Skip to main content
SpringerLink
Log in

Localization of serotonin and its possible role in early embryos of Tritonia diomedea (Mollusca: Nudibranchia)

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

A classical neurotransmitter serotonin (5-HT) was detected immunochemically using laser scanning microscopy at the early stages of Tritonia diomedea development. At the one- to eight-cell stages, immunolabeling suggested the presence of 5-HT in the cytoplasm close to the animal pole. At the morula and blastula stages, a group of micromeres at the animal pole showed immunoreactivity. At the gastrula stage no immunoreactive cells were detected, but they arose again at the early veliger stage. Antagonists of 5-HT2 receptors, ritanserin and cyproheptadine, as well as lipophilic derivatives of dopamine blocked cleavage divisions or distorted their normal pattern. These effects were prevented by 5-HT and its highly lipophilic derivates, serotoninamides of polyenoic fatty acids, but not by the hydrophilic (quaternary) analog of 5-HT, 5-HTQ. The results confirm our earlier suggestion that endogenous 5-HT in pre-nervous embryos acts as a regulator of cleavage divisions in nudibranch molluscs.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1A–P.
Fig. 2A–C.
Fig. 3A–D.

Similar content being viewed by others

References

  • Bezuglov VV, Manevich EM, Archakov AV, Bobrov MY, Kuklev DV, Petrukhina GN, Makarov VA, Buznikov GA (1997) Artificially functionalized polyenoic fatty acids as new lipid bioregulators. Russ J Bioorgan Chem 23:211–220

    CAS  Google Scholar 

  • Bezuglov V, Bobrov M, Gretskaya N, Gonchar A, Zinchenko G, Melck D, Bisogno T, Di Marzo V, Kuklev D, Rossi J-C, Vidal J-P, Durand T (2001) Synthesis and biological evaluation of novel cannabimimetic amides of polyunsaturated fatty acids with dopamine. Bioorg Med Chem Lett 11:447–449

    Article  CAS  PubMed  Google Scholar 

  • Buznikov GA (1967) Low molecular weight regulators of embryonic development (in Russian). Nauka, Moscow

  • Buznikov GA (1990) Neurotransmitters in embryogenesis. Harwood Academic Press, Chur, Switzerland

  • Buznikov GA, Bezuglov VV (2000) 5-Hydroxytryptamides and 3-hydroxytyramides of polyenoic fatty acids as a tool for studying the pre-nervous biogenic monoamines functions. Russ J Physiol 86:1093–1108

    CAS  Google Scholar 

  • Buznikov GA, Kost AN, Kucherova NF, Mndzhoyan AL, Suvorov NN, Berdysheva LV (1970) The role of neurohumours in early embryogenesis. III. Pharmacological analysis of the role of neurohumours in cleavage divisions. J Embryol Exp Morphol 23:549–569

    CAS  PubMed  Google Scholar 

  • Buznikov GA, Markova LN, Miloshevic I, Rakic L, Turpaev TM (1986) The localization of serotonin-like substance in embryos with mosaic type of development (in Russian). Dokl AN SSSR 287:1506–1508

    Google Scholar 

  • Buznikov GA, Nikitina LA, Galanov AY, Malchenko LA, Trubnikova OB (1993) The control of oocyte maturation in the starfish and amphibians by serotonin and its antagonists. Int J Dev Biol 37:363–364

    CAS  PubMed  Google Scholar 

  • Buznikov GA, Shmukler YB, Lauder JM (1996) From oocyte to neurone: do neurotransmitters function in the same way throughout development? Cell Mol Neurobiol 16:533–559

    Google Scholar 

  • Buznikov GA, Lambert HW, Lauder JM (2001) Serotonin and serotonin-like substances as regulators of early embryogenesis and morphogenesis. Cell Tissue Res 305:177–186

    CAS  PubMed  Google Scholar 

  • 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 floridae. Histochem J 33:413–420

    Article  CAS  PubMed  Google Scholar 

  • Cerda J, Reich G, Wallace RA, Selman K (1998) Serotonin inhibition of steroid-induced meiotic maturation in the teleost Fundulus heteroclitus: role of cyclic AMP and protein kinases. Mol Reprod Dev 49:333–341

    Article  CAS  PubMed  Google Scholar 

  • Colas JF, Launay JM, Maroteaux L (1999a) Maternal and zygotic control of serotonin biosynthesis are both necessary for Drosophila germband extension. Mech Dev 87:67–76

