Skip to main content
SpringerLink
Log in

Distribution of peptidergic nerve fibres in bullfrog lingual papillae demonstrated by a combination of double immunofluorescence labelling and a multiple dye filter

  • Papers
  • Published:
The Histochemical Journal Aims and scope Submit manuscript

Summary

Immunoreactivity of substance P, calcitonin gene-related peptide, vasoactive intestinal polypeptide, neuropeptide Y, and galanin is localized in nerve fibres distributed in the fungiform and filiform papillae of the tongue of the bullfrog,Rana catesbeiana. A combination of indirect double immunofluorescence labelling and a multiple dye filter system clearly demonstrated that all substance P fibres in the connective tissue core of the fungiform and filiform papillae, and within the rim of ciliated cells located on the top of the fungiform papillae showed coexistence with calcitonin gene-related peptide. A few fibres in the epithelial discs, which are located in the centre of the top of the fungiform papillae, showed the immunoreactivity of calcitonin gene-related peptide alone. There were no substance P fibres which showed coexistence with vasoactive intestinal polypeptide, galanin, and neuropeptide Y. In high magnification images, substance P and vasoactive intestinal polypeptide, and substance P and galanin fibres were recognized as two interwined fibres within the same thin nerve bundle. No immunoreactivity of leucine- and methionine-enkephalins can be detected.

These findings suggest that the chemoreceptor function of the bullfrog gustatory organ may be under the control of complicated peptidergic innervation.

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

Similar content being viewed by others

References

  • Baecker, B., Yanaihara, N. &Forssmann, W.G. (1983) VIP innervation of the tongue in vertebrates.Anat. Embryol. 167, 173–89.

    Article  PubMed  CAS  Google Scholar 

  • Dehan, R.S. &Graziadei, P.P.C. (1971) Functional anatomy of frog's taste organs.Experientia 27, 823–6.

    Article  PubMed  CAS  Google Scholar 

  • Finger, T. E. (1986) Peptide immunohistochemistry demonstrates multiple classes of perigemmal nerve fibers in the circumvallata papilla of the rat.Chem. Senses. 11, 135–44.

    CAS  Google Scholar 

  • Graziadei, P. P. C. &Dehan, R. S. (1971) The ultrastructure of frog's taste organs.Acta Anat. 80, 563–603.

    PubMed  CAS  Google Scholar 

  • Hirata, K. &Kanaseki, T. (1987) Substance P-like immunoreactive fibers in the frog taste organs.Experientia 43, 386–9.

    Article  PubMed  CAS  Google Scholar 

  • Ichikawa, H., Nishikawa, S., Wakisaka, S., Matsuo, S., Takano, Y. &Akai, Y. (1988) Coexistence of vasoactive intestinal polypeptide-and substance P-like immunoreactivities in the tongue of the guinea pig.Neurosci. Lett. 89, 283–5.

    Article  PubMed  CAS  Google Scholar 

  • Jaeger, C.B. &Hillman, D.E. (1976) Morphology of gustatory organs. InFrog Neurobiology (edited by R. Llians & W. Precht) pp. 587–606. Heidelberg: Springer-Verlag.

    Google Scholar 

  • Kawakami, T., Kusakabe, T. &Takenaka, T. (1995) Distribution of immunoreactive neuropeptides in the pancreas of the bullfrog,Rana catesbeiana, demonstrated by immunofluorescence.Cell Tissue Res. 280, 307–11.

    PubMed  CAS  Google Scholar 

  • Kinnman, E. &Aldskogius, H. (1991) The role of substance P and calcitonin gene-related peptide containing nerve fibers in maintaining fungiform taste buds in the rat after a chronic chorda tympani nerve injury.Exp. Neurol. 113, 85–91.

    Article  PubMed  CAS  Google Scholar 

  • Kline, L.W., Kaneko, T., Chiu, K.W., Harvey, S. &Pang, P.T.K. (1988) Calcitonin gene-related peptide in the bullfrog,Rana catesbeiana: Localization and vascular actions.Gen. Comp. Endocrinol. 72, 123–9.

