Abstract
Forty serotonin-related neurochemicals were tested on embryos and larvae of Lytechinus variegatus and other sea urchin species. Some of these substances (agonists of 5-HT1 receptors, antagonists of 5-HT2, 5-HT3 or 5-HT4 receptors, and inhibitors of the serotonin transporter, SERT) perturbed post-blastulation development, eliciting changes in embryonic/larval phenotypes typical for each class of receptor ligand. These developmental malformations were prevented completely or partially by serotonin (5-HT) or 5-HT analogs (5-HTQ, AA-5-HT), providing evidence for the putative localization of cellular targets. Immunoreactive 5-HT, 5-HT receptors and SERT were found in pre-nervous embryos and larvae of both L. variegatus and Strongylocentrotus droebachiensis. During gastrulation, these components of the serotonergic system were localized to the archenteron (primary gut), mesenchyme-like cells, and often the apical ectoderm. These results provide evidence that pre-nervous 5-HT may regulate early events of sea urchin embryogenesis, mediated by 5-HT receptors or the 5-HT transporter.
Similar content being viewed by others
References
G. A. Buznikov (1967) Low molecular weight regulators of early development, In Russian Publ House Nauka, Moscow
J. A. Wallace (1982) ArticleTitleMonoamines in the early chick embryo: demonstration of serotonin synthesis and the regional distribution of serotonin-concentrating cells during morphogenesis Am. J. Anat. 165 261–276 Occurrence Handle10.1002/aja.1001650304 Occurrence Handle6758566
D. J. Walther M. Bader (1999) ArticleTitleSerotonin synthesis in murine embryonic stem cells Brain Res. Mol. Brain Res. 68 55–63 Occurrence Handle10.1016/S0169-328X(99)00046-7 Occurrence Handle10320783
J. F. Colas J. M. Launay J. L. Vonesch P. Hickel L. Maroteaux (1999) ArticleTitleSerotonin synchronises convergent extension of ectoderm with morphogenetic gastrulation movements in Drosophila Mech. Dev. 87 77–91 Occurrence Handle10.1016/S0925-4773(99)00141-0 Occurrence Handle10495273
J. F. Colas J. M. Launay L. Maroteaux (1999) ArticleTitleMaternal and zygotic control of serotonin biosynthesis are both necessary for Drosophila germband extension Mech. Dev. 87 67–76 Occurrence Handle10.1016/S0925-4773(99)00140-9 Occurrence Handle10495272
A. Hay-Schmidt (2000) ArticleTitleThe evolution of the serotonergic nervous system Proc. R. Soc. Lond. B: Biol. Sci. 267 1071–1079 Occurrence Handle10.1098/rspb.2000.1111
G. A. Buznikov H. W. Lambert J. M. Lauder (2001) ArticleTitleSerotonin and serotonin-like substances as regulators of early embryogenesis and morphogenesis Cell Tissue Res. 305 177–186 Occurrence Handle10.1007/s004410100408 Occurrence Handle11545255
S. Candiani A. Augello D. Oliveri M. Passalacqua R. Pennati F. Bernardi ParticleDe M. Pestarino (2001) ArticleTitleImmunocytochemical localization of serotonin in embryos, larvae and adults of the lancelet, Branchiostoma floridae Histochem. J. 33 413–420 Occurrence Handle10.1023/A:1013775927978 Occurrence Handle11858461
R. Deguchi M. Morisawa (2003) ArticleTitleExternal Ca2+ is predominantly used for cytoplasmic and nuclear Ca2+ increases in fertilized oocytes of the marine bivalve Mactra chinensis J. Cell Sci. 116 367–376 Occurrence Handle10.1242/jcs.00221 Occurrence Handle12482922
