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Hypertonicity augments bullfrog taste nerve responses to inorganic salts

  • Sensory Physiology
  • Published:
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Abstract

The tonicity of taste stimulating solutions has been usually ignored, though taste substances themselves yielded the tonicity. We investigated the effect of hypertonicity on bullfrog taste nerve responses to inorganic salts by adding nonelectrolytes such as urea and sucrose that elicited no taste nerve responses. Here, we show that hypertonicity alters bullfrog taste nerve-response magnitude and firing pattern. The addition of urea or sucrose enhances the taste nerve-response magnitude to NaCl and shifts the concentration-response curve to the left. The effect of hypertonicity on responses to CaCl2 is bimodal; hypertonicity suppresses CaCl2 responses at concentrations less than ~30 mM and enhances them at concentrations greater than ~30 mM. The hypertonicity also enhances response magnitude to other monovalent salts. The extent of the enhancing effects depends on the difference between the mobility of the cation and anion in the salt. We quantitatively suggest that both the enhancing and suppressing effects result from the magnitude and direction of local circuit currents generated by diffusion potentials across tight junctions surrounding taste receptor cells.

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References

  1. Akisaka T, Oda M (1978) Taste buds in the vallate papillae of the rat studied with freeze-fracture preparation. Arch Histologicum Japonicum Nihon Soshikigaku Kiroku 41(1):87–98

    Article  CAS  Google Scholar 

  2. Amasheh S, Meiri N, Gitter AH, Schoneberg T, Mankertz J, Schulzke JD, Fromm M (2002) Claudin-2 expression induces cation-selective channels in tight junctions of epithelial cells. J Cell Sci 115(Pt 24):4969–4976

    Article  PubMed  CAS  Google Scholar 

  3. Caprio J (1975) High sensitivity of catfish taste receptors to amino acids. Comp Biochem Physiol 52(1):247–251

    Article  CAS  Google Scholar 

  4. Claude P, Goodenough DA (1973) Fracture faces of zonulae occludentes from “tight” and “leaky” epithelia. J Cell Biol 58(2):390–400

    Article  PubMed  CAS  Google Scholar 

  5. Colegio OR, Van Itallie C, Rahner C, Anderson JM (2003) Claudin extracellular domains determine paracellular charge selectivity and resistance but not tight junction fibril architecture. Am J Physiol Cell Physiol 284(6):C1346–C1354

    PubMed  CAS  Google Scholar 

  6. Colegio OR, Van Itallie CM, McCrea HJ, Rahner C, Anderson JM (2002) Claudins create charge-selective channels in the paracellular pathway between epithelial cells. Am J Physiol Cell Physiol 283(1):C142–C147

    PubMed  CAS  Google Scholar 

  7. Erlij D, Martinez-Palomo A (1972) Opening of tight junctions in frog skin by hypertonic urea solutions. J Membr Biol 9(3):229–240

    PubMed  CAS  Google Scholar 

  8. Finger TE, Danilova V, Barrows J, Bartel DL, Vigers AJ, Stone L, Hellekant G, Kinnamon SC (2005) ATP signaling is crucial for communication from taste buds to gustatory nerves. Science (New York, NY) 310(5753):1495–1499

    Article  CAS  Google Scholar 

  9. Furue H, Yoshii K (1997) In situ tight-seal recordings of taste substance-elicited action currents and voltage-gated Ba currents from single taste bud cells in the peeled epithelium of mouse tongue. Brain Res 776(1–2):133–139

    Article  PubMed  CAS  Google Scholar 

  10. Furuse M, Furuse K, Sasaki H, Tsukita S (2001) Conversion of zonulae occludentes from tight to leaky strand type by introducing claudin-2 into Madin–Darby canine kidney I cells. J Cell Biol 153(2):263–272

    Article  PubMed  CAS  Google Scholar 

  11. Holland VF, Zampighi GA, Simon SA (1989) Morphology of fungiform papillae in canine lingual epithelium: location of intercellular junctions in the epithelium. J Comp Neurol 279(1):13–27

    Article  PubMed  CAS  Google Scholar 

  12. Huang YA, Dando R, Roper SD (2009) Autocrine and paracrine roles for ATP and serotonin in mouse taste buds. J Neurosci 29(44):13909–13918

    Article  PubMed  CAS  Google Scholar 

  13. Jahnke K, Baur P (1979) Freeze-fracture study of taste bud pores in the foliate papillae of the rabbit. Cell Tissue Res 200(2):245–256

    Article  PubMed  CAS  Google Scholar 

  14. Kamo N, Kashiwagura T, Kobatake Y, Kurihara K (1978) Role of membrane-bound calcium in taste reception of the frog. J Physiol 282:115–129

    PubMed  CAS  Google Scholar 

  15. Kumazawa T, Kurihara K (1990) Large enhancement of canine taste responses to sugars by salts. J Gen Physiol 95(5):1007–1018

