CatSpers from invertebrate and vertebrate species.The putative pore regions of CatSpers from selected species, corresponding to amino acids 210–239 of human CatSper3 (GenBank Accession No., NP_821138.1), were aligned and manually edited to improve alignments. Invertebrate CatSpers are indicated with white rectangular bars and vertebrate CatSpers with gray rectangular bars. The key aspartate residue of CatSpers is overlined with an asterisk symbol. For abbreviations, please refer to the Fig. 1 legend.
Mentions: The transmembrane segments (TMS) and the putative pore region of human and mouse CatSpers are highly conserved [17]. Sequence alignment of CatSper sequences identified in this study showed similar observations across invertebrate and vertebrate species (Fig. 2). The key aspartate residue of CatSpers, presumably corresponding to the highly conserved glutamate residues (or occasionally aspartate residues) in the pore loop regions that underlie Ca2+ selectivity in many CaV channels [46], is absolutely conserved (Fig. 2).

Bottom Line: The development of the CatSper channel complex with four CatSpers and CatSperbeta originated as early as primitive metazoans such as the Cnidarian Nematostella vectensis.The CatSper channel complex underwent rapid evolution and functional divergence, while distinct evolutionary constraints appear to have acted on different domains and specific sites of the four CatSper genes.These results reveal unique evolutionary characteristics of sperm-specific Ca2+ channels and their adaptation to sperm biology through metazoan evolution.

View Article: PubMed Central - PubMed

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

ABSTRACT
The mammalian CatSper ion channel family consists of four sperm-specific voltage-gated Ca2+ channels that are crucial for sperm hyperactivation and male fertility. All four CatSper subunits are believed to assemble into a heteromultimeric channel complex, together with an auxiliary subunit, CatSperbeta. Here, we report a comprehensive comparative genomics study and evolutionary analysis of CatSpers and CatSperbeta, with important correlation to physiological significance of molecular evolution of the CatSper channel complex. The development of the CatSper channel complex with four CatSpers and CatSperbeta originated as early as primitive metazoans such as the Cnidarian Nematostella vectensis. Comparative genomics revealed extensive lineage-specific gene loss of all four CatSpers and CatSperbeta through metazoan evolution, especially in vertebrates. The CatSper channel complex underwent rapid evolution and functional divergence, while distinct evolutionary constraints appear to have acted on different domains and specific sites of the four CatSper genes. These results reveal unique evolutionary characteristics of sperm-specific Ca2+ channels and their adaptation to sperm biology through metazoan evolution.

Show MeSH
Related in: MedlinePlus