S. A. Doran R. Koss C. H. Tran K. J. Christopher W. J. Gallin J. I. Goldberg (2004) ArticleTitleEffect of serotonin on ciliary beating and intracellular calcium concentration in identified populations of embryonic ciliary cells J. Exp. Biol. 207 1415–1429 Occurrence Handle10.1242/jeb.00924 Occurrence Handle15010492
P. Gaspar O. Cases L. Maroteaux (2003) ArticleTitleThe developmental role of serotonin: news from mouse molecular genetics Nat. Rev. Neurosci. 4 1002–1012 Occurrence Handle10.1038/nrn1256 Occurrence Handle14618156
G. Il’kova P. Rehak J. Vesela S. Cikos D. Fabian S. Czikkova J. Koppel (2004) ArticleTitleSerotonin localization and its functional significance during mouse preimplantation embryo development Zygote 12 205–213 Occurrence Handle10.1017/S0967199404002862 Occurrence Handle15521710
J. A. Kreiling K. Jessen-Eller J. Miller R. F. Seegal C. L. Reinisch (2001) ArticleTitleEarly development of the serotonergic and dopaminergic nervous system in Spisula solidissima (surf clam) larvae Comp. Biochem. Physiol. A Mol. Integr. Physiol. 130 341–351 Occurrence Handle10.1016/S1095-6433(01)00394-4 Occurrence Handle11544079
J. M. Lauder (1993) ArticleTitleNeurotransmitters as growth regulatory signals: role of receptors and second messengers Trends Neurosci. 16 233–240 Occurrence Handle10.1016/0166-2236(93)90162-F Occurrence Handle7688165
M. Levin (2004) ArticleTitleA novel immunohistochemical method for evaluation of antibody specificity and detection of labile targets in biological tissue J. Biochem. Biophys. Methods 58 85–96 Occurrence Handle10.1016/S0165-022X(03)00149-0 Occurrence Handle14597192
R. Pennati S. Groppelli C. Sotgia G. Zega M. Pestarino F. Bernardi ParticleDe (2003) ArticleTitleWAY-100635, an antagonist of 5-HT(1A) receptor, causes malformations of the CNS in ascidian embryos Dev. Genes Evol. 213 187–192 Occurrence Handle12684776
Y. Sheng L. Wang X. S. Liu V. Montplaisir M. Tiberi J. M. Baltz X. J. Liu (2005) ArticleTitleA 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. 202 777–786 Occurrence Handle10.1002/jcp.20170 Occurrence Handle15499574
S. A. Stricker T. L. Smythe (2000) ArticleTitleMultiple triggers of oocyte maturation in nemertean worms: the roles of calcium and serotonin J. Exp. Zool. 287 243–261 Occurrence Handle10.1002/1097-010X(20000801)287:3<243::AID-JEZ6>3.0.CO;2-B Occurrence Handle10900444
G. A. Buznikov Y. B. Shmukler J. M. Lauder (1996) ArticleTitleFrom oocyte to neuron: do neurotransmitters function in the same way throughout development? Cell Mol. Neurobiol. 16 537–559 Occurrence Handle10.1007/BF02152056 Occurrence Handle8956008
T. Gustafson M. Toneby (1970) ArticleTitleOn the role of serotonin and acetylcholine in sea urchin morphogenesis Exp. Cell Res. 62 102–117 Occurrence Handle10.1016/0014-4827(79)90512-3 Occurrence Handle4394736
T. Gutafson M. I. Toneby (1971) ArticleTitleHow genes control morphogenesis. The role of serotonin and acetylcholine in morphogenesis Am. Sci. 59 452–462 Occurrence Handle5089200
G. A. Buznikov (1990) Neurotransmitters in Embryogenesis Harwood Academic Press Chur, Switzerland
F. Renaud E. Parisi A. Capasso P. Prisco ParticleDe (1983) ArticleTitleOn the role of serotonin and 5-methoxy-tryptamine in the regulation of cell division in sea urchin eggs Dev. Biol. 98 37–46 Occurrence Handle10.1016/0012-1606(83)90333-0 Occurrence Handle6305746
