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Analysis of Schistosoma mansoni genes shared with Deuterostomia and with possible roles in host interactions.

Venancio TM, DeMarco R, Almeida GT, Oliveira KC, Setubal JC, Verjovski-Almeida S - BMC Genomics (2007)

Bottom Line: In this work we found 427 genes conserved in the Deuterostomia group that have orthologs in S. mansoni and no members in any nematodes and insects so far sequenced.Using S. mansoni homologs, we have employed a parsimonious rationale to compute the total gene losses/gains in nematodes, arthropods and deuterostomes under either the Coelomata or the Ecdysozoa evolutionary hypotheses; our results show a lower losses/gains number under the latter hypothesis.Given their known functions in Deuterostomia, it is possible that some of them have been co-opted to perform functions related (directly or indirectly) to host adaptation or interaction with host signaling processes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratory of Bioinformatics; Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo, 05508-900 São Paulo, SP, Brazil. venancio@iq.usp.br

ABSTRACT

Background: Schistosoma mansoni is a blood helminth parasite that causes schistosomiasis, a disease that affects 200 million people in the world. Many orthologs of known mammalian genes have been discovered in this parasite and evidence is accumulating that some of these genes encode proteins linked to signaling pathways in the parasite that appear to be involved with growth or development, suggesting a complex co-evolutionary process.

Results: In this work we found 427 genes conserved in the Deuterostomia group that have orthologs in S. mansoni and no members in any nematodes and insects so far sequenced. Among these genes we have identified Insulin Induced Gene (INSIG), Interferon Regulatory Factor (IRF) and vasohibin orthologs, known to be involved in mammals in mevalonate metabolism, immune response and angiogenesis control, respectively. We have chosen these three genes for a more detailed characterization, which included extension of their cloned messages to obtain full-length sequences. Interestingly, SmINSIG showed a 10-fold higher expression in adult females as opposed to males, in accordance with its possible role in regulating egg production. SmIRF has a DNA binding domain, a tryptophan-rich N-terminal region and several predicted phosphorylation sites, usually important for IRF activity. Fourteen different alternatively spliced forms of the S. mansoni vasohibin (SmVASL) gene were detected that encode seven different protein isoforms including one with a complete C-terminal end, and other isoforms with shorter C-terminal portions. Using S. mansoni homologs, we have employed a parsimonious rationale to compute the total gene losses/gains in nematodes, arthropods and deuterostomes under either the Coelomata or the Ecdysozoa evolutionary hypotheses; our results show a lower losses/gains number under the latter hypothesis.

Conclusion: The genes discussed which are conserved between S. mansoni and deuterostomes, probably have an ancient origin and were lost in Ecdysozoa, being still present in Lophotrochozoa. Given their known functions in Deuterostomia, it is possible that some of them have been co-opted to perform functions related (directly or indirectly) to host adaptation or interaction with host signaling processes.

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Schematic representation of the two main hypotheses for the relationships between animal phyla. A – Acoelomata-Pseudocoelomata-Coelomata hypothesis; B – Lophotrocozoa-Ecdysozoa-Deuterostomia hypothesis. This scheme is illustrative and branch lengths do not reflect evolutionary distances.
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Figure 1: Schematic representation of the two main hypotheses for the relationships between animal phyla. A – Acoelomata-Pseudocoelomata-Coelomata hypothesis; B – Lophotrocozoa-Ecdysozoa-Deuterostomia hypothesis. This scheme is illustrative and branch lengths do not reflect evolutionary distances.

Mentions: The schistosoma genus is part of the platyhelminth phylum, which has been traditionally regarded as one of the first diverging phyla of the bilaterian group in the acoelomate-pseudoceolomate-celomate (APC) theory (Figure 1A), which groups bilaterally symmetrical animals based on the presence of coelom (a body cavity lined by an epithelium derived from mesenchyme, e.g. human pleural cavity) [13,14]. This view is based on a gradualist scenario in which the first bilaterian ancestral was acoelomate and some of its descendants developed coelomic cavities originating the various coelomate phyla. Recent analysis of molecular data and embryonic development suggested that platyhelminths are not in the basal position of bilateria, but are derived from an ancestral coelomate [15-17]. This new phylogeny classifies bilaterian animals in deuterostomes (the first opening, the blastopore, becomes the anus) and protostomes (the first opening becomes the mouth). The Deuterostomia group includes all chordates and echinoderms. Protostomes are further divided in Lophotrochozoa (animals with a feeding structure called lophophore; e.g. platyhelminths, annelids and mollusks) and Ecdysozoa (animals that undergo ecdysis or moulting, e.g. insects and nematodes) [15-17]. This hypothesis is named LED (Lophotrochozoa-Ecdysozoa-Deuterostomia) (see Figure 1B).


