Retinoic acid down-regulates the expression of EmH-3 homeobox-containing gene in the freshwater sponge Ephydatia muelleri

Nikko, Elina; Vyver, Gisèle Van De; Richelle-Maurer, Evelyn

doi:10.1016/s0047-6374(01)00235-4

Cited by 17 publications

(14 citation statements)

References 54 publications

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“…Although there are now some data on devel- opmental roles of RA signaling emerging from invertebrate chordates, there is still an obvious lack of information on the role(s) of RA in non-chordates. Even if low concentrations of 9-cis and all-trans RA have been observed in regenerating limb blastemas of the crab Uca pugilator (Hopkins, 2001) and effects of treatments with RA agonists or antagonists have been described in sea urchins (Sciarrino and Matranga, 1995;Kuno et al, 1999), mollusks (Créton et al, 1993) crustaceans (Chung et al, 1998;Hopkins, 2001;Söderhäll et al, 2006), insects (Picking et al, 1996;Shim et al, 1997;Sun et al, 1993), planarians (Romero and Bueno, 2001), cnidarians (Müller, 1984), and sponges (Imsiecke et al, 1994;Nikko et al, 2001;Wiens et al, 2003), the actual presence and putative roles of RA signaling during development in these taxa remain elusive. Thus, to fully understand the origin and evolution of RA signaling during embryonic development, we need to broaden the sampling of animal taxa and apply more sophisticated experimental tools to non-vertebrate model systems.…”

Section: Discussionmentioning

confidence: 99%

Retinoic acid signaling in development: Tissue‐specific functions and evolutionary origins

Campo-Paysaa

Marlétaz

Laudet

et al. 2008

Genesis

118

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Summary: Retinoic acid (RA) is a vitamin A-derived morphogen important for axial patterning and organ formation in developing vertebrates and invertebrate chordates (tunicates and cephalochordates). Recent analyses of genomic data have revealed that the molecular components of the RA signaling cascade are also present in other invertebrate groups, such as hemichordates and sea urchins. In this review, we reassess the evolutionary origins of the RA signaling pathway by examining the presence of key factors of this signaling cascade in different metazoan genomes and by comparing tissue-specific roles for RA during development of different animals. This discussion of genomic and developmental data suggests that RA signaling might have originated earlier in metazoan evolution than previously thought. On the basis of this hypothesis, we conclude by proposing a scenario for the evolution of RA functions during development, which highlights functional gains and lineage-specific losses during metazoan diversification. genesis 46:640-656,

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Section: Discussionmentioning

confidence: 99%

Retinoic acid signaling in development: Tissue‐specific functions and evolutionary origins

Campo-Paysaa

Marlétaz

Laudet

et al. 2008

Genesis

118

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“…We show using the primmorph system that retinoic acid causes both an involution of the intact S. domuncula organisms under formation of the asexual reproduction bodies, the gemmules, and a similar regression in vitro. Using retinoic acid concentrations that cause similar effects in other sponge systems, especially in freshwater sponges (Imsiecke et al, 1994;Nikko et al, 2001). Sponges, individuals and primmorphs, reacted to concentrations of 1-50·µmol·l -1 retinoic acid by tissue regression.…”

Section: Discussionmentioning

confidence: 99%

“…In the freshwater sponge Ephydatia muelleri, however, retinoic acid initiates morphogenetic events leading to formation of buds/gemmules (Imsiecke et al, 1994). At micromolar concentrations, retinoic acid causes a downregulation in the expression of the EmH-3 homeobox-containing gene in E. muelleri (Nikko et al, 2001), which led the authors to conclude that retinoic acid and the responsive EmH-3 gene are involved in differentiation and redifferentiation of archaeocytes to choanocytes, and hence in formation of a functional aquiferous system.…”

mentioning

confidence: 99%

Retinoid X receptor and retinoic acid response in the marine sponge Suberites domuncula

Wiens

Batel

Korzhev

et al. 2003

Journal of Experimental Biology

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SUMMARY To date no nuclear receptors have been identified or cloned from the phylogenetically oldest metazoan phylum, the Porifera (sponges). We show that retinoic acid causes tissue regression in intact individuals of the demosponge Suberites domuncula and in primmorphs, special three-dimensional cell aggregates. Primmorphs were cultivated on a galectin/poly-L-lysine matrix in order to induce canal formation. In the presence of 1 or 50 μmol l–1 retinoic acid these canals undergo regression, a process that is reversible. We also cloned the cDNA from S. domunculaencoding the retinoid X receptor (RXR), which displays the two motifs of nuclear hormone receptors, the ligand-binding and the DNA-binding domains, and performed phylogenetic analyses of this receptor. RXR expression undergoes strong upregulation in response to treatment with retinoic acid, whereas the expression of the sponge caspase is not increased. The gene encoding the LIM homeodomain protein was found to be strongly upregulated in response to retinoic acid treatment. These data indicate that the RXR and its ligand retinoic acid play a role in the control of morphogenetic events in sponges.

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“…The attractiveness of this model, which was highlighted by Yoko Watanabe through the film 'Life of the freshwater sponge' (Tokyo Film Corporation http://tokyocinema.net/EnglVieo.htm), has led to more recent studies on signalling and coordination of sponge behaviour (Elliott and Leys, 2007;Elliott and Leys, 2010), epithelia Adams, 2010), patterning and most recently, sensory cells (Ludeman et al, 2014). And since freshwater sponges are easily obtained and cultured in Europe, Japan and North America, there is a body of knowledge on the genetics of development (Richelle-Maurer et al, 1998;RichelleMaurer and Van de Vyver, 1999;Nikko et al, 2001;Funayama et al, 2005a;Funayama et al, 2005b;Mohri et al, 2008;Funayama et al, 2010;Holstien et al, 2010;Funayama, 2013) and even the possibility of using RNA interference methods (Rivera et al, 2011). Typically, gemmules are collected during winter months and kept refrigerated to hatch as needed in the lab, but it is also possible to keep a population over the long term by returning hatched batches to lakes.…”

Section: Model Systems In Poriferamentioning

confidence: 99%

Elements of a ‘nervous system’ in sponges

Leys

2015

Journal of Experimental Biology

128

123

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Genomic and transcriptomic analyses show that sponges possess a large repertoire of genes associated with neuronal processes in other animals, but what is the evidence these are used in a coordination or sensory context in sponges? The very different phylogenetic hypotheses under discussion today suggest very different scenarios for the evolution of tissues and coordination systems in early animals. The sponge genomic 'toolkit' either reflects a simple, pre-neural system used to protect the sponge filter or represents the remnants of a more complex signalling system and sponges have lost cell types, tissues and regionalization to suit their current suspensionfeeding habit. Comparative transcriptome data can be informative but need to be assessed in the context of knowledge of sponge tissue structure and physiology. Here, I examine the elements of the sponge neural toolkit including sensory cells, conduction pathways, signalling molecules and the ionic basis of signalling. The elements described do not fit the scheme of a loss of sophistication, but seem rather to reflect an early specialization for suspension feeding, which fits with the presumed ecological framework in which the first animals evolved.

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Retinoic acid down-regulates the expression of EmH-3 homeobox-containing gene in the freshwater sponge Ephydatia muelleri

Cited by 17 publications

References 54 publications

Retinoic acid signaling in development: Tissue‐specific functions and evolutionary origins

Retinoic acid signaling in development: Tissue‐specific functions and evolutionary origins

Retinoid X receptor and retinoic acid response in the marine sponge Suberites domuncula

Elements of a ‘nervous system’ in sponges

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