Log in

Expression of Components of the Serotonergic System in Folliculogenesis and Preimplantation Development in Mice

  • Short Communications
  • Published:
Russian Journal of Developmental Biology Aims and scope Submit manuscript

Abstract

The functions of serotonin include the growth and development regulation of female germ cells as well as early embryo development. RT-PCR analysis of mRNA expression of the genes of the enzymes for synthesis and degradation and transporters and receptors of serotonin during folliculogenesis and preimplantation development of mice was performed to discover the particular mechanisms of these functions. The mRNA of tryptophan hydroxylase tph1 and monoaminoxidase maoa; membrane transporter sert and vesicular transporter vmat2; and serotonin receptors htr1b, htr1d, htr2a, htr5b, and htr7 were revealed in granulosa cells. The expression of mRNA of the aromatic amino acid decarboxylase ddc and the htr2b receptor additionally appears in the yellow body. The expression of mRNA of the genes of the tph2, ddc, and maoa enzymes; the sert, vmat1, and vmat2 transporters; and quite a number of receptors is observed during the preimplantation development, and it is transitory in most of them. The expression of all components and its dynamics suggest that the serotonergic signaling system is functionally active in mouse folliculogenesis and preimplantation development.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (France)

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Amireault, P. and Dubé, F., Intracellular cAMP and calcium signaling by serotonin in mouse cumulus-oocyte complexes, Mol. Pharmacol., 2005a, vol. 68, no. 6, pp. 1678–1687.

    PubMed  CAS  Google Scholar 

  • Amireault, P. and Dubé, F., Serotonin and its antidepressant-sensitive transport in mouse cumulus-oocyte complexes and early embryos, Biol. Reprod., 2005b, vol. 73, no. 2, pp. 358–365.

    Article  PubMed  CAS  Google Scholar 

  • Azmitia, E.C., Modern views on an ancient chemical: serotonin effects on cell proliferation, maturation, and apoptosis, Brain Res. Bull., 2001, vol. 56, no. 5, pp. 413–424.

    Article  PubMed  CAS  Google Scholar 

  • Basu, B., Desai, R., Balaji, J., et al., Serotonin in preimplantation mouse embryos is localized to the mitochondria and can modulate mitochondrial potential, Reproduction, 2008, vol. 135, no. 5, pp. 657–669.

    Article  PubMed  CAS  Google Scholar 

  • Battista, P.J. and Condon, W.A., Serotonin-induced stimulation of progesterone production by cow luteal cells in vitro, J. Reprod. Fertil., 1986, no. 1, pp. 231–238.

    Article  Google Scholar 

  • Bòdis, J., Bognàr, Z., Hartmann, G., et al., Measurement of noradrenaline, dopamine and serotonin contents in follicular fluid of human Graafian follicles after superovulation treatment, Gynecol. Obstet. Invest., 1992, vol. 33, no. 3, pp. 165–167.

    Article  PubMed  Google Scholar 

  • Bòdis, J., Hartmann, G., Török, A., et al., Relationship between the monoamine and gonadotropin content in follicular fluid of preovulatory Graafian follicles after superovulation treatment, Exp. Clin. Endocrinol., 1993, vol. 101, no. 3, pp. 178–182.

    Article  PubMed  Google Scholar 

  • Burnik Papler, T., Vrtacnik Bokal, E., Maver, A., et al., Transcriptomic analysis and meta-analysis of human granulosa and cumulus cells, PLoS One, 2015, vol. 10, no. 8, p. e0136473.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Buznikov, G.A., Nizkomolekulyarnye regulyatory zarodyshevogo razvitiya (Low-Molecular-Weight Regulators of Embryonic Development), Moscow: Nauka, 1967.

    Google Scholar 

  • Buznikov, G.A., Neirotransmittery v embriogeneze (Neurotransmitters in Embryogenesis), Moscow: Nauka, 1987.

    Google Scholar 

  • Buznikov, G.A., Preneural tansmitters as regulators of embryogenesis. Current state of problem, Russ. J. Dev. Biol., 2007, vol. 38, no. 4, pp. 213–221.