    Article  PubMed  CAS  Google Scholar 

  16. Michlig S, Damak S, Le Coutre J (2007) Claudin-based permeability barriers in taste buds. J Comp Neurol 502(6):1003–1011

    Article  PubMed  CAS  Google Scholar 

  17. Miyake M, Kamo N, Kurihara K, Kobatake Y (1976) Physicochemical studies of taste reception. III. Interpretation of the water response in taste reception. Biochim Biophys Acta 436(4):843–855

    Article  PubMed  CAS  Google Scholar 

  18. Miyake M, Kamo N, Kurihara K, Kobatake Y (1976) Pysicochemical studies of taste reception. V. Suppressive effect of salts on sugar response of the frog. Biochim Biophys Acta 436(4):856–862

    Article  PubMed  CAS  Google Scholar 

  19. Ogawa H, Sato M, Yamashita S (1968) Multiple sensitivity of chordat typani fibres of the rat and hamster to gustatory and thermal stimuli. J Physiol 199(1):223–240

    PubMed  CAS  Google Scholar 

  20. 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(3):657–667

    Article  PubMed  CAS  Google Scholar 

  21. Simon SA (1992) Influence of tight junctions on the interaction of salts with lingual epithelia: responses of chorda tympani and lingual nerves. Mol Cell Biochem 114(1–2):43–48

    PubMed  CAS  Google Scholar 

  22. Sugawara M, Kashiwayanagi M, Kurihara K (1989) Mechanism of the water response in frog gustation: possible significance of surface potential. Brain Res 486(2):269–273

    Article  PubMed  CAS  Google Scholar 

  23. Ussing HH (1965) Relationship between osmotic reactions and active sodium transport in the frog skin epithelium. Acta Physiol Scand 63:141–155

    Article  PubMed  CAS  Google Scholar 

  24. Ussing HH (1966) Anomalous transport of electrolytes and sucrose through the isolated frog skin induced by hypertonicity of the outside bathing solution. Ann N Y Acad Sci 137(2):543–555

    Article  PubMed  CAS  Google Scholar 

  25. Ye Q, Heck GL, DeSimone JA (1991) The anion paradox in sodium taste reception: resolution by voltage-clamp studies. Science (New York, NY) 254(5032):724–726

    Article  CAS  Google Scholar 

  26. Ye Q, Heck GL, DeSimone JA (1993) Voltage dependence of the rat chorda tympani response to Na+ salts: implications for the functional organization of taste receptor cells. J Neurophysiol 70(1):167–178

    PubMed  CAS  Google Scholar 

  27. Yoshii K, Kamo N, Kurihara K, Kobatake Y (1979) Gustatory responses of eel palatine receptors to amino acids and carboxylic acids. J Gen Physiol 74(3):301–317

    Article  PubMed  CAS  Google Scholar 

  28. Yoshii K, Kobatake Y, Kurihara K (1981) Selective enhancement and suppression of frog gustatory responses to amino acids. J Gen Physiol 77(4):373–385

    Article  PubMed  CAS  Google Scholar 

  29. Yoshii K, Yokouchi C, Kurihara K (1986) Synergistic effects of 5′-nucleotides on rat taste responses to various amino acids. Brain Res 367(1–2):45–51

    Article  PubMed  CAS  Google Scholar 

  30. Yu AS, Enck AH, Lencer WI, Schneeberger EE (2003) Claudin-8 expression in Madin–Darby canine kidney cells augments the paracellular barrier to cation permeation. J Biol Chem 278(19):17350–17359

    Article  PubMed  CAS  Google Scholar 

  31. Zotterman Y (1949) The response of the frog’s taste fibres to the application of pure water. Acta Physiol Scand 18(2–3):181–189

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Graduate School of Life Science and Systems Engineering, Kyushu Institute of Technology, Kitakyushu, 808-0196, Japan

    Namie Beppu, Yoko Higure, Kazunori Mashiyama, Yoshitaka Ohtubo & Kiyonori Yoshii

  2. Graduate school of Engineering, Saitama Institute of Technology, Fukaya, 369-0293, Japan

    Takashi Kumazawa

Authors
  1. Namie Beppu
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  2. Yoko Higure
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  3. Kazunori Mashiyama
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  4. Yoshitaka Ohtubo
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  5. Takashi Kumazawa
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  6. Kiyonori Yoshii
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Correspondence to Kiyonori Yoshii.

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Beppu, N., Higure, Y., Mashiyama, K. et al. Hypertonicity augments bullfrog taste nerve responses to inorganic salts. Pflugers Arch - Eur J Physiol 463, 845–851 (2012). https://doi.org/10.1007/s00424-012-1097-8

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  • DOI: https://doi.org/10.1007/s00424-012-1097-8

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