    Article  CAS  PubMed  Google Scholar 

  • Colas JF, Launay JM, Vonesch JM, Hickel P, Maroteaux L (1999b) Serotonin synchronises convergent extension of ectoderm with morphogenetic gastrulation movements in Drosophila. Mech Dev 87:77–91

    Article  CAS  PubMed  Google Scholar 

  • Cornea-Hebert V, Riad M, Wu C, Singh SK, Descarries L (1999) Cellular and subcellular distribution of the serotonin 5-HT2A receptor in the central nervous system of adult rat. J Comp Neurol 409:187–209

    CAS  PubMed  Google Scholar 

  • Cornea-Hebert V, Watkins KC, Roth BL, Kroeze WK, Gaudreau P, Leclerc N, Descarries L (2001) Similar ultrastructural distribution of the 5-HT2A serotonin receptor and microtubule-associated protein MAP1A in cortical dendrites of adult rat. Neuroscience 113:23–35

    Article  Google Scholar 

  • Dickinson AJ, Croll RP, Voronezhskaya EE (2000) Development of embryonic cells containing serotonin, catecholamines, and FMRFamide-related peptides in Aplysia californica. Biol Bull 199:305–315

    CAS  PubMed  Google Scholar 

  • Del Rio MJ, Velez-Pardo C, Ebinger G, Vauquelin G (1995) Serotonin binding proteins "SBP": target proteins and tool for in vitro neurotoxicity studies. Gen Pharmacol 26:1633–1641

    Article  PubMed  Google Scholar 

  • Doherty MD, Pickel VM (2000) Ultrastructural localization of the serotonin 2A receptor in dopaminergic neurons in the ventral tegmental area. Brain Res 864:176–185

    Article  CAS  PubMed  Google Scholar 

  • Emanuelsson H (1974) Localization of serotonin in cleavage embryos of Ophryotrocha labronica La Greca and Bacci. Roux Arch Entwickl Mech 175:253–271

    Google Scholar 

  • Emanuelsson H (1992) Autoradiographic localization in polychaete embryos of tritiated mesulergine, a selective antagonist of serotonin receptors that inhibits early polychaete development. Int J Dev Biol 36:293–302

    CAS  PubMed  Google Scholar 

  • Gustafson T, Toneby M (1970) On the role of serotonin and acetylcholine in sea urchin morphogenesis. Exp Cell Res 62:102–117

    CAS  PubMed  Google Scholar 

  • Hoyer D, Hannon JP, Martin GR (2002) Molecular, pharmacological and functional diversity of 5-HT receptors. Pharmacol Biochem Behav 71:533–554

    Article  CAS  PubMed  Google Scholar 

  • Kempf SC, Page LR, Pires A (1997) Development of serotonin-like immunoreactivity in the embryos and larvae of nudibranch mollusks with emphasis on the structure and possible function of the apical sensory organ. J Comp Neurol 386:507–528

    CAS  PubMed  Google Scholar 

  • Koshtoyants KS, Buznikov GA, Manukhin BN (1961) The possible role of 5-hydroxytryptamine in the motor activity of embryos of some marine gastropods. Comp Biochem Physiol 3:20–26

    CAS  Google Scholar 

  • Krantic S, Guerrier P, Dube F (1993) Meiosis reinitiation in surf clam oocytes is mediated via 5-hydroxytryptamine (serotonin) membrane receptor and a vitelline envelope-associated high affinity binding site. J Biol Chem 268:7983–7989

    CAS  PubMed  Google Scholar 

  • Leclerc C, Guerrier P, Moreau M (2000) Role of dihydropyridine-sensitive calcium channels in meiosis and fertilization in the bivalve molluscs Ruditapes philippinarum and Crassostrea gigas. Biol Cell 92:285–299

    Article  CAS  PubMed  Google Scholar 

  • Marois R, Carew TJ (1997a) Ontogeny of serotonergic neurons in Aplysia californica. J Comp Neurol 386:477–490

    Article  CAS  PubMed  Google Scholar 

  • Marois R, Carew TJ (1997b) Fine structure of the apical ganglion and its serotonergic cells in the larva of Aplysia californica. Biol Bull 192:388–398

    CAS  PubMed  Google Scholar 

  • Mayerhofer A, Smith GD, Danilchik M, Levine JE, Wolf DP, Dissen GA, Ojeda SR (1998) Oocytes are a source of catecholamines in the primate ovary: evidence for a cell-cell regulatory loop. Proc Natl Acad Sci U S A 95:10990–10995

    Article  CAS  PubMed  Google Scholar 

  • Page LR, Parries SC (2000) Comparative study of the apical ganglion in planktotrophic caenogastropod larvae: ultrastructure and immunoreactivity to serotonin. J Comp Neurol 418:383–401

