Skip to main content
SpringerLink
Log in

Immunoreactivity to molluskan neuropeptides in the central and stomatogastric nervous systems of the earthworm, Lumbricus terrestris L.

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

Abstract

Polyclonal antisera against two related command neuropeptides (CNP2 and CNP4) described in neurons of the terrestrial snail Helix were used in a study of the nervous system of the earthworm Lumbricus. The CNP-like peptides belong to the same neuropeptide subfamily and bear a C-terminal signature sequence Tyr-Pro-Arg-X. The distribution patterns of immunoreactive (IR) neurons were studied in the central nervous system (CNS), skin, and stomatogastric nervous system of the earthworm. IR neurons were found in all CNS ganglia, the patterns being similar for both antibodies used. Several clusters of IR cells were observed in the cerebral and subesophageal ganglia. In the ventral cord ganglia, the number of IR cells decreased in the rostro-caudal direction, and the IR cells sent their fibers mostly into the median fiber bundle. Segmental nerves contained no IR fibers. After injury of the worm body, the number of IR neurons in the CNS significantly increased. In the skin, IR sensory neurons were present in sensory buds. The stomatogastric ganglia only contained IR fibers. Numerous scattered IR neurons were found in the inner subepithelial layer of the esophagus and formed the enteric plexus in which the cell bodies displayed a segmentally repeated pattern. Possible involvement of CNP-like-IR neurons in central integratory processes, sensory processes, and the regulation of feeding is discussed.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Al-Yousuf S (1990) Neuropeptides in annelids. Prog Clin Biol Res 342:232–241

    PubMed  CAS  Google Scholar 

  • Alumets J, Håkanson R, Sundler F, Thorell J (1979) Neuronal localization of immunoreactive enkephalin and beta-endorphin in the earthworm. Nature 279:805–806

    Article  PubMed  CAS  Google Scholar 

  • Aros B, Wenger T, Röhlich P, Vigh B, Vigh-Teichmann I (1980a) Immunocytochemical studies on the central nervous system of the earthworm, Lumbricus terrestris. Acta Biol 31:13–23

    CAS  Google Scholar 

  • Aros B, Wenger T, Vigh B, Vigh-Teichmann I (1980b) Immunohistochemical localization of substance P and ACTH-like activity in the central nervous system of the earthworm Lumbricus terrestris L. Acta Histochem 66:262–268

    PubMed  CAS  Google Scholar 

  • Balaban PM (1991) Command neurons, command function and decision making. In: Sakharov DA, Winlow W (eds) Simple nervous systems. Manchester University Press, Manchester, pp 360–374

    Google Scholar 

  • Balaban PM, Poteryaev DA, Zakharov IS, Uvarov P, Malyshev A, Belyavsky AV (2001) Up- and down-regulation of Helix command-specific 2 (HCS2) gene expression in the nervous system of terrestrial snail Helix lucorum. Neuroscience 103:551–559

    Article  PubMed  CAS  Google Scholar 

  • Banvolgyi T, Barna J, Csoknya M, Lengvari I, Hamori J (1994) The number of ganglion cells in the intact and regenerated nervous system in the earthworm (Lumbricus terrestris). Acta Biol Hung 45:179–184

    PubMed  CAS  Google Scholar 

  • Banvolgyi T, Barna J, Csoknya M, Hamori J, Elekes K (2000) Reorganization of peptidergic systems during brain regeneration in Eisenia fetida (Oligochaeta, Annelida). Acta Biol Hung 51:409–416

    PubMed  CAS  Google Scholar 

  • Barna J, Csoknya M, Lazar Zs, Bartho L, Hamori J, Elekes K (2001) Distribution and action of some putative neurotransmitters in the stomatogastric nervous system of the earthworm, Eisenia fetida (Oligochaeta, Annelida). J Neurocytol 30:313–325

    Article  PubMed  CAS  Google Scholar 

  • Barr PJ (1991) Mammalian subtilisins: the long-sought dibasic processing endopeptidases. Cell 66:1–3

    Article  PubMed  CAS  Google Scholar 

  • Bogdanov YuD, Balaban PM, Poteryaev DA, Zakharov IS, Belyavsky AV (1998) Putative neuropeptides and an EF-hand motif region are encoded by a novel gene expressed in the four giant interneurons of the terrestrial snail. Neuroscience 85:637–647

