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Developmentally regulated expression, alternative splicing and distinct sub-groupings in members of the Schistosoma mansoni venom allergen-like (SmVAL) gene family.

Chalmers IW, McArdle AJ, Coulson RM, Wagner MA, Schmid R, Hirai H, Hoffmann KF - BMC Genomics (2008)

Bottom Line: The Sperm-coating protein/Tpx-1/Ag5/PR-1/Sc7 (SCP/TAPS) domain is found across phyla and is a major structural feature of insect allergens, mammalian sperm proteins and parasitic nematode secreted molecules.Analysis of SmVAL6 transcript diversity demonstrated statistically significant, developmentally regulated, alternative splicing.Our results highlight the existence of two distinct SCP/TAPS protein types within the Platyhelminthes and across taxa.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Pathology, University of Cambridge, Tennis Court Road, Cambridge, CB2 1QP, UK. iwc21@cam.ac.uk

ABSTRACT

Background: The Sperm-coating protein/Tpx-1/Ag5/PR-1/Sc7 (SCP/TAPS) domain is found across phyla and is a major structural feature of insect allergens, mammalian sperm proteins and parasitic nematode secreted molecules. Proteins containing this domain are implicated in diverse biological activities and may be important for chronic host/parasite interactions.

Results: We report the first description of an SCP/TAPS gene family (Schistosoma mansoni venom allergen-like (SmVALs)) in the medically important Platyhelminthes (class Trematoda) and describe individual members' phylogenetic relationships, genomic organization and life cycle expression profiles. Twenty-eight SmVALs with complete SCP/TAPS domains were identified and comparison of their predicted protein features and gene structures indicated the presence of two distinct sub-families (group 1 & group 2). Phylogenetic analysis demonstrated that this group 1/group 2 split is zoologically widespread as it exists across the metazoan sub-kingdom. Chromosomal localisation and PCR analysis, coupled to inspection of the current S. mansoni genomic assembly, revealed that many of the SmVAL genes are spatially linked throughout the genome. Quantitative lifecycle expression profiling demonstrated distinct SmVAL expression patterns, including transcripts specifically associated with lifestages involved in definitive host invasion, transcripts restricted to lifestages involved in the invasion of the intermediate host and transcripts ubiquitously expressed. Analysis of SmVAL6 transcript diversity demonstrated statistically significant, developmentally regulated, alternative splicing.

Conclusion: Our results highlight the existence of two distinct SCP/TAPS protein types within the Platyhelminthes and across taxa. The extensive lifecycle expression analysis indicates several SmVAL transcripts are upregulated in infective stages of the parasite, suggesting that these particular protein products may be linked to the establishment of chronic host/parasite interactions.

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Phylogenetic analysis of SmVALs and representative metazoan SCP/TAPS proteins reveal a clear and evolutionary distant split between group 1 and group 2 proteins. Phylogenetic trees were inferred by MrBayes 3.1.2 and illustrated by Treeview as described in Methods. Relative branch lengths are indicated, as are the Bayesian posterior probability support values that are greater than 0.5. A) A rooted phylogram is illustrated for the 29 SmVAL SCP/TAPS domain-containing proteins. B) An unrooted phylogram is illustrated for the representative metazoan SCP/TAPS domain-containing proteins. The non-S. mansoni protein sequences used have the following GenBank accession numbers: Vv Vesv5 [AAA30333], Dm AGR [AAB92563], Na ASP2 [AAP41952], Ce SCL1 [NP_502502], Ct Tex31 [CAD36507], Bm VAL1 [AAK12274], Ce CE09088 [NP_494312], Dm CG4270 [NP_608663], Hs GAPR1 [Q9H4G4], Ss NIE [AAD46493], Hh Helothermine [2122236A] and Hs CRISP1 [CAC34980]. Branch length represents the number of amino acid changes calculated by the WAG model and is indicated by the scale bars.
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Figure 2: Phylogenetic analysis of SmVALs and representative metazoan SCP/TAPS proteins reveal a clear and evolutionary distant split between group 1 and group 2 proteins. Phylogenetic trees were inferred by MrBayes 3.1.2 and illustrated by Treeview as described in Methods. Relative branch lengths are indicated, as are the Bayesian posterior probability support values that are greater than 0.5. A) A rooted phylogram is illustrated for the 29 SmVAL SCP/TAPS domain-containing proteins. B) An unrooted phylogram is illustrated for the representative metazoan SCP/TAPS domain-containing proteins. The non-S. mansoni protein sequences used have the following GenBank accession numbers: Vv Vesv5 [AAA30333], Dm AGR [AAB92563], Na ASP2 [AAP41952], Ce SCL1 [NP_502502], Ct Tex31 [CAD36507], Bm VAL1 [AAK12274], Ce CE09088 [NP_494312], Dm CG4270 [NP_608663], Hs GAPR1 [Q9H4G4], Ss NIE [AAD46493], Hh Helothermine [2122236A] and Hs CRISP1 [CAC34980]. Branch length represents the number of amino acid changes calculated by the WAG model and is indicated by the scale bars.