    Article  PubMed  CAS  Google Scholar 

  • Kuramoto, H. (1988) An immunohistochemical study of cellular and nervous elements in the taste organ of the bullfrog,Rana catesbeiana.Arch Histol. Cytol. 51, 205–21.

    PubMed  CAS  Google Scholar 

  • Kusakabe, T., Kawakami, T., Hori, H., Bandou, Y. &Takenaka, T. (1993a) Immunohistochemical coexistence of calcitonin gene-related peptide and substance P in the nerve fibers of the internal gills of bullfrog (Rana catesbeiana) larvae.Neurosci. Lett. 158, 59–62.

    Article  PubMed  CAS  Google Scholar 

  • Kusakabe, T., Kawakami, T., Tanabe, Y., Fujii, S., Bandou, Y. &Takenaka, T. (1993b) Coexistence of substance P and calcitonin gene-related peptide in the nerve fibers of the carotid labyrinth of the bullfrog,Rana catesbeiana.Brain Res. 603, 153–6.

    Article  PubMed  CAS  Google Scholar 

  • Kusakabe, T., Kawakami, T. &Takenaka, T. (1994a) Coexistence of substance P, neuropeptide Y, VIP, and CGRP in the nerve fibers of the carotid labyrinth of the bullfrog,Rana catebeiana: a double-labelling immunofluorescence study in combination with alternate consecutive sections.Cell Tissue Res. 276, 91–7.

    Article  PubMed  CAS  Google Scholar 

  • Kusakabe, T., Kawakami, T. &Takenaka, T. (1994b) Localization of immunoreactive neuropeptides in the kidney of the bullfrog,Rana catesbeiana, by immunofluorescence.Cell Tissue Res. 278, 41–4.

    PubMed  CAS  Google Scholar 

  • Kusakabe, T., Kawakami, T. &Takenaka, T. (1995a) Peptidergic innervation in the amphibian carotid labyrinth.Histol. Histopathol. 10, 185–202.

    PubMed  CAS  Google Scholar 

  • Kusakabe, T., Kawakami, T., Ono, M., Hori, H., Sawada, H. &Takenaka, T. (1995b) Distribution of galanin-immunoreactive nerve fibers in the carotid labyrinth of the bullfrog,Rana catesbeiana: comparison with substance P-immunoreactive fibers.Cell Tissue Res. 281, 63–7.

    PubMed  CAS  Google Scholar 

  • Lundberg, J.M., Hökfelt, T., Anggard, A., Pernow, B. &Emson, P. (1979) Immunohistochemical evidence for substance P immunoreactive nerve fibers in the taste buds of the cat.Acta Physiol. Scand. 107, 389–91.

    PubMed  CAS  Google Scholar 

  • Lundberg, J.M., Franco-Cereceda Hua, X., Hökfelt, T. &Fischer, A. (1985) Co-existence of substance P and calcitonin generelated peptide-like immunoreactivities in sensory nerves in relation to cardiovascular and bronchoconstrictor effects of capsaicin.Eur. J. Pharmacol. 108, 315–19.

    Article  PubMed  CAS  Google Scholar 

  • Luts, A., Montavon, P., Lindstrand, K. &Sundler, F. (1990) Peptide-containing nerve fibers in the circumvallate papillae.Regul. Pep. 27, 209–26.

    Article  CAS  Google Scholar 

  • Montavon, P., Lindstrand, K., Luts, A. &Sundler, F. (1991) Peptide-containing nerve fibers in the fungiform papillae of pigs and rats.Regul. Pep. 32, 141–50.

    CAS  Google Scholar 

  • Murray, R.G. (1973) The ultrastructure of taste buds. InThe Ultrastructure of Sensory Organs (edited by J. Friedmann) pp. 1–39. Amsterdam: North-Holland.

    Google Scholar 

  • Nagy, J.I., Goedert, M., Hunt, A.P. &Bond A. (1982) The nature of substance P-containing nerve fibers in taste papillae of the rat tongue.Neuroscience 7, 3137–51.