    CAS  PubMed  Google Scholar 

  • Renaud F, Parisi E, Capasso A, De Prisco P (1983) On the role of serotonin and 5-methoxy-tryptamine in the regulation of cell division in sea urchin eggs. Dev Biol 98:37–46

    CAS  PubMed  Google Scholar 

  • Rodriguez JJ, Doherty MD, Pickel VM (2000) N -Methyl- d -aspartate (NMDA) receptors in the ventral tegmental area: subcellular distribution and colocalization 5-hydroxytryptamine2A receptors. J Neurosci Res 60:202–211

    Article  CAS  PubMed  Google Scholar 

  • Rowe SJ, Messenger NJ, Warner AE (1993) The role of noradrenaline in the differentiation of amphibian embryonic neurons. Development 19:1343–1357

    Google Scholar 

  • Sakharov DA (1991) Use of transmitter precursors in gastropod neuroethology. In: Kits KS, Boer HH, Joosse J (eds) Molluscan neurobiology. North Holland, Amsterdam, pp 236–242

  • Serafeim A, Grafton G, Chamba A, Gregory CD, Blakely LD, Bowery NG, Barnes NM, Gordon J (2002) 5-Hydroxytryptamine drives apoptosis in biopsylike Burkitt lymphoma cells: reversal by selective serotonin reuptake inhibitors. Neoplasia 99:2545–2553

    Article  CAS  Google Scholar 

  • Stricker SA, Smythe TL (2000) Multiple triggers of oocyte maturation in nemertean worms: the roles of calcium and serotonin. J Exp Zool 287:243–281

    Article  CAS  PubMed  Google Scholar 

  • Toneby M (1977) Functional aspects of 5-hydroxytryptamine and dopamine in early embryogenesis of Echinoidea and Asteroidea. Doctor's dissertation, Stockholm University

  • Voronezhskaya EE, Tyurin SA, Nezlin LP (2002) Neuronal development in larval chiton Ishchnochiton hakodadensis (Mollusca: Polyplacophora). J Comp Neurol 444:25--38

    Article  PubMed  Google Scholar 

  • Wallace JA (1982) Monoamines in the early chick embryo: demonstration of serotonin synthesis and the regional distribution of serotonin-concentrating cells during morphogenesis. Am J Anat 165:261–276

    CAS  PubMed  Google Scholar 

  • Weiss ER, Maness P, Lauder JM (1998) Why do neurotransmitters act like growth factors? Perspect Dev Neurobiol 5:323–335

    CAS  PubMed  Google Scholar 

  • Willows AOD, Nikitina LA, Bezuglov VV, Gretskaya NM, Buznikov GA (2000) About possible functional interaction between serotonin and neuropeptides in control processes of embryogenesis (experiments on embryos of Tritonia diomedea). Russ J Dev Biol 31:106–112

    CAS  Google Scholar 

Download references

Acknowledgements

The authors are indebted to Dr. Jean M. Lauder (Department of Cell and Developmental Biology, University of North Carolina, Chapel Hill, NC, USA) for helpful comments.

Author information

Authors and Affiliations

  1. Institute of Developmental Biology, Russian Academy of Sciences, Moscow, Russia

    Gennady A. Buznikov, Lyudmila A. Nikitina, Elena E. Voronezhskaya & Leonid P. Nezlin

  2. Institute of Bioorganic Chemistry, , Moscow, Russia

    Vladimir V. Bezuglov

  3. Friday Harbor Laboratories, University of Washington, Friday Harbor, WA, USA

    A. O. Dennis Willows

  4. Department of Neurophysiology, University of Göttingen, Humboldtallee 23, 37073, Göttingen, Germany

    Leonid P. Nezlin

Authors
  1. Gennady A. Buznikov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lyudmila A. Nikitina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elena E. Voronezhskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vladimir V. Bezuglov
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. O. Dennis Willows
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Leonid P. Nezlin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Leonid P. Nezlin.

Additional information

This study was supported by Grass Foundation Awards for 1998/1999 and 1999/2000, and RFBI grant nos. 99-04-48514 and 02-04-48129

Rights and permissions

Reprints and permissions

About this article

Cite this article

Buznikov, G.A., Nikitina, L.A., Voronezhskaya, E.E. et al. Localization of serotonin and its possible role in early embryos of Tritonia diomedea (Mollusca: Nudibranchia). Cell Tissue Res 311, 259–266 (2003). https://doi.org/10.1007/s00441-002-0666-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-002-0666-0

Keywords

Search

Navigation