A Novel Dop2/Invertebrate-Type Dopamine Signaling System Potentially Mediates Stress, Female Reproduction, and Early Development in the Pacific Oyster (Crassostrea gigas).
Dop2/INDR
Dopamine receptor
Mollusk
Osmotic stress
Reproduction
Tyramine receptor
Journal
Marine biotechnology (New York, N.Y.)
ISSN: 1436-2236
Titre abrégé: Mar Biotechnol (NY)
Pays: United States
ID NLM: 100892712
Informations de publication
Date de publication:
Oct 2021
Oct 2021
Historique:
received:
29
04
2021
accepted:
20
07
2021
pubmed:
9
8
2021
medline:
11
11
2021
entrez:
8
8
2021
Statut:
ppublish
Résumé
The dopaminergic signaling pathway is involved in many physiological functions in vertebrates, but poorly documented in protostome species except arthropods. We functionally characterized a novel dopamine receptor in the Pacific oyster (Crassostrea gigas), activated by dopamine and tyramine with different efficacy and potency orders. This receptor - Cragi-DOP2R - belongs to the D
Identifiants
pubmed: 34365528
doi: 10.1007/s10126-021-10052-5
pii: 10.1007/s10126-021-10052-5
doi:
Substances chimiques
Receptors, Dopamine
0
Dopamine
VTD58H1Z2X
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
683-694Subventions
Organisme : Fonds Européen de Développement Régional
ID : FEDER/FSE 2014-2020
Organisme : Agence Nationale de la Recherche
ID : 14CE02 0020
Commentaires et corrections
Type : ErratumIn
Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Abrieux A, Debernard S, Maria A et al (2013) Involvement of the G-protein-coupled dopamine/ecdysteroid receptor DopEcR in the behavioral response to sex pheromone in an insect. PLoS One 8:e72785
doi: 10.1371/journal.pone.0072785
pubmed: 24023771
pmcid: 3762930
Alessi AM, O’Connor V, Aonuma H, Newland PL (2014) Dopaminergic modulation of phase reversal in desert locusts. Front Behav Neurosci 8:1–15
doi: 10.3389/fnbeh.2014.00371
Anador S, Brown C, Adebesin D et al (2011) Identification of dopamine D2 receptors in Gill of Crassostrea virginica. In Vivo (Brooklyn) 32:74–79
Badariotti F, Kypriotou M, Lelong C et al (2006) The phylogenetically conserved molluscan chitinase-like protein 1 (Cg-Clp1), homologue of human HC-gp39, stimulates proliferation and regulates synthesis of extracellular matrix components of mammalian chondrocytes. J Biol Chem 281:29583–29596
doi: 10.1074/jbc.M605687200
pubmed: 16882657
Barron AB, Søvik E, Cornish JL (2010) The roles of dopamine and related compounds in reward-seeking behavior across animal phyla. Front Behav Neurosci 4:1–9
doi: 10.3389/fnbeh.2010.00163
Bauknecht P, Jékely G (2017) Ancient coexistence of norepinephrine, tyramine, and octopamine signaling in bilaterians. BMC Biol 15:1–12
doi: 10.1186/s12915-016-0341-7
Beggs KT, Hamilton IS, Kurshan PT et al (2005) Characterization of a D2-like dopamine receptor (AmDOP3) in honey bee, Apis mellifera. Insect Biochem Mol Biol 35:873–882
doi: 10.1016/j.ibmb.2005.03.005
pubmed: 15944083
Blenau W, Erber J, Baumann A (1998) Characterization of a dopamine D1 receptor from Apis mellifera: cloning, functional expression, pharmacology, and mRNA localization in the brain. J Neurochem 70:15–23
doi: 10.1046/j.1471-4159.1998.70010015.x
pubmed: 9422342
Carginale V, Borrelli L, Capasso A, Parisi E (1995) Changes in dopamine uptake and developmental effects of dopamine receptor inactivation in the sea urchin. Mol Reprod Dev 40:379–385
doi: 10.1002/mrd.1080400315
pubmed: 7772349
Carroll MA, Catapane EJ (2007) The nervous system control of lateral ciliary activity of the gill of the bivalve mollusc, Crassostrea virginica. Comp Biochem Physiol 148:445–450
doi: 10.1016/j.cbpa.2007.06.003
