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Analysis of the Na+/Ca2+ exchanger gene family within the phylum Nematoda.

He C, O'Halloran DM - PLoS ONE (2014)

Bottom Line: The most notable feature of the resulting phylogenies was the heterogeneous evolution observed within exchanger subtypes.Specifically, in the case of the CCX exchangers we did not detect members of this class in three Clade III nematodes.We also provided re-annotation for predicted CCX gene structures from Heterorhabditis bacteriophora and Caenorhabditis japonica by RT-PCR and sequencing.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, The George Washington University, Washington, D.C., United States of America; Institute for Neuroscience, The George Washington University, Washington, D.C., United States of America.

ABSTRACT
Na+/Ca2+ exchangers are low affinity, high capacity transporters that rapidly transport calcium at the plasma membrane, mitochondrion, endoplasmic (and sarcoplasmic) reticulum, and the nucleus. Na+/Ca2+ exchangers are widely expressed in diverse cell types where they contribute homeostatic balance to calcium levels. In animals, Na+/Ca2+ exchangers are divided into three groups based upon stoichiometry: Na+/Ca2+ exchangers (NCX), Na+/Ca2+/K+ exchangers (NCKX), and Ca2+/Cation exchangers (CCX). In mammals there are three NCX genes, five NCKX genes and one CCX (NCLX) gene. The genome of the nematode Caenorhabditis elegans contains ten Na+/Ca2+ exchanger genes: three NCX; five CCX; and two NCKX genes. Here we set out to characterize structural and taxonomic specializations within the family of Na+/Ca2+ exchangers across the phylum Nematoda. In this analysis we identify Na+/Ca2+ exchanger genes from twelve species of nematodes and reconstruct their phylogenetic and evolutionary relationships. The most notable feature of the resulting phylogenies was the heterogeneous evolution observed within exchanger subtypes. Specifically, in the case of the CCX exchangers we did not detect members of this class in three Clade III nematodes. Within the Caenorhabditis and Pristionchus lineages we identify between three and five CCX representatives, whereas in other Clade V and also Clade IV nematode taxa we only observed a single CCX gene in each species, and in the Clade III nematode taxa that we sampled we identify NCX and NCKX encoding genes but no evidence of CCX representatives using our mining approach. We also provided re-annotation for predicted CCX gene structures from Heterorhabditis bacteriophora and Caenorhabditis japonica by RT-PCR and sequencing. Together, these findings reveal a complex picture of Na+/Ca2+ transporters in nematodes that suggest an incongruent evolutionary history of proteins that provide central control of calcium dynamics.

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Structures within NCX, NCKX, and CCX proteins, and an overview of the pipeline used to detect orthologs of these proteins in twelve species of nematodes.(A) Cartoon depicting structures within the NCX, NCKX, and CCX (NCLX) proteins. (B) Overview of a pipeline used to detect orthologous sodium calcium exchanger genes in twelve different species of nematodes.
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pone-0112841-g001: Structures within NCX, NCKX, and CCX proteins, and an overview of the pipeline used to detect orthologs of these proteins in twelve species of nematodes.(A) Cartoon depicting structures within the NCX, NCKX, and CCX (NCLX) proteins. (B) Overview of a pipeline used to detect orthologous sodium calcium exchanger genes in twelve different species of nematodes.

Mentions: The genomes of the nematodes sampled (Strongyloides ratti, Haemonchus contortus, Heterorhabditis bacteriophora, Caenorhabditis elegans, Caenorhabditis brenneri, Caenorhabditis japonica, Caenorhabditis briggsae, Caenorhabditis remanei, Pristionchus pacificus, Brugia malayi, Loa loa, and Ascaris suum) were searched for NCX, NCKX and CCX protein sequences with bidirectional BlastX and BlastP searches using WormBase ver.WS243 [28], Ensembl [29], Nematode.net [30], InParanoid [31]; and OrthoMCL [32] using curated NCX, NCKX, and CCX sequences from C. elegans, Drosophila melanogaster, and mammals as starting material. Specific structural signatures unique to each sodium calcium exchanger subtype were used to parse matches (Figure 1A), which were filtered through Interpro [33] and SMARTDB [34] to organize hits into either: Sodium Calcium Exchangers (NCX), Potassium dependent Sodium Calcium Exchangers (NCKX), or Sodium Calcium Lithium Exchanger (NCLX [aka CCX]) subtypes (Figure 1B).