    Article  PubMed  CAS  Google Scholar 

  • Brownlee DJA, Fairweather I (1999) Exploring the neurotransmitter labyrinth in nematodes. Trends Neurosci 22:16–24

    Article  PubMed  CAS  Google Scholar 

  • Choi M-Y, Rafaeli A, Jurenka RA (2001) Pyrokinin/PBAN-like peptides in the central nervous system of Drosophila melanogaster. Cell Tissue Res 306:459–465

    Article  PubMed  CAS  Google Scholar 

  • Csoknya M, Lengvari I, Benedeczky I, Hamori J (1992) Immunohistochemical and ultrastructural study of the enteric nervous system of earthworm, Lumbricus terrestris L. Acta Biol Hung 43:241–251

    PubMed  CAS  Google Scholar 

  • Csoknya M, Lengvari I, Hiripi L, Eckert M, Rapus J, Elekes K (1996) Octopamine in the central nervous system of Oligochaeta: an immunocytochemical and biochemical study. Cell Tissue Res 285:27–37

    Article  Google Scholar 

  • Csoknya M, Barna J, Banvolgyi T, Hiripi L, Eckert M, Hamori J, Elekes K (1997) Octopamine-containing neurons in the alimentary tract of the earthworm (Eisenia fetida). Brain Res 778:414–417

    Article  PubMed  CAS  Google Scholar 

  • Curry WJ, Fairweather I, Johnston CF, Halton DW, Buchanan KD (1989) Immunocytochemical demonstration of vertebrate neuropeptides in the earthworm Lumbricus terrestris (Annelida, Oligochaeta). Cell Tissue Res 257:577–586

    Article  CAS  Google Scholar 

  • Friedländer B (1888) Beiläge zur Kenntnis des Centralnervensystems von Lumbricus. Z Wiss Zool 47:47–84

    Google Scholar 

  • Fujisawa Y, Kubota I, Nomoto K, Minakata H, Yasuda-Kamatani Y, Ikeda T, Muneoka Y (1993) A Mytilus peptide related to the small cardioactive peptides (SCPs): structure determination and pharmacological characterization. Comp Biochem Physiol 104C:469–475

    CAS  Google Scholar 

  • Günther J (1971a) Der cytologische Aufbau der dorsalen Riesenfasern von Lumbricus terrestris L. Z Wiss Zool 183:51–70

    Google Scholar 

  • Günther J (1971b) Mikroanatomie des Bauchmarks von Lumbricus terrestris L. Z Morphol Tiere 70:141–182

    Google Scholar 

  • Günther J, Walther JB (1971) Funktionelle Anatomie der dorsalen Riesenfaser-Systeme von Lumbricus terrestris L. (Annelida, Oligochaeta). Z Morphol Tiere 70:253–280

    Article  Google Scholar 

  • Hasegawa K, Kobayashi H (1991) Immunohistochemical localization of endothelin-1 in the nervous system of the earthworm Eisenia foetida. Gen Comp Endocrinol 81:433–441

    Google Scholar 

  • Ierusalimsky VN, Balaban PM (2003) Novel family of neuropeptides: immunoreactive neurons in several invertebrate species. VI IBRO Congress, Prague, Abstracts, 2380

    Google Scholar 

  • Ierusalimsky VN, Boguslavsky DV, Belyavsky AV, Balaban PM (2003) Helix peptide immunoreactivity pattern in the nervous system of juvenile Aplysia. Mol Br Res 120:84–89

    Article  CAS  Google Scholar 

  • Kaloustian KV, Edmands JA (1986) Immunochemical evidence for substance P-like peptide in tissues of the earthworm Lumbricus terrestris: action on intestinal contraction. Comp Biochem Physiol [C] 83:329–333

    Article  CAS  Google Scholar 

  • Knapp MF, Mill PJ (1971) The fine structure of ciliated sensory cells in the epidermis of the earthworm Lumbricus terrestris. Tissue Cell 3:623–636

