Skip to main content

Advertisement

SpringerLink
Log in

A Calcium-Receptor Agonist Induces Gustatory Neural Responses in Bullfrogs

  • Original Paper
  • Published:
Cellular and Molecular Neurobiology Aims and scope Submit manuscript

Abstract

The effect of calcium-sensing receptor (CaR) agonists on frog gustatory responses was studied using glossopharyngeal nerve recording and whole-cell patch-clamp recording of isolated taste disc cells. Calcimimetic NPS R-467 dissolved in normal saline solution elicited a large transient response in the nerve. The less active enantiomer of the compound, NPS S-467 induced only a small neural response. The EC50 for NPS R-467 was about 20 μM. Cross-adaptation experiments were performed to examine the effect of 30 μM NPS R-467 and 100 μM quinine on the gustatory neural response. The magnitude of the R-467-induced response after adaptation to quinine was approximately equal to that after adaptation to normal saline solution, indicating that the receptor site for NPS R-467 is different from the site for quinine. NPS R-467 (100 μM) also induced an inward current accompanied with conductance increase and large depolarization in two (13%) of 15 rod cells, and a sustained decrease in outward current and small depolarization in six (40%) other rod cells. NPS S-467 (100 μM) induced a sustained decrease in outward current and depolarization in five (50%) of 10 rod cells. Another calcimimetic cinacalcet (100 μM) induced an inward current accompanied with conductance increase in three (27%) of 11 rod cells. The results suggest that NPS R-467 induces neural responses through cell responses unrelated to a resting K+ conductance decrease.

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

Similar content being viewed by others

References

  • Bigiani AR, Roper SD (1991) Mediation of responses to calcium in taste cells by modulation of a potassium conductance. Science 252:126–128

    Article  PubMed  CAS  Google Scholar 

  • Bigiani AR, Delay RJ, Chaudhari N, Kinnamon SC, Roper SD (1997) Responses to glutamate in rat taste cells. J Neurophysiol 77:3048–3059

    PubMed  CAS  Google Scholar 

  • Casella C, Rapuzzi G (1957) Azione dell’acqua, del CaCl2 e del NaCl sui ricettori linguali della Rana. Arch Sci Biol Bologna 41:191–203

    PubMed  CAS  Google Scholar 

  • Chandrashekar J, Hoon MA, Ryba NJ, Zuker CS (2006) The receptors and cells for mammalian taste. Nature 444:288–294

    Article  PubMed  CAS  Google Scholar 

  • Clapp TR, Medler KF, Damak S, Margolskee RF, Kinnamon SC (2006) Mouse taste cells with G protein-coupled taste receptors lack voltage-gated calcium channels and SNP-25. BMC Biol 4:7

    Article  PubMed  CAS  Google Scholar 

  • Conigrave AD, Brown EM (2006) Taste receptors in the gastrointestinal tract. II. L-amino acid sensing by calcium-sensing receptors: implications for GI physiology. Am J Physiol 291:G753–G761

    CAS  Google Scholar 

  • Fujiyama R, Miyamoto T, Sato T (1994) Differential distribution of two Ca2+-dependent and -independent K+ channels throughout receptive and basolateral membranes of bullfrog taste cells. Pflügers Arch 429:285–290

    Article  PubMed  CAS  Google Scholar 

  • Gilbertson TA, Boughter JD Jr (2003) Taste transduction: appetizing times in gustation. Neuroreport 14:905–911

    Article  PubMed  CAS  Google Scholar 

  • Go Y (2006) Lineage-specific expansions and contractions of the bitter taste receptor gene repertoire in vertebrates. Mol Biol Evol 23:964–972

    Article  PubMed  CAS  Google Scholar 

  • Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391:85–100

    Article  PubMed  CAS  Google Scholar 

  • Hofer AM, Brown EM (2003) Extracellular calcium sensing and signalling. Nat Rev Mol Cell Biol 4:530–538

    Article  PubMed  CAS  Google Scholar 

  • Hubbard PC, Ingleton PM, Bendell LA, Barata EN, Canario AV (2002) Olfactory sensitivity to changes in environmental [Ca2+] in the freshwater teleost Carassius auratus: an olfactory role for the Ca2+-senseing receptor? J Exp Biol 205:2755–2764

    PubMed  CAS  Google Scholar 

  • Junge D, Brodwick MS (1970) Stimulation of frog gustatory units by calcium. Comp Biochem Physiol 35:623–630

    Article  CAS  Google Scholar 

  • Kinnamon SC, Roper SD (1988a) Evidence for a role of voltage-sensitive apical K+ channels in sour and salt taste transduction. Chem Senses 13:115–121

    Article  CAS  Google Scholar 

  • Kinnamon SC, Roper SD (1988b) Membrane properties of isolated mudpuppy taste cells. J Gen Physiol 91:351–371

    Article  PubMed  CAS  Google Scholar 

  • Kinnamon SC, Dionne VE, Beam KG (1988) Apical localization of K+ channels in taste cells provides the basis four sour taste transduction. Proc Natl Acad Sci USA 85:7023–7027

    Article  PubMed  CAS  Google Scholar 

  • Kitada Y (1978) Inhibitory effects of cations on the Ca2+ response of water fibers in the frog tongue. Jpn J Physiol 28:413–422

    PubMed  CAS  Google Scholar 

  • Kitada Y (1984) Two different receptor sites for Ca2+ and Na+ in frog taste responses. Neurosci Lett 47:63–68

    Article  PubMed  CAS  Google Scholar 

  • Lindemann B (2001) Receptors and transduction in taste. Nature 413:219–225

    Article  PubMed  CAS  Google Scholar 

  • Naito T, Saito Y, Yamamoto J, Nozaki Y, Tomura K, Hazama M, Nakanishi S, Brenner S (1998) Putative pheromone receptors related to the Ca2+-sensing receptor in Fugu. Proc Natl Acad Sci USA 95:5178–5181