Mentions: To investigate the phylogenetic relationship within the SmVAL family, the predicted 29 complete SCP/TAPS domains were used to construct a phylogram using Bayesian analysis of a conserved (within all 29 SCP/TAPS domains) 84 amino acid region (split across six regions) identified by GBLOCKs [30] (Fig. 2A). The derived phylogram contained two main SmVAL clades (with 100% support) – one harbouring the six SCP/TAPS domains from the group 2 SmVALs and the other containing the 23 SCP/TAPS domains from the group 1 SmVALs (Fig. 2A). These two clades are also well-supported (99% bootstrap value) in the consensus phylogenetic tree constructed by the Neighbor-Joining algorithm (see Additional file 1). Phylogenetic analyses of this type have also been performed for SCP/TAPS domain- containing proteins within Drosophila melanogaster [7] and clearly demonstrate that distinct group 1/2 sub-divisions exist within SCP/TAPS family members of other species.


Developmentally regulated expression, alternative splicing and distinct sub-groupings in members of the Schistosoma mansoni venom allergen-like (SmVAL) gene family.

Chalmers IW, McArdle AJ, Coulson RM, Wagner MA, Schmid R, Hirai H, Hoffmann KF - BMC Genomics (2008)

Phylogenetic analysis of SmVALs and representative metazoan SCP/TAPS proteins reveal a clear and evolutionary distant split between group 1 and group 2 proteins. Phylogenetic trees were inferred by MrBayes 3.1.2 and illustrated by Treeview as described in Methods. Relative branch lengths are indicated, as are the Bayesian posterior probability support values that are greater than 0.5. A) A rooted phylogram is illustrated for the 29 SmVAL SCP/TAPS domain-containing proteins. B) An unrooted phylogram is illustrated for the representative metazoan SCP/TAPS domain-containing proteins. The non-S. mansoni protein sequences used have the following GenBank accession numbers: Vv Vesv5 [AAA30333], Dm AGR [AAB92563], Na ASP2 [AAP41952], Ce SCL1 [NP_502502], Ct Tex31 [CAD36507], Bm VAL1 [AAK12274], Ce CE09088 [NP_494312], Dm CG4270 [NP_608663], Hs GAPR1 [Q9H4G4], Ss NIE [AAD46493], Hh Helothermine [2122236A] and Hs CRISP1 [CAC34980]. Branch length represents the number of amino acid changes calculated by the WAG model and is indicated by the scale bars.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
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Figure 2: Phylogenetic analysis of SmVALs and representative metazoan SCP/TAPS proteins reveal a clear and evolutionary distant split between group 1 and group 2 proteins. Phylogenetic trees were inferred by MrBayes 3.1.2 and illustrated by Treeview as described in Methods. Relative branch lengths are indicated, as are the Bayesian posterior probability support values that are greater than 0.5. A) A rooted phylogram is illustrated for the 29 SmVAL SCP/TAPS domain-containing proteins. B) An unrooted phylogram is illustrated for the representative metazoan SCP/TAPS domain-containing proteins. The non-S. mansoni protein sequences used have the following GenBank accession numbers: Vv Vesv5 [AAA30333], Dm AGR [AAB92563], Na ASP2 [AAP41952], Ce SCL1 [NP_502502], Ct Tex31 [CAD36507], Bm VAL1 [AAK12274], Ce CE09088 [NP_494312], Dm CG4270 [NP_608663], Hs GAPR1 [Q9H4G4], Ss NIE [AAD46493], Hh Helothermine [2122236A] and Hs CRISP1 [CAC34980]. Branch length represents the number of amino acid changes calculated by the WAG model and is indicated by the scale bars.
Mentions: To investigate the phylogenetic relationship within the SmVAL family, the predicted 29 complete SCP/TAPS domains were used to construct a phylogram using Bayesian analysis of a conserved (within all 29 SCP/TAPS domains) 84 amino acid region (split across six regions) identified by GBLOCKs [30] (Fig. 2A). The derived phylogram contained two main SmVAL clades (with 100% support) – one harbouring the six SCP/TAPS domains from the group 2 SmVALs and the other containing the 23 SCP/TAPS domains from the group 1 SmVALs (Fig. 2A). These two clades are also well-supported (99% bootstrap value) in the consensus phylogenetic tree constructed by the Neighbor-Joining algorithm (see Additional file 1). Phylogenetic analyses of this type have also been performed for SCP/TAPS domain- containing proteins within Drosophila melanogaster [7] and clearly demonstrate that distinct group 1/2 sub-divisions exist within SCP/TAPS family members of other species.

