Skip to main content
Log in

A Novel Dop2/Invertebrate-Type Dopamine Signaling System Potentially Mediates Stress, Female Reproduction, and Early Development in the Pacific Oyster (Crassostrea gigas)

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

A Correction to this article was published on 09 October 2021

This article has been updated

Abstract

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 D1-like family of receptors and corresponds to the first representative of the Dop2/invertebrate-type dopamine receptor (Dop2/INDR) group ever identified in Lophotrochozoa. Cragi-DOP2R transcripts were expressed in various adult tissues, with higher expression levels in the visceral ganglia and the gills. Following an experiment under acute osmotic conditions, Cragi-DOP2R transcripts significantly increased in the visceral ganglia and decreased in the gills, suggesting a role of dopamine signaling in the mediation of osmotic stress. Furthermore, a role of the Cragi-DOP2R signaling pathway in female gametogenesis and in early oyster development was strongly suggested by the significantly higher levels of receptor transcripts in mature female gonads and in the early embryonic stages.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Change history

References

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alessi AM, O’Connor V, Aonuma H, Newland PL (2014) Dopaminergic modulation of phase reversal in desert locusts. Front Behav Neurosci 8:1–15

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Bauknecht P, Jékely G (2017) Ancient coexistence of norepinephrine, tyramine, and octopamine signaling in bilaterians. BMC Biol 15:1–12

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galtsoff PS (1964) The american oyster Crassostrea virginica Gmelin. Fish Bull Fish Wildl Serv 64:457

    Google Scholar 

  • Gerhardt CC, Bakker RA, Piek GJ et al (1997) Molecular cloning and pharmacological characterization of a molluscan octopamine receptor. Mol Pharmacol 51:293–300

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Han KA, Millar NS, Grotewiel MS, Davis RL (1996) DAMB, a novel dopamine receptor expressed specifically in Drosophila mushroom bodies. Neuron 16:1127–1135

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kebabian J, Caine D (1979) Multiple receptors for dopamine. Nature 277:93–96

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Kumar S, Stecher G, Li M et al (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lange AB (2009) Tyramine: From octopamine precursor to neuroactive chemical in insects. Gen Comp Endocrinol 162:18–26

    Article  CAS  PubMed  Google Scholar 

  • Li B, Ruotti V, Stewart RM et al (2009) RNA-Seq gene expression estimation with read mapping uncertainty. Bioinformatics 26:493–500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu C, Kaeser PS (2019) Mechanisms and regulation of dopamine release. Curr Opin Neurobiol 57:46–53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • McLean KW, Whiteley AH (1974) RNA synthesis during the early development of the pacific oyster, Crassostrea gigas. Exp Cell Res 87:132–138

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Missale C, Russel Nash S, Robinson SW et al (1998) Dopamine receptors: from structure to function. Physiol Rev 78:189–225

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Mustard JA, Beggs KT, Mercer AR (2005) Molecular biology of the invertebrate dopamine receptors. Arch Insect Biochem Physiol 59:103–117

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Osada M, Matsutani T, Nomura T (1987) Implication of catecholamines during spawning in marine bivalve molluscs. Int J Invertebr Reprod Dev 12:241–251

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Osinga TE, Links TP, Dullaart RPF et al (2017) Emerging role of dopamine in neovascularization of pheochromocytoma and paraganglioma. FASEB J 31:2226–2240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peñaloza C, Gutierrez AP, Eöry L et al (2021) A chromosome-level genome assembly for the Pacific oyster Crassostrea gigas. Gigascience 10:1–9

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Roeder T (2005) Tyramine and octopamine: ruling behavior and metabolism. Annu Rev Entomol 50:447–477

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava DP (2005) Rapid, nongenomic responses to ecdysteroids and catecholamines mediated by a novel Drosophila G-protein-coupled receptor. J Neurosci 25:6145–6155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Suo S, Sasagawa N, Ishiura S (2002) Identification of a dopamine receptor from Caenorhabditis elegans. Neurosci Lett 319:13–16

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verlinden H (2018) Dopamine signalling in locusts and other insects. Insect Biochem Mol Biol 97:40–52

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Zhang G, Fang X, Guo X et al (2012) The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490:49–54

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to Marie-Pierre Dubos for her technical assistance.

Funding

This work was funded by the ANR project NEMO (Agence Nationale de la Recherche 14CE02 0020). J.S.’s PhD fellowship was co-financed by the NEMO project and by the European Union within the framework of the operational program FEDER/FSE 2014–2020.

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization: P.F. Methodology: J.S, E.R-D, P.F. Software: J.S, L.LF. Validation: J.S, P.F. Formal analysis: J.S, L.LF, E.R-D, P.F. Investigation: J.S, P.F. Writing — original draft: J.S, P.F. Writing — review and editing: J.S, P.F. Supervision, P.F. Project administration, P.F. Funding acquisition: P.F.

Corresponding author

Correspondence to Julie Schwartz.

Ethics declarations

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The original online version of this article was revised: The captured ESM file was inadvertently not updated. The correct version is included herewith.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 379 KB)

Supplementary file2 (DOCX 44 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schwartz, J., Réalis-Doyelle, E., Le Franc, L. et al. A Novel Dop2/Invertebrate-Type Dopamine Signaling System Potentially Mediates Stress, Female Reproduction, and Early Development in the Pacific Oyster (Crassostrea gigas). Mar Biotechnol 23, 683–694 (2021). https://doi.org/10.1007/s10126-021-10052-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-021-10052-5

Keywords

Navigation