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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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Phylogenetic tree of the 6-TMS bacterial ion channel family.A bootstrapped maximum parsimony tree was constructed with a NaV channel homologue in choanoflagellates (MbrNaV-S3L) as an outgroup. Two CatSper sequences, NveCatSper2 and HsaCatSper2, and two putative CaV channel homologues, MbrCaVS5-1 and NveCaV-S17, are also included. The position of the key aspartate residue in the pore region of two bacterial proteins is marked by gray circles. Bootstrap values of >50 are shown at corresponding branches. Each branch of the tree is labeled with the GI numbers in the NCBI protein database for most organisms. NaChBac, NaVSP and NaVPZ channels were functionally characterized previously [36], [61]. Abbreviations: Hsa, H. sapiens; Mbr, M. brevicollis; Nve, N. vectensis.
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pone-0003569-g005: Phylogenetic tree of the 6-TMS bacterial ion channel family.A bootstrapped maximum parsimony tree was constructed with a NaV channel homologue in choanoflagellates (MbrNaV-S3L) as an outgroup. Two CatSper sequences, NveCatSper2 and HsaCatSper2, and two putative CaV channel homologues, MbrCaVS5-1 and NveCaV-S17, are also included. The position of the key aspartate residue in the pore region of two bacterial proteins is marked by gray circles. Bootstrap values of >50 are shown at corresponding branches. Each branch of the tree is labeled with the GI numbers in the NCBI protein database for most organisms. NaChBac, NaVSP and NaVPZ channels were functionally characterized previously [36], [61]. Abbreviations: Hsa, H. sapiens; Mbr, M. brevicollis; Nve, N. vectensis.

Mentions: Our database search did not identify the putative primordial CatSper sequence. It remains possible that the introduction of the primordial, probably distantly related, CatSper channel could be made through horizontal gene transfer between prokaryotes and primitive metazoan species, such as single 6-TMS domain NaV channels NaVBP [19], NaChBac [61], and 11 bacterial NaChBac homologues [36]. All these bacterial NaV channel homologues share a glutamate residue as the key acidic residue in the putative channel pore region [36], in contrast to the key aspartate residue conserved in CatSpers (Fig. 2). We analyzed 40 more bacterial protein sequences (protein cluster CLS1187052), which display high sequence homology and structural similarity to NaChBac. None of these 40 bacterial homologues grouped with CatSper sequences (Fig. 5). However, two (GI No. 56963529 and 134099759) have the key aspartate residue in the putative pore region, and it would be interesting compare their Ca2+-selectivity, voltage-dependence and kinetics with the CatSper channel.


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)

Phylogenetic tree of the 6-TMS bacterial ion channel family.A bootstrapped maximum parsimony tree was constructed with a NaV channel homologue in choanoflagellates (MbrNaV-S3L) as an outgroup. Two CatSper sequences, NveCatSper2 and HsaCatSper2, and two putative CaV channel homologues, MbrCaVS5-1 and NveCaV-S17, are also included. The position of the key aspartate residue in the pore region of two bacterial proteins is marked by gray circles. Bootstrap values of >50 are shown at corresponding branches. Each branch of the tree is labeled with the GI numbers in the NCBI protein database for most organisms. NaChBac, NaVSP and NaVPZ channels were functionally characterized previously [36], [61]. Abbreviations: Hsa, H. sapiens; Mbr, M. brevicollis; Nve, N. vectensis.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2572835&req=5

pone-0003569-g005: Phylogenetic tree of the 6-TMS bacterial ion channel family.A bootstrapped maximum parsimony tree was constructed with a NaV channel homologue in choanoflagellates (MbrNaV-S3L) as an outgroup. Two CatSper sequences, NveCatSper2 and HsaCatSper2, and two putative CaV channel homologues, MbrCaVS5-1 and NveCaV-S17, are also included. The position of the key aspartate residue in the pore region of two bacterial proteins is marked by gray circles. Bootstrap values of >50 are shown at corresponding branches. Each branch of the tree is labeled with the GI numbers in the NCBI protein database for most organisms. NaChBac, NaVSP and NaVPZ channels were functionally characterized previously [36], [61]. Abbreviations: Hsa, H. sapiens; Mbr, M. brevicollis; Nve, N. vectensis.
Mentions: Our database search did not identify the putative primordial CatSper sequence. It remains possible that the introduction of the primordial, probably distantly related, CatSper channel could be made through horizontal gene transfer between prokaryotes and primitive metazoan species, such as single 6-TMS domain NaV channels NaVBP [19], NaChBac [61], and 11 bacterial NaChBac homologues [36]. All these bacterial NaV channel homologues share a glutamate residue as the key acidic residue in the putative channel pore region [36], in contrast to the key aspartate residue conserved in CatSpers (Fig. 2). We analyzed 40 more bacterial protein sequences (protein cluster CLS1187052), which display high sequence homology and structural similarity to NaChBac. None of these 40 bacterial homologues grouped with CatSper sequences (Fig. 5). However, two (GI No. 56963529 and 134099759) have the key aspartate residue in the putative pore region, and it would be interesting compare their Ca2+-selectivity, voltage-dependence and kinetics with the CatSper channel.

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