Analysis of the Na+/Ca2+ exchanger gene family within the phylum Nematoda.

He C, O'Halloran DM - PLoS ONE (2014)

Structures within NCX, NCKX, and CCX proteins, and an overview of the pipeline used to detect orthologs of these proteins in twelve species of nematodes.(A) Cartoon depicting structures within the NCX, NCKX, and CCX (NCLX) proteins. (B) Overview of a pipeline used to detect orthologous sodium calcium exchanger genes in twelve different species of nematodes.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4232491&req=5

pone-0112841-g001: Structures within NCX, NCKX, and CCX proteins, and an overview of the pipeline used to detect orthologs of these proteins in twelve species of nematodes.(A) Cartoon depicting structures within the NCX, NCKX, and CCX (NCLX) proteins. (B) Overview of a pipeline used to detect orthologous sodium calcium exchanger genes in twelve different species of nematodes.
Mentions: The genomes of the nematodes sampled (Strongyloides ratti, Haemonchus contortus, Heterorhabditis bacteriophora, Caenorhabditis elegans, Caenorhabditis brenneri, Caenorhabditis japonica, Caenorhabditis briggsae, Caenorhabditis remanei, Pristionchus pacificus, Brugia malayi, Loa loa, and Ascaris suum) were searched for NCX, NCKX and CCX protein sequences with bidirectional BlastX and BlastP searches using WormBase ver.WS243 [28], Ensembl [29], Nematode.net [30], InParanoid [31]; and OrthoMCL [32] using curated NCX, NCKX, and CCX sequences from C. elegans, Drosophila melanogaster, and mammals as starting material. Specific structural signatures unique to each sodium calcium exchanger subtype were used to parse matches (Figure 1A), which were filtered through Interpro [33] and SMARTDB [34] to organize hits into either: Sodium Calcium Exchangers (NCX), Potassium dependent Sodium Calcium Exchangers (NCKX), or Sodium Calcium Lithium Exchanger (NCLX [aka CCX]) subtypes (Figure 1B).

Bottom Line: The most notable feature of the resulting phylogenies was the heterogeneous evolution observed within exchanger subtypes.Specifically, in the case of the CCX exchangers we did not detect members of this class in three Clade III nematodes.We also provided re-annotation for predicted CCX gene structures from Heterorhabditis bacteriophora and Caenorhabditis japonica by RT-PCR and sequencing.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, The George Washington University, Washington, D.C., United States of America; Institute for Neuroscience, The George Washington University, Washington, D.C., United States of America.

ABSTRACT
Na+/Ca2+ exchangers are low affinity, high capacity transporters that rapidly transport calcium at the plasma membrane, mitochondrion, endoplasmic (and sarcoplasmic) reticulum, and the nucleus. Na+/Ca2+ exchangers are widely expressed in diverse cell types where they contribute homeostatic balance to calcium levels. In animals, Na+/Ca2+ exchangers are divided into three groups based upon stoichiometry: Na+/Ca2+ exchangers (NCX), Na+/Ca2+/K+ exchangers (NCKX), and Ca2+/Cation exchangers (CCX). In mammals there are three NCX genes, five NCKX genes and one CCX (NCLX) gene. The genome of the nematode Caenorhabditis elegans contains ten Na+/Ca2+ exchanger genes: three NCX; five CCX; and two NCKX genes. Here we set out to characterize structural and taxonomic specializations within the family of Na+/Ca2+ exchangers across the phylum Nematoda. In this analysis we identify Na+/Ca2+ exchanger genes from twelve species of nematodes and reconstruct their phylogenetic and evolutionary relationships. The most notable feature of the resulting phylogenies was the heterogeneous evolution observed within exchanger subtypes. Specifically, in the case of the CCX exchangers we did not detect members of this class in three Clade III nematodes. Within the Caenorhabditis and Pristionchus lineages we identify between three and five CCX representatives, whereas in other Clade V and also Clade IV nematode taxa we only observed a single CCX gene in each species, and in the Clade III nematode taxa that we sampled we identify NCX and NCKX encoding genes but no evidence of CCX representatives using our mining approach. We also provided re-annotation for predicted CCX gene structures from Heterorhabditis bacteriophora and Caenorhabditis japonica by RT-PCR and sequencing. Together, these findings reveal a complex picture of Na+/Ca2+ transporters in nematodes that suggest an incongruent evolutionary history of proteins that provide central control of calcium dynamics.

Show MeSH