Serotonin and its metabolism in basal deuterostomes: insights fromStrongylocentrotus purpuratusandXenoturbella bocki

Abstract

SUMMARY Serotonin (5-HT), an important molecule in metazoans, is involved in a range of biological processes including neurotransmission and neuromodulation. Both its creation and release are tightly regulated, as is its removal. Multiple neurochemical pathways are responsible for the catabolism of 5-HT and are phyla specific; therefore, by elucidating these catabolic pathways we glean greater understanding of the relationships and origins of various transmitter systems. Here, 5-HT catabolic pathways were studied in Strongylocentrotus purpuratus and Xenoturbella bocki, two organisms occupying distinct positions in deuterostomes. The 5-HTrelated compounds detected in these organisms were compared with those reported in other phyla. In S. purpuratus, 5-HT-related metabolites include N-acetyl serotonin, -glutamyl-serotonin and 5-hydroxyindole acetic acid; the quantity and type were found to vary based on the specific tissues analyzed. In addition to these compounds, varying levels of tryptamine were also seen. Upon addition of a 5-HT precursor and a monoamine oxidase inhibitor, 5-HT itself was detected. In similar experiments using X. bocki tissues, the 5-HT-related compounds found included 5-HT sulfate, -glutamyl-serotonin and 5-hydroxyindole acetic acid, as well as 5-HT and tryptamine. The sea urchin metabolizes 5-HT in a manner similar to both gastropod mollusks, as evidenced by the detection of -glutamyl-serotonin, and vertebrates, as indicated by the presence of 5-hydroxyindole acetic acid and N-acetyl serotonin. In contrast, 5-HT metabolism in X. bocki appears more similar to common protostome 5-HT catabolic pathways.

Comparative Neurobiology of Biogenic Amines in Animal Models in Deuterostomes

“…Moreover, the distribution of the serotonergic system in lancelet has also been studied indirectly through the expression pattern of its biosynthesis enzymes: tryptophan hydroxylase (TpH, the limiting enzyme in serotonin synthesis) and a serotonin transporter (SERT), confirming previous immunohistochemical analyses (Candiani et al, 2012). A recent work also highlighted that the development of lancelet serotonergic cells is controlled by the retinoic acid Welsh and Loveland, 1968;Nilsson et al, 1988;De Bernardi et al, 2006;Pennati et al, 2007a;Razy-Krajka et al, 2012;Braun and Stach, 2016 Phallusia mammillata Sensory vesicle, papillae, epidermal neurons Pennati et al, 2001Pennati et al, , 2003Zega et al, 2005 Styela Yaguchi et al, 2000Yaguchi et al, , 2011Yaguchi et al, , 2014Yaguchi and Katow, 2003;Katow et al, 2004, Katow et al, 2007Katow, 2008;Yao et al, 2010 Strongylocentrotus purpuratus Anterior neuroectoderm; apical organ •• Bisgrove and Burke, 1986;Burke et al, 2006Burke et al, , 2014Yaguchi et al, 2006Yaguchi et al, , 2010Materna and Cameron, 2008;Wei et al, 2009Wei et al, , 2016Squires et al, 2010;Range et al, 2013;Garner et al, 2016;Anishchenko et al, 2018;Perillo et al, 2018;Wood et al, 2018 Paracentrotus Burke et al, 2006;Leguia and Wessel, 2006;Sutherby et al, 2012...…”

Capillary electrophoresis hyphenated with UV‐native‐laser induced fluorescence detection (CE/UV‐native‐LIF)

“…Using X. bocki tissues, 5‐hydroxytryptamin sulfate, γ‐glutamyl‐serotonin, and 5‐hydroxyindole acetic acid, as well as SER and tryptamine, were identified (Fig. ) .…”

Analysis and measurement of serotonin

“…Serotonin has since been detected in diverse species and been shown to be distributed widely in the plant and animal kingdoms. Serotonin is found in vertebrates, invertebrates, plants, and bacteria (Erland, Turi, & Saxena, ; O'Mahony, Clarke, Borre, Dinan, & Cryan, ; Squires et al, ; Stuart, Zhang, Jakubowski, Romanova, & Sweedler, ; Vleugels, Verlinden, & Vanden Broeck, ).…”