Molecular Signatures of the Three Stem Cell Lineages in Hydra and the Emergence of Stem Cell Function at the Base of Multicellularity

Hemmrich, Georg; Khalturin, Konstantin; Boehm, Anna-Marei; Puchert, Malte; Anton-Erxleben, Friederike; Wittlieb, Jörg; Klostermeier, Ulrich C.; Rosenstiel, Philip; Oberg, Hans‐Heinrich; Domazet-Lošo, Tomislav; Sugimoto, Toshimi; Niwa, Hitoshi; Bosch, Thomas C. G.

doi:10.1093/molbev/mss134

Cited by 145 publications

(154 citation statements)

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“…To characterize the cell type involved in tumorigenesis in more detail, we employed molecular markers specific for Hydra's germ-line restricted ISCs. In situ hybridization with a Cnnos1-specific probe 16,22 revealed in both lines that tumours are composed, at least in part, of interstitial cells expressing the Cnnos1 gene ( Supplementary Fig. 3).…”

Section: Morphology and Histologymentioning

confidence: 99%

“…Gametogenesis in Hydra, which is triggered by changes in environmental conditions 13,14 , involves mitotic proliferation of committed precursor cells followed by terminal differentiation into eggs and sperm. Despite the apparent morphological simplicity of the Hydra body plan, the proliferation and differentiation behaviour of the cell lineages is tightly controlled 15,16 , allowing stable maintenance of tissue homeostasis for extended periods. In fact, due to the asexual mode of reproduction by budding Hydra is one of the very few examples of animals, which appear to be effectively immortal 17,18 .…”

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Naturally occurring tumours in the basal metazoan Hydra

et al. 2014

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

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Section: Morphology and Histologymentioning

confidence: 99%

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Naturally occurring tumours in the basal metazoan Hydra

et al. 2014

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“…22 These sequences were used in the study to query the up to this former date non-public Compagen database which contains transcriptomic data from Hydra vulgaris AEP (Hemmrich et al 2012). There was only little sequence divergence between Hydra vulgaris and Hydra vulgaris AEP according to the database information.…”

Section: Sequence and Structure Of Hysycp1 And Hysycp3mentioning

confidence: 99%

“…Thus, the found database sequences of Hydra Syce2 and Hydra Tex12 48 were used to query the Hydra vulgaris AEP transcriptome data on the Compagen server (Hemmrich et al 2012). The respective proteins of Hydra vulgaris AEP match with 98% (HySYCE2) and 99% (HyTex12) sequence identity.…”

Section: Expression Of Hysyce2 and Hytex12 In Hydra Vulgaris Aepmentioning

confidence: 99%

“…Amino acids 1-122 of this sequence align to the amino acids 226-347 of the human and the mouse SYCP2. A BLAST search in the Hydra vulgaris AEP transcriptome of the Compagen server (Hemmrich et al 2012) acids from two different contigs, the first containing the aligned amino acids 1-99 of Hym-SYCP2 with a sequence identity of 96%. These residues mainly correspond to the conserved region which was also kept for reconstruction of the phylogenetic tree.…”

Section: Sequence and Expression Of The Sycp2 Orthologue In Hydra Vulmentioning

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Evolutionary history of the mammalian synaptonemal complex

et al. 2016

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Regeneration inHydra

Galliot

2013

Encyclopedia of Life Sciences

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Hydra freshwater polyps have a remarkable ability to regenerate after bisection or even after dissociation, and thus offer a unique model system to investigate the cellular and molecular basis of eumetazoan regeneration. From a single cut along the body column two different types of regeneration arise: foot regeneration from the apical part and head regeneration from the basal part. The high proportion of stem cells in the Hydra body column supports these fast and efficient processes. Grafting experiments proved that the gastric tissue in the head‐regenerating tip rapidly develops a de novo organising activity, as evidenced by the induction of an ectopic axis when transplanted onto a host. The molecular mechanisms involved in this transformation rely on the immediate activation of the mitogen activated protein kinase (MAPK) pathway and the subsequent activation of the canonical Wnt3 pathway. This early phase is followed by a patterning phase, when head regeneration requires de novo neurogenesis. Key Concepts: Hydra is a bilayered freshwater solitary polyp that belongs to Cnidaria, a phylum that also includes jellyfish, sea anemones and corals. Cnidaria as sister group to bilaterians, belongs to Eumetazoa, that is, all animals that have a differentiated gut and nervous system. Hydra tissues contain three distinct stem cell populations that continuously cycle but cannot replace each other. The ectodermal and endodermal myoepithelial cells are differentiated cells that are also unipotent stem cells. These cells that cycle rather slowly provide all epithelial cells; however, these two lineages cannot replace each other. By contrast, the third lineage is multipotent, that is, the interstitial stem cells that cycle much faster (every 24–30 h) and provide nerve cells, nematocytes, gland cells as well as germinal cells. Head regeneration requires a complex 3D reconstruction when foot regeneration appears much simpler, similar to tissue repair. Head regeneration relies on a head organising activity that develops in several hours after bisection from the gastric tissue in the regenerating tip. This activity can be quantified at every time point of the regenerative process by lateral transplantation. Successive waves of gene and protein regulations characterise each phase of head regeneration: immediate, early, early‐late and late. The immediate activation of the MAPK/RSK/CREB pathway followed by the early activation of the Wnt3 pathway participates in the establishment of the head organising activity. After midgastric bisection, activation of the MAPK pathway leads to injury‐induced apoptosis of the interstitial cells, a cellular event that initiates head regeneration by activating the Wnt3 pathway in interstitial progenitors and subsequently in endodermal epithelial cells. Head regeneration in Hydra is highly plastic, as it is maintained, although at a slower pace, when cell cycling is transiently inhibited or slowed down in the early phase of head regeneration. This suggests that cell proliferation is not essential for Hydra regeneration, at least during the early phase, a condition named morphallaxis. Interstitial cycling cells play an important role at the early phase of head regeneration: those located at the tip receive signals from the apoptotic cells and rapidly divide, whereas those located more distantly migrate towards the wound. Both processes lead to the formation of a dense zone of progenitors in the regenerating tip. Head regeneration in Hydra is highly plastic, as it is maintained after elimination of the interstitial cell lineage, indicating that epithelial cells alone can drive the head regeneration process efficiently although with a significant delay. Since 2002, transgenic strategies were successfully developed in Hydra , allowing first the transient expression of reporter constructs, and since 2006 the establishment of stable transgenic lines.

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Molecular Signatures of the Three Stem Cell Lineages in Hydra and the Emergence of Stem Cell Function at the Base of Multicellularity

Cited by 145 publications

References 72 publications

Naturally occurring tumours in the basal metazoan Hydra

Naturally occurring tumours in the basal metazoan Hydra

Evolutionary history of the mammalian synaptonemal complex

Regeneration inHydra

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