Skip to main content
Log in

Substance P- and cholecytokinin-like immunoreactivity during post-metamorphic development of the central nervous system in the ascidian Ciona intestinalis

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Following metamorphosis, the neural ganglion of ascidians is thought to be formed via the proliferation of epithelial cells comprising the ciliated duct. In adults, neuronal cell bodies expressing substance P- and gastrin/cholecystokinin-like immunoreactivity exhibit clearly defined patterns of distribution. Previous work shows that these patterns are re-established during regeneration of the adult ganglion. We have used antisera against substance P and cholecystokinin to monitor the formation of these patterns during normal post metamorphic development in Ciona intestinalis. Substance P cells first appear in the ganglion in animals of 1 mm body length. Cholecystokinin antiserum was not used at this stage but revealed a clear adult-like pattern of cells in the anterior region at the 3 to 5-mm stage. Substance P cells do not exhibit an adult pattern until animals have a body length of more than 10 mm. Proliferation in the neural complex was studied using the bromodeoxyuridine/anti-bromodeoxyuridine technique. Results suggest a mechanism whereby cells are born in the ciliated duct and later migrate to the ganglion. Double-labelling experiments indicate that more than 11 days elapse between cell birthdates and the expression of either of the peptides. Data presented suggest that the distributional patterns for these peptides during normal development are similar to those seen during regeneration.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Baguñà J, Salò E, Auladell MC (1989a) Regeneration and pattern formation in planarians III. Evidence that neoblasts are totipotent stem cells and the source of blastema cells. Development 107:77–86

    Google Scholar 

  • Baguñà J, Salò E, Romero R (1989b) Effects of activators and antagonists of the neuropeptides substance P and substance K on cell proliferation in planarians. Int J Dev Biol 33:261–266

    Google Scholar 

  • Bollner T, Beesley PW, Thorndyke MC (1991) Birth-dates and differentiation of cells during neural complex regeneration in the ascidian Ciona intestinalis. Regul Pept 35:227

    Google Scholar 

  • Bollner T, Beesley PW, Thorndyke MC (1992) The pattern of substance P- and cholecystokinin-like immunoreactivity during regeneration of the neural complex in the ascidian Ciona intestinalis. J Comp Neurol 325:572–580

    Google Scholar 

  • Bollner T, Beesley PW, Thorndyke MC (1993) Distribution of GABA-like immunoreactivity during post-metamorphic development and regeneration of the central nervous system in the ascidian Ciona intestinalis. Cell Tissue Res 272:553–561

    Google Scholar 

  • Cloney RA (1977) Ascidian metamorphosis: review and analysis. In: Chia FS, Rice ME (eds) Settlement and metamorphosis of marine invertebrate larvae. Elsevier, New York, pp 255–282

    Google Scholar 

  • Elwyn A (1937) Some stages in the development of the neural complex in Ecteinascida turbinata. Bull Neurol Inst NY 6:163–177

    Google Scholar 

  • Georges D (1985) Presence of cells resembling serotonergic elements in four species of tunicates. Cell Tissue Res 242:341–348

    Google Scholar 

  • Johnsen AH, Rehfeld JF (1990) Cionin: a disulfotyrosyl hybrid of cholecystokinin and gastrin from the neural ganglion of the protochordate Ciona intestinalis. J Biol Chem 265:3054–3058

    Google Scholar 

  • Kowaleysky A (1866) Entwicklungsgeschichte der einfachen Ascidien. Mem Acad At Petersbourg 7:1–19

    Google Scholar 

  • Nicol D, Meinertzhagen IA (1988a) Development of the central nervous system of the larval asicidan, Ciona intestinalis L. I. The early lineages of the neural plate. Dev Biol 130:721–736

    Google Scholar 

  • Nicol D, Meinertzhagen IA (1988b) Development of the central nervous system of the larval ascidian, Ciona intestinalis L. II. Neural plate morphogenesis and cell lineages during neurulation. Dev Biol 130:737–766

    Google Scholar 

  • Nicol D, Meinertzhagen IA (1991) Cell counts and maps in the larval central nervous system of the ascidian Ciona intestinalis (L). J Comp Neurol 309:415–429

    Google Scholar 

  • O'Neil GS, Conlon JM, Deacon CF, Thorndyke MC (1987) Tachykinins in the central and peripheral nervous system of the ascidian Ciona intestinalis. Gen Comp Endocrinol 66:314–322

    Google Scholar 

  • Palmberg I (1986) Cell migration and differentiation during wound healing and regeneration in Microstomum lineare (Turbellaria). Hydrobiologia 132:182–188

    Google Scholar 

  • Plickert G, Kroiher M, Munck A (1988) Cell proliferation and early differentiation during embryonic development and metamorphosis of Hydractinia echinata. Development 103:795–803

    Google Scholar 

  • Thorndyke MC, Bevis PJR (1984) Comparative studies on the effects of cholecystokinins, caerulin, bombesin 6–14 nonapeptide and physalaemin on gastric secretion in the ascidian Styela clava. Gen Comp Endocrinol 55:251–259

    Google Scholar 

  • Thorndyke MC, Georges D (1988) Functional aspects of peptide neurohormones in protochordates. In: Thorndyke MC, Goldsworthy GJ (eds) Neurohormones in invertebrates. Cambridge University Press, Cambridge, pp 235–258

    Google Scholar 

  • Venuti JM, Jeffery WR (1989) Cell lineage and determination of cell fate in ascidian embryos. Int J Dev Biol 33:197–212

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bollner, T., Beesley, P.W. & Thorndyke, M.C. Substance P- and cholecytokinin-like immunoreactivity during post-metamorphic development of the central nervous system in the ascidian Ciona intestinalis . Cell Tissue Res 272, 545–552 (1993). https://doi.org/10.1007/BF00318561

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00318561

Key words

Navigation