The Evolution of Nuclear Receptors: Evidence from the Coral Acropora

Grasso, Lauretta C.; Hayward, David C.; Trueman, John W. H.; Hardie, Kate M.; Janssens, P.A.; Ball, Eldon E.

doi:10.1006/mpev.2001.0994

Cited by 47 publications

(46 citation statements)

References 44 publications

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“…(c) Nuclear receptor signalling [83,84]; thus, the expansive diversity in this group of proteins may have evolved with the independent origins of numerous diverse ligand binding capabilities [85]. Unlike the other cell signalling mechanisms discussed here, NRs act as both the receptor and the effector molecule, providing the most direct link between the extracellular signal and the transcriptional response.…”

Section: (B) Canonical Wnt Signallingmentioning

confidence: 99%

Phylogenetic evidence for the modular evolution of metazoan signalling pathways

Babonis¹,

Martindale²

2017

Phil. Trans. R. Soc. B

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One contribution of 17 to a theme issue 'Evo-devo in the genomics era, and the origins of morphological diversity'. Communication among cells was paramount to the evolutionary increase in cell type diversity and, ultimately, the origin of large body size. Across the diversity of Metazoa, there are only few conserved cell signalling pathways known to orchestrate the complex cell and tissue interactions regulating development; thus, modification to these few pathways has been responsible for generating diversity during the evolution of animals. Here, we summarize evidence for the origin and putative function of the intracellular, membrane-bound and secreted components of seven metazoan cell signalling pathways with a special focus on early branching metazoans (ctenophores, poriferans, placozoans and cnidarians) and basal unikonts (amoebozoans, fungi, filastereans and choanoflagellates). We highlight the modular incorporation of intra-and extracellular components in each signalling pathway and suggest that increases in the complexity of the extracellular matrix may have further promoted the modulation of cell signalling during metazoan evolution. Most importantly, this updated view of metazoan signalling pathways highlights the need for explicit study of canonical signalling pathway components in taxa that do not operate a complete signalling pathway. Studies like these are critical for developing a deeper understanding of the evolution of cell signalling.This article is part of the themed issue 'Evo-devo in the genomics era, and the origins of morphological diversity'.

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Section: (B) Canonical Wnt Signallingmentioning

confidence: 99%

Phylogenetic evidence for the modular evolution of metazoan signalling pathways

Babonis¹,

Martindale²

2017

Phil. Trans. R. Soc. B

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“…The orphan COUP-TF nuclear receptors form a highly evolutionarily-conserved family with COUP-TF homologues identified in a wide range of metazoans from cnidarians to protostomes and deuterostomes Escriva et al (1997), Langlois et al (2000), Grasso et al (2001), Devine et al (2002), Gauchat et al (submitted). These transcription factors show an extensive degree of homology in their DNA-binding as well as ligand-binding domains.…”

Section: Prdl-b and Hycoup-th Are Regulatory Genes Expressed In Both mentioning

confidence: 99%

Neuronal evolution: analysis of regulatory genes in a first-evolved nervous system, the hydra nervous system

2004

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Cnidarians represent the first animal phylum with an organized nervous system and a complex active behavior. The hydra nervous system is formed of sensory-motoneurons, ganglia neurons and mechanoreceptor cells named nematocytes, which all differentiate from a common stem cell. The neurons are organized as a nerve net and a subset of neurons participate in a more complex structure, the nerve ring that was identified in most cnidarian species at the base of the tentacles. In order to better understand the genetic control of this neuronal network, we analysed the expression of evolutionarily-conserved regulatory genes in the hydra nervous system. The PRD-CLASS homeogene, prdl-b, and the nuclear orphan receptor, hyCOUP-TF, are expressed at strong levels in proliferating nematoblasts, a lineage where they were found repressed during patterning and morphogenesis, and at low levels in distinct subsets of neurons. Interestingly, PRD-CLASS homeobox and COUP-TF genes are also expressed during neurogenesis in bilaterians, suggesting that mechanoreceptor and neuronal cells derive from a common ancestral cell. Moreover, the PRD-CLASS homeobox gene prdl-a, the ANTP-CLASS homeobox gene msh, and the thrombospondin-related gene TSP1, which are expressed in distinct subset of neurons in the adult polyp, are also expressed during early budding and/or head regeneration. These data strengthen the fact that two distinct regulations, one for neurogenesis and another for patterning, already apply to these regulatory genes, a feature also identified in bilaterian related-genes.

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“…The overall protein sequence similarity/identity of the sponge RXR to these metazoan sequences is around 20-35%. No nuclear receptor/nuclear hormone receptor molecule other than in Metazoans has been found in, for example, plants or yeast (see Grasso et al, 2001), indicating that the sponge RXR is phylogenetically the oldest one known. Fig.·2.…”

Section: Phylogenetic Analysis Of Sponge Rxr: Total Sequencementioning

confidence: 99%

“…In the coral Acropora millepora, receptors were detected that share some similarity to retinoid X receptors (RXRs) (Grasso et al, 2001), but to date molecular data on the presence of nuclear hormone receptors in the Porifera, the phylogenetically oldest metazoan phylum, are missing. Several RXRs are activated by known regulatory ligands; receptors for whom the ligands have not yet been identified were termed 'orphan receptors' (Aranda and Pascual, 2001).…”

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confidence: 99%

“…The decision to use RXR was based on the facts that (i) in sponges, retinoic acid causes morphogenetic responses, (ii) related receptors had already been isolated from the coral Acropora millepora (Grasso et al, 2001) and the Cnidarian Tripedalia cystophora (Kostrouch et al, 1998) and (iii) RXR heterodimerizes with other nuclear receptors. RXRs form heterodimers with orphan receptors involved in lipid metabolism; these receptors bind their ligands with lower affinity than the endocrine steroid receptors and function as lipid sensors/regulators (Chawla et al, 2001).…”

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confidence: 99%

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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 Evolution of Nuclear Receptors: Evidence from the Coral Acropora

Cited by 47 publications

References 44 publications

Phylogenetic evidence for the modular evolution of metazoan signalling pathways

Phylogenetic evidence for the modular evolution of metazoan signalling pathways

Neuronal evolution: analysis of regulatory genes in a first-evolved nervous system, the hydra nervous system

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

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