Advertisement

The Histochemical Journal

, Volume 33, Issue 7, pp 413–420 | Cite as

Immunocytochemical Localization of Serotonin in Embryos, Larvae and Adults of the Lancelet, Branchiostoma Floridae

  • S. Candiani
  • A. Augello
  • D. Oliveri
  • M. Passalacqua
  • R. Pennati
  • F. De Bernardi
  • M. Pestarino
Article

Abstract

Serotonin (5-hydroxytryptamine) is a biogenic amine distributed throughout the metazoans and has an old evolutionary history. It is involved as a developmental signal in the early morphogenesis of both invertebrates and vertebrates, whereas in adults it acts mainly as a neurotransmitter and gastrointestinal hormone. In vertebrates, serotonin regulates the morphogenesis of the central nervous system and the specification of serotonergic as well as dopaminergic neurons. The present study uses, as an experimental model, an invertebrate chordate, the lancelet Branchiostoma floridae, characterized by its remarkable homologies with vertebrates that allows the 'bauplan' of the probable ancestor of vertebrates to be outlined. In particular, the involvement of serotonin as a developmental signal in embryos and larvae, as well as a neurotransmitter and gastrointestinal hormone in adult specimens of Branchiostoma floridae, gives further support to a common origin of cephalocordates and vertebrates.

