Abstract
We have identified eleven novel aminergic-like G-protein coupled receptor (GPCRs) sequences (named AmphiAmR1-11) by searching the genomic trace sequence database for the amphioxus species, Branchiostoma floridae. They share many of the structural motifs that have been used to characterize vertebrate and invertebrate aminergic GPCRs. A preliminary classification of these receptors has been carried out using both BLAST and Hidden Markov Model analyses. The amphioxus genome appears to express a number of D1-like dopamine receptor sequences, including one related to insect dopamine receptors. It also expresses a number of receptors that resemble invertebrate octopamine/tyramine receptors and others that resemble vertebrate α-adrenergic receptors. Amphioxus also expresses receptors that resemble vertebrate histamine receptors. Several of the novel receptor sequences have been identified in amphioxus cDNA libraries from a number of tissues.
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Airriess CN, Rudling JE, Midgley JM, Evans PD (1997) Selective inhibition of adenylyl cyclase by octopamine via a human cloned α2A-adrenoceptor. Brit J Pharmacol 122:191–198
Balfanz S, Strünker T, Frings S, Baumann A (2005) A family of octapamine receptors that specifically induce cyclic AMP production or Ca2+ release in Drosophila melanogaster. J Neurochem 93:440–451
Ballesteros JA, Weinstein WH (1995) Integrated methods for the construction of three-dimensional models and computational probing of structure-function relations in G-protein coupled receptors. Methods Neurosci 25:366–428
Bargmann CI (1998) The neurobiology of the Caenorhabditis elegans genome. Science 282:2028–2033
Beggs KT, Hamilton IS, Kurshan PT, Mustard JA, Mercer AR (2005) Characterization of a D2-like dopamine receptor (AmDOP3) in honeybee. Apis mellifera. Insect Biochem Mol Biol 35:873–882
Blenau W, Balfanz S, Baumann A (2000) Am tyr1. Characterization of a gene from honeybee (Apis mellifera) brain encoding a functional tyramine receptor. J Neurochem 74:900–908
Bockaert J, Pin JP (1999) Molecular tinkering of G-protein coupled receptors: an evolutionary success. EMBO J 18:1723–1729
Borowsky B, Adham N, Jones KA, Raddatz R, Artymyshyn R, Ogozalek KL, Durkin MM, Lakhlani PP, Bonini JA, Pathirana S, Boyle N, Pu X, Kouranova E, Lichtblau H, Ochoa FY, Branchek TA, Gerald C (2001) Trace amines: identification of a family of mammalian G-protein coupled receptors. Proc Natl Acad Sci USA 98:8966–8971
Brody T, Cravchik A (2000) Drosophila melanogaster G-protein coupled receptors. J Cell Biol 150:F83–F88
Callier S, Snapyan M, Le Crom S, Prou D, Vincent J-D, Vernier P (2003) Evolution and cell biology of dopamine receptors in vertebrates. Biol Cell 95:489–502
Candiani S, Augello A, Oliveri D, Passalacqua M, Pennati R, De Bernardi F, Pestarino M (2001) Immunocytochemical localization of serotonin in embryos, larvae and adults of the lancelet, Branchiostoma florida. Histochem J 33:413–420
Candiani S, Oliveri D, Parodi M, Castagnola P, Pestarino M (2005) AmphiD1/β, a dopamine D1/β-adrenergic receptor from the amphioxus Branchiostoma floridae: evolutionary aspects of the catecholaminergic system during development. Dev Genes Evol 215:631–638
Cardinaud B, Gibert J-M, Liu F, Sugamori KS, Vincent J-D, Niznik HB, Vernier P (1998) Evolution and origin of the diversity of dopamine receptors in vertebrates. Adv Pharmacol 42:936–940
Dehal P et al (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157–2167
Delsuc F, Brinkmann H, Chourrout D, Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965–968
Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763
Evans PD, Siegler MVS (1982) Octopamine mediated relaxation of maintained and catch tension in locust skeletal muscle. J Physiol (Lond) 324:93–112
Evans PD, Maqueira B (2005) Insect octopamine receptors; a new classification scheme based on studies of cloned Drosophila G-protein coupled receptors. Invert Neurosci 5:111–118