Analysis of Schistosoma mansoni genes shared with Deuterostomia and with possible roles in host interactions.

Venancio TM, DeMarco R, Almeida GT, Oliveira KC, Setubal JC, Verjovski-Almeida S - BMC Genomics (2007)

Schematic representation of the two main hypotheses for the relationships between animal phyla. A – Acoelomata-Pseudocoelomata-Coelomata hypothesis; B – Lophotrocozoa-Ecdysozoa-Deuterostomia hypothesis. This scheme is illustrative and branch lengths do not reflect evolutionary distances.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2194728&req=5

Figure 1: Schematic representation of the two main hypotheses for the relationships between animal phyla. A – Acoelomata-Pseudocoelomata-Coelomata hypothesis; B – Lophotrocozoa-Ecdysozoa-Deuterostomia hypothesis. This scheme is illustrative and branch lengths do not reflect evolutionary distances.
Mentions: The schistosoma genus is part of the platyhelminth phylum, which has been traditionally regarded as one of the first diverging phyla of the bilaterian group in the acoelomate-pseudoceolomate-celomate (APC) theory (Figure 1A), which groups bilaterally symmetrical animals based on the presence of coelom (a body cavity lined by an epithelium derived from mesenchyme, e.g. human pleural cavity) [13,14]. This view is based on a gradualist scenario in which the first bilaterian ancestral was acoelomate and some of its descendants developed coelomic cavities originating the various coelomate phyla. Recent analysis of molecular data and embryonic development suggested that platyhelminths are not in the basal position of bilateria, but are derived from an ancestral coelomate [15-17]. This new phylogeny classifies bilaterian animals in deuterostomes (the first opening, the blastopore, becomes the anus) and protostomes (the first opening becomes the mouth). The Deuterostomia group includes all chordates and echinoderms. Protostomes are further divided in Lophotrochozoa (animals with a feeding structure called lophophore; e.g. platyhelminths, annelids and mollusks) and Ecdysozoa (animals that undergo ecdysis or moulting, e.g. insects and nematodes) [15-17]. This hypothesis is named LED (Lophotrochozoa-Ecdysozoa-Deuterostomia) (see Figure 1B).

Bottom Line: In this work we found 427 genes conserved in the Deuterostomia group that have orthologs in S. mansoni and no members in any nematodes and insects so far sequenced.Using S. mansoni homologs, we have employed a parsimonious rationale to compute the total gene losses/gains in nematodes, arthropods and deuterostomes under either the Coelomata or the Ecdysozoa evolutionary hypotheses; our results show a lower losses/gains number under the latter hypothesis.Given their known functions in Deuterostomia, it is possible that some of them have been co-opted to perform functions related (directly or indirectly) to host adaptation or interaction with host signaling processes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratory of Bioinformatics; Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo, 05508-900 São Paulo, SP, Brazil. venancio@iq.usp.br

ABSTRACT

Background: Schistosoma mansoni is a blood helminth parasite that causes schistosomiasis, a disease that affects 200 million people in the world. Many orthologs of known mammalian genes have been discovered in this parasite and evidence is accumulating that some of these genes encode proteins linked to signaling pathways in the parasite that appear to be involved with growth or development, suggesting a complex co-evolutionary process.

Results: In this work we found 427 genes conserved in the Deuterostomia group that have orthologs in S. mansoni and no members in any nematodes and insects so far sequenced. Among these genes we have identified Insulin Induced Gene (INSIG), Interferon Regulatory Factor (IRF) and vasohibin orthologs, known to be involved in mammals in mevalonate metabolism, immune response and angiogenesis control, respectively. We have chosen these three genes for a more detailed characterization, which included extension of their cloned messages to obtain full-length sequences. Interestingly, SmINSIG showed a 10-fold higher expression in adult females as opposed to males, in accordance with its possible role in regulating egg production. SmIRF has a DNA binding domain, a tryptophan-rich N-terminal region and several predicted phosphorylation sites, usually important for IRF activity. Fourteen different alternatively spliced forms of the S. mansoni vasohibin (SmVASL) gene were detected that encode seven different protein isoforms including one with a complete C-terminal end, and other isoforms with shorter C-terminal portions. Using S. mansoni homologs, we have employed a parsimonious rationale to compute the total gene losses/gains in nematodes, arthropods and deuterostomes under either the Coelomata or the Ecdysozoa evolutionary hypotheses; our results show a lower losses/gains number under the latter hypothesis.

Conclusion: The genes discussed which are conserved between S. mansoni and deuterostomes, probably have an ancient origin and were lost in Ecdysozoa, being still present in Lophotrochozoa. Given their known functions in Deuterostomia, it is possible that some of them have been co-opted to perform functions related (directly or indirectly) to host adaptation or interaction with host signaling processes.

Show MeSH
Related in: MedlinePlus