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Olfactory Transduction Channels and Their Modulation by Varieties of Volatile Substances

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Book cover Taste and Smell

Part of the book series: Topics in Medicinal Chemistry ((TMC,volume 23))

Abstract

Olfaction starts at the sensory cilia of the olfactory receptor cell. One of the unusual features of this signal transduction is that the underlying ion channels are directly exposed to the external environment, so that the channel and olfactory senses can be modified by externally applied chemicals even by the airborne stimuli. In the human history, such properties have long been used as an olfactory masking that erases unpleasant smells present in the environment. It has been shown that a part of masking is responsible for direct suppression by odorants of olfactory signal transduction channels. It has also been shown that similar suppression by off-flavors included in foods and beverages brings negative effects on pleasant scents and flavors by suppressing original odor of products. In this chapter, we focus on the olfactory signal conversion system and its modulation by diverse types of volatile substances.

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References

  1. Menco BP, Morrison EE (2003) Morphology of the mammalian olfactory epithelium: form, fine structure, function, and pathology. In: Doty RL (ed) Handbook of olfaction and gustation. Marcel Dekker, New York, pp 17–49

    Google Scholar 

  2. Pevsner J, Sklar PB, Snyder SH (1986) Odorant-binding protein: localization to nasal glands and secretions. Proc Natl Acad Sci U S A 83(13):4942–4946

    Article  CAS  Google Scholar 

  3. Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65(1):175–187

    Article  CAS  Google Scholar 

  4. Firestein S (2001) How the olfactory system makes sense of scents. Nature 413(6852):211–218

    Article  CAS  Google Scholar 

  5. Firestein S, Shepherd GM (1995) Interaction of anionic and cationic currents leads to a voltage dependence in the odor response of olfactory receptor neurons. J Neurophysiol 73(2):562–567

    CAS  Google Scholar 

  6. Frings S, Lynch JW, Lindemann B (1992) Properties of cyclic nucleotide-gated channels mediating olfactory transduction. Activation, selectivity, and blockage. J Gen Physiol 100(1):45–67

    Article  CAS  Google Scholar 

  7. Frings S, Reuter D, Kleene SJ (2000) Neuronal Ca2+ -activated Cl channels – homing in on an elusive channel species. Prog Neurobiol 60(3):247–289

    Article  CAS  Google Scholar 

  8. Gold GH (1999) Controversial issues in vertebrate olfactory transduction. Annu Rev Physiol 61:857–871

    Article  CAS  Google Scholar 

  9. Gold GH, Nakamura T, Lowe G (1990) Studies on the mechanism of olfactory transduction in vertebrates. Neurosci Res Suppl 12:S127–134

    Article  CAS  Google Scholar 

  10. Kaupp UB, Seifert R (2002) Cyclic nucleotide-gated ion channels. Physiol Rev 82(3):769–824

    Article  CAS  Google Scholar 

  11. Kleene SJ (1999) Both external and internal calcium reduce the sensitivity of the olfactory cyclic-nucleotide-gated channel to CAMP. J Neurophysiol 81(6):2675–2682

    CAS  Google Scholar 

  12. Pifferi S, Menini A, Kurahashi T (2010) Chapter 8. Signal transduction in vertebrate olfactory cilia. In: Menini A (ed) The neurobiology of olfaction. CRC Press/Taylor & Francis, Boca Raton, pp 203–224

    Google Scholar 

  13. Reisert J, Matthews HR (2001) Response properties of isolated mouse olfactory receptor cells. J Physiol 530(Pt 1):113–122

    Article  CAS  Google Scholar 

  14. Schild D, Restrepo D (1998) Transduction mechanisms in vertebrate olfactory receptor cells. Physiol Rev 78(2):429–466

    CAS  Google Scholar 

  15. Takeuchi H, Kurahashi T (2003) Identification of second messenger mediating signal transduction in the olfactory receptor cell. J Gen Physiol 122(5):557–567

