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Idk why I thought it was bo I and J Mc17 -positive nematoblasts and cniwi -positive interstitial stem cells. K Mc17 -positive nematoblasts. L Cniwi -negative nematocyte. M— O Coexpression of mc17 and cniwi in nematoblasts. P Cniwi -positive nematocyte. As shown previously 19 — 22 , interstitial stem cells express cniwi and cnvas1 whereas nematoblast precursors specifically express the minicollagen mc We therefore asked next if foxO overexpression in interstitial cells could affect the expression of stem cell genes.
As assessed by double in situ hybridization in polyps transfected with the control construct, nematocyte precursors express minicollagen mc17 whereas interstitial stem cells express cniwi Fig. Mature nematocytes never express cniwi Fig. In transgenic polyps overexpressing foxO in the interstitial cell lineage, we observe not only a higher density of nematoblast progenitor cells Fig.
Most strikingly, cniwi transcripts can even be found in terminally differentiated nematocytes such as stenoteles or isorhizas in both transgenic lines Figs. Thus, overexpression of foxO appears to induce expression of stem cell genes in terminally differentiated somatic cells.
This finding resembles earlier observations in C. To further investigate functions of FoxO in Hydra stem cells, we knocked down its expression in ectodermal and endodermal epithelial cells using a stable hairpin transcription approach Fig. We have analyzed six independent transgenic lines three endodermal, two ectodermal, and one ecto- and endodermal. By examining the expression patterns of endodermal transcription factors known to be important for foot formation, we observed that both nk2 homeobox nk2 2 and erythroblast transformation-specific 2 ets2 are strongly expressed in the enlarged stalk structures Fig.
Measuring of the expression field of pedibin revealed Fig. The finding that mc17 -expressing progenitor cells, which normally are never present in foot tissue, are absent from the enlarged stalks of transgenic polyps Fig. S5 B supports this view. Quantification of growth rate under standard culture conditions shows that polyps with foxO -deficient endoderm have a reduced population growth rate, with a doubling time of 6 d compared with 4 d for the control transgenic line Fig.
A Construct used for foxO down-regulation. As indicated above Fig. We therefore wondered if FoxO is required for the expression of these genes in epithelial tissue. As shown in Fig. These findings indicate once more that cnvas1 and cniwi are FoxO target genes and resemble earlier observations in C.
Taken together, these observations raise the possibility that foxO -deficient epithelial cells are driven into terminal differentiation, indicating that FoxO function is necessary for stem cell self-renewal and continuous growth. Our findings are intriguing in light of prior data showing that FoxO plays a key role in controlling life span and stress resistance in both C. Analysis of the hydramacin , periculin2b , and arminin promoters reveals the presence of numerous FoxO-binding sites Fig. S6 , indicating that FoxO can directly bind to these regulatory regions, acting either as repressor or as transcriptional activator Thus, in addition to its importance in stem cell homeostasis, FoxO appears to have an unexpected role in controlling innate immune genes in Hydra.
By the following three lines of evidence we have established that FoxO controls stem cell behavior in Hydra summarized in Fig. S7 A and schematized in Fig. S7 B : i foxO is strongly expressed in all three stem cell lineages; ii overexpression of foxO in interstitial stem cells stimulates stem cell and progenitor cell proliferation and confers stemness by activation of stem cell genes to terminally differentiated cells such as nematocytes; and iii silencing of foxO in epithelial cells increases the number of terminally differentiated foot cells at the cost of growth rate and causes down-regulation of stem cell genes as well as changes in expression of genes controlling the functionality of the innate immune system.
Based on the findings in Hydra we propose a general model in which FoxO plays a key role in controlling longevity Fig. According to this model, in immortal Hydra the high expression of foxO in all three stem cell lineages is crucial for the continuous self-renewal capacity and unlimited life span as well as the continuous maintenance of the functionality of the innate immune system.
In contrast, the aging process of most organisms is caused by a reduction of foxO activity, which decreases functions of the immune system and stem cells. Aging in stem cell systems from flies to humans is associated with progressive loss of stem cell number and activity Experimental evidence in flies, worms, and mice indicates that changes in life span indeed can occur through changes in foxO expression.
Moreover, specific mutations in the sequence of foxO3a significantly increase human life span 9 — 13 , Model of the role of FoxO in controlling longevity. Decline of foxO expression results in aging and death. Increase of foxO expression delays aging by maintaining stem cell self-renewal and functionality of the immune system.