S. Yaguchi K. Kanoh S. Amemiya H. Katow (2000) ArticleTitleInitial analysis of immunochemical cell surface properties, location and formation of the serotonergic apical ganglion in sea urchin embryos Dev. Growth Differ. 42 479–488 Occurrence Handle10.1046/j.1440-169x.2000.00535.x Occurrence Handle11041489
H. Katow S. Yaguchi M. Kiyomoto M. Washio (2004) ArticleTitleThe 5-HT receptor cell is a new member of secondary mesenchyme cell descendants and forms a major blastocoelar network in sea urchin larvae Mech. Dev. 121 325–337 Occurrence Handle10.1016/j.mod.2004.03.005 Occurrence Handle15110043
K. G. Anitole-Misleh K. M. Brown (2004) ArticleTitleDevelopmental regulation of catecholamine levels during sea urchin embryo morphogenesis Comp. Biochem. Physiol. A Mol. Integr. Physiol. 137 39–50 Occurrence Handle10.1016/j.cbpb.2003.09.001 Occurrence Handle14720589
G. A. Buznikov V. I. Podmarev (1990) Animal species for developmental studies T. A. Dettlaff S. G. Vassetsky (Eds) Invertebrates EditionNumber1 Plenum New York and London 253–285
P. J. Pauwels (2000) ArticleTitleDiverse signalling by 5-hydroxytryptamine (5-HT) receptors Biochem. Pharmacol. 60 1743–1750 Occurrence Handle10.1016/S0006-2952(00)00476-7 Occurrence Handle11108789
A. J. Tierney (2001) ArticleTitleStructure and function of invertebrate 5-HT receptors: a review Comp. Biochem. Physiol. A Mol. Integr. Physiol. 128 791–804 Occurrence Handle10.1016/S1095-6433(00)00320-2 Occurrence Handle11282322
D. Hoyer J. P. Hannon G. R. Martin (2002) ArticleTitleMolecular, pharmacological and functional diversity of 5-HT receptors Pharmacol. Biochem. Behav. 71 533–554 Occurrence Handle10.1016/S0091-3057(01)00746-8 Occurrence Handle11888546
J. A. Wallace P. Petrusz J. M. Lauder (1982) ArticleTitleSerotonin immunocytochemistry in the adult and develo** rat brain: methodological and pharmacological considerations Brain Res. Bull. 9 117–129 Occurrence Handle10.1016/0361-9230(82)90127-7 Occurrence Handle6756548
J. R. Raymond J. Kim R. E. Beach C. C. Tisher (1993) ArticleTitleImmunohistochemical map** of cellular and subcellular distribution of 5-HT1A receptors in rat and human kidneys Am. J. Physiol. 264 F9–19 Occurrence Handle8430834
J. Hardin J. A. Coffman S. D. Black D. R. McClay (1992) ArticleTitleCommitment along the dorsoventral axis of the sea urchin embryo is altered in response to NiCl2 Development 116 671–685 Occurrence Handle1289059
D. R. Sherwood D. R. McClay (1999) ArticleTitleLvNotch signaling mediates secondary mesenchyme specification in the sea urchin embryo Development 126 1703–1713 Occurrence Handle10079232
G. M. Wessel D. R. McClay (1985) ArticleTitleSequential expression of germ-layer specific molecules in the sea urchin embryo Dev. Biol. 111 451–463 Occurrence Handle10.1016/0012-1606(85)90497-X Occurrence Handle2412914
D. W. Bonhaus C. Bach A. DeSouza F. H. Salazar B. D. Matsuoka P. Zuppan H. W. Chan R. M. Eglen (1995) ArticleTitleThe pharmacology and distribution of human 5-hydroxytryptamine2B (5-HT2B) receptor gene products: comparison with 5-HT2A and 5-HT2C receptors Br. J. Pharmacol. 115 622–628 Occurrence Handle7582481
E. Fiorica-Howells L. Maroteaux M. D. Gershon (2000) ArticleTitleSerotonin and the 5-HT(2B) receptor in the development of enteric neurons J. Neurosci. 20 294–305 Occurrence Handle10627607
V. J. Aloyo K. D. Dave T. Rahman J. A. Harvey (2001) ArticleTitleSelective and divergent regulation of cortical 5-HT(2A) receptors in rabbit J. Pharmacol. Exp. Ther. 299 1066–1072 Occurrence Handle11714896
