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Naturally occurring tumours in the basal metazoan Hydra.

ABSTRACT: The molecular nature of malignant tumors is well studied in vertebrates, while their evolutionary origin remains unknown. In particular, there is no evidence for naturally occurring malignant tumors in pre-bilaterian animals, such as sponges and cnidarians. This is somewhat surprising given that recent computational studies have predicted that all metazoans are prone to develop tumors. Here we provide first evidence for naturally occurring tumors in Hydra oligactis. Histological, cellular and molecular data reveal that these tumors are transplantable and caused by differentiation arrest of female gametes. Growth of tumor cells is independent from the cellular environment. Tumor bearing polyps have significantly reduced fitness. In addition, Hydra tumors show a greatly altered transcriptome that mimics expression shifts in vertebrate cancers. Therefore, this study shows, that invasive tumors have deep roots in animal phylogeny, and that early branching animals may be informative in revealing the fundamental mechanisms of tumorigenesis.

ORGANISM(S): Hydra oligactis

PROVIDER: GSE56287 | GEO | 2014/06/24

SECONDARY ACCESSION(S): PRJNA242842

REPOSITORIES: GEO

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Project description:Animals capable of whole-body regeneration can fully restore any tissue lost due to injury. Because different types of injury may require the regeneration of different structures, transcription during whole-body regeneration needs to dynamically adapt to meet the requirements specific to any given injury. However, the regulatory mechanisms responsible for modulating the transcriptional response to injury are poorly understood at the molecular level. We therefore used the highly regenerative cnidarian polyp, Hydra vulgaris, to better understand how transcription in wounded tissue responds to its surrounding tissue environment to enable the restoration of the original body plan. We comprehensively characterized changes in transcript abundance and chromatin accessibility during two types of regeneration, oral and aboral regeneration, and found that the initial transcriptional response to injury was the same regardless of the injury’s tissue environment. This initial response included the activation of the canonical Wnt signaling pathway, which specifies oral tissue in cnidarians, likely through the direct upregulation of Wnt ligands by conserved injury responsive bZIP transcription factors. The duration of the injury-induced increase in Wnt signaling depended on the injury’s tissue context, as Wnt signaling was activated only transiently during aboral regeneration but showed sustained activation during oral regeneration. Inhibiting TCF, the transcription factor downstream of canonical Wnt signaling, delayed the onset of oral- and aboral-specific transcription genome-wide, suggesting that proper regulation of canonical Wnt signaling is critical for both types of regeneration. Finally, we found that Wnt signaling was also activated by puncture wounds, and that removing pre-existing organizers induced these injuries to undergo ectopic head regeneration. These findings suggest that head regeneration is the default response to injury in Hydra, and that other wound repair outcomes are the result of inhibitory signals produced by the surrounding tissue environment. Furthermore, our work raises the possibility that Wnt signaling may be part of an ancient and conserved wound response program that predates the split of bilaterians and cnidarians over 500 million years ago.

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Naturally occurring tumours in the basal metazoan Hydra.

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