    Article  CAS  Google Scholar 

  16. Pifferi S, Dibattista M, Sagheddu C, Boccaccio A, Al Qteishat A, Ghirardi F, Tirindelli R, Menini A (2009) Calcium-activated chloride currents in olfactory sensory neurons from mice lacking bestrophin-2. J Physiol 587(Pt 17):4265–4279

    Article  CAS  Google Scholar 

  17. Pifferi S, Pascarella G, Boccaccio A, Mazzatenta A, Gustincich S, Menini A, Zucchelli S (2006) Bestrophin-2 is a candidate calcium-activated chloride channel involved in olfactory transduction. Proc Natl Acad Sci U S A 103(34):12929–12934

    Article  CAS  Google Scholar 

  18. Stephan AB, Shum EY, Hirsh S, Cygnar KD, Reisert J, Zhao H (2009) ANO2 is the cilial calcium-activated chloride channel that may mediate olfactory amplification. Proc Natl Acad Sci U S A 106(28):11776–11781

    Article  CAS  Google Scholar 

  19. Kurahashi T (1989) Activation by odorants of cation-selective conductance in the olfactory receptor cell isolated from the newt. J Physiol 419:177–192

    Article  CAS  Google Scholar 

  20. Kurahashi T, Lowe G, Gold GH (1994) Suppression of odorant responses by odorants in olfactory receptor cells. Science 265(5168):118–120

    Article  CAS  Google Scholar 

  21. Kurahashi T, Menini A (1997) Mechanism of odorant adaptation in the olfactory receptor cell. Nature 385(6618):725–729

    Article  CAS  Google Scholar 

  22. Kurahashi T, Yau KW (1993) Co-existence of cationic and chloride components in odorant-induced current of vertebrate olfactory receptor cells. Nature 363(6424):71–74

    Article  CAS  Google Scholar 

  23. Lowe G, Gold GH (1991) The spatial distributions of odorant sensitivity and odorant-induced currents in salamander olfactory receptor cells. J Physiol 442:147–168

    Article  CAS  Google Scholar 

  24. Ache BW, Zhainazarov A (1995) Dual second-messenger pathways in olfactory transduction. Curr Opin Neurobiol 5(4):461–466

    Article  CAS  Google Scholar 

  25. Fadool DA, Ache BW (1992) Plasma membrane inositol 1,4,5-trisphosphate-activated channels mediate signal transduction in lobster olfactory receptor neurons. Neuron 9(5):907–918

    Article  CAS  Google Scholar 

  26. Restrepo D, Miyamoto T, Bryant BP, Teeter JH (1990) Odor stimuli trigger influx of calcium into olfactory neurons of the channel catfish. Science 249(4973):1166–1168

    Article  CAS  Google Scholar 

  27. Schild D, Lischka FW, Restrepo D (1995) InsP3 causes an increase in apical [Ca2+]i by activating two distinct current components in vertebrate olfactory receptor cells. J Neurophysiol 73(2):862–866

    CAS  Google Scholar 

  28. Suzuki N (1994) IP3-activated ion channel activities in olfactory receptor neurons from different vertebrate species. In: Olfaction and taste XI. Springer, Berlin, pp 173–177

    Chapter  Google Scholar 

  29. Kashiwayanagi M, Shimano K, Kurihara K (1996) Existence of multiple receptors in single neurons: responses of single bullfrog olfactory neurons to many cAMP-dependent and independent odorants. Brain Res 738(2):222–228

    Article  CAS  Google Scholar 

  30. Kaur R, Zhu XO, Moorhouse AJ, Barry PH (2001) IP3-gated channels and their occurrence relative to CNG channels in the soma and dendritic knob of rat olfactory receptor neurons. J Membr Biol 181(2):91–105

    Article  CAS  Google Scholar 

  31. Vogl A, Noe J, Breer H, Boekhoff I (2000) Cross-talk between olfactory second messenger pathways. Eur J Biochem 267(14):4529–4535

    Article  CAS  Google Scholar 

  32. Chen S, Lane AP, Bock R, Leinders-Zufall T, Zufall F (2000) Blocking adenylyl cyclase inhibits olfactory generator currents induced by “IP(3)-odors”. J Neurophysiol 84(1):575–580