Universally expressed foxO in Hydra results in a continuous self-renewal capacity of stem cells and immortality. Our results also delineate a role for FoxO in innate immunity. AMPs in both plants and animals are activated through pattern recognition receptors in response to microbe-associated molecular patterns. Although our observations do not elucidate the precise genetic network responsible for FoxO-mediated AMP activation, they are consistent with previous observations in flies 33 and make a significant prediction: control of stem cell self-renewal may be tightly coupled to innate immune pathways, and aging may be the consequence of both reduced stem cell function and altered innate immune defense.
This may be a common feature in plants and animals because stem cells in the shoot apical meristem of plants express high levels of a peptide controlling immune signaling and microbe interaction Taken together, studies of FoxO in Hydra have several important implications.
They not only reveal FoxO as a molecular factor that has contributed to the early evolution of stem cells, but also highlight intriguing similarities between Hydra and other multicellular organisms including humans, in the mechanisms that maintain stemness 14 — 17 and control life span 9 , 12 , 13 , 23 , 36 , Thus, the work furthers our understanding of stem cell self-renewal at the beginning of animal evolution and also has implications for regenerative medicine and cellular aging.
Experiments were carried out using H. The stable knockdown of foxO was achieved by generating transgenic polyps expressing a foxO hairpin construct under control of actin promoter. As control, transgenic lines expressing eGFP in the endodermal and ectodermal epithelial cell and interstitial cell lineage, respectively, were used 3 , 4. SI Materials and Methods include more information. For analysis of cell proliferation, animals were exposed for 6 h to BrdU 39 , macerated 40 , and subjected to BrdU detection 39 as described previously.
Gene expression analysis in foxO gain-of-function and loss-of-function strains was done by in situ hybridization and double in situ hybridization as described previously 3 , Phylogenetic analyses were based on 31 amino acid sequences of the forkhead domain, aligned using ClustalW The most parsimonious tree was found using MEGA 4 Maximum-parsimony and Maximum-likelihood bootstrap values were calculated based on 1, replicates.
Bayesian posterior probabilities were calculated using MrBayes version 3. SI Materials and Methods includes more information. The authors declare no conflict of interest. Data deposition: The sequences reported in this paper have been deposited in the GenBank database accession nos. This article contains supporting information online at www.
National Center for Biotechnology Information , U. Published online Nov Klostermeier , b Javier A. Bosch a, 2. Ulrich C. Javier A. Thomas C. Author information Copyright and License information Disclaimer. E-mail: ed. Copyright notice. This article has been corrected. This article has been cited by other articles in PMC. Keywords: adult stem cell, differentiation. Open in a separate window. Discussion By the following three lines of evidence we have established that FoxO controls stem cell behavior in Hydra summarized in Fig.
Materials and Methods Animals and Culture Conditions. Generation of Transgenic H. BrdU Labeling and Detection. In Situ Hybridization. Phylogenetic Analysis. Supplementary Material Supporting Information: Click here to view. Footnotes The authors declare no conflict of interest. References 1. Mortality patterns suggest lack of senescence in hydra. Exp Gerontol. Bosch TC. Hydra and the evolution of stem cells. Khalturin K, et al. Transgenic stem cells in Hydra reveal an early evolutionary origin for key elements controlling self-renewal and differentiation.
Dev Biol. Transgenic Hydra allow in vivo tracking of individual stem cells during morphogenesis. The Hydra polyp: Nothing but an active stem cell community. Dev Growth Differ. Fujisawa T, Sugiyama T. Genetic analysis of developmental mechanisms in Hydra. Characterization of a nematocyst-deficient strain. J Cell Sci. Hemmrich G, Bosch TC.
Compagen, a comparative genomics platform for early branching metazoan animals, reveals early origins of genes regulating stem-cell differentiation. Hemmrich G, et al. Molecular signatures of the three stem cell lineages in hydra and the emergence of stem cell function at the base of multicellularity.
Mol Biol Evol. Flachsbart F, et al. The Drosophila forkhead transcription factor FOXO mediates the reduction in cell number associated with reduced insulin signaling. J Biol. Kenyon C.
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Pro]Risen and Ridd1ck Cheating. Legend]hydra vs Artofsunzi bo11 prize money? Remove game please - Match ID 1v1 by Dario. This article contains supporting information online at www. National Center for Biotechnology Information , U. Published online Nov Klostermeier , b Javier A. Bosch a, 2. Ulrich C. Javier A. Thomas C. Author information Copyright and License information Disclaimer.