Keywords

Nervous System Central Nervous System Serotonin Experimental Model Evolutionary History 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aiello E (1974) The control of ciliary activity in metazoa. In: Sleigh MA, ed. Cilia and Flagella. London: Academic Press, pp. 353–376.Google Scholar
  2. Anadòn R, Adrio F, Rodriguez-Moldes I (1998) Distribution of GABA immunoreactivity in the central and peripheral nervous system of amphioxus (Branchiostoma lanceolatum Pallas). J Comp Neurol 401: 293–307.Google Scholar
  3. Barnes NM, Sharp T (1999) A review of central 5-HT receptors and their function. Neuropharmacology 38: 1083–1152.Google Scholar
  4. Beccari N (1943) Il midollo spinale e formazioni encefaliche nei Leptocardii. Neurologia Comparata. Firenze: Sansoni Edizioni Scientifiche, pp. 35–38.Google Scholar
  5. Bisgrove BW, Burke RD (1986) Development of serotonergic neurons in embryos of the sea urchin Strongylocentrotus purpuratus. Dev Growth Differ 28: 569–574.Google Scholar
  6. Bodis J, Hartmann G, Tinnenberg HR, Torok A, Hanf V, Papenfuss F, Schwarz H (1993) Relationships between the monoamine, progesterone and estradiol content in follicular fluid of preovulatory graafian follicles after superovulation treatment. Gynecol Obstet Invest 35: 232–235.Google Scholar
  7. Bone Q(1960) The central nervous system in amphioxus. J Comp Neurol 115: 27–64.Google Scholar
  8. Buznikov GA (1984) The action of neurotransmitters and related substances on early embryogenesis. Pharmacol Ther 25: 23–59.Google Scholar
  9. Buznikov GA (1990) Neurotransmitters in Embryogenesis. Chur: Harwood Academic Publishers.Google Scholar
  10. Buznikov GA (1991) The biogenic amines as regulators of early (pre-nervous) embryogenesis: New data. Adv Exp Med Biol 296: 33–48.Google Scholar
  11. Buznikov GA, Sakharova AV, Manukhin BN, Markova LN (1972) The role of neurohumours in early embryogenesis. J Embryol Exp Morph 27: 339–351.Google Scholar
  12. Buznikov GA, Shmukler YB (1981) Possible role of “prenervous” neurotransmitters in cellular interactions of early embryogenesis: A hypothesis. Neurochem Res 6: 55–68.Google Scholar
  13. Buznikov GA, Nikitina LA, Galanov AY, Malchenko LA, Trubnikova OB (1993) The control of oocyte maturation in the starfish and amphibians by serotonin and its antagonists. Int J Dev Biol 37: 363–364.Google Scholar
  14. Buznikov GA, Shmukler YB, Lauder JA (1996) From oocyte to neuron: Do neurotransmitters function in the same way throughout development? Cell Mol Neurobiol 16: 533–559.Google Scholar
  15. Buznikov GA, Lambert HW, Lauder JM (2001) Serotonin and serotoninlike substances as regulators of early embryogenesis and morphogenesis. Cell Tissue Res 305: 177–186.Google Scholar
  16. Cappellini C, Malatesta P, Costa B, Marracci S, Nardi I, Martini C (1999) Characterisation of a cloned Xenopus laevis serotonin 5-HT1A receptor expressed in the NIH-3T3 cell line. Mol Brain Res 63: 380–383.Google Scholar
  17. Colas JF, Launay JM, Maroteaux L (1999a) Maternal and zygotic control of serotonin biosynthesis are both necessary for Drosophila germband extension. Mech Dev 87: 67–76.Google Scholar
  18. Colas JF, Launay JM, Vonesch JL, Hickel P, Maroteaux L (1999b) Serotonin synchronises convergent extension of ectoderm with morphogenetic gastrulation movements in Drosophila. Mech Dev 87: 77–91.Google Scholar
  19. Conklin EG (1932) The embriology of amphioxus. J Morphol 54: 69–151.Google Scholar
  20. Csaba G, Bierbauer J (1974) Investigation on the specificity of hormone receptors in Planarians. Gen Comp Endocrinol 22: 132–134.Google Scholar
  21. Csaba G, Nagy SU, Lantos T (1978) Cyclic AMP and its functional relationship in Tetrahymena: A comparison between phagocytosis and glucose uptake. Acta Biol Med Germ 37: 505–507.Google Scholar
  22. Diefenbach TJ, Koehncke NK, Goldberg JI (1991) Characterisation and development of rotational behaviour in Helisoma embryos – role of endogenous serotonin. J Neurobiol 22: 922–934.Google Scholar
  23. Diefenbach TJ, Koss R, Goldberg JI (1998) Early development of an identified serotonergic neuron in Helisoma trivolvis embryos: Serotonin expression, de-expression, and uptake. ENC 1: 361–376.Google Scholar
  24. Ebbesson LO, Holqvist B, Ostholm T, Ekstrom P (1992) Transient serotonin-immunoreactive neurones coincide with a critical period of neural development in coho salmon (Onchorhynchus kisutch). Cell Tissue Res 268: 389–392.Google Scholar
  25. Emerit MB, Riad M, Hamon M (1992) Trophic effects of neurotransmitters during brain maturation. Biol Neonate 62: 193–201.Google Scholar
  26. Eriksson K, Gustaffson M, Akerlind G (1993) High-performance liquid chromatography analysis of monoamines in the cestode Diphyllobothrium dendriticum. Parasitol Res 79: 699–702.Google Scholar
  27. Erspamer V (1946) Presenza di enteramina o di una sostanza enteraminosimile negli estratti gastrointestinali e splenici dei pesci e negli estratti gastroenterici delle Ascidie. Experientia 2: 369–371.Google Scholar
