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Mol Biol Evol. 2015 Aug;32(8):1928-47. doi: 10.1093/molbev/msv079. Epub 2015 Apr 3.

A Comprehensive Transcriptomic and Proteomic Analysis of Hydra Head Regeneration.

Author information

1
Centre for Organismal Studies (COS), Heidelberg University, Heidelberg, Germany.
2
Max Planck Institute (MPI) for Heart and Lung Research, Bad Nauheim, Germany.
3
Functional Proteome Analysis Unit, German Cancer Research Center (DKFZ), Heidelberg, Germany.
4
Okazaki Institute for Integrative Bioscience, National Institute for Basic Biology, Myodaiji, Okazaki, Japan.
5
Max Planck Institute (MPI) for Heart and Lung Research, Bad Nauheim, Germany CECAD, University of Cologne, Germany.
6
Centre for Organismal Studies (COS), Heidelberg University, Heidelberg, Germany Molecular Genetics Unit, Okinawa Institute of Science and Technology, Okinawa, Japan.
7
Centre for Organismal Studies (COS), Heidelberg University, Heidelberg, Germany thomas.holstein@cos.uni.heidelberg.de.

Abstract

The cnidarian freshwater polyp Hydra sp. exhibits an unparalleled regeneration capacity in the animal kingdom. Using an integrative transcriptomic and stable isotope labeling by amino acids in cell culture proteomic/phosphoproteomic approach, we studied stem cell-based regeneration in Hydra polyps. As major contributors to head regeneration, we identified diverse signaling pathways adopted for the regeneration response as well as enriched novel genes. Our global analysis reveals two distinct molecular cascades: an early injury response and a subsequent, signaling driven patterning of the regenerating tissue. A key factor of the initial injury response is a general stabilization of proteins and a net upregulation of transcripts, which is followed by a subsequent activation cascade of signaling molecules including Wnts and transforming growth factor (TGF) beta-related factors. We observed moderate overlap between the factors contributing to proteomic and transcriptomic responses suggesting a decoupled regulation between the transcriptional and translational levels. Our data also indicate that interstitial stem cells and their derivatives (e.g., neurons) have no major role in Hydra head regeneration. Remarkably, we found an enrichment of evolutionarily more recent genes in the early regeneration response, whereas conserved genes are more enriched in the late phase. In addition, genes specific to the early injury response were enriched in transposon insertions. Genetic dynamicity and taxon-specific factors might therefore play a hitherto underestimated role in Hydra regeneration.

KEYWORDS:

Cnidaria; Hydra; evolution of regeneration; proteomics and transcriptomics

PMID:
25841488
PMCID:
PMC4833066
DOI:
10.1093/molbev/msv079
[Indexed for MEDLINE]
Free PMC Article

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