Genetic analysis of developmental mechanisms in hydra

Terada, Hiroyuki; Sugiyama, T.; Shigenaka, Yoshinobu

doi:10.1016/0012-1606(88)90137-6

Cited by 29 publications

(10 citation statements)

References 10 publications

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“…When expression of XPF was compared across three main stem cell types of hydra – ectodermal epithelial, endodermal epithelial, and interstitial cells – it was found to be predominant in the interstitial cells ( Figure 9B ). The results were confirmed using sf-1, a temperature sensitive variant of H. magnipapillata , that loses its interstitial cells at non-permissive temperature ( Terada et al, 1988 ). In interstitial cell-depleted hydra, expression of XPF as seen by semi-quantitative RT-PCR, decreased almost 3-fold, showing direct correlation between the number of interstitial cells and the level of XPF expression ( Figure 9C ; Barve et al, 2013b ).…”

Section: Ner Pathway Genes In Hydramentioning

confidence: 68%

DNA Repair Repertoire of the Enigmatic Hydra

2021

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Since its discovery by Abraham Trembley in 1744, hydra has been a popular research organism. Features like spectacular regeneration capacity, peculiar tissue dynamics, continuous pattern formation, unique evolutionary position, and an apparent lack of organismal senescence make hydra an intriguing animal to study. While a large body of work has taken place, particularly in the domain of evolutionary developmental biology of hydra, in recent years, the focus has shifted to molecular mechanisms underlying various phenomena. DNA repair is a fundamental cellular process that helps to maintain integrity of the genome through multiple repair pathways found across taxa, from archaea to higher animals. DNA repair capacity and senescence are known to be closely associated, with mutations in several repair pathways leading to premature ageing phenotypes. Analysis of DNA repair in an animal like hydra could offer clues into several aspects including hydra’s purported lack of organismal ageing, evolution of DNA repair systems in metazoa, and alternative functions of repair proteins. We review here the different DNA repair mechanisms known so far in hydra. Hydra genes from various DNA repair pathways show very high similarity with their vertebrate orthologues, indicating conservation at the level of sequence, structure, and function. Notably, most hydra repair genes are more similar to deuterostome counterparts than to common model invertebrates, hinting at ancient evolutionary origins of repair pathways and further highlighting the relevance of organisms like hydra as model systems. It appears that hydra has the full repertoire of DNA repair pathways, which are employed in stress as well as normal physiological conditions and may have a link with its observed lack of senescence. The close correspondence of hydra repair genes with higher vertebrates further demonstrates the need for deeper studies of various repair components, their interconnections, and functions in this early metazoan.

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Section: Ner Pathway Genes In Hydramentioning

confidence: 68%

DNA Repair Repertoire of the Enigmatic Hydra

2021

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“…To investigate how epithelial cells adapt to the loss of neurogenesis, we used three well-established procedures that deplete the stock of cycling interstitial cells and abolish neurogenesis in Hydra , either chemically with HU [ 21 ] or Col [ 22 ] treatments, or physically through HS applied to the thermosensitive strain Hv_Sf1 [ 24 , 27 ] ( figure 2 a ) . HU and Col both inhibit cell cycle progression, although at distinct phases, DNA replication for HU, microtubule polymerization and mitotic progression for Col. As a consequence, cycling interstitial cells undergo cell death within 2 days, similarly to the heat-sensitive cycling interstitial cells of the Hv_Sf1 strain upon HS [ 54 , 55 ]. To verify the efficiency of these procedures, we examined the cellular composition of epidermis of animals exposed to one or the other treatment and we noted the absence of i-cells and nematoblasts 7–10 days after treatment ( figure 2 b ).…”

Section: Resultsmentioning

confidence: 99%

“…Seven days after the third HU pulse or after HS treatment (i.e. on day 11), i-cells, which normally represent 20–26% of the total cell number [ 54 ], decrease to less than 2% and nematoblasts are completely absent, whereas nematocytes, nerve and gland cells are still present. The effect of Col treatment is more pronounced, also affecting the differentiated cells of the interstitial lineage (nematocytes, neurons, gland cells) whose number is rapidly reduced ( figure 2 c ).…”

