July 2012, 3:15,
Open Access This content is freely available online to anyone, anywhere at any time.
Date: 23 Jul 2012
The expression of Delta ligands in the sponge Amphimedon queenslandica suggests an ancient role for Notch signaling in metazoan development
Intercellular signaling via the Notch pathway regulates cell fate, patterning, differentiation and proliferation, and is essential for the proper development of bilaterians and cnidarians. To investigate the origins of the Notch pathway, we are studying its deployment in a representative of an early branching lineage, the poriferan Amphimedon queenslandica. The A. queenslandica genome encodes a single Notch receptor and five membrane-bound Delta ligands, as well as orthologs of many genes that enact and regulate canonical Notch signaling events in other animals.
In the present report we analyze the structure of the five A. queenslandica Deltas using bioinformatic methods, and characterize their developmental expression via whole mount in situ hybridization and histological staining.
Sequence analysis of the A. queenslandica Delta ligands highlights the conservation of their extracellular domains. This contrasts with the divergence of their intracellular regions, each of which is predicted to bear a unique repertoire of protein interaction motifs. In keeping with this diversity, these ligands are expressed differentially and dynamically throughout A. queenslandica embryogenesis, both in cell type specific patterns and broader regional domains. Notably, this expression coincides with the development of the photosensitive larval pigment ring, the non-ciliated cuboidal cells located at the anterior pole of the larva, and the intraepithelial flask cells and globular cells that are presumed to have sensory and/or secretory roles.
Based on the dynamic and complex patterns of expression of these Delta ligands and the Notch receptor, we propose that the Notch signaling pathway is involved in regulating the development of diverse cell types in A. queenslandica. From these observations we infer that Notch signaling is a conserved feature of metazoan development, ancestrally contributing to cell determination, patterning and differentiation processes.
Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier MEA, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, Larroux C, Putnam NH, Stanke M, Adamska M, Darling A, Degnan SM, Oakley TH, Plachetzki D, Zhai Y, Adamski M, Calcino A, Cummins SF, Goodstein DM, Harris C, Jackson D, Leys SP, Shu S, Woodcroft BJ, Vervoort M, Kosik KS, Manning G, Degnan BM, Rokhsar DS: The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 2010, 466:720–726.PubMedCrossRef
Artavanis-Tsakonas S, Matsuno K, Fortini ME: Notch signaling. Science 1995, 14:225–232.CrossRef
Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sørensen MV, Haddock SH, Schmidt-Rhaesa A, Okusu A, Kristensen RM, Wheeler WC, Martindale MQ, Giribet G: Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 2008, 452:745–749.PubMedCrossRef
Philippe H, Derelle R, Lopez P, Pick K, Borchiellini C, Boury-Esnault N, Vacelet J, Renard E, Houliston E, Queinnec E, Da Silva C, Wincker P, Le Guyader H, Leys S, Jackson DJ, Schreiber F, Erpenbeck D, Morgenstern B, Woerheide G, Manuel M: Phylogenomics revives traditional views on deep animal relationships. Curr Biol 2009, 19:706–712.PubMedCrossRef
Puntervoll P, Linding R, Gemund C, Chabanis-Davidson S, Mattingsda M, Cameron S, Martin DMA, Ausiello G, Brannetti B, Costantini A, Ferre F, Maselli V, Via A, Cesareni G, Diella F, Superti-Furga G, Wyrwicz L, Ramu C, McGuigan C, Gudavalli R, Letunic I, Bork P, Rychlewski L, Kuster B, Helmer-Citterich M, Hunter WN, Aasland R, Gibson TJ: ELM server: a new resource for investigating short functional sites in modular eukaryotic proteins. Nucleic Acids Res 2003, 31:3625–3630.PubMedCrossRef
Lissemore JL, Starmer WT: Phylogenetic analysis of vertebrate and invertebrate Delta/Serrate/Lag-2 (DSL) proteins. Mol Phylo Evol 1999, 11:308–319.CrossRef
Cordle J, Johnson S, Zi J, Tay Y, Roversi P, Wilkin MB, Hernández de Madrid B, Shimizu H, Jensen S, Whiteman P, Jin B, Redfield C, Baron M, Lea SM, Handford PA: A conserved face of the Jagged/Serrate DSL domain is involved in Notch trans-activation and cis-inhibition. Nat Struct Mol Biol 2008, 15:849–857.PubMedCrossRef
Sun X, Artavanis-Tsakonas S: Secreted forms of DELTA and SERRATE define antagonists of Notch signaling in Drosophila. Development 1997, 124:3439–3448.PubMed
Schweisguth F: Regulation of Notch signaling activity. Curr Biol 2004, 14:R129-R138.PubMed
Renard E, Vacelet J, Gazave E, Lapebie P, Borchiellini C, Ereskovsky AV: Origin of the neuro-sensory system: new and expected insights from sponges. Integ Zool 2009, 4:294–308.CrossRef
Degnan SM, Degnan BM: The initiation of metamorphosis as an ancient polyphenic trait and its role in metazoan life-cycle evolution. Phil Trans R Soc B 2010, 365:653–669.CrossRef
Leys SP, Degnan BM: Embryogenesis and metamorphosis in a haplosclerid demosponge: gastrulation and transdifferentiation of larval ciliated cells to choanocytes. Invert Biol 2002, 121:171–189.CrossRef
Haenlin H, Kramatschek B, Campos-Ortega JA: The pattern of transcription of the neurogenic gene Delta of Drosophila melanogaster. Development 1990, 110:905–914.PubMed
Müller WEG: The stem cell concept in sponges (Porifera): Metazoan traits. Sem Cell Dev Biol 2007, 17:481–491.CrossRef
Edgar RC: MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinforma 2004, 5:113.CrossRef
Galtier N, Gouy M, Gautier C: SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 1996, 12:543–548.PubMed
Leys SP, Larroux C, Gauthier M, Adamska M, Fahey B, Richards GS, Degnan SM, Degnan BM: Isolation of Amphimedon developmental material. CSH Protocols 2008.
Larroux C, Fahey B, Adamska M, Richards GS, Gautheir M, Green K, Lovas E, Degnan BM: Whole-mount in situ hybridization in Amphimedon. CSH Protocols 2008.
- The expression of Delta ligands in the sponge Amphimedon queenslandica suggests an ancient role for Notch signaling in metazoan development
- Open Access
- Available under Open Access This content is freely available online to anyone, anywhere at any time.
- Online Date
- July 2012
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- BioMed Central
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