Evans PD, O’Shea M (1977) An octopaminergic neuron modulates neuromuscular transmission in the locust. Nature 270:257-259
Felsenstein J (1993) 3.6 edn. Department of Genetics, University of Washington, Washington
Flower DR (1999) Modelling G-protein coupled receptors for drug design. Biochim Biophys Acta 1422:207–234
Fredricksson R, Lagerström MC, Lundin L-G, Schiöth HB (2003) The G-protein coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups and fingerprints. Mol Pharmacol 63:1256–1272
Garcia-Fernàndez J (2006) Amphioxus: a peaceful anchovy fillet to illuminate chordate evolution (1). Int J Biol Sci 2:30–31
Gebhardt S, Homberg U (2004) Immunocytochemistry of histamine in the brain of the locust Schistocerca gregaria. Cell Tissue Res 317:195–205
Gee H (2006) Careful with that amphioxus. Nature 439:923–924
Gloriam DEI, Schiöth HB, Fredricksson R (2005) Nine new human Rhodopsin family G-protein coupled receptors: identification, sequence characterization and evolutionary relationship. Biochim Biophys Acta 17722:235–246
Graham A (2000) The evolution of the vertebrates—genes and development. Curr Opin Genet Dev 10:624–628
Han KA, Millar NS, Davis RL (1998) A novel octopamine receptor with preferential expression in Drosophila mushroom bodies. J Neurosci 18:3650–3658
Hauser F, Cazzamali G, Williamson M, Blenau W, Grimmelikhuijzen CJ (2006) A review of neurohormone GPCRs present in the fruitfly, Drosophila melanogaster, and the honeybee, Apis mellifera. Prog Neurobiol 80:1–19
Hearn MG, Ren Y, McBride EW, Reveillaud I, Beinborn M, Kopin AS (2002) A Drosophila dopamine 2-like receptor: molecular characterization and identification of multiple alternatively spliced variants. Proc Natl Acad Sci USA 99:14544–14559
Holland PW (1999) Gene duplication: past, present and future. Semin Cell Dev Biol 10:541–547
Holland LZ, Holland ND (1999) Chordate origins of the vertebrate central nervous system. Curr Opin Neurobiol 9:596–602
Holland ND, Holland LZ (1993) Serotonin-containing cells in the nervous system and other tissues during ontogeny of a lancelet. Branchiostoma floridae. Acta Zool (Stockh) 74:195–204
Horn F, Weare J, Beukers MW, Hörsch S, Bairoch A, Che W, Edvardsen Ø, Campagne F, Vriend G (1998) GPCRDB information system for G-protein coupled receptors. Nucleic Acids Res 31:294–297
Humphries MA, Mustard JA, Hunter SJ, Mercer A, Ward V, Ebert PR (2003) Invertebrate D2 type dopamine receptor exhibits age-based plasticity of expression in the mushroom body of the honeybee brain. J Neurobiol 55:315–330
Kapsimali M, Vidal B, Gonzalez A, Dufour S, Vernier P (2000) Distribution of the mRNA encoding the four dopamine D(1) receptor subtypes in the brain of the european eel (Anguilla anguilla): comparative approach to the function of D(1) receptors in vertebrates. J Comp Neurol 419:320–343
Kimura Y, Yoshida M, Morisawa M (2003) Interaction between noradrenaline or adrenaline and the β1-adrenergic receptor in the nervous system triggers early metamorphosis of larvae in the ascidian. Ciona savignyi. Dev Biol 258:129–140
Koyanagi M, Terakita A, Kubokawa K,.Shichida Y (2002) Amphioxus homologs of Go-coupled rhodopsin and peropsin having 11-cis- and all-trans- retinals as their chromophores. FEBS Lett 531:525–528
Krogh A, Larsson B, von Heijne G., Sonnhammer EL (2001) Predicting transmembrane protein topology with a Hidden Markov model: application to complete genomes. J Mol Biol 305:567–580
Le Crom S, Sugamori KS, Sidhu A, Niznik HB, Vernier P (2004) Delineation of the conserved functional properties of D1A, D1B and D1C dopamine receptor subtypes in vertebrates. Biol Cell 96:383–394
Maqueira B, Chatwin H, Evans PD (2005) Identification and characterization of a novel family of Drosophila β-adrenergic-like octopamine G-protein coupled receptors. J Neurochem 94:547–560
