Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-24T02:27:59.579Z Has data issue: false hasContentIssue false
  • English
  • Français

Expression and functional activity of neurotransmitter system components in sea urchins’ early development†

Published online by Cambridge University Press:  29 April 2015

Denis A. Nikishin ,
Ivan Milošević ,
Milorad Gojković ,
Ljubisav Rakić ,
Vladimir V. Bezuglov  and
Yuri B. Shmukler
Denis A. Nikishin
Affiliation:
N.K. Koltzov Institute of Developmental Biology, Russian Academy of Sciences, Moscow, Russia. M.V. Lomonosov Moscow State University, Moscow, Russia.
Ivan Milošević
Affiliation:
Institute of Marine Biology, Kotor, Montenegro.
Milorad Gojković
Affiliation:
Institute of Marine Biology, Kotor, Montenegro.
Ljubisav Rakić
Affiliation:
Serbian Academy of Science and Art, Belgrade, Serbia.
Vladimir V. Bezuglov
Affiliation:
M.M. Shemyakin and Yu.A. Ovchinnikov Institute of Bio-Organic Chemistry, Russian Academy of Sciences, Moscow, Russia.
Yuri B. Shmukler*
Affiliation:
26, Vavilov St, Moscow 119334, Russia N.K. Koltzov Institute of Developmental Biology, Russian Academy of Sciences, Moscow, Russia.
*
All correspondence to: Yuri B. Shmukler. 26, Vavilov St, Moscow 119334, Russia. Tel: +7 499 135 0052. Fax: +7 499 135 8012. E-mail: yurishmukler@yahoo.com
Get access Rights & Permissions [Opens in a new window]

Summary

Reverse-transcription polymerase chain reaction (RT-PCR) investigation of the expression of the components supposedly taking part in serotonin regulation of the early development of Paracentrotus lividus has shown the presence of transcripts of five receptors, one of which has conservative amino acid residues characteristic of monoaminergic receptors. At the early stages of embryogenesis the expressions of serotonin transporter (SERT) and noradrenaline transporter (NET) were also recognized. The activities of the enzymes of serotonin synthesis and serotonin transporter were shown using immunohistochemistry and incubation with para-chlorophenylalanine (PСРА) and 5-hydroxytryptophan (HTP). Pharmacological experiments have shown a preferential cytostatic activity of ligands characterized as mammalian 5-hydroxytryptamine (5-HT)1-antagonists. On the basis of the sum of the data from molecular biology and embryo physiological experiments, it is suggested that metabotropic serotonin receptors and membrane transporters take part in the regulatory processes of early sea urchin embryogenesis.

Keywords

EmbryoReceptorSea urchinSerotoninTransporter
Type
Research Article
Information
Zygote , Volume 24 , Issue 2 , April 2016 , pp. 206 - 218
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

In memory of Prof. Gennady A. Buznikov, pioneer of embryonic transmitter research.