I. T. Forbes S. Dabbs D. M. Duckworth P. Ham G. E. Jones F. D. King D. V. Saunders F. E. Blaney C. B. Naylor G. S. Baxter T. P. Blackburn G. A. Kennett M. D. Wood (1996) ArticleTitleSynthesis, biological activity, and molecular modeling of selective 5-HT(2C/2B) receptor antagonists J. Med. Chem. 39 4966–4977 Occurrence Handle10.1021/jm960571v Occurrence Handle8960557
Y. B. Shmukler G. A. Buznikov M. J. Whitaker (1999) ArticleTitleAction of serotonin antagonists on cytoplasmic calcium levels in early embryos of sea urchin Lytechinus pictus Int. J. Dev. Biol. 43 179–182 Occurrence Handle10235395
G. A. Buznikov V. V. Bezuglov (2000) ArticleTitle[Polyenic acid 5-hydroxytryptamides and 3-hydroxytyramides as tools for studying of the pre-nervous biogenic monoamine functions] Ross Fiziol Zh Im I M Sechenova 86 1093–1108 Occurrence Handle11081216
Z. **a J. A. Gray B. A. Compton-Toth B. L. Roth (2003) ArticleTitleA direct interaction of PSD-95 with 5-HT2A serotonin receptors regulates receptor trafficking and signal transduction J. Biol. Chem. 278 21901–21908 Occurrence Handle10.1074/jbc.M301905200 Occurrence Handle12682061
S. A. Berry M. C. Shah N. Khan B. L. Roth (1996) ArticleTitleRapid agonist-induced internalization of the 5-hydroxytryptamine2A receptor occurs via the endosome pathway in vitro Mol. Pharmacol. 50 306–313 Occurrence Handle8700138
A. Bhatnagar D. L. Willins J. A. Gray J. Woods J. L. Benovic B. L. Roth (2001) ArticleTitleThe dynamin-dependent, arrestin-independent internalization of 5-hydroxytryptamine 2A (5-HT2A) serotonin receptors reveals differential sorting of arrestins and 5-HT2A receptors during endocytosis J. Biol. Chem. 276 8269–8277 Occurrence Handle10.1074/jbc.M006968200 Occurrence Handle11069907
B. L. Roth D. L. Willins K. Kristiansen W. K. Kroeze (1998) ArticleTitle5-Hydroxytryptamine2-family receptors (5-hydroxytryptamine2A, 5-hydroxytryptamine2B, 5-hydroxytryptamine2C): where structure meets function Pharmacol. Ther. 79 231–257 Occurrence Handle10.1016/S0163-7258(98)00019-9 Occurrence Handle9776378
D. L. Willins L. Alsayegh S. A. Berry J. R. Backstrom E. Sanders-Bush L. Friedman N. Khan B. L. Roth (1998) ArticleTitleSerotonergic antagonist effects on trafficking of serotonin 5-HT2A receptors in vitro and in vivo Ann. NY Acad. Sci. 861 121–127 Occurrence Handle9928248
N. R. Hanley J. G. Hensler (2002) ArticleTitleMechanisms of ligand-induced desensitization of the 5-hydroxytryptamine(2A) receptor J. Pharmacol. Exp. Ther. 300 468–477 Occurrence Handle10.1124/jpet.300.2.468 Occurrence Handle11805206
J. A. Gray A. Bhatnagar V. V. Gurevich B. L. Roth (2003) ArticleTitleThe interaction of a constitutively active arrestin with the arrestin-insensitive 5-HT(2A) receptor induces agonist-independent internalization Mol. Pharmacol. 63 961–972 Occurrence Handle10.1124/mol.63.5.961 Occurrence Handle12695524
G. A. Buznikov T. A. Slotkin J. M. Lauder (2003) ArticleTitleSea urchin embryos and larvae as biosensors for neurotoxicants Curr. Prot. Toxicol. 2 161–1624
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
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 30, 825–837 (2005). https://doi.org/10.1007/s11064-005-6876-6
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s11064-005-6876-6