| BMC Evolutionary Biology | |
| The GPCR repertoire in the demosponge Amphimedon queenslandica: insights into the GPCR system at the early divergence of animals | |
| Helgi B Schiöth2  Narayanan Manoj1  Robert Fredriksson2  Michael J Williams2  Markus Sällman Almén2  Rohit Dnyansagar1  Arunkumar Krishnan2  | |
| [1] Department of Biotechnology, Indian Institute of Technology Madras, Chennai 600036, India;Department of Neuroscience, Functional Pharmacology, Uppsala University, Biomedical Center, Uppsala, 75 124, Sweden | |
| 关键词: Eumetazoa; Porifera; Signal transduction; Adhesion; G protein-coupled receptors; Neurotransmitters; | |
| Others : 1121729 DOI : 10.1186/s12862-014-0270-4 |
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| received in 2014-06-07, accepted in 2014-12-12, 发布年份 2014 | |
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【 摘 要 】
Background
G protein-coupled receptors (GPCRs) play a central role in eukaryotic signal transduction. However, the GPCR component of this signalling system, at the early origins of metazoans is not fully understood. Here we aim to identify and classify GPCRs in Amphimedon queenslandica (sponge), a member of an earliest diverging metazoan lineage (Porifera). Furthermore, phylogenetic comparisons of sponge GPCRs with eumetazoan and bilaterian GPCRs will be essential to our understanding of the GPCR system at the roots of metazoan evolution.
Results
We present a curated list of 220 GPCRs in the sponge genome after excluding incomplete sequences and false positives from our initial dataset of 282 predicted GPCR sequences obtained using Pfam search. Phylogenetic analysis reveals that the sponge genome contains members belonging to four of the five major GRAFS families including Glutamate (33), Rhodopsin (126), Adhesion (40) and Frizzled (3). Interestingly, the sponge Rhodopsin family sequences lack orthologous relationships with those found in eumetazoan and bilaterian lineages, since they clustered separately to form sponge specific groups in the phylogenetic analysis. This suggests that sponge Rhodopsins diverged considerably from that found in other basal metazoans. A few sponge Adhesions clustered basal to Adhesion subfamilies commonly found in most vertebrates, suggesting some Adhesion subfamilies may have diverged prior to the emergence of Bilateria. Furthermore, at least eight of the sponge Adhesion members have a hormone binding motif (HRM domain) in their N-termini, although hormones have yet to be identified in sponges. We also phylogenetically clarified that sponge has homologs of metabotropic glutamate (mGluRs) and GABA receptors.
Conclusion
Our phylogenetic comparisons of sponge GPCRs with other metazoan genomes suggest that sponge contains a significantly diversified set of GPCRs. This is evident at the family/subfamily level comparisons for most GPCR families, in particular for the Rhodopsin family of GPCRs. In summary, this study provides a framework to perform future experimental and comparative studies to further verify and understand the roles of GPCRs that predates the divergence of bilaterian and eumetazoan lineages.
【 授权许可】
2014 Krishnan et al.; licensee BioMed Central.
【 预 览 】
| Files | Size | Format | View |
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| 20150213010836812.pdf | 3294KB | ||
| Figure 5. | 131KB | Image | |
| Figure 4. | 105KB | Image | |
| Figure 3. | 123KB | Image | |
| Figure 2. | 116KB | Image | |
| Figure 1. | 96KB | Image |
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【 参考文献 】
- [1]Rask-Andersen M, Almen MS, Schioth HB: Trends in the exploitation of novel drug targets. Nat Rev Drug Discov 2011, 10(8):579-590.
- [2]Lagerström MC, Schiöth HB: Structural diversity of G protein-coupled receptors and significance for drug discovery. Nat Rev Drug Discov 2008, 7(4):339-357.
- [3]Schioth HB, Fredriksson R: The GRAFS classification system of G-protein coupled receptors in comparative perspective. Gen Comp Endocrinol 2005, 142(1–2):94-101.
- [4]Fredriksson R, Lagerstrom MC, Lundin LG, Schioth HB: The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol Pharmacol 2003, 63(6):1256-1272.
- [5]Brody T, Cravchik A: Drosophila melanogaster G protein-coupled receptors. J Cell Biol 2000, 150(2):F83-F88.
