Serotonin Receptors and Their Involvement in Melanization of Sensory Cells in Ciona intestinalis - PubMed (original) (raw)

Serotonin Receptors and Their Involvement in Melanization of Sensory Cells in Ciona intestinalis

Silvia Mercurio et al. Cells. 2023.

Abstract

Serotonin (5-hydroxytryptamine (5-HT)) is a biogenic monoamine with pleiotropic functions. It exerts its roles by binding to specific 5-HT receptors (5HTRs) classified into different families and subtypes. Homologs of 5HTRs are widely present in invertebrates, but their expression and pharmacological characterization have been scarcely investigated. In particular, 5-HT has been localized in many tunicate species but only a few studies have investigated its physiological functions. Tunicates, including ascidians, are the sister group of vertebrates, and data about the role of 5-HTRs in these organisms are thus important for understanding 5-HT evolution among animals. In the present study, we identified and described 5HTRs in the ascidian Ciona intestinalis. During development, they showed broad expression patterns that appeared consistent with those reported in other species. Then, we investigated 5-HT roles in ascidian embryogenesis exposing C. intestinalis embryos to WAY-100635, an antagonist of the 5HT1A receptor, and explored the affected pathways in neural development and melanogenesis. Our results contribute to unraveling the multifaceted functions of 5-HT, revealing its involvement in sensory cell differentiation in ascidians.

Keywords: G-protein-coupled receptors; ascidian; bipolar tail neurons; epidermal sensory neurons; melanin synthesis; peripheral nervous system; pigment; pigmented sensory organs; serotonin evolution; tunicate.

PubMed Disclaimer

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1

Figure 1

Phylogenetic tree of metabotropic serotonin receptors in vertebrates and Ciona. The evolutionary history was inferred using both the maximum likelihood (ML) and neighbor-joining (NJ) methods. The NJ tree is shown with bootstrap values for both NJ and ML analyses (first and second values, respectively). The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (500 replicates) is shown next to the branches. Bootstrap identical values in both NJ and MK are shown only once and values under 50% were collapsed. Differences in the two analyses are reported in the ML with an absent value. The tree was rooted using rat metabotropic glutamate receptor sequences as an outgroup.

Figure 2

Figure 2

Expression profile of serotonin receptors during C. intestinalis development. Expression of 5HTRs by whole mount in situ hybridization in five developmental stages: early gastrula stage (EGAS) (A,H,O,V); mid gastrula stage (MGAS) (B,I,P,W); neurula stage (NEU) (C,J,Q,X); mid-tailbud stage (MTB) (D,K,R,Y); late tailbud stage (LTB) (E,L,S,Z); and larva stage (only trunk and the beginning of the tail is shown; F,M,T,A’). Representative microscopy transverse sections of hybridized samples are shown in G (neurula stage), N (initial tailbud stage), and U and B’ (mid-tailbud stage). Scale bars: 25 µm (B–E); 50 µm (A,F).

Figure 3

Figure 3

Effects of WAY-100635 treatment on larval morphology. Control samples (A,B) and larvae exposed to 10 µM (C,D), 25 µM (E,F), and 50 µM (G,H) WAY-100635. General morphology and magnification of larval trunk are displayed. Scale bars: 100 µm (A) and 50 µm (B). Abbreviations: SV = sensory vesicle; ot = otolith; oc = ocellus; * = palps.

Figure 4

Figure 4

Effects of WAY-100635 treatment on genes involved in pigment cell formation. Expression patterns of Ci-Tyr, Ci-Trp 1/2, Ci-Rab 32/38, and Ci-Tcf in control (Co) (A–D) and embryos exposed to 25 (E–H) and 50 (I–L) µM WAY-100635 at mid-tailbud stage. Scale bar: 50 µm.

Figure 5

Figure 5

Effects of WAY-100635 on neural differentiation. Expression pattern of neural markers in mid-tailbud embryos (Ci-Six 3/6: (A,D); Ci-Pou IV: (I,L)) and larvae (Ci-Pans: (B,E); Ci-TH: (C,F); Ci-Opsin: (G,J); and Ci-Synapsin: (H,K)) of C. intestinalis. Scale bars: 50 µm.

Similar articles

Cited by

References

    1. Berger M., Gray J.A., Roth B.L. The expanded biology of serotonin. Annu. Rev. Med. 2009;60:355–366. doi: 10.1146/annurev.med.60.042307.110802. - DOI - PMC - PubMed
    1. Lv J., Liu F. The role of serotonin beyond the central nervous system during embryogenesis. Front. Cell. Neurosci. 2017;11:74. doi: 10.3389/fnpit.2017.00400. - DOI - PMC - PubMed
    1. Canesi L., Miglioli A., Balbi T., Fabbri E. Physiological roles of serotonin in bivalves: Possible interference by environmental chemicals resulting in neuroendocrine disruption. Front. Endocrinol. 2022;13:792589. doi: 10.3389/fendo.2022.792589. - DOI - PMC - PubMed
    1. Tecott L.H. Serotonin and the Orchestration of Energy Balance. Cell Metab. 2007;6:352–361. doi: 10.1016/j.cmet.2007.09.012. - DOI - PubMed
    1. Gaspar P., Cases O., Maroteaux L. The developmental role of serotonin: News from mouse molecular genetics. Nat. Rev. Neurosci. 2003;4:1002–1012. doi: 10.1038/nrn1256. - DOI - PubMed

Publication types

MeSH terms

Substances

Grants and funding

A.P. was supported by the H2020 Marie Sklodowska-Curie COFUND “ARDRE” research grant, no. 847681.

LinkOut - more resources