    PubMed  CAS  Google Scholar 

  • Nishimoto, T., Araki, M., Inagaki, S., Shiosaka, S., Shimizu, Y., Yamamoto, K., Senba, E., Sakanaka, M., Takasuki, K., Hara, Y., Takagi, H., Matsuzaki, T. &Tohyama, M. (1982) On the distribution and origins of substance P in the papillae of the rat tongue: an experimental and immunohistochemical study.J. Comp. Neurol. 207, 85–92.

    Article  PubMed  CAS  Google Scholar 

  • Rapuzzi, G. &Casella, C. (1965) Innervation of the fungiform papillae in the frog tongue.J. Neurophysiol. 28, 154–65.

    PubMed  CAS  Google Scholar 

  • Rosenfeld, M.G., Mermod, J.-J., Amara, S.G., Swanson, L.W., Sawchenko, P.E., Rivier, J., Vale, W.W. &Evans, R.M. (1983) Production of a novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing.Nature 304, 129–35.

    Article  PubMed  CAS  Google Scholar 

  • Stensaas, L.J. (1971) The fine structure of fungiform papillae and epithelium of the tongue of South American toad,Calyptocephalella gayi.Am. J. Anat. 131, 443–62.

    Article  PubMed  CAS  Google Scholar 

  • Sundler, F., Brodin, E., Ekblad, E., Hakanson, R. &Uddman, R. (1985) Sensory nerve fibers: distribution of substance P, neurokinin A and calcitonin gene-related peptide. InTachykinin Antagonists (edited by R. Håkanson & F. Sundler), pp. 3–14. Amsterdam: Elsevier.

    Google Scholar 

  • Terenghi, G., Polak, J.M., Rodrigo, J., Mulderry, P.K. &Bloom, S.R. (1986) Calcitonin gene-related peptide-immunoreactive nerves in the tongue, epiglotis and pharynx of the rat: occurrence, distribution and origin.Brain Res. 365, 1–14.

    Article  PubMed  CAS  Google Scholar 

  • Uga, S. &Hama, K. (1967) Electron microscopic studies on the synaptic region of the taste organ of carps and frogs.J. Electronmicrosc. 16, 269–76.

    CAS  Google Scholar 

  • Yamasaki, H., Kubota, Y., Takagi, H. &Tohyama, M. (1984) Immunoelectronmicroscopic study of the fine structure of substance P-containing fibers in the taste buds of the rat.J. Comp. Neurol. 227, 380–93.

    Article  PubMed  CAS  Google Scholar 

  • Yamasaki, H., Kubota, Y. &Tohyama, M. (1985) Ontogeny of substance P-containing fibers in the taste buds and surrounding epithelium. I. Light microscopic analysis.Dev. Brain Res. 18, 301–5.

    Article  CAS  Google Scholar 

  • Zamboni, L. &Demartino, C. (1967) Buffered picric acid formaldehyde: a new rapid fixative for electron microscopy.J. Cell Biol. 35, 148A.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, Yokohama City University School of Medicine, 3-9 Fukuura, Kanazawa-ku, 236, Yokohama, Japan

    Tatsumi Kusakabe, Michio Ono & Hajime Sawada

  2. Department of Physiology, Yokohama City University School of Medicine, 3-9 Fukuura, Kanazawa-ku, 236, Yokohama, Japan

    Tadashi Kawakami & Toshifumi Takenaka

Authors
  1. Tatsumi Kusakabe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tadashi Kawakami
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michio Ono
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hajime Sawada
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Toshifumi Takenaka
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kusakabe, T., Kawakami, T., Ono, M. et al. Distribution of peptidergic nerve fibres in bullfrog lingual papillae demonstrated by a combination of double immunofluorescence labelling and a multiple dye filter. Histochem J 28, 289–297 (1996). https://doi.org/10.1007/BF02409017

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02409017

Keywords

Search

Navigation