Catapane EJ, Stefano GB, Aiello E (1978) Pharmacological study of the reciprocal dual innervation of the lateral ciliated gill epithelium by the CNS of Mytilus edulis (Bivalvia). J Exp Biol 74:101–113
Catapane EJ, Stefano GB, Aiello E (1979) Neurophysiological correlates of the dopaminergic cilio-inhibitory mechanism of Mytilus edulis. J Exp Biol 83:315–23
Cazzamali G, Klaerke DA, Grimmelikhuijzen CJP (2005) A new family of insect tyramine receptors. Biochem Biophys Res Commun 338:1189–1196
doi: 10.1016/j.bbrc.2005.10.058
pubmed: 16274665
De Rosa MJ, Veuthey T, Florman J et al (2019) The flight response impairs cytoprotective mechanisms by activating the insulin pathway. Nature 573:135–138
doi: 10.1038/s41586-019-1524-5
pubmed: 31462774
Dufour S, Quérat B, Tostivint H et al (2020) Origin and evolution of the neuroendocrine control of reproduction in vertebrates, with special focus on genome and gene duplications. Physiol Rev 100:869–943
doi: 10.1152/physrev.00009.2019
pubmed: 31625459
Ebert PR, Rowland JE, Toma DP (1998) Isolation of seven unique biogenic amine receptor clones from the honey bee by library scanning. Insect Mol Biol 7:151–162
doi: 10.1046/j.1365-2583.1998.72059.x
pubmed: 9535160
Feng G, Hannan F, Evans PD et al (1996) Cloning and functional characterization of a novel dopamine receptor from Drosophila melanogaster. J Neurosci 16:3925–3933
doi: 10.1523/JNEUROSCI.16-12-03925.1996
Galtsoff PS (1964) The american oyster Crassostrea virginica Gmelin. Fish Bull Fish Wildl Serv 64:457
Gerhardt CC, Bakker RA, Piek GJ et al (1997) Molecular cloning and pharmacological characterization of a molluscan octopamine receptor. Mol Pharmacol 51:293–300
doi: 10.1124/mol.51.2.293
pubmed: 9203635
Gotzes F, Balfanz S, Baumann A (1994) Primary structure and functional characterization of a Drosophila dopamine receptor with high homology to human D1/5 receptors. Recept Channels 2:131–141
pubmed: 7953290
Han KA, Millar NS, Grotewiel MS, Davis RL (1996) DAMB, a novel dopamine receptor expressed specifically in Drosophila mushroom bodies. Neuron 16:1127–1135
doi: 10.1016/S0896-6273(00)80139-7
pubmed: 8663989
Hearn MG, Ren Y, McBride EW et al (2002) A Drosophila dopamine 2-like receptor: molecular characterization and identification of multiple alternatively spliced variants. Proc Natl Acad Sci 99:14554–14559
doi: 10.1073/pnas.202498299
pubmed: 12391323
pmcid: 137921
Hill CA, Doyle T, Nuss AB et al (2016) Comparative pharmacological characterization of D1-like dopamine receptors from Anopheles gambiae, Aedes aegypti and Culex quinquefasciatus suggests pleiotropic signaling in mosquito vector lineages. Parasit Vectors 9:1–6
doi: 10.1186/s13071-016-1477-6
Himmelreich S, Masuho I, Berry JA et al (2017) Dopamine receptor DAMB signals via Gq to mediate forgetting in Drosophila. Cell Rep 21:2074–2081
doi: 10.1016/j.celrep.2017.10.108
pubmed: 29166600
pmcid: 6168074
Huang J, Ohta H, Inoue N et al (2009) Molecular cloning and pharmacological characterization of a Bombyx mori tyramine receptor selectively coupled to intracellular calcium mobilization. Insect Biochem Mol Biol 39:842–849
doi: 10.1016/j.ibmb.2009.10.001
pubmed: 19833207
Ji P, Xu F, Huang B et al (2016) Molecular characterization and functional analysis of a putative octopamine/tyramine receptor during the developmental stages of the pacific oyster, Crassostrea gigas. PLoS One 11:1–18
doi: 10.1371/journal.pone.0168574
Jones HD, Richards OG (1993) The effects of acetylcholine, dopamine and 5-hydroxytryptamine on water pumping rate and pressure in the mussel Mytilus edulis L. J Exp Mar Bio Ecol 170:227–240
doi: 10.1016/0022-0981(93)90154-G
Kang XL, Zhang JY, Wang D et al (2019) The steroid hormone 20-hydroxyecdysone binds to dopamine receptor to repress lepidopteran insect feeding and promote pupation. PLoS Genet 15:1–32