  28. Erspamer V, Asero B (1952) Identification of enteramine, the specific hormone of the enterochromaffin cell system, as 5-hydroxytryptamine. Nature 169: 800.Google Scholar
  29. Franquinet R (1979) Rôle de la serotonine et des catecholamines dans la régénération de la planaire Polycelis tenuis. J Embryol Exp Morphol 51: 85–95.Google Scholar
  30. Fritsch HAR (1976) The occurrence of argyrophilic and argentaffin cells in the gut of Ciona intestinalis L. Cell Tissue Res 175: 131–135.Google Scholar
  31. Fritsch HAR, van Noorden S, Pearse ADE (1982) Gastro-intestinal and neurohormonal peptides in the alimentary tract and cerebral complex of Ciona intestinalis (Ascidiacea). Cell Tissue Res 223: 369–402.Google Scholar
  32. Fujii K, Takeda N (1988) Phylogenetic detection of serotonin immunoreactive cells in the central nervous system of invertebrates. Comp Biochem Physiol 89C: 233–239.Google Scholar
  33. Fujita T, Kobayashi S (1974) The cells and hormones of the GEP endocrine system. The current studies. In: Fujita T, ed. Gastro-Entero-Pancreatic Endocrine System. A Cell Biological Approach. Tokyo: Igaku Shoin, pp. 1–16.Google Scholar
  34. Georges D (1985) Presence of cells resembling serotonergic elements in four species of tunicates. Cell Tissue Res 242: 341–348.Google Scholar
  35. Gerzeli G (1961) Presence of enterochromaffin cells in the gut of amphioxus. Nature 4760: 237–238.Google Scholar
  36. Gerzeli G (1963) Le cellule enterocromaffini nei Tunicata. Pubbl Staz Zool Napoli 33: 117–124.Google Scholar
  37. Hamdan FF, Ungrin MD, Abramovitz M, Ribeiro P (1999) Characterisation of a novel serotonin receptor from Caenorhabditis elegans: Cloning and expression of two splice variants. J Neurochem 72: 1372–1383.Google Scholar
  38. Hansson SR, Mezey E, Hoffman BJ (1998) Serotonin transporter messenger RNA in the developing rat brain: Early expression in serotonergic neurons and transient expression in non-serotonergic neurons. Neuroscience 83: 1185–1201.Google Scholar
  39. Hay-Schmidt A (1990) Catecholamine-containing, serotonin-like, and FMRFamide-like immunoreactive neurons and processes in the nervous system of the early actinotroch larva of Phoronis muelleri (Phoronida): Distribution and development. Can J Zool 68: 1525–1536.Google Scholar
  40. Helluy S, Sandeman S, Beltz B, Sandeman D (1993) Comparative brain ontogeny of the crayfish and clawed lobster: Implications of direct and larval development. J Comp Neurol 335: 343–354.Google Scholar
  41. Holland ND, Holland LZ (1989) Fine structural study of the cortical reaction and formation of the egg coats in a lancelet (= amphioxus), Branchiostoma floridae (Phylum Chordata: Subphylum Cephalochordata = Acrania). Biol Bull 176: 111–122.Google Scholar
  42. Holland ND, Holland LZ (1993) Serotonin-containing cells in the nervous system and other tissues during ontogeny of a lancelet, Branchiostoma floridae. Acta Zool (Stockholm) 74: 195–204.Google Scholar
  43. Huang W, Fang Y, Su H, Qi X (1991) Immunohistochemical localisation of 5-HT in amphioxus. Chin Sci Bull 36: 329–332.Google Scholar
  44. Hulting G (1973) Intestinal enterochromaffin cells in Branchiostoma lanceolatum studied by fluorescence and electron microscopy. Acta Zool (Stockholm) 54: 173–178.Google Scholar
  45. Hynes M, Rosenthal A (1999) Specification of dopaminergic and serotonergic neurons in the vertebrate CNS. Curr Opin Neurobiol 9: 26–36.Google Scholar
  46. Kempf SC, Page LR, Pires A (1997) Development of serotonin-like immunoreactivity in the embryos and larvae of nudibranch molluscs with emphasis on the structure and possible function of the apical sensory organ. J Comp Neurol 386: 507–528.Google Scholar
  47. Krantic S, Dube F, Guerrier P (1993) Evidence for a new subtype of serotonin receptor in oocytes of the surf clam Spisula solidissima. Gen Comp Endocrinol 90: 125–131.Google Scholar
  48. Lacalli TC (1994) Apical organs, epithelial domains, and the origin of the chordate central nervous system. Amer Zool 34: 533–541.Google Scholar
  49. Lacalli TC (1996) Frontal eye circuitry, rostral sensory pathways and brain organization in amphioxus larvae: Evidence from 3D reconstructions. Phil Trans R Soc Lond B 351: 243–263.Google Scholar
  50. Lauder JM (1993) Neurotransmitters as growth regulatory signals: Role of receptors and second messengers. Trends Neurosci 16: 233–240.Google Scholar
  51. Lauder JM, Tamir H, Sadler TW (1988) Serotonin and morphogenesis. Development 102: 709–720.Google Scholar
  52. Marracci S, Cini D, Nardi I (1997) Cloning and developmental expression of 5-HT1A receptor gene in Xenopus laevis. Mol Brain Res 47: 67–77.Google Scholar
  53. Moiseivitsch JRD, Lauder JM (1995) Serotonin regulates mouse cranial neurula crest migration. Proc Natl Acad Sci USA 92: 7182–7186.Google Scholar
  54. Neckameyer WS, White K (1992) Asingle locus encodes both phenylalanine hydroxylase and tryptophan hydroxylase activities in Drosophila. J Biol Chem 267: 4199–4206.Google Scholar