    Article  CAS  Google Scholar 

  • Buznikov, G.A. and Shmukler, Yu.B., Effect of antimediator preparations on the intercellular relations in early embryos of the sea urchin, Ontogenez, 1978, vol. 9, no. 2, pp. 173–178.

    PubMed  CAS  Google Scholar 

  • Buznikov, G.A., Kost, A.N., Kucherova, N.F., et al., The role of neurohumours in early embryogenesis. III. Pharmacological analysis of the role of neurohumours in cleavage divisions, J. Embryol. Exp. Morphol., 1970, vol. 23, no. 3, pp. 549–569.

    PubMed  CAS  Google Scholar 

  • Buznikov, G.A., Nikitina, L.A., Galanov, A.Y., et al., The control of oocyte maturation in the starfish and amphibians by serotonin and its antagonists, Int. J. Dev. Biol., 1993, vol. 37, no. 2, pp. 363–364.

    PubMed  CAS  Google Scholar 

  • Buznikov, G.A., Peterson, R.E., Nikitina, L.A., et al., The pre-nervous serotonergic system of develo** sea urchin embryos and larvae: pharmacologic and immunocytochemical evidence, Neurochem. Res., 2005, vol. 30, nos. 6–7, pp. 825–837.

    Article  PubMed  CAS  Google Scholar 

  • Callebert, J., Esteve, J.M., Herve, P., et al., Evidence for a control of plasma serotonin levels by 5-hydroxytryptamine 2B receptors in mice, Pharmacology, 2006, vol. 317, no. 2, pp. 724–731.

    CAS  Google Scholar 

  • Cerdà, J., Subhedar, N., Reich, G., et al., Oocyte sensitivity to serotonergic regulation during the follicular cycle of the teleost Fundulus heteroclitus, Biol. Reprod., 1998, vol. 59, no. 1, pp. 53–61.

    Article  PubMed  Google Scholar 

  • Chen, Z., Zuo, X., Li, H., et al., Effects of melatonin on maturation, histone acetylation, autophagy of porcine oocytes and subsequent embryonic development, Anim. Sci. J., 2017, Mar 27 [Epub ahead of print].

    Google Scholar 

  • Côté, F., Fligny, C., Bayard, E., et al., Maternal serotonin is crucial for murine embryonic development, Proc. Natl. Acad. Sci. U. S. A., 2007, vol. 104, no. 1, pp. 329–334.

    Article  PubMed  Google Scholar 

  • Dietrich, J.E. and Hiiragi, T., Stochastic patterning in the mouse pre-implantation embryo, Development, 2007, vol. 134, no. 23, pp. 4219–4231.

    Article  PubMed  CAS  Google Scholar 

  • Dubé, F. and Amireault, P., Local serotonergic signaling in mammalian follicles, oocytes and early embryos, Life Sci., 2007, vol. 81, nos. 25–26, pp. 1627–1637.

    Article  PubMed  CAS  Google Scholar 

  • Dyban, A.P., Puchkov, V.F., Baranov, V.S., et al., Laboratory mammals: mouse Mus musculus, rat Rattus norvegicus, rabbit Oryctolagus cuniculus, and hamster Cricetus griseous, in Ob”ekty biologii razvitiya (Objects of Developmental Biology), Moscow: Nauka, 1975, pp. 505–566.

    Google Scholar 

  • Graveleau, C., Paust, H.J., Schmidt-Grimminger, D., et al., Presence of a 5-HT7 receptor positively coupled to adenylate cyclase activation in human granulosalutein cells, J. Clin. Endocrinol. Metab., 2000, vol. 85, no. 3, pp. 1277–1286.

    PubMed  CAS  Google Scholar 

  • Greiner, M., Paredes, A., Rey-Ares, V., et al., Catecholamine uptake, storage, and regulated release by ovarian granulosa cells, Endocrinology, 2008, vol. 149, no. 10, pp. 4988–4996.

