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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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SmVAL6 genomic structure analysis reveals a highly complex gene composed of 38 exons. SmVAL6 exons are represented by boxes, with exon length (in base pairs) given above each box. Introns are represented by lines, with intron length (in base pairs) shown below each line. Exons are coloured to indicate: SCP/TAPS domain (red), untranslated region (white) and remaining ORF (blue). Each successive exon has been ascribed a number (underlined numbers below the exons). Exons that introduce a premature stop codon are highlighted with an asterisk and dashed lines represent separate exons created by competing 3' splice sites. The exon specific annealing positions of primers VAL6 var F and VAL6 var R, used for developmentally-regulated alternative splicing analysis, are indicated.
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Figure 5: SmVAL6 genomic structure analysis reveals a highly complex gene composed of 38 exons. SmVAL6 exons are represented by boxes, with exon length (in base pairs) given above each box. Introns are represented by lines, with intron length (in base pairs) shown below each line. Exons are coloured to indicate: SCP/TAPS domain (red), untranslated region (white) and remaining ORF (blue). Each successive exon has been ascribed a number (underlined numbers below the exons). Exons that introduce a premature stop codon are highlighted with an asterisk and dashed lines represent separate exons created by competing 3' splice sites. The exon specific annealing positions of primers VAL6 var F and VAL6 var R, used for developmentally-regulated alternative splicing analysis, are indicated.

Mentions: Despite the conserved intron/exon structure (within the group 2 SmVALs) comprising the SCP/TAPS domain of SmVAL6, the intron/exon structure coding for the C-terminus of SmVAL6 is notable in its complexity. Unlike all other family members, the large and extended genomic DNA (gDNA) region 3' of the SCP/TAPS domain is composed of numerous small exons. In total, the gene encoding the SmVAL6 1302 bp transcript is comprised of 38 exons, with 17 smaller than 20 bp (Fig. 5).


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)

SmVAL6 genomic structure analysis reveals a highly complex gene composed of 38 exons. SmVAL6 exons are represented by boxes, with exon length (in base pairs) given above each box. Introns are represented by lines, with intron length (in base pairs) shown below each line. Exons are coloured to indicate: SCP/TAPS domain (red), untranslated region (white) and remaining ORF (blue). Each successive exon has been ascribed a number (underlined numbers below the exons). Exons that introduce a premature stop codon are highlighted with an asterisk and dashed lines represent separate exons created by competing 3' splice sites. The exon specific annealing positions of primers VAL6 var F and VAL6 var R, used for developmentally-regulated alternative splicing analysis, are indicated.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2270263&req=5

Figure 5: SmVAL6 genomic structure analysis reveals a highly complex gene composed of 38 exons. SmVAL6 exons are represented by boxes, with exon length (in base pairs) given above each box. Introns are represented by lines, with intron length (in base pairs) shown below each line. Exons are coloured to indicate: SCP/TAPS domain (red), untranslated region (white) and remaining ORF (blue). Each successive exon has been ascribed a number (underlined numbers below the exons). Exons that introduce a premature stop codon are highlighted with an asterisk and dashed lines represent separate exons created by competing 3' splice sites. The exon specific annealing positions of primers VAL6 var F and VAL6 var R, used for developmentally-regulated alternative splicing analysis, are indicated.
Mentions: Despite the conserved intron/exon structure (within the group 2 SmVALs) comprising the SCP/TAPS domain of SmVAL6, the intron/exon structure coding for the C-terminus of SmVAL6 is notable in its complexity. Unlike all other family members, the large and extended genomic DNA (gDNA) region 3' of the SCP/TAPS domain is composed of numerous small exons. In total, the gene encoding the SmVAL6 1302 bp transcript is comprised of 38 exons, with 17 smaller than 20 bp (Fig. 5).

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.

Show MeSH