doi: 10.1371/journal.pgen.1008331
Katow H, Suyemitsu T, Ooka S et al (2010) Development of a dopaminergic system in sea urchin embryos and larvae. J Exp Biol 213:2808–2819
doi: 10.1242/jeb.042150
pubmed: 20675551
Kebabian J, Caine D (1979) Multiple receptors for dopamine. Nature 277:93–96
doi: 10.1038/277093a0
Khotimchenko YS (1982) Effect of noradrenaline, dopamine and adrenolytics on growth and maturation of the sea urchin, Strongylocentrotus nudus agassiz. Int J Invertebr Reprod 4:369–373
doi: 10.1080/01651269.1982.10553445
King C, Myrthil M, Carroll MA, Catapane EJ (2008) Effects of p-aminosalicylic acid on the neurotoxicity of manganese and levels of dopamine and serotonin in the nervous system and innervated organs of Crassostrea virginica. In Vivo (brooklyn) 29:26–34
Kumar S, Stecher G, Li M et al (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549
doi: 10.1093/molbev/msy096
pubmed: 5967553
pmcid: 5967553
Lacoste A, Malham SK, Cueff A et al (2001a) Evidence for a form of adrenergic response to stress in the mollusc Crassostrea gigas. J Exp Biol 204:1247–1255
doi: 10.1242/jeb.204.7.1247
Lacoste A, Malham SK, Cueff A, Poulet SA (2001b) Stress-induced catecholamine changes in the hemolymph of the oyster Crassostrea gigas. Gen Comp Endocrinol 122:181–188
doi: 10.1006/gcen.2001.7629
pubmed: 11316423
Lange AB (2009) Tyramine: From octopamine precursor to neuroactive chemical in insects. Gen Comp Endocrinol 162:18–26
doi: 10.1016/j.ygcen.2008.05.021
pubmed: 18588893
Li B, Ruotti V, Stewart RM et al (2009) RNA-Seq gene expression estimation with read mapping uncertainty. Bioinformatics 26:493–500
doi: 10.1093/bioinformatics/btp692
pubmed: 20022975
pmcid: 2820677
Liu C, Kaeser PS (2019) Mechanisms and regulation of dopamine release. Curr Opin Neurobiol 57:46–53
doi: 10.1016/j.conb.2019.01.001
pubmed: 30769276
pmcid: 6629510
Liu Z, Wang L, Yan Y et al (2018) D1 dopamine receptor is involved in shell formation in larvae of Pacific oyster Crassostrea gigas. Dev Comp Immunol 84:337–342
doi: 10.1016/j.dci.2018.03.009
pubmed: 29550270
Liu Z, Zhou Z, Wang L et al (2016) CgA1AR-1 acts as an alpha-1 adrenergic receptor in oyster Crassostrea gigas mediating both cellular and humoral immune response. Fish Shellfish Immunol 58:50–58
doi: 10.1016/j.fsi.2016.09.022
pubmed: 27633678
Liu Z, Zhou Z, Zhang Y et al (2020) Ocean acidification inhibits initial shell formation of oyster larvae by suppressing the biosynthesis of serotonin and dopamine. Sci Total Environ 735:139469
doi: 10.1016/j.scitotenv.2020.139469
pubmed: 32498014
Martínez-Ramírez AC, Ferré J, Silva FJ (1992) Catecholamines in Drosophila melanogaster: DOPA and dopamine accumulation during development. Insect Biochem Mol Biol 22:491–494
doi: 10.1016/0965-1748(92)90145-5
McLean KW, Whiteley AH (1974) RNA synthesis during the early development of the pacific oyster, Crassostrea gigas. Exp Cell Res 87:132–138
doi: 10.1016/0014-4827(74)90534-5
pubmed: 4858305
Meyer JM, Ejendal KFK, Avramova LV et al (2012) A “genome-to-lead” approach for insecticide discovery: pharmacological characterization and screening of Aedes aegypti D1-like dopamine receptors. PLoS Negl Trop Dis 6:e1478
doi: 10.1371/journal.pntd.0001478
pubmed: 22292096
pmcid: 3265452
Meyer JM, Ejendal KFK, Watts VJ, Hill CA (2011) Molecular and pharmacological characterization of two D1-like dopamine receptors in the lyme disease vector, Ixodes scapularis. Insect Biochem Mol Biol 41:563–571
doi: 10.1016/j.ibmb.2011.03.008
pubmed: 21457782
Missale C, Russel Nash S, Robinson SW et al (1998) Dopamine receptors: from structure to function. Physiol Rev 78:189–225
doi: 10.1152/physrev.1998.78.1.189
pubmed: 9457173