References

Amireault, P. & Dubé, F. (2005). Serotonin and its antidepressant-sensitive transport in mouse cumulus–oocyte complexes and early embryos. Biol. Reprod. 73, 358–65.CrossRefGoogle ScholarPubMed
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 amides of polyunsaturated fatty acids with dopamine. Bioorg. Med. Chem. Lett. 11, 447–9.CrossRefGoogle ScholarPubMed
Bisogno, T., Melck, D., De Petrocellis, L., Bobrov, M.Y., Gretskaya, N.M., Bezuglov, V.V., Sitachitta, N., Gerwick, W.H. & Di Marzo, V. (1998). Arachidonoyl serotonin and other novel inhibitors of fatty acid amide hydrolase. Biochem. Biophys. Res. Commun. 248, 515–22.CrossRefGoogle ScholarPubMed
Buznikov, G.A. (1967). The Low Molecular Weight Regulators in Embryonic Development. Moscow: Nauka, 265 pp., [in Russian].Google Scholar
Buznikov, G.A. (1984). The action of neurotransmitters and related substances on early embryogenesis. Pharmacol. Ther. 25, 23–59.CrossRefGoogle ScholarPubMed
Buznikov, G.A. (1989). Transmitters in early embryogenesis: new data. Russ. J. Dev. Biol. 20, 427–35.Google ScholarPubMed
Buznikov, G.A. & Grigoriev, N.G. (1990). The influence of biogenic monoamines and their antagonists on the cortical layer of cytoplasm of early sea urchin embryos. J. Evol. Biochem. Physiol. 26, 614–22.Google Scholar
Buznikov, G.A. & Podmarev, V.I. (1975). Sea urchins Strongylocentrotus droebachiensis, S. nudus, S. intermedius . In: Objects of Developmental Biology (p. 579). Moscow: Nauka [in Russian].Google Scholar
Buznikov, G.A. & Shmukler, Y.B. (1978). Effect of anti-mediator drugs on intercellular communication in early embryos of sea urchins. Russ. J. Dev. Biol. 9, 173–8.Google Scholar
Buznikov, G.A., Chudakova, I.V. & Zvezdina, N.D. (1964). The role of neurohumours in early embryogenesis.: I. Serotonin content of developing embryos of sea urchin and loach. J. Embryol. Exp. Morphol. 12, 563–73.Google Scholar
Buznikov, G.A., Manukhin, B.N., Rakic, L., Turpaev, T.M., Aroyan, A.A., Akopyan, P.R., Kucherova, I.F., Ovsepyan, T.R. & Yakhontov, L.N. (1976). About hypersensitivity of sea urchin embryos to antagonists of acetylcholine and monoamines. J. Evol. Biochem. Physiol. 12, 31–7.Google Scholar
Buznikov, G.A., Manukhin, B.N., Rakic, L., Kudriashova, N.I. & Mndzhoian, O.L. (1979). Sensitivity of fragmented and stratified sea urchin embryos to cytotoxic neuropharmacological preparations. Russ. J. Dev. Biol. 10, 372–80.Google ScholarPubMed
Buznikov, G.A., Shmukler, Y.B. & Lauder, J.M. (1996). From oocyte to neuron: do neurotransmitters function in the same way throughout development? Cell. Mol. Neurobiol. 16, 537–59.CrossRefGoogle ScholarPubMed
Buznikov, G.A., Nikitina, L.A., Voronezhskaya, E.E., Bezuglov, V.V, Willows, A.O.D. & Nezlin, L.P. (2003). Localization of serotonin and its possible role in early embryos of Tritonia diomedea (Mollusca: Nudibranchia). Cell Tissue Res. 311, 259–66.CrossRefGoogle ScholarPubMed
Buznikov, G.A., Peterson, R.E., Nikitina, L.A., Bezuglov, V.V & Lauder, J.M. (2005). The pre-nervous serotonergic system of developing sea urchin embryos and larvae: pharmacologic and immunocytochemical evidence. Neurochem. Res. 30 (6–7), 825–37.CrossRefGoogle ScholarPubMed
Carginale, V., Capasso, A., Madonna, L., Borrelli, L. & Parisi, E. (1992). Adenylate cyclase from sea urchin eggs is positively and negatively regulated by D-1 and D-2 dopamine receptors. Exp. Cell. Res. 203, 491–4.CrossRefGoogle ScholarPubMed
Côté, F., Fligny, C., Bayard, E., Launay, J., Gershon, M.D., Mallet, J. & Vodjdani, G. (2007). Maternal serotonin is crucial for murine embryonic development. Proc. Natl. Acad. Sci. USA 104, 329–34.CrossRefGoogle ScholarPubMed
Doran, S.A., Doran, S.A., Koss, R., Tran, C.H., Christopher, K.J., Gallin, W.J. & Goldberg, J.I. (2004). Effect of serotonin on ciliary beating and intracellular calcium concentration in identified populations of embryonic ciliary cells. J. Exp. Biol. 207, 1415–29.CrossRefGoogle ScholarPubMed
Dubé, F. & Amireault, P. (2007). Local serotonergic signaling in mammalian follicles, oocytes and early embryos. Life Sci. 81 (25–26), 1627–37.CrossRefGoogle ScholarPubMed
Hoyer, D., Clarke, D.E., Fozard, J.R., Hartig, P.R., Martin, G.R., Mylecharane, E.J., Saxena, P.R. & Humphrey, P.P. (1994). International Union of Pharmacology classification of receptors for 5-hydroxytryptamine (serotonin). Pharmacol. Rev. 46, 157–203.Google ScholarPubMed