- [6]Krishnan A, Almen MS, Fredriksson R, Schioth HB: Remarkable similarities between the hemichordate (Saccoglossus kowalevskii) and vertebrate GPCR repertoire. Gene 2013, 526(2):122-133.
- [7]Nordstrom KJ, Fredriksson R, Schioth HB: The amphioxus (Branchiostoma floridae) genome contains a highly diversified set of G protein-coupled receptors. BMC Evol Biol 2008, 8:9. BioMed Central Full Text
- [8]Kamesh N, Aradhyam GK, Manoj N: The repertoire of G protein-coupled receptors in the sea squirt Ciona intestinalis. BMC Evol Biol 2008, 8:129. BioMed Central Full Text
- [9]Krishnan A, Almén MS, Fredriksson R, Schiöth HB: The origin of GPCRs: identification of mammalian like Rhodopsin, Adhesion, Glutamate and Frizzled GPCRs in fungi. PLoS ONE 2012, 7(1):e29817.
- [10]de Mendoza A, Sebe-Pedros A, Ruiz-Trillo I: The evolution of the GPCR signaling system in eukaryotes: modularity, conservation, and the transition to metazoan multicellularity. Genome Biol Evol 2014, 6(3):606-619.
- [11]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 DC, Zhai Y, Adamski M, Calcino A, Cummins SF, Goodstein DM, Harris C, Jackson DJ, Leys SP, Shu S, Woodcroft BJ, Vervoort M, Kosik KS, et al.: The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 2010, 466(7307):720-726.
- [12]Conaco C, Neveu P, Zhou H, Arcila ML, Degnan SM, Degnan BM, Kosik KS: Transcriptome profiling of the demosponge Amphimedon queenslandica reveals genome-wide events that accompany major life cycle transitions. BMC Genomics 2012, 13:209. BioMed Central Full Text
- [13]Sakarya O, Armstrong KA, Adamska M, Adamski M, Wang IF, Tidor B, Degnan BM, Oakley TH, Kosik KS: A post-synaptic scaffold at the origin of the animal kingdom. PLoS One 2007, 2(6):e506.
- [14]Adamska M, Larroux C, Adamski M, Green K, Lovas E, Koop D, Richards GS, Zwafink C, Degnan BM: Structure and expression of conserved Wnt pathway components in the demosponge Amphimedon queenslandica. Evol Dev 2010, 12(5):494-518.
- [15]King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chapman J, Fairclough S, Hellsten U, Isogai Y, Letunic I, Marr M, Pincus D, Putnam N, Rokas A, Wright KJ, Zuzow R, Dirks W, Good M, Goodstein D, Lemons D, Li W, Lyons JB, Morris A, Nichols S, Richter DJ, Salamov A, Sequencing JG, Bork P, Lim WA, Manning G, et al.: The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 2008, 451(7180):783-788.
- [16]Suga H, Chen Z, de Mendoza A, Sebe-Pedros A, Brown MW, Kramer E, Carr M, Kerner P, Vervoort M, Sanchez-Pons N, Torruella G, Derelle R, Manning G, Lang BF, Russ C, Haas BJ, Roger AJ, Nusbaum C, Ruiz-Trillo I: The Capsaspora genome reveals a complex unicellular prehistory of animals. Nat Commun 2013, 4:2325.
- [17]Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U, Kawashima T, Kuo A, Mitros T, Salamov A, Carpenter ML, Signorovitch AY, Moreno MA, Kamm K, Grimwood J, Schmutz J, Shapiro H, Grigoriev IV, Buss LW, Schierwater B, Dellaporta SL, Rokhsar DS: The Trichoplax genome and the nature of placozoans. Nature 2008, 454(7207):955-960.
- [18]Nordstrom KJ, Sallman Almen M, Edstam MM, Fredriksson R, Schioth HB: Independent HHsearch, Needleman–Wunsch-based, and motif analyses reveal the overall hierarchy for most of the G protein-coupled receptor families. Mol Biol Evol 2011, 28(9):2471-2480.