Mitsumasu K, Ohta H, Tsuchihara K et al (2008) Molecular cloning and characterization of cDNAs encoding dopamine receptor-1 and -2 from brain-suboesophageal ganglion of the silkworm, Bombyx mori. Insect Mol Biol 17:185–195
doi: 10.1111/j.1365-2583.2008.00792.x
pubmed: 18353107
Mustard JA, Beggs KT, Mercer AR (2005) Molecular biology of the invertebrate dopamine receptors. Arch Insect Biochem Physiol 59:103–117
doi: 10.1002/arch.20065
pubmed: 15986382
Mustard JA, Blenau W, Hamilton IS et al (2003) Analysis of two D1-like dopamine receptors from the honey bee Apis mellifera reveals agonist-independent activity. Mol Brain Res 113:67–77
doi: 10.1016/S0169-328X(03)00091-3
pubmed: 12750008
Nuss AB, Ejendal KFK, Doyle TB et al (2015) Dopamine receptor antagonists as new mode-of-action insecticide leads for control of aedes and culex mosquito vectors. PLoS Negl Trop Dis 9:1–19
doi: 10.1371/journal.pntd.0003515
Ohta H, Tsuchihara K, Mitsumasu K et al (2009) Comparative pharmacology of two D1-like dopamine receptors cloned from the silkworm Bombyx mori. Insect Biochem Mol Biol 39:342–347
doi: 10.1016/j.ibmb.2009.01.011
pubmed: 19507304
Osada M, Matsutani T, Nomura T (1987) Implication of catecholamines during spawning in marine bivalve molluscs. Int J Invertebr Reprod Dev 12:241–251
doi: 10.1080/01688170.1987.10510324
Osada M, Nomura T (1989) Estrogen effect on the seasonal levels of catecholamines in the scallop Patinopecten yessoensis. Comp Biochem Physiol Part C Comp Pharmacol 93:349–353
doi: 10.1016/0742-8413(89)90246-6
Osinga TE, Links TP, Dullaart RPF et al (2017) Emerging role of dopamine in neovascularization of pheochromocytoma and paraganglioma. FASEB J 31:2226–2240
doi: 10.1096/fj.201601131R
pubmed: 28264974
pmcid: 5434646
Peñaloza C, Gutierrez AP, Eöry L et al (2021) A chromosome-level genome assembly for the Pacific oyster Crassostrea gigas. Gigascience 10:1–9
doi: 10.1093/gigascience/giab020
Popolo M, McCarthy DM, Bhide PG (2004) Influence of dopamine on precursor cell proliferation and differentiation in the embryonic mouse telencephalon. Dev Neurosci 26:229–244
doi: 10.1159/000082140
pubmed: 15711063
Reale V, Hannan F, Hall LM, Evans PD (1997) Agonist-specific coupling of a cloned Drosophila melanogaster D1-like dopamine receptor to multiple second messenger pathways by synthetic agonists. J Neurosci 17:6545–6553
doi: 10.1523/jneurosci.17-17-06545.1997
pubmed: 9254667
pmcid: 6573129
Réalis-Doyelle E, Schwartz J, Dubos MP, Favrel P (2021) Molecular and physiological characterization of a crustacean cardioactive signaling system in a lophotrochozoan – the Pacific oyster (Crassostrea gigas): a role in reproduction and salinity acclimation. J Exp Biol 224:jeb241588
Riviere G, Klopp C, Ibouniyamine N et al (2015) GigaTON: an extensive publicly searchable database providing a new reference transcriptome in the pacific oyster Crassostrea gigas. BMC Bioinformatics 16:401
doi: 10.1186/s12859-015-0833-4
pubmed: 26627443
pmcid: 4667447
Rodet F, Lelong C, Dubos MP et al (2005) Molecular cloning of a molluscan gonadotropin-releasing hormone receptor orthologue specifically expressed in the gonad. Biochim Biophys Acta - Gene Struct Expr 1730:187–195
doi: 10.1016/j.bbaexp.2005.05.012
Roeder T (2005) Tyramine and octopamine: ruling behavior and metabolism. Annu Rev Entomol 50:447–477
doi: 10.1146/annurev.ento.50.071803.130404
pubmed: 15355245
Roeder T (2020) The control of metabolic traits by octopamine and tyramine in invertebrates. J Exp Biol 223:jeb194282
Schwartz J, Réalis-Doyelle E, Dubos MP et al (2019) Characterization of an evolutionarily conserved calcitonin signalling system in a lophotrochozoan, the Pacific oyster (Crassostrea gigas). J Exp Biol 222:jeb201319