  55. Nguyen L, Rigo JM, Rocher V, Belachew S, Malgrange B, Rogister B, Leprince P, Moonen G (2001) Neurotransmitters as early signals for central nervous system development. Cell Tissue Res 305: 187–202.Google Scholar
  56. Nolen TG, Carew TJ (1994) Ontogeny of the serotonin-immunoreactive neurons in juvenile Aplysia californica: Implications for the development of learning. Behav Neural Biol 61: 282–295.Google Scholar
  57. Obermüller-wilán H, van Veen T (1981) Monoamines in the brain of the lancelet, Branchiostoma lanceolatum. Cell Tissue Res 221: 245–246.Google Scholar
  58. Osborne, NN (1982) Assay, distribution and functions of serotonin in nervous tissues. In: Osborne NN, ed. Biology of Serotonergic Transmission. Chichester: John Wiley, pp. 7–27.Google Scholar
  59. Osborne NN, Neuhof V, Ewers E, Robertson A (1979) Putative neurotransmitters in the cerebral ganglia of the tunicate Ciona intestinalis. Comp Biochem Physiol 63C: 209–213.Google Scholar
  60. Parent A (1981) The anatomy of serotonin-containing neurons across phylogeny. In: Jacob BL, Gelperin A, eds. Serotonin Neurotransmission and Behavior. Cambridge: The MIT Press, pp. 1–34.Google Scholar
  61. Pestarino M (1982) Occurrence of different secretin-like cells in the digestive tract of the ascidian Styela plicata (Urochordata, Ascidiacea). Cell Tissue Res 226: 231–235.Google Scholar
  62. Pierre J, Reperant I, Ward R, Vesselkin NP, Rio JP, Miceli D, Kratshin I (1992) The serotonergic system of the brain of the lamprey, Lampetra fluviatilis:An evolutionary perspective. J Chem Neuroanat 5: 195–219.Google Scholar
  63. Ranganathan R, Cannon SC, Horvitz R (2000) MOD-1 is a serotoningated chloride channel that modulates locomotory behaviour in C. elegans. Nature 408: 470–475.Google Scholar
  64. Rios H, Brusco A, Pecci Saavedra J (1997) Development of serotonergic chick retinal neurons. Int J Dev Neurosci 15: 729–738.Google Scholar
  65. Ruppert EE, Barnes RD (1994) Invertebrate Zoology. 6th edn. Philadelphia: Saunders College Publishing.Google Scholar
  66. Sakharov DA, Salimova N (1982) Serotonin-containing cells in the ascidian endostyle. Experientia 38: 802–803.Google Scholar
  67. Sanderson MJ, Dirksen ER, Satir P (1985) The antagonistic effects of 5-hydroxytryptamine and methylxanthine on the gill cilia of Mytilus edulis. Cell Motil 5: 293–309.Google Scholar
  68. Saudou F, Boschert U, Amlaiky N, Plassat JL, Hen R (1992) A family of Drosophila serotonin receptors with distinct intracellular signalling properties and expression patterns. Embo J 11: 7–17.Google Scholar
  69. Schulte E, Riehl R (1977) Elektronenmikroskipische Untersuchungen an den Oralcirren und der Haut von Branchiostoma lanceolatum. Helgolaender wissenschafliche Meeresuntersuchungen 29: 337–357.Google Scholar
  70. Shmukler YB, Buznikov GA, Whitaker MJ (1999) Action of serotonin antagonists on cytoplasmic calcium levels in early embryos of sea urchin Lytechinus pictus. Int J Dev Biol 43: 179–182.Google Scholar
  71. Stokes MD, Holland ND (1995) Embryos and larvae of a lancelet, Branchiostoma floridae, from hatching through metamorphosis: Growth in the laboratory and external morphology. Acta Zool (Stockholm) 76: 105–120.Google Scholar
  72. Sugamori KS, Sunahara RK, Guan HC, Bulloch AGM, Tensen CP, Seeman P, Niznik HB, Vantol HHM (1993) Serotonin receptor cDNA cloned from Lymnaea stagnalis. Proc Natl Acad Sci USA 90: 11–15.Google Scholar
  73. Syed NI, Winlow W (1989) Morphology and electrophysiology of neurons innervating the ciliated locomotor epithelium in Lymnaea stagnalis (L.). Comp Biochem Physiol 93A: 633–644.Google Scholar
  74. Takeda N (1992) Biogenic monoamine system detected simultaneously in the neural complex of the ascidian, Ciona intestinalis. Comp Biochem Physiol 103C: 489–493.Google Scholar
  75. Turlejski K (1996) Evolutionary ancient roles of serotonin: Long-lasting regulation of activity and development. Acta Neurobiol Exp 56: 619–636.Google Scholar
  76. Versaux-Botteri C, Dalil N, Kenigfest N, Reperant J, Vesselkin N, Nguyn-legros J (1991) Immunohistochemical localization of retinal serotonin cells in the lamprey (Lampetra fluviatilis). Visual Neurosci 7: 171–177.Google Scholar
  77. Welsh JH, Loveland RE (1968) 5-Hydroxytryptamine in the ascidian Ciona intestinalis L. Comp Biochem Physiol 27: 719–722.Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • S. Candiani
    • 1
  • A. Augello
    • 1
  • D. Oliveri
    • 1
  • M. Passalacqua
    • 2
  • R. Pennati
    • 3
  • F. De Bernardi
    • 3
  • M. Pestarino
    • 4
  1. 1.Dipartimento di Biologia Sperimentale, Ambientale ed Applicata, Sezione di Neuroendocrinologia e Biologia dello SviluppoUniversità di GenovaGenovaItaly
  2. 2.Dipartimento di Medicina Sperimentale, Sezione di BiochimicaUniversità di GenovaGenovaItaly
  3. 3.Dipartimento di BiologiaUniversità di MilanoMilanoItaly
  4. 4.Dipartimento di Biologia Sperimentale, Ambientale ed Applicata, Sezione di Neuroendocrinologia e Biologia dello SviluppoUniversità di GenovaGenovaItaly

Personalised recommendations