- [19]Degnan BM, Adamska M, Craigie A, Degnan SM, Fahey B, Gauthier M, Hooper JN, Larroux C, Leys SP, Lovas E, Richards GS: The demosponge amphimedon queenslandica: reconstructing the ancestral metazoan genome and deciphering the origin of animal multicellularity. CSH Protoc 2008, 2008:pdb emo108.
- [20]Leys SP, Hill A: The physiology and molecular biology of sponge tissues. Adv Mar Biol 2012, 62:1-56.
- [21]Fahey B, Degnan BM: Origin of animal epithelia: insights from the sponge genome. Evol Dev 2010, 12(6):601-617.
- [22]Miller DJ, Ball EE: Animal evolution: the enigmatic phylum placozoa revisited. Curr Biol 2005, 15(1):R26-R28.
- [23]Technau U, Steele RE: Evolutionary crossroads in developmental biology: Cnidaria. Development 2011, 138(8):1447-1458.
- [24]Watanabe H, Fujisawa T, Holstein TW: Cnidarians and the evolutionary origin of the nervous system. Dev Growth Differ 2009, 51(3):167-183.
- [25]Harmar AJ: Family-B G-protein-coupled receptors. Genome Biol 2001, 2(12):REVIEWS3013. BioMed Central Full Text
- [26]Nordström KJV, Lagerström MC, Wallér LMJ, Fredriksson R, Schiöth HB: The Secretin GPCRs Descended from the Family of Adhesion GPCRs. Mol Biol Evol 2009, 26(1):71-84.
- [27]Cardoso JC, Pinto VC, Vieira FA, Clark MS, Power DM: Evolution of secretin family GPCR members in the metazoa. BMC Evol Biol 2006, 6:108. BioMed Central Full Text
- [28]Fredriksson R, Schioth HB: The repertoire of G-protein-coupled receptors in fully sequenced genomes. Mol Pharmacol 2005, 67(5):1414-1425.
- [29]Resnick D, Pearson A, Krieger M: The SRCR superfamily: a family reminiscent of the Ig superfamily. Trends Biochem Sci 1994, 19(1):5-8.
- [30]Sarrias MR, Gronlund J, Padilla O, Madsen J, Holmskov U, Lozano F: The Scavenger Receptor Cysteine-Rich (SRCR) domain: an ancient and highly conserved protein module of the innate immune system. Crit Rev Immunol 2004, 24(1):1-37.
- [31]Riesgo A, Farrar N, Windsor PJ, Giribet G, Leys SP: The analysis of eight transcriptomes from all poriferan classes reveals surprising genetic complexity in sponges. Mol Biol Evol 2014, 31(5):1102-1120.
- [32]Martindale MQ: The evolution of metazoan axial properties. Nat Rev Genet 2005, 6(12):917-927.
- [33]Muller WE: The origin of metazoan complexity: porifera as integrated animals. Integr Comp Biol 2003, 43(1):3-10.
- [34]Jekely G: Global view of the evolution and diversity of metazoan neuropeptide signaling. Proc Natl Acad Sci U S A 2013, 110(21):8702-8707.
- [35]Strotmann R, Schrock K, Boselt I, Staubert C, Russ A, Schoneberg T: Evolution of GPCR: change and continuity. Mol Cell Endocrinol 2011, 331(2):170-178.
- [36]Mirabeau O, Joly JS: Molecular evolution of peptidergic signaling systems in bilaterians. Proc Natl Acad Sci U S A 2013, 110(22):E2028-E2037.
- [37]Anctil M: Chemical transmission in the sea anemone Nematostella vectensis: a genomic perspective. Comp Biochem Physiol Part D Genomics Proteomics 2009, 4(4):268-289.
- [38]Ryan JF, Pang K, Schnitzler CE, Nguyen AD, Moreland RT, Simmons DK, Koch BJ, Francis WR, Havlak P, Smith SA, Putnam NH, Haddock SH, Dunn CW, Wolfsberg TG, Mullikin JC, Martindale MQ, Baxevanis AD: The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 2013, 342(6164):1242592.
- [39]Holland LZ, Carvalho JE, Escriva H, Laudet V, Schubert M, Shimeld SM, Yu JK: Evolution of bilaterian central nervous systems: a single origin? Evodevo 2013, 4(1):27. BioMed Central Full Text
- [40]Brooke NM, Holland PW: The evolution of multicellularity and early animal genomes. Curr Opin Genet Dev 2003, 13(6):599-603.