    CAS  Google Scholar 

  33. Takeuchi H, Ishida H, Hikichi S, Kurahashi T (2009) Mechanism of olfactory masking in the sensory cilia. J Gen Physiol 133(6):583–601

    Article  CAS  Google Scholar 

  34. Takeuchi H, Kurahashi T (2005) Mechanism of signal amplification in the olfactory sensory cilia. J Neurosci 25(48):11084–11091

    Article  CAS  Google Scholar 

  35. Flannery RJ, French DA, Kleene SJ (2006) Clustering of cyclic-nucleotide-gated channels in olfactory cilia. Biophys J 91(1):179–188

    Article  CAS  Google Scholar 

  36. Nakamura T, Gold GH (1987) A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature 325(6103):442–444

    Article  CAS  Google Scholar 

  37. Kurahashi T (1990) The response induced by intracellular cyclic AMP in isolated olfactory receptor cells of the newt. J Physiol 430:355–371

    Article  CAS  Google Scholar 

  38. Kurahashi T, Kaneko A (1991) High density cAMP-gated channels at the ciliary membrane in the olfactory receptor cell. Neuroreport 2(1):5–8

    Article  CAS  Google Scholar 

  39. Kurahashi T, Kaneko A (1993) Gating properties of the cAMP-gated channel in toad olfactory receptor cells. J Physiol 466:287–302

    CAS  Google Scholar 

  40. Lancet D (1986) Vertebrate olfactory reception. Annu Rev Neurosci 9:329–355

    Article  CAS  Google Scholar 

  41. Kurahashi T, Shibuya T (1990) Ca2(+)-dependent adaptive properties in the solitary olfactory receptor cell of the newt. Brain Res 515(1-2):261–268

    Article  CAS  Google Scholar 

  42. Zufall F, Firestein S (1993) Divalent cations block the cyclic nucleotide-gated channel of olfactory receptor neurons. J Neurophysiol 69(5):1758–1768

    CAS  Google Scholar 

  43. Kleene SJ (1997) High-gain, low-noise amplification in olfactory transduction. Biophys J 73(2):1110–1117

    Article  CAS  Google Scholar 

  44. Larsson HP, Kleene SJ, Lecar H (1997) Noise analysis of ion channels in non-space-clamped cables: estimates of channel parameters in olfactory cilia. Biophys J 72(3):1193–1203

    Article  CAS  Google Scholar 

  45. Reisert J, Bauer PJ, Yau KW, Frings S (2003) The Ca-activated Cl channel and its control in rat olfactory receptor neurons. J Gen Physiol 122(3):349–363

    Article  CAS  Google Scholar 

  46. Lowe G, Gold GH (1993) Nonlinear amplification by calcium-dependent chloride channels in olfactory receptor cells. Nature 366(6452):283–286

    Article  CAS  Google Scholar 

  47. Matsuzaki O, Bakin RE, Cai X, Menco BP, Ronnett GV (1999) Localization of the olfactory cyclic nucleotide-gated channel subunit 1 in normal, embryonic and regenerating olfactory epithelium. Neuroscience 94(1):131–140

    Article  CAS  Google Scholar 

  48. 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. Pflugers Arch 391(2):85–100

    Article  CAS  Google Scholar 

  49. Takeuchi H, Kurahashi T (2008) Distribution, amplification, and summation of cyclic nucleotide sensitivities within single olfactory sensory cilia. J Neurosci 28(3):766–775

    Article  CAS  Google Scholar 

  50. Kleene SJ, Gesteland RC (1991) Calcium-activated chloride conductance in frog olfactory cilia. J Neurosci 11(11):3624–3629

    CAS  Google Scholar 

  51. Takeuchi H, Kurahashi T (2002) Photolysis of caged cyclic AMP in the ciliary cytoplasm of the newt olfactory receptor cell. J Physiol 541(Pt 3):825–833

    Article  CAS  Google Scholar 

  52. Ben-Chaim Y, Cheng MM, Yau KW (2011) Unitary response of mouse olfactory receptor neurons. Proc Natl Acad Sci U S A 108(2):822–827