    Article  PubMed  CAS  Google Scholar 

  • Grigor’ev, N.G., Cortical cytoplasmic layer—a possible site of action of prenervous transmitters, Zh. Evol. Biokhim. Fiziol., 1988, vol. 24, no. 5, pp. 625–629.

    PubMed  Google Scholar 

  • Hinckley, M., Vaccari, S., Horner, K., et al., The G-protein-coupled receptors GPR3 and GPR12 are involved in cAMP signaling and maintenance of meiotic arrest in rodent oocytes, Dev. Biol., 2005, vol. 287, no. 2, pp. 249–261.

    Article  PubMed  CAS  Google Scholar 

  • Il’ková, G., Rehák, P., Veselá, J., et al., Serotonin localization and its functional significance during mouse preimplantation embryo development, Zygote, 2004, vol. 12, no. 3, pp. 205–213.

    Article  PubMed  CAS  Google Scholar 

  • Koppan, M., Bodis, J., Verzar, Z., et al., Serotonin may alter the pattern of gonadotropin-induced progesterone release of human granulosa cells in superfusion system, Endocrine, 2004, vol. 24, no. 2, pp. 155–159.

    Article  PubMed  CAS  Google Scholar 

  • Krantic, S., Dube, F., Quirion, R., et al., Pharmacology of the serotonin-induced meiosis reinitiation in spisula solidissima oocytes, Dev. Biol., 1991, vol. 146, no. 2, pp. 491–498.

    Article  PubMed  CAS  Google Scholar 

  • Lara, H.E., Ferruz, J.L., Luza, S., et al., Activation of ovarian sympathetic nerves in polycystic ovary syndrome, Endocrinology, 1993, vol. 133, pp. 2690–2695.

    Article  PubMed  CAS  Google Scholar 

  • Levin, M., Buznikov, G.A., and Lauder, J.M., Of minds and embryos: left-right asymmetry and the serotonergic controls of pre-neural morphogenesis, Dev. Neurosci., 2006, vol. 28, no. 3, pp. 171–185.

    Article  PubMed  CAS  Google Scholar 

  • Lister, A., Regan, C., Van Zwol, J., et al., Inhibition of egg production in zebrafish by fluoxetine and municipal effluents: a mechanistic evaluation, Aquat. Toxicol., 2009, vol. 95, no. 4, pp. 320–329.

    Article  PubMed  CAS  Google Scholar 

  • Mayerhofer, A., Smith, G.D., Danilchik, M., et al., Oocytes are a source of catecholamines in the primate ovary: evidence for a cell-cell regulatory loop, Proc. Natl. Acad. Sci. U. S. A., 1998, vol. 95, no. 18, pp. 10990–10995.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moore, C.J., DeLong, N.E., Chan, K.A., et al., Perinatal administration of a selective serotonin reuptake inhibitor induces impairments in reproductive function and follicular dynamics in female rat offspring, Reprod. Sci., 2015, vol. 22, no. 10, pp. 1297–1311.

    Article  PubMed  CAS  Google Scholar 

  • Nikishin, D.A., Kremnyov, S.V., Konduktorova, V.V., et al., Expression of serotonergic system components during early Xenopus embryogenesis, Int. J. Dev. Biol., 2012, vol. 56, no. 5, pp. 385–391.

    Article  PubMed  CAS  Google Scholar 

  • Qin, L., Zhao, D., Xu, J., et al., The vascular permeabilizing factors histamine and serotonin induce angiogenesis through TR3/Nur77 and subsequently truncate it through thrombospondin-1, Blood, 2013, vol. 121, no. 11, pp. 2154–2164.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sakaguchi, K., Itoh, M.T., Takahashi, N., et al., The rat oocyte synthesizes melatonin, Reprod. Fertil. Dev., 2013, vol. 25, no. 4, pp. 674–682.

    Article  PubMed  CAS  Google Scholar 

  • Sheng, Y., Wang, L., Liu, X.S.J., et al., A serotonin receptor antagonist induces oocyte maturation in both frogs and mice: evidence that the same G protein-coupled receptor is responsible for maintaining meiosis arrest in both species, J. Cell Physiol., 2005, vol. 202, no. 3, pp. 777–786.