Selcho M, Pauls D, Han K-A et al (2009) The role of dopamine in drosophila larval classical olfactory conditioning. PLoS One 4:e5897
doi: 10.1371/journal.pone.0005897
pubmed: 19521527
pmcid: 2690826
Srivastava DP (2005) Rapid, nongenomic responses to ecdysteroids and catecholamines mediated by a novel Drosophila G-protein-coupled receptor. J Neurosci 25:6145–6155
doi: 10.1523/JNEUROSCI.1005-05.2005
pubmed: 15987944
pmcid: 6725065
Sugamori KS, Demchyshyn LL, McConkey F et al (1995) A primordial dopamine D1-like adenylyl cyclase-linked receptor from Drosophila melanogaster displaying poor affinity for benzazepines. FEBS Lett 362:131–138
doi: 10.1016/0014-5793(95)00224-W
pubmed: 7720859
Sunahara RK, Niznik HB, Weiner DM et al (1990) Human dopamine D1 receptor encoded by an intronless gene on chromosome 5. Nature 347:80–83
doi: 10.1038/347080a0
pubmed: 1975640
Suo S, Sasagawa N, Ishiura S (2002) Identification of a dopamine receptor from Caenorhabditis elegans. Neurosci Lett 319:13–16
doi: 10.1016/S0304-3940(01)02477-6
pubmed: 11814642
Tank AW, Lee Wong D (2015) Peripheral and central effects of circulating catecholamines. Compr Physiol 5:1–15
Tinikul Y, Joffre Mercier A, Soonklang N, Sobhon P (2008) Changes in the levels of serotonin and dopamine in the central nervous system and ovary, and their possible roles in the ovarian development in the giant freshwater prawn, Macrobrachium rosenbergii. Gen Comp Endocrinol 158:250–258
doi: 10.1016/j.ygcen.2008.07.009
pubmed: 18713629
Tinikul Y, Soonthornsumrith B, Phoungpetchara I et al (2009) Effects of serotonin, dopamine, octopamine, and spiperone on ovarian maturation and embryonic development in the giant freshwater prawn, Macrobrachium rosenbergii (De Man, 1879). Crustaceana 82:1007–1022
doi: 10.1163/156854009X448844
Troppmann B, Balfanz S, Krach C et al (2014) Characterization of an invertebrate-type dopamine receptor of the American cockroach, Periplaneta americana. Int J Mol Sci 15:629–653
doi: 10.3390/ijms15010629
pubmed: 24398985
pmcid: 3907829
Verlinden H (2018) Dopamine signalling in locusts and other insects. Insect Biochem Mol Biol 97:40–52
doi: 10.1016/j.ibmb.2018.04.005
pubmed: 29680287
Verlinden H, Vleugels R, Verdonck R et al (2015) Pharmacological and signalling properties of a D2-like dopamine receptor (Dop3) in Tribolium castaneum. Insect Biochem Mol Biol 56:9–20
doi: 10.1016/j.ibmb.2014.11.002
pubmed: 25449128
Wragg RT, Hapiak V, Miller SB et al (2007) Tyramine and octopamine independently inhibit serotonin-stimulated aversive behaviors in Caenorhabditis elegans through two novel amine receptors. J Neurosci 27:13402–13412
doi: 10.1523/JNEUROSCI.3495-07.2007
pubmed: 18057198
pmcid: 6673087
Wu SF, Xu G, Stanley D et al (2015) Dopamine modulates hemocyte phagocytosis via a D1-like receptor in the rice stem borer, Chilo suppressalis. Sci Rep 5:1–13
doi: 10.1038/srep12247
Xu G, Wu S-F, Gu G-X et al (2017) Pharmacological characterization of dopamine receptors in the rice striped stem borer, Chilo suppressalis. Insect Biochem Mol Biol 83:80–93
doi: 10.1016/j.ibmb.2017.03.004
pubmed: 28302436
Yang B, Ni J, Zeng Z et al (2013) Cloning and characterization of the dopamine like receptor in the oyster Crassostrea angulata: expression during the ovarian cycle. Comp Biochem Physiol - B Biochem Mol Biol 164:168–175
doi: 10.1016/j.cbpb.2012.12.006
pubmed: 23274282
Yurchenko OV, Skiteva OI, Voronezhskaya EE, Dyachuk VA (2018) Nervous system development in the Pacific oyster, Crassostrea gigas (Mollusca: Bivalvia). Front Zool 15:1–21
doi: 10.1186/s12983-018-0259-8
Zhang G, Fang X, Guo X et al (2012) The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490:49–54
doi: 10.1038/nature11413
pubmed: 22992520
pmcid: 22992520