    Article  PubMed  CAS  Google Scholar 

  • Krajniak KG, Klohr RW (1999) The effects of FMRFamide, serotonin, and acetylcholine on the isolated crop-gizzard of the earthworm, Lumbricus terrestris. Comp Biochem Physiol [A] 123:409–415

    Google Scholar 

  • Lengvari I, Csoknya M, Merchenthaler I, Hamori J (1992) Immunohistochemical study of the nervous system in earthworm (Lumbricus terrestris L.). Acta Biol Hung 43:253–258

    PubMed  CAS  Google Scholar 

  • Lengvari I, Csoknya M, Lubics A, Szelier M, Hamori J (1994) Proctolin immunoreactive elements in the nervous system of earthworm (Lumbricus terrestris). Acta Biol Hung 45:337–345

    PubMed  CAS  Google Scholar 

  • Lkhider M, Marcel R, Tramu G (1987) Establishment of a map of neurons in the brain of Eisenia fetida (Annelida, Oligochaeta) containing substances immunologically specific to vertebrate peptides (in French). Gen Comp Endocrinol 65:457–468

    Article  PubMed  CAS  Google Scholar 

  • Lubics A, Reglodi D, Slezak S, Szelier M, Lengvari I (1997) Co-localization of serotonin and FMRFamide-like immunoreactivities in the central nervous system of the earthworm, Eisenia fetida. Acta Histochem 99:459–467

    PubMed  CAS  Google Scholar 

  • Lubics A, Reglodi D, Szelier M, Lengvari I, Kozicz T (2003) Comparative distribution of urocortin- and CRF-like immunoreactivities in the nervous system of the earthworm Lumbricus terrestris. Peptides 24:205–213

    Article  PubMed  CAS  Google Scholar 

  • Marchand CR, Griffond B, Mounzih K, Colard C (1991) Distribution of methionine-enkephalin-like and FMRFamide-like immunoreactivities in the central nervous system (including dorsal bodies) of the snail Helix aspersa Muller. Zool Sci 8:905–913

    Google Scholar 

  • Mill PJ (1978) Sense organs and sensory pathways. In: Mill PJ (ed) Physiology of Annelids. Academic Press, London, pp 63–114

    Google Scholar 

  • Nachman RJ, Roberts VA, Dyson HL, Holman GM, Tainer JA (1991) Active conformation of an insect neuropeptide family. Proc Natl Acad Sci USA 88:4518–4522

    Article  PubMed  CAS  Google Scholar 

  • Nakayama K, Watanabe T, Nakagawa T, Kim WS, Nagahama M, Hosaka M, Hatsuzawa K, Kondoh-Hashiba K, Murakami K (1992) Consensus sequence for precursor processing at mono-arginyl sites. Evidence for the involvement of a Kex2-like endoprotease in precursor cleavages at both dibasic and mono-arginyl sites. J Biol Chem 267:16335–16340

    PubMed  CAS  Google Scholar 

  • Ogawa F (1939) The nervous system of earthworm (Pheritima communissima) in different ages. Sci Rep Tohoku Univ Ser 4:395–488

    Google Scholar 

  • Oumi T, Ukena K, Matsushima O, Ikeda T, Fujita T, Minakata H, Nomoto K (1994) Annetocin: an oxytocin-related peptide isolated from the earthworm, Eisenia foetida. Biochem Biophys Res Commun 198:393–399

    Article  PubMed  CAS  Google Scholar 

  • Predel R, Nachman RJ, Gade G (2001) Myostimulatory neuropeptides in cockroaches: structures, distribution, pharmacological activities, and mimetic analogs. J Insect Physiol 47:311–324

    Article  PubMed  CAS  Google Scholar 

  • Reglodi D, Lubics A, Slezak S, Szelier M, Lengvari I (1997a) Substance P immunoreactive elements in the nervous system of earthworm (Lumbricus terrestris). Acta Biol Hung 48:189–200

    PubMed  CAS  Google Scholar 

  • Reglodi D, Slezak S, Lubics A, Szelier M, Elekes K, Lengvari I (1997b) Distribution of FMRFamide-like immunoreactivity in the nervous system of Lumbricus terrestris. Cell Tissue Res 288:575–582