- [41]Abedin M, King N: Diverse evolutionary paths to cell adhesion. Trends Cell Biol 2010, 20(12):734-742.
- [42]Ruiz-Trillo I, Burger G, Holland PW, King N, Lang BF, Roger AJ, Gray MW: The origins of multicellularity: a multi-taxon genome initiative. Trends Genet 2007, 23(3):113-118.
- [43]Lange M, Norton W, Coolen M, Chaminade M, Merker S, Proft F, Schmitt A, Vernier P, Lesch KP, Bally-Cuif L: The ADHD-susceptibility gene lphn3.1 modulates dopaminergic neuron formation and locomotor activity during zebrafish development. Mol Psychiatry 2012, 17(9):946-954.
- [44]Arcos-Burgos M, Jain M, Acosta MT, Shively S, Stanescu H, Wallis D, Domene S, Velez JI, Karkera JD, Balog J, Berg K, Kleta R, Gahl WA, Roessler E, Long R, Lie J, Pineda D, Londoño AC, Palacio JD, Arbelaez A, Lopera F, Elia J, Hakonarson H, Johansson S, Knappskog PM, Haavik J, Ribases M, Cormand B, Bayes M, Casas M, et al.: A common variant of the latrophilin 3 gene, LPHN3, confers susceptibility to ADHD and predicts effectiveness of stimulant medication. Mol Psychiatry 2010, 15(11):1053-1066.
- [45]Langenhan T, Aust G, Hamann J: Sticky signaling--adhesion class G protein-coupled receptors take the stage. Sci Signal 2013, 6(2):re3.
- [46]Silva JP, Lelianova VG, Ermolyuk YS, Vysokov N, Hitchen PG, Berninghausen O, Rahman MA, Zangrandi A, Fidalgo S, Tonevitsky AG, Dell A, Volynski KE, Ushkaryov YA: Latrophilin 1 and its endogenous ligand Lasso/teneurin-2 form a high-affinity transsynaptic receptor pair with signaling capabilities. Proc Natl Acad Sci U S A 2011, 108(29):12113-12118.
- [47]Boucard AA, Ko J, Sudhof TC: High affinity neurexin binding to cell adhesion G-protein-coupled receptor CIRL1/latrophilin-1 produces an intercellular adhesion complex. J Biol Chem 2012, 287(12):9399-9413.
- [48]O’Sullivan ML, de Wit J, Savas JN, Comoletti D, Otto-Hitt S, Yates JR 3rd, Ghosh A: FLRT proteins are endogenous latrophilin ligands and regulate excitatory synapse development. Neuron 2012, 73(5):903-910.
- [49]Aumailley M: The laminin family. Cell Adh Migr 2013, 7(1):48-55.
- [50]van Roy F, Berx G: The cell-cell adhesion molecule E-cadherin. Cell Mol Life Sci 2008, 65(23):3756-3788.
- [51]Halbleib JM, Nelson WJ: Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev 2006, 20(23):3199-3214.
- [52]Paavola KJ, Hall RA: Adhesion G protein-coupled receptors: signaling, pharmacology, and mechanisms of activation. Mol Pharmacol 2012, 82(5):777-783.
- [53]DeLorey RWOaTM,: GABA Synthesis, Uptake and Release. 6th edition. Lippincott-Raven, Philadelphia; 1999.
- [54]Eichinger L, Pachebat JA, Glockner G, Rajandream MA, Sucgang R, Berriman M, Song J, Olsen R, Szafranski K, Xu Q, Tunggal B, Kummerfeld S, Madera M, Konfortov BA, Rivero F, Bankier AT, Lehmann R, Hamlin N, Davies R, Gaudet P, Fey P, Pilcher K, Chen G, Saunders D, Sodergren E, Davis P, Kerhornou A, Nie X, Hall N, Anjard C, et al.: The genome of the social amoeba Dictyostelium discoideum. Nature 2005, 435(7038):43-57.