E-mail: ed. Copyright notice. This article has been corrected. This article has been cited by other articles in PMC. Keywords: adult stem cell, differentiation. Open in a separate window. Discussion By the following three lines of evidence we have established that FoxO controls stem cell behavior in Hydra summarized in Fig.
Materials and Methods Animals and Culture Conditions. Generation of Transgenic H. BrdU Labeling and Detection. In Situ Hybridization. Phylogenetic Analysis. Supplementary Material Supporting Information: Click here to view. Footnotes The authors declare no conflict of interest. References 1. Mortality patterns suggest lack of senescence in hydra. Exp Gerontol. Bosch TC. Hydra and the evolution of stem cells.
Khalturin K, et al. Transgenic stem cells in Hydra reveal an early evolutionary origin for key elements controlling self-renewal and differentiation. Dev Biol. Transgenic Hydra allow in vivo tracking of individual stem cells during morphogenesis. The Hydra polyp: Nothing but an active stem cell community. Dev Growth Differ. Fujisawa T, Sugiyama T. Genetic analysis of developmental mechanisms in Hydra. Characterization of a nematocyst-deficient strain. J Cell Sci.
Hemmrich G, Bosch TC. Compagen, a comparative genomics platform for early branching metazoan animals, reveals early origins of genes regulating stem-cell differentiation. Hemmrich G, et al. Molecular signatures of the three stem cell lineages in hydra and the emergence of stem cell function at the base of multicellularity. Mol Biol Evol. Flachsbart F, et al. The Drosophila forkhead transcription factor FOXO mediates the reduction in cell number associated with reduced insulin signaling.
J Biol. Kenyon C. A pathway that links reproductive status to lifespan in Caenorhabditis elegans. Ann N Y Acad Sci. Li Y, et al. Hum Mol Genet. Salih DA, Brunet A. FoxO transcription factors in the maintenance of cellular homeostasis during aging. Curr Opin Cell Biol. Miyamoto K, et al. Foxo3a is essential for maintenance of the hematopoietic stem cell pool. Cell Stem Cell. Tothova Z, Gilliland DG. FoxO transcription factors and stem cell homeostasis: Insights from the hematopoietic system.
Renault VM, et al. FoxO3 regulates neural stem cell homeostasis. Paik JH, et al. FoxOs cooperatively regulate diverse pathways governing neural stem cell homeostasis. Zhang X, et al. FOXO1 is an essential regulator of pluripotency in human embryonic stem cells. Nat Cell Biol. The germ line and somatic stem cell gene Cniwi in the jellyfish Podocoryne carnea. Int J Dev Biol. Universal occurrence of the vasa-related genes among metazoans and their germline expression in Hydra.
Dev Genes Evol. Adamczyk P, et al. Minicollagen, a novel minicollagen isolated from Hydra, forms tubule structures in nematocysts. J Mol Biol. David CN, et al. Evolution of complex structures: Minicollagens shape the cnidarian nematocyst. Trends Genet. A soma-to-germline transformation in long-lived Caenorhabditis elegans mutants.
The novel signal peptides, pedibin and Hym, lower positional value thereby enhancing foot formation in hydra. Pawelec G. Immunosenescence comes of age. EMBO Rep. Bosch TC, et al. Uncovering the evolutionary history of innate immunity: The simple metazoan Hydra uses epithelial cells for host defence. Dev Comp Immunol. Augustin R, et al. Activity of the novel peptide arminin against multiresistant human pathogens shows the considerable potential of phylogenetically ancient organisms as drug sources.
Antimicrob Agents Chemother. How Hydra senses and destroys microbes. Semin Immunol. Jung S, et al. Hydramacin-1, structure and antibacterial activity of a protein from the basal metazoan Hydra. J Biol Chem. Greer EL, Brunet A. FOXO transcription factors at the interface between longevity and tumor suppression. Where simplicity meets complexity: Hydra, a model for host-microbe interactions.
Adv Exp Med Biol. Becker T, et al. FOXO-dependent regulation of innate immune homeostasis. Zeng Y, et al. FOXO transcription factors in ageing and cancer. Acta Physiol Oxf ; 1 — Mass culture of hydra: An improved method and its application to other aquatic invertebrates. Lab Anim. Pattern of epithelial cell cycling in hydra. David CN. A quantitative method for maceration of Hydra tissue. Two-color double-labeling in situ hybridization of whole-mount Hydra using RNA probes for five different Hydra neuropeptide preprohormones: Evidence for colocalization.
Cell Tissue Res. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res.
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