Abstract—
Serotonin is a regulator of early embryonic development and has a complete functional system in preimplantation mammalian embryos. In the present work, the spatial distribution of serotonin, the vesicular monoamine transporter VMAT2, and the 5-HT1D and 5-HT2A receptors at different stages of early embryonic development was described. Serotonin, the VMAT2 transporter, and the 5-HT1D receptor are visualized in the cortical compartment of cells, whereas the 5-HT2A receptor has a more even distribution throughout the cytoplasm. The comparison showed that there were no statistically significant differences between the immunoreactive particle sizes of serotonin and the VMAT2 transporter, suggesting the presence of vesicles in which serotonin accumulates with the involvement of VMAT2 for further intercellular signal transduction. Moreover, the patterns of immunoreactivity of the two serotonin receptors, 5-HT1D and 5-HT2A, differ markedly, which may indicate that they simultaneously serve different functions in early embryogenesis.
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REFERENCES
Lodish H., Berk A., Zipursky S.L. 2000. Molecular cell biology: Neurotransmitters, synapses, and impulse transmission (4th ed.). New York: W. H. Freeman.
Torres G., Gainetdinov R., Caron M. 2003. Plasma membrane monoamine transporters: Structure, regulation, and function. Nat. Rev. Neurosci. 4, 13–25.
Xing L., Huttner W.B. 2020. Neurotransmitters as modulators of neural progenitor cell proliferation during mammalian neocortex development. Front. Cell Dev. Biol. 8, 391.
Yamamoto K., Vernier P. 2011. The evolution of dopamine systems in chordates. Front. Neuroanat. 5, 21.
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. Development. 12 (4), 563–573.
Buznikov G.A. 1967. Low-molecular regulators of embryonic development. Moscow: Nauka.
Buznikov G.A. 1987. Neurotransmitters in embryogenesis. Moscow: Nauka.
Buznikov G.A. 2007. Preneural transmitters as regulators of embryogenesis. Current state of problem. Russ. J. Dev. Biol. 38 (4), 213–220.
Shmukler Y.B., Nikishin D.A. 2022. Non-neuronal transmitter systems in bacteria, non-nervous eukaryotes, and invertebrate embryos. Biomolecules. 12 (2), 271.
Dubé F., Amireault P. 2007. Local serotonergic signaling in mammalian follicles, oocytes and early embryos. Life Sci. 81 (25–26), 1627–1637.
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, 533–559.
Amireault P., Dubé F. 2005. Serotonin and its antidepressant sensitive transport in mouse cumulus-oocyte complexes and early embryos. Biol. Reprod. 73 (2), 358–365.
Basu B., Desai R., Balaji J., Chaerkady R., Sriram V., Maiti S., Panicker M.M. 2008. Serotonin in pre-implantation mouse embryos is localized to the mitochondria and can modulate mitochondrial potential. Reproduction. 135 (5), 657.
Amireault P., Dube F. 2005. Intracellular cAMP and calcium signaling by serotonin in mouse cumulus–oocyte complexes. Mol. Pharmacol. 68 (6), 1678–1687.
Nikishin D.A., Khramova Y.V., Bagayeva T.S., Semenova M.L., Shmukler Y.B. 2018. Expression of components of the serotonergic system in folliculogenesis and preimplantation development in mice. Russ. J. Dev. Biol. 49 (3), 184–192.
Il’kova G., Rehak P., Vesela J., Čikoš S., Fabian D., Czikková S., Koppel J. 2004. Serotonin localization and its functional significance during mouse preimplantation embryo development. Zygote. 12, 205–213.
Nikishin D.A., Khramova Y.V., Alyoshina N.M., Malchenko L.A., Shmukler Y.B. 2021. Oocyte-mediated effect of serotonin on the functional status of granulosa cells. Russ. J. Dev. Biol. 52 (2), 97–104.
Shmukler Y., Nikishin D. 2012. Transmitters in blastomere interactions. Cell Interactions. 31–65.
Kamal M., Jockers R. 2011. Biological significance of GPCR heteromerization in the neuro-endocrine system. Front. Endocrinol. 2, 2.
Bader M. 2019. Serotonylation: Serotonin signaling and epigenetics. Front. Mol. Neurosci. 12, 288.
Funding
The work of V.F., A.I., M.K., and D.N. was supported by the Russian Science Foundation (project no. 22-74-10 009, https://rscf.ru/project/22-74-10 009/). Yu.Sh. and D.N. carried out experiments using the equipment of the Core Centrum of the Institute of Developmental Biology RAS. The work was conducted in the frames of IDB RAS RP no. 0108-2019-0003 in 2023.
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The authors declare that there are no obvious or potential conflicts of interest related to the publication of this article.
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All procedures carried out with experimental animals, methods of pain relief, euthanasia, and animal care before and after experimental interventions, were performed in accordance with Protocol no. 40 of September 17, 2021, of the Commission on Bioethics of the IDB RAS.
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Translated by V. Frolova
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Frolova, V.S., Ivanova, A.D., Konorova, M.S. et al. Spatial Organization of the Components of the Serotonergic System in the Early Mouse Development. Biochem. Moscow Suppl. Ser. A 17 (Suppl 1), S59–S64 (2023). https://doi.org/10.1134/S1990747823060041
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DOI: https://doi.org/10.1134/S1990747823060041