Section: Resultsmentioning

confidence: 99%

Loss of neurogenesis inHydraleads to compensatory regulation of neurogenic and neurotransmission genes in epithelial cells

Wenger¹,

Buzgariu²,

Galliot³

2016

Phil. Trans. R. Soc. B

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Hydra continuously differentiates a sophisticated nervous system made of mechanosensory cells (nematocytes) and sensory–motor and ganglionic neurons from interstitial stem cells. However, this dynamic adult neurogenesis is dispensable for morphogenesis. Indeed animals depleted of their interstitial stem cells and interstitial progenitors lose their active behaviours but maintain their developmental fitness, and regenerate and bud when force-fed. To characterize the impact of the loss of neurogenesis in Hydra, we first performed transcriptomic profiling at five positions along the body axis. We found neurogenic genes predominantly expressed along the central body column, which contains stem cells and progenitors, and neurotransmission genes predominantly expressed at the extremities, where the nervous system is dense. Next, we performed transcriptomics on animals depleted of their interstitial cells by hydroxyurea, colchicine or heat-shock treatment. By crossing these results with cell-type-specific transcriptomics, we identified epithelial genes up-regulated upon loss of neurogenesis: transcription factors (Dlx, Dlx1, DMBX1/Manacle, Ets1, Gli3, KLF11, LMX1A, ZNF436, Shox1), epitheliopeptides (Arminins, PW peptide), neurosignalling components (CAMK1D, DDCl2, Inx1), ligand-ion channel receptors (CHRNA1, NaC7), G-Protein Coupled Receptors and FMRFRL. Hence epitheliomuscular cells seemingly enhance their sensing ability when neurogenesis is compromised. This unsuspected plasticity might reflect the extended multifunctionality of epithelial-like cells in early eumetazoan evolution.

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“…To confirm above results we used sf-1, a temperature sensitive variant of H. magnipapillata that loses its interstitial cells at non-permissive temperature (28°C) [31], [32]. XPF expression was analysed by semi-quantitative RT-PCR in sf-1 and control wild-type H. magnipapillata independently exposed to permissive (18°C) and non-permissive temperatures.…”

Section: Resultsmentioning

confidence: 99%

Conservation of the Nucleotide Excision Repair Pathway: Characterization of Hydra Xeroderma Pigmentosum Group F Homolog

Barve

Ghaskadbi

2013

PLoS ONE

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Hydra, one of the earliest metazoans with tissue grade organization and nervous system, is an animal with a remarkable regeneration capacity and shows no signs of organismal aging. We have for the first time identified genes of the nucleotide excision repair (NER) pathway from hydra. Here we report cloning and characterization of hydra homolog of xeroderma pigmentosum group F (XPF) gene that encodes a structure-specific 5′ endonuclease which is a crucial component of NER. In silico analysis shows that hydra XPF amino acid sequence is very similar to its counterparts from other animals, especially vertebrates, and shows all features essential for its function. By in situ hybridization, we show that hydra XPF is expressed prominently in the multipotent stem cell niche in the central region of the body column. Ectoderm of the diploblastic hydra was shown to express higher levels of XPF as compared to the endoderm by semi-quantitative RT-PCR. Semi-quantitative RT-PCR analysis also demonstrated that interstitial cells, a multipotent and rapidly cycling stem cell lineage of hydra, express higher levels of XPF mRNA than other cell types. Our data show that XPF and by extension, the NER pathway is highly conserved during evolution. The prominent expression of an NER gene in interstitial cells may have implications for the lack of senescence in hydra.

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Genetic analysis of developmental mechanisms in hydra

Cited by 29 publications

References 10 publications

DNA Repair Repertoire of the Enigmatic Hydra

DNA Repair Repertoire of the Enigmatic Hydra

Loss of neurogenesis inHydraleads to compensatory regulation of neurogenic and neurotransmission genes in epithelial cells

Conservation of the Nucleotide Excision Repair Pathway: Characterization of Hydra Xeroderma Pigmentosum Group F Homolog

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