    Article  PubMed  CAS  Google Scholar 

  • Nemeth EF, Steffey ME, Hammerland LG, Hung BC, Van Wagenen BC, DelMar EG, Balandrin MF (1998) Calcimimetics with potent and selective activity on the parathyroid calcium receptor. Proc Natl Acad Sci USA 95:4040–4045

    Article  PubMed  CAS  Google Scholar 

  • Nemeth EF, Heaton WH, Miller M, Fox J, Balandrin MF, Van Wagenen BC, Colloton M, Karbon W, Scherrer J, Shatzen E, Rishton G, Scully S, Qi M, Harris R, Lacey D, Martin D (2004) Pharmacodynamics of the type II calcimimetic compound cinacalcet HCl. J Pharmacol Exptl Ther 308:627–635

    Article  CAS  Google Scholar 

  • Nomura H, Sakada S (1965) On the “water response” of frog’s tongue. Jpn J Physiol 15:433–445

    Google Scholar 

  • Okada Y, Miyamoto T, Sato T (1994) Activation of a cation conductance by acetic acid in taste cells isolated from the bullfrog. J Exp Biol 187:19–31

    PubMed  CAS  Google Scholar 

  • Okada Y, Fujiyama R, Miyamoto T, Sato T (1996) Vasopressin modulates membrane properties of taste cells isolated from bullfrogs. Chem Senses 21: 739–745

    Article  PubMed  CAS  Google Scholar 

  • Okada Y, Fujiyama R, Miyamoto T, Sato T (1998) Inositol 1,4,5-trisphophate activates non-selective cation conductance via intracellular Ca2+ increase in isolated frog taste cells. Eur J Neurosci 10:1376–1382

    Article  PubMed  CAS  Google Scholar 

  • Okada Y, Fujiyama R, Miyamoto T, Sato T (2001) Saccharin activates cation conductance via inositol 1,4,5-trisphosphate production in a subset of isolated rod taste cells in the frog. Eur J Neurosci 13:308–314

    Article  PubMed  CAS  Google Scholar 

  • Osculati F, Sbarbati A (1995) The frog taste disc: a prototype of the vertebrate gustatory organ. Prog Neurobiol 46:351–399

    Article  PubMed  CAS  Google Scholar 

  • Romanov RA, Rogachevskaja OA, Bystrova MF, Jiang P, Margolskee RF, Kolesnikov SS (2007) Afferent neurotransmission mediated by hemichannels in mammalian taste cells. EMBO J 26:657–667

    Article  PubMed  CAS  Google Scholar 

  • Quinn SJ, Kifor O, Trivedi S, Diaz R, Vassilev P, Brown E (1998) Sodium and ionic strength sensing by the calcium receptor. J Biol Chem 273:19579–19586

    Article  PubMed  CAS  Google Scholar 

  • Suwabe T, Kitada Y (2004) Voltage-gated inward currents of morphologically identified cells of the frog taste disc. Chem Senses 29:61–73

    Article  PubMed  CAS  Google Scholar 

  • Washburn DL, Smith PM, Ferguson AV (1999) Control of neuronal excitability by an ion-sensing receptor (correction of anion-sensing). Eur J Neurosci 11:1947–1954

    Article  PubMed  CAS  Google Scholar 

  • Yano S, Brown EM, and Chattopadhyay N (2004) Calcium-sensing recptor in the brain. Cell Calcium 35:257–264

    Article  PubMed  CAS  Google Scholar 

  • Ye C, Kanazirska M, Quinn S, Brown EM, Vassilev PM (1996) Modulation by polycationic Ca2+-sensing receptor agonists of nonselective cation channels in rat hippocampal neurons. Biochem Biophys Res Commun 224:271–280

    Article  PubMed  CAS  Google Scholar 

  • Zotterman Y (1949) The responses of the frog’s taste fibres to the application of pure water. Acta Physiol Scand 18:181–189

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Dr. Edward F. Nemeth of NPS Pharmaceuticals (Salt Lake City, UT, USA) for the generous gifts of NPS R-467 and S-467. This work was supported by Grants-in-Aid (17570064) from Japan Society for the Promotion of Science to Y.O.

Author information

Authors and Affiliations

  1. Integrative Sensory Physiology, Graduate School of Biomedical Sciences, Nagasaki University, 1-7-1 Sakamoto, Nagasaki, Nagasaki, 852-8588, Japan

    Yukio Okada, Rie Fujiyama, Jorge L. Zeredo & Kazuo Toda

  2. Department of Physiology, Faculty of Medicine, University of Ruhuna, Galle, Sri Lanka

    Kotapola G. Imendra

  3. Cell Biology, Graduate School of Biomedical Sciences, Nagasaki University, Nagasaki, Nagasaki, 852-8588, Japan

    Toshihiro Miyazaki

  4. Orthodontics and Biomedical Engineering, Graduate School of Biomedical Sciences, Nagasaki University, Nagasaki, Nagasaki, 852-8588, Japan

    Hitoshi Hotokezaka

Authors
  1. Yukio Okada
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kotapola G. Imendra
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Toshihiro Miyazaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hitoshi Hotokezaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rie Fujiyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jorge L. Zeredo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kazuo Toda
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yukio Okada.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Okada, Y., Imendra, K.G., Miyazaki, T. et al. A Calcium-Receptor Agonist Induces Gustatory Neural Responses in Bullfrogs. Cell Mol Neurobiol 27, 771–781 (2007). https://doi.org/10.1007/s10571-007-9171-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10571-007-9171-z

Keywords

Search

Navigation