    Article  PubMed  CAS  Google Scholar 

  • Reglodi D, Lubics A, Szelier M, Lengvari I (1999) Gastrin- and cholecystokinin-like immunoreactivities in the nervous system of the earthworm. Peptides 20:569–577

    Article  PubMed  CAS  Google Scholar 

  • Reglodi D, Lengvari I, Szelier M, Vigh S, Arimura A (2000) Distribution of PACAP-like immunoreactivity in the nervous system of oligochaeta. Peptides 21:183–188

    Article  PubMed  CAS  Google Scholar 

  • Retzius G (1892) Das Nervensystem der Lumbricinen. Biol Untersuch 3:1–16

    Google Scholar 

  • Rzasa PJ, Kaloustian KV, Prokop EK (1984) Immunochemical evidence for met-enkephalin-like and leu-enkephalin-like peptides in tissues of the earthworm, Lumbricus terrestris. Comp Biochem Physiol [C] 77:345–350

    Article  CAS  Google Scholar 

  • Schürmann FW, Günther J (1973) Ultrastructure of the dorsal giant fibre system in the ventral nerve cord of the earthworm. I. Somata of the giant fibres. Z Zellforsch Mikrosk Anat 139:351–368

    Article  PubMed  Google Scholar 

  • Somogyvari-Vigh A, Reglodi D, Li M, Lengvari I, Vigh S, Arimura A (2000) Tissue distribution of PACAP27 and −38 in oligochaeta: PACAP27 is the predominant form in the nervous system of Lumbricus polyphemus. Peptides 21:1185–1191

    Article  PubMed  CAS  Google Scholar 

  • Spörhase-Eichmann U, Gras H, Schürmann FW (1987a) Patterns of serotonin-immunoreactive neurons in the central nervous system of the earthworm Lumbricus terrestris L. I. Ganglia of the ventral nerve cord. Cell Tissue Res 249:601–614

    Google Scholar 

  • Spörhase-Eichmann U, Gras H, Schürmann FW (1987b) Patterns of serotonin-immunoreactive neurons in the central nervous system of the earthworm Lumbricus terrestris L. II. Rostral and caudal ganglia. Cell Tissue Res 249:625–632

    Article  Google Scholar 

  • Spörhase-Eichmann U, Winkler M, Schürmann FW (1998) Dopaminergic sensory cells in the epidermis of the earthworm. Naturwissenschaften 85:547–550

    Article  Google Scholar 

  • Sundler F, Håkanson R, Alumets J, Walles B (1977) Neuronal localization of pancreatic polypeptide (PP) and vasoactive intestinal peptide (VIP) immunoreactivity in the earthworm (Lumbricus terrestris). Brain Res Bull 2:61–65

    Article  PubMed  CAS  Google Scholar 

  • Telkes I, Csoknya M, Buzas P, Gabriel R, Hamori J, Elekes K (1996) GABA-immunoreactive neurons in the central and peripheral nervous system of the earthworm, Lumbricus terrestris (Oligochaeta, Annelida). Cell Tissue Res 285:463–475

    Article  CAS  Google Scholar 

  • Ukena K, Oumi T, Morishita F, Furukawa Y, Matsushima O, Takahama H, Miyata S, Ikeda T, Minakata H, Nomoto K (1997) Immunochemical demonstration of Eisenia tetradecapeptide, a bioactive peptide isolated from the gut of the earthworm Eisenia foetida, in tissues of the earthworm. Cell Tissue Res 288:567–573

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Higher Nervous Activity and Neurophysiology, 5A Butlerova Street, Moscow, 117485, Russia

    Victor N. Ierusalimsky & Pavel M. Balaban

Authors
  1. Victor N. Ierusalimsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pavel M. Balaban
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Victor N. Ierusalimsky.

Additional information

This work was supported by INTAS (grant 01-2117), CRDF (grant RB1-2321-MO-02), and the Russian Foundation for Basic Research (grants 05-04-48724 and 03-04-48179).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ierusalimsky, V.N., Balaban, P.M. Immunoreactivity to molluskan neuropeptides in the central and stomatogastric nervous systems of the earthworm, Lumbricus terrestris L.. Cell Tissue Res 325, 555–565 (2006). https://doi.org/10.1007/s00441-006-0176-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-006-0176-6

Keywords

Search

Navigation