Moret F, Christiaen L, Deyts C, Blin M, Joly J-S, Vernier P (2005) The dopamine-synthesizing cells in the swimming larva of the tunicate Ciona intestinalis are located only in the hypothalamus-related domain of the sensory vesicle. Eur J Neurosci 21:3043–3055
Moret F, Guilland J-C, Coudouel S, Rochette L, Vernier P (2004) Distribution of tyrosine hydroxylase, dopamine, and serotonin in the central nervous system of amphioxus (Branchiostoma lanceolatum): implications for the evolution of catecholamine systems in vertebrates. J Comp Neurol 468:135–150
Mustard JA, Beggs KT, Mercer AR (2005) Molecular biology of the invertebrate dopamine receptors. Arch Insect Biochem Physiol 59:103–117
Panopoulou G, Hennig S, Groth D, Krause A, Poustka AJ, Herwig R, Vingron M, Lehrach H (2003) New evidence for genome-wide duplications at the origin of vertbrates using an Amphioxus gene set and completed animal genomes. Genome Res 13:1056–1066
Perez DM (2003) The evolutionary triumphant G-protein coupled receptor. Mol Pharmacol 63:1202–1205
Schubert M, Escriva H, Xavier-Neto J, Laudet V (2006) Amphioxus and tunicates as evolutionary model systems. Trends Ecol Evol 21:269–277
Shi L, Javitch JA (2002) The binding site of aminergic G-protein coupled receptors: the transmembrane segments and second extracellular loop. Ann Rev Pharmacol Toxicol 42:437–467
Srivastava DP, Reale V, Burman C, Chatwin H, Evans PD (2005a) Biogenic amines and steroids activate a β-adrenergic-like Amphioxus G-protein coupled receptor (GPCR). Soc Neurosci Abstr 31:34.18
Srivastava DP, Yu EJ, Kennedy K, Chatwin H, Reale V, Hamon M., Smith T, Evans PD (2005b) Rapid, non-genomic responses to ecdysteroids and catecholamines mediated by a novel Drosophila G-protein coupled receptor. J Neurosci 25:6145–6155
Staden R, Beal KF, Bonfield JK (2000) The Staden package, 1998. Meth Mol Biol 132: 115–130
Stajich JE, Block D, Boulez K, Brenner SE, Chervitz SA, Dagdigian C, Fuellen G, Gilbert JGR, Korf I, Lapp H, Lehvaslaiho H, Matsalla C, Mungall CJ, Osbourns BI, Pocock MR, Schattner P, Senger M, Stein LD, Stupka E, Wilkinson MD, Birney E (2002) The Bioperl toolkit: perl modules for the life sciences. Genome Res 12: 1611–1618
Thompson JD, Higgins DG, Gibson TJ (1994) ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Vanden Broeck J, Vulsteke V, Huybrechts R, DeLoof A (1995) Characterization of a cloned locust tyramine receptor cDNA by functional expression in permanently transformed Drosophila S2 cells. J Neurochem 64:2387–2395
Vernier P, Cardinaud B, Valdenaire O, Philippe H, Vincent J-D (1995) An evolutionary view of drug-receptor interaction: the bioamine receptor family. Trends Pharmacol Sci 16:375–381
Vincent JD, Cardinaud B, Vernier P (1998) L’évolution des récepteurs des monoamines et l’émergence des systèmes motivationnels et émotionnels chez les vertébrés. Bull Acad Natl Med 182:1505–1516
Xhaard H, Rantanen V-V, Nyrönen T, Johnson MS (2006) Molecular evolution of adrenoceptors and dopamine receptors: implications for the binding of catecholamines. J Med Chem 49:1706–1719
Zheng Y, Hirschberg B, Yuan J, Wang AP, Hunt DC, Ludmerer SW, Schmatz DM, Cully DF et al (2002) Identification of two novel Drosophila melanogaster histamine-gated chloride subunits expressed in the eye. J Biol Chem 277:2000–2005
Acknowledgments
This work was supported by the BBSRC through the Babraham Institute. We thank Dr. Mikhail Matz, Whitney Laboratory, University of Florida, St Augustine, USA for kindly supplying us with the amphioxus cDNA libraries used in this study.
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Burman, C., Maqueira, B., Coadwell, J. et al. Eleven new putative aminergic G-protein coupled receptors from Amphioxus (Branchiostoma floridae): identification, sequence analysis and phylogenetic relationship. Invert Neurosci 7, 87–98 (2007). https://doi.org/10.1007/s10158-006-0041-z
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DOI: https://doi.org/10.1007/s10158-006-0041-z