Bottom Line: The Sperm-coating protein/Tpx-1/Ag5/PR-1/Sc7 (SCP/TAPS) domain is found across phyla and is a major structural feature of insect allergens, mammalian sperm proteins and parasitic nematode secreted molecules.Analysis of SmVAL6 transcript diversity demonstrated statistically significant, developmentally regulated, alternative splicing.Our results highlight the existence of two distinct SCP/TAPS protein types within the Platyhelminthes and across taxa.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Pathology, University of Cambridge, Tennis Court Road, Cambridge, CB2 1QP, UK. iwc21@cam.ac.uk

ABSTRACT

Background: The Sperm-coating protein/Tpx-1/Ag5/PR-1/Sc7 (SCP/TAPS) domain is found across phyla and is a major structural feature of insect allergens, mammalian sperm proteins and parasitic nematode secreted molecules. Proteins containing this domain are implicated in diverse biological activities and may be important for chronic host/parasite interactions.

Results: We report the first description of an SCP/TAPS gene family (Schistosoma mansoni venom allergen-like (SmVALs)) in the medically important Platyhelminthes (class Trematoda) and describe individual members' phylogenetic relationships, genomic organization and life cycle expression profiles. Twenty-eight SmVALs with complete SCP/TAPS domains were identified and comparison of their predicted protein features and gene structures indicated the presence of two distinct sub-families (group 1 & group 2). Phylogenetic analysis demonstrated that this group 1/group 2 split is zoologically widespread as it exists across the metazoan sub-kingdom. Chromosomal localisation and PCR analysis, coupled to inspection of the current S. mansoni genomic assembly, revealed that many of the SmVAL genes are spatially linked throughout the genome. Quantitative lifecycle expression profiling demonstrated distinct SmVAL expression patterns, including transcripts specifically associated with lifestages involved in definitive host invasion, transcripts restricted to lifestages involved in the invasion of the intermediate host and transcripts ubiquitously expressed. Analysis of SmVAL6 transcript diversity demonstrated statistically significant, developmentally regulated, alternative splicing.

Conclusion: Our results highlight the existence of two distinct SCP/TAPS protein types within the Platyhelminthes and across taxa. The extensive lifecycle expression analysis indicates several SmVAL transcripts are upregulated in infective stages of the parasite, suggesting that these particular protein products may be linked to the establishment of chronic host/parasite interactions.

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