- [55]Prabhu Y, Muller R, Anjard C, Noegel AA: GrlJ, a Dictyostelium GABAB-like receptor with roles in post-aggregation development. BMC Dev Biol 2007, 7:44. BioMed Central Full Text
- [56]Skerry TM, Genever PG: Glutamate signalling in non-neuronal tissues. Trends Pharmacol Sci 2001, 22(4):174-181.
- [57]Elliott GRD, Leys SP: Evidence for glutamate, GABA and NO in coordinating behaviour in the sponge, Ephydatia muelleri (Demospongiae, Spongillidae). J Exp Biol 2010, 213(13):2310-2321.
- [58]Moroz LL, Kocot KM, Citarella MR, Dosung S, Norekian TP, Povolotskaya IS, Grigorenko AP, Dailey C, Berezikov E, Buckley KM, Ptitsyn A, Reshetov D, Mukherjee K, Moroz TP, Bobkova Y, Yu F, Kapitonov VV, Jurka J, Bobkov YV, Swore JJ, Girardo DO, Fodor A, Gusev F, Sanford R, Bruders R, Kittler E, Mills CE, Rast JP, Derelle R, Solovyev VV, et al.: The ctenophore genome and the evolutionary origins of neural systems. Nature 2014, 510(7503):109-114.
- [59]Nedergaard M, Takano T, Hansen AJ: Beyond the role of glutamate as a neurotransmitter. Nat Rev Neurosci 2002, 3(9):748-755.
- [60]Niimura Y: On the origin and evolution of vertebrate olfactory receptor genes: comparative genome analysis among 23 chordate species. Genome Biol Evol 2009, 1:34-44.
- [61]Krishnan A, Almen MS, Fredriksson R, Schioth HB: Insights into the origin of nematode chemosensory GPCRs: putative orthologs of the Srw family are found across several phyla of protostomes. PLoS One 2014, 9(3):e93048.
- [62]Nikitin M: Bioinformatic prediction of Trichoplax adhaerens regulatory peptides. Gen Comp Endocrinol 2014, pii: S0016-6480(14)00126-9.
- [63]Kersey PJ, Staines DM, Lawson D, Kulesha E, Derwent P, Humphrey JC, Hughes DS, Keenan S, Kerhornou A, Koscielny G, Langridge N, McDowall MD, Megy K, Maheswari U, Nuhn M, Paulini M, Pedro H, Toneva I, Wilson D, Yates A, Birney E: Ensembl Genomes: an integrative resource for genome-scale data from non-vertebrate species. Nucleic Acids Res 2012, 40(Database issue):D91-D97.
- [64]Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor M, Goodstein D, Kuo A, Minovitsky S, Nikitin R, Ohm RA, Otillar R, Poliakov A, Ratnere I, Riley R, Smirnova T, Rokhsar D, Dubchak I: The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res 2012, 40(Database issue):D26-D32.
- [65]Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer ELL, Eddy SR, Bateman A, Finn RD: The Pfam protein families database. Nucleic Acids Res 2011, 40(D1):D290-D301.
- [66]Eddy SR: Accelerated profile HMM searches. PLoS Comput Biol 2011, 7(10):e1002195.
- [67]Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz HR, Ceric G, Forslund K, Eddy SR, Sonnhammer ELL, Bateman A: The Pfam protein families database. Nucleic Acids Res 2007, 36(Database):D281-D288.
- [68]Käll L, Krogh A, Sonnhammer ELL: A combined transmembrane topology and signal peptide prediction method. J Mol Biol 2004, 338(5):1027-1036.
- [69]Tusnády GE, Simon I: The HMMTOP transmembrane topology prediction server. Bioinformatics 2001, 17(9):849-850.
- [70]Katoh K, Toh H: Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 2008, 9(4):286-298.
- [71]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19(12):1572-1574.
- [72]Stamatakis A: RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22(21):2688-2690.
- [73]Darriba D, Taboada GL, Doallo R, Posada D: ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 2011, 27(8):1164-1165.
- [74]Whelan S, Goldman N: A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 2001, 18(5):691-699.
- [75]Krishnan A, Dnyansagar R, Almén MS, Williams MJ, Fredriksson R, Narayanan M, Schiöth HB: Data from: The GPCR repertoire in the demosponge Amphimedon queenslandica: insights into the GPCR system at the early divergence of animals. Dryad Data Repository. doi: 10.5061/dryad.43t7r.
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