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Analysis of the immune-related transcriptome of a lophotrochozoan model, the marine annelid Platynereis dumerilii.

ABSTRACT: BACKGROUND:The marine annelid Platynereis dumerilii (Polychaeta, Nereididae) has been recognized as a slow-evolving lophotrochozoan that attracts increasing attention as a valuable model for evolutionary and developmental research. Here, we analyzed its immune-related transcriptome. For targeted identification of immune-induced genes we injected bacterial lipopolysaccharide, a commonly used elicitor of innate immune responses, and applied the suppression subtractive hybridization technique that selectively amplifies cDNAs of differentially expressed genes. RESULTS:Sequence analysis of 288 cDNAs revealed induced expression of numerous genes whose potential homologues from other animals mediate recognition of infection (e.g. complement receptor CD35), signaling (e.g. myc and SOCS), or act as effector molecules like ferritins and the bactericidal permeability-increasing protein. Interestingly, phylogenetic analyses implicate that immune-related genes identified in P. dumerilii are more related to counterparts from Deuterostomia than are those from Ecdysozoa, similarly as recently described for opsin and intron-rich genes. CONCLUSION:Obtained results may allow for a better understanding of Platynereis immunity and support the view that P. dumerilii represents a suitable model for analyzing immune responses of Lophotrochozoa.

SUBMITTER: Altincicek B

PROVIDER: S-EPMC1939704 | biostudies-literature | 2007 Jul

REPOSITORIES: biostudies-literature

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Analysis of the immune-related transcriptome of a lophotrochozoan model, the marine annelid Platynereis dumerilii.

Altincicek Boran B Vilcinskas Andreas A

Frontiers in zoology 20070706

<h4>Background</h4>The marine annelid Platynereis dumerilii (Polychaeta, Nereididae) has been recognized as a slow-evolving lophotrochozoan that attracts increasing attention as a valuable model for evolutionary and developmental research. Here, we analyzed its immune-related transcriptome. For targeted identification of immune-induced genes we injected bacterial lipopolysaccharide, a commonly used elicitor of innate immune responses, and applied the suppression subtractive hybridization techniq ...[more]

PMID: 17617895

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Project description:BackgroundWnt signaling pathways are highly conserved signal transduction pathways important for axis formation, cell fate specification, and organogenesis throughout metazoan development. Within the various Wnt pathways, the frizzled transmembrane receptors (Fzs) and secreted frizzled-related proteins (sFRPs) play central roles in receiving and antagonizing Wnt signals, respectively. Despite their importance, very little is known about the frizzled-related gene family (fzs & sfrps) in lophotrochozoans, especially during early stages of spiralian development. Here we ascertain the frizzled-related gene complement in six lophotrochozoan species, and determine their spatial and temporal expression pattern during early embryogenesis and larval stages of the marine annelid Platynereis dumerilii.ResultsPhylogenetic analyses confirm conserved homologs for four frizzled receptors (Fz1/2/7, Fz4, Fz5/8, Fz9/10) and sFRP1/2/5 in five of six lophotrochozoan species. The sfrp3/4 gene is conserved in one, divergent in two, and evidently lost in three lophotrochozoan species. Three novel fz-related genes (fzCRD1-3) are unique to Platynereis. Transcriptional profiling and in situ hybridization identified high maternal expression of fz1/2/7, expression of fz9/10 and fz1/2/7 within animal and dorsal cell lineages after the 32-cell stage, localization of fz5/8, sfrp1/2/5, and fzCRD-1 to animal-pole cell lineages after the 80-cell stage, and no expression for fz4, sfrp3/4, and fzCRD-2, and -3 in early Platynereis embryos. In later larval stages, all frizzled-related genes are expressed in distinct patterns preferentially in the anterior hemisphere and less in the developing trunk.ConclusionsLophotrochozoans have retained a generally conserved ancestral bilaterian frizzled-related gene complement (four Fzs and two sFRPs). Maternal expression of fz1/2/7, and animal lineage-specific expression of fz5/8 and sfrp1/2/5 in early embryos of Platynereis suggest evolutionary conserved roles of these genes to perform Wnt pathway functions during early cleavage stages, and the early establishment of a Wnt inhibitory center at the animal pole, respectively. Numerous frizzled receptor-expressing cells and embryonic territories were identified that might indicate competence to receive Wnt signals during annelid development. An anterior bias for frizzled-related gene expression in embryos and larvae might point to a polarity of Wnt patterning systems along the anterior-posterior axis of this annelid.

Dataset Information

Analysis of the immune-related transcriptome of a lophotrochozoan model, the marine annelid Platynereis dumerilii.

Publications

Analysis of the immune-related transcriptome of a lophotrochozoan model, the marine annelid Platynereis dumerilii.

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