    Article  PubMed  CAS  Google Scholar 

  • Shmukler, Yu.B., Cell–cell interactions in the early sea urchin embryos. III. Effect of neuropharmacological drugs on cleavage type of half embryos of Scaphechinus mirabilis, Ontogenez, 1981, vol. 12, no. 4, pp. 404–409.

    CAS  Google Scholar 

  • Shmukler, Y.B., Silvestre, F., and Tosti, E., 5-HT-receptive structures are localized in the interblastomere cleft of Paracentrotus lividus early embryos, Zygote, 2008, vol. 16, no. 1, pp. 79–86.

    Article  PubMed  CAS  Google Scholar 

  • Shuey, D.L., Sadler, T.W., Tamir, H., et al., Serotonin and morphogenesis. transient expression of serotonin uptake and binding protein during craniofacial morphogenesis in the mouse, Anat. Embryol. (Berl.), 1993, vol. 187, no. 1, pp. 75–85.

    Article  CAS  Google Scholar 

  • Stepinska, U., Kuwana, T., and Olszanska, B., Serotonin receptors are selectively expressed in the avian germ cells and early embryos, Zygote, 2014, vol. 23, no. 3, pp. 1–12.

    Google Scholar 

  • Stricker, S.A. and Smythe, T.L., 5-HT causes an increase in cAMP that stimulates, rather than inhibits, oocyte maturation in marine nemertean worms, Development, 2001, vol. 128, no. 8, pp. 1415–1427.

    PubMed  CAS  Google Scholar 

  • Tanaka, E., Baba, N., Toshida, K., et al., Serotonin stimulates steroidogenesis in rat preovulatory follicles: involvement of 5-HT2 receptor, Life Sci., 1993, vol. 53, no. 7, pp. 563–570.

    Article  PubMed  CAS  Google Scholar 

  • Terranova, P.F., Uilenbroek, J.T., Saville, L., et al., Serotonin enhances oestradiol production by hamster preovulatory follicles in vitro: effects of experimentally induced atresia, J. Endocrinol., 1990, vol. 125, no. 3, pp. 433–438.

    Article  PubMed  CAS  Google Scholar 

  • Tinikul, Y., Joffre Mercier, A., Soonklang, N., et al., 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., 2008, vol. 158, no. 3, pp. 250–258.

    Article  PubMed  CAS  Google Scholar 

  • Veselá, J., Rehák, P., Mihalik, J., et al., Expression of serotonin receptors in mouse oocytes and preimplantation embryos, Physiol. Res., 2003, vol. 52, no. 2, pp. 223–228.

    PubMed  Google Scholar 

  • Wang, Q. and He, M., Molecular characterization and analysis of a putative 5-HT receptor involved in reproduction process of the pearl oyster Pinctada fucata, Gen. Comp. Endocrinol., 2014, vol. 204, pp. 71–79.

    Article  PubMed  CAS  Google Scholar 

  • Zamani, A. and Qu, Z., Serotonin activates angiogenic phosphorylation signaling in human endothelial cells, FEBS Lett., 2012, vol. 586, no. 16, pp. 2360–2365.

    Article  PubMed  CAS  Google Scholar 

  • Zatylny, C., Durantou, F., Boucaud-Camou, E., et al., Evidence of 5-hydroxytryptamine synthesis in the follicles of Sepia officinalis and direct involvement in the control of egg-laying, Mol. Reprod. Dev., 2000, vol. 55, no. 2, pp. 182–188.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. A. Nikishin.

Additional information

Original Russian Text © D.A. Nikishin, Yu.V. Khramova, T.S. Bagayeva, M.L. Semenova, Yu.B. Shmukler, 2018, published in Ontogenez, 2018, Vol. 49, No. 3.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nikishin, D.A., Khramova, Y.V., Bagayeva, T.S. et al. Expression of Components of the Serotonergic System in Folliculogenesis and Preimplantation Development in Mice. Russ J Dev Biol 49, 184–192 (2018). https://doi.org/10.1134/S1062360418030062

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062360418030062

Keywords

Navigation