Kaeser, G.E., Rabe, B.A. & Saha, M.S. (2011). Cloning and characterization of GABAA α subunits and GABAB subunits in Xenopus laevis during development. Dev. Dyn. 240, 862–73.CrossRefGoogle ScholarPubMed
Kamal, M. & Jockers, R. (2011). Biological Significance of GPCR heteromerization in the neuro-endocrine system. Front. Endocrinol. 2, 1–14.CrossRefGoogle ScholarPubMed
Landau, M.A., Buznikov, G.A., Kabankin, A.S., Kolbanov, V.M., Suvorov, N.N. & Teplitz, N.A. (1977). Embryotoxic activity of indole derivatives. Pharm. Chem. J. 11, 57–60.CrossRefGoogle Scholar
Markova, L.N., Buznikov, G.A., Kovaćević, N., Rakić, L., Salimova, N.B. & Volina, E.V. (1985). Histochemical study of biogenic monoamines in early (“Prenervous”) and late embryos of sea urchins. Int. J. Dev. Neurosci. 3, 493–9.CrossRefGoogle ScholarPubMed
Nagy, A., Hegyi, H., Farkas, K., Tordai, H., Kozma, E., Bányai, L. & Patthy, L. (2008). Identification and correction of abnormal, incomplete and mispredicted proteins in public databases. BMC Bioinform. 9, 353.CrossRefGoogle ScholarPubMed
Nikishin, D.A., Kremnyov, S.V, Konduktorova, V.V & Shmukler, Y.B. (2012a). Expression of serotonergic system components during early Xenopus embryogenesis. Int. J. Dev. Biol. 56, 385–91.CrossRefGoogle ScholarPubMed
Nikishin, D.A., Semenova, M.N. & Shmukler, Y.B. (2012b). Expression of transmitter receptor genes in early development of sea urchin Paracentrotus lividus . Russ. J. Dev. Biol. 43, 181–4.CrossRefGoogle ScholarPubMed
Padayatti, P.S., Wang, L., Gupta, S., Orban, T., Sun, W., Salom, D., Jordan, S.R., Palczewski, K. & Chance, M.R. (2013). A hybrid structural approach to analyze ligand binding by the serotonin type 4 receptor (5-HT4). Mol. Cell. Proteomics 12, 1259–71.CrossRefGoogle ScholarPubMed
Penado, K.M., Rudnick, G. & Stephan, M.M. (1998). Critical amino acid residues in transmembrane span 7 of the serotonin transporter identified by random mutagenesis. J. Biol. Chem. 273, 28098–106.CrossRefGoogle ScholarPubMed
Van Rhee, A.M. & Jacobson, K.A. (1996). Molecular architecture of G protein-coupled receptors. Drug Dev. Res. 37, 1–38.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Richerson, G.B. & Wu, Y. (2003). Dynamic equilibrium of neurotransmitter transporters: not just for reuptake anymore. J. Neurophysiol. 90, 1363–74.CrossRefGoogle Scholar
Rostomyan, M.A., Abramyan, K.S., Buznikov, G.A. & Gusareva, E.V. (1985). Electron-cytochemical detection of adenylate cyclase in the early embryo of the sea urchin. Cell Tissue Biol. 27, 877–81.Google Scholar
Schuldiner, S., Shirvan, A. & Linial, M. (1995). Vesicular neurotransmitter transporters: from bacteria to humans. Physiol. Rev. 75, 369–92.CrossRefGoogle ScholarPubMed
Shmukler, Y.B. (1981). Cellular interactions in early embryos of sea urchins. III. Effect of neuropharmacological drugs on the type of cleavage of half embryos of Scaphechinus mirabilis . Russ. J. Dev. Biol. 12, 404–9.Google Scholar
Shmukler, Y.B., Grigoriev, N.G., Buznikov, G.A. & Turpaev, T.M. (1986). The influence of second messengers and related substances on the sensitivity of early embryos to cytostatic neurochemicals. Comp. Biochem. Physiol. C 83, 423–7.Google Scholar
Shmukler, Y.B. (1993). Possibility of membrane reception of neurotransmitter in sea urchin early embryos. Comp. Biochem. Physiol. C 106, 269–73.Google ScholarPubMed
Shmukler, Y.B. (2010). A “micromere model” of cell-cell interactions in sea urchin early embryos. Biophysics 55, 399–405.CrossRefGoogle Scholar
Tusnády, G.E. & Simon, I. (1998). Principles governing amino acid composition of integral membrane proteins: application to topology prediction. J. Mol. Biol. 283, 489–506.CrossRefGoogle ScholarPubMed
Tusnády, G.E. & Simon, I. (2001). The HMMTOP transmembrane topology prediction server. Bioinformatics 17, 849–50.CrossRefGoogle ScholarPubMed
Veselá, J., Rehák, P., Mihalik, J., Czikková, S., Pokorný, J. & Koppel, J. (2003). Expression of serotonin receptors in mouse oocytes and preimplantation embryos. Physiol. Res. 52, 223–8.CrossRefGoogle ScholarPubMed
Yavarone, M.S., Shuey, D.L., Tamir, H., Sadler, T.W. & Lauder, J.M. (1993). Serotonin and cardiac morphogenesis in the mouse embryo. Teratology 47, 573–84.CrossRefGoogle ScholarPubMed