    Article  CAS  Google Scholar 

  53. Bhandawat V, Reisert J, Yau KW (2005) Elementary response of olfactory receptor neurons to odorants. Science 308(5730):1931–1934

    Article  CAS  Google Scholar 

  54. Lamb TD, Pugh EN Jr (1992) A quantitative account of the activation steps involved in phototransduction in amphibian photoreceptors. J Physiol 449:719–758

    Article  CAS  Google Scholar 

  55. Pugh EN Jr, Lamb TD (1990) Cyclic GMP and calcium: the internal messengers of excitation and adaptation in vertebrate photoreceptors. Vision Res 30(12):1923–1948

    Article  CAS  Google Scholar 

  56. Pugh EN Jr, Nikonov S, Lamb TD (1999) Molecular mechanisms of vertebrate photoreceptor light adaptation. Curr Opin Neurobiol 9(4):410–418

    Article  CAS  Google Scholar 

  57. Getchell TV, Shepherd GM (1978) Adaptive properties of olfactory receptors analysed with odour pulses of varying durations. J Physiol 282:541–560

    Article  CAS  Google Scholar 

  58. Bradley J, Bonigk W, Yau KW, Frings S (2004) Calmodulin permanently associates with rat olfactory CNG channels under native conditions. Nat Neurosci 7(7):705–710

    Article  CAS  Google Scholar 

  59. Chen TY, Yau KW (1994) Direct modulation by Ca(2+)-calmodulin of cyclic nucleotide-activated channel of rat olfactory receptor neurons. Nature 368(6471):545–548

    Article  CAS  Google Scholar 

  60. Munger SD, Lane AP, Zhong H, Leinders-Zufall T, Yau KW, Zufall F, Reed RR (2001) Central role of the CNGA4 channel subunit in Ca2 + -calmodulin-dependent odor adaptation. Science 294(5549):2172–2175

    Article  CAS  Google Scholar 

  61. Song Y, Cygnar KD, Sagdullaev B, Valley M, Hirsh S, Stephan A, Reisert J, Zhao H (2008) Olfactory CNG channel desensitization by Ca2+/CaM via the B1b subunit affects response termination but not sensitivity to recurring stimulation. Neuron 58(3):374–386

    Article  CAS  Google Scholar 

  62. Ukhanov K, Corey EA, Brunert D, Klasen K, Ache BW (2010) Inhibitory odorant signaling in Mammalian olfactory receptor neurons. J Neurophysiol 103(2):1114–1122

    Article  CAS  Google Scholar 

  63. Yamada H, Nakatani K (2001) Odorant-induced hyperpolarization and suppression of cAMP-activated current in newt olfactory receptor neurons. Chem Senses 26(1):25–34

    Article  CAS  Google Scholar 

  64. Chen TY, Takeuchi H, Kurahashi T (2006) Odorant inhibition of the olfactory cyclic nucleotide-gated channel with a native molecular assembly. J Gen Physiol 128(3):365–371

    Article  CAS  Google Scholar 

  65. Takeuchi H, Kato H, Kurahashi T (2013) 2,4,6-trichloroanisole is a potent suppressor of olfactory signal transduction. Proc Natl Acad Sci U S A 110(40):16235–16240

    Article  CAS  Google Scholar 

  66. Breunig E, Kludt E, Czesnik D, Schild D (2011) The styryl dye FM1-43 suppresses odorant responses in a subset of olfactory neurons by blocking cyclic nucleotide-gated (CNG) channels. J Biol Chem 286(32):28041–28048

    Article  CAS  Google Scholar 

  67. Qu W, Moorhouse AJ, Lewis TM, Pierce KD, Barry PH (2005) Mutation of the pore glutamate affects both cytoplasmic and external dequalinium block in the rat olfactory CNGA2 channel. Eur Biophys J 34(5):442–453

    Article  CAS  Google Scholar 

  68. Rosenbaum T, Gordon-Shaag A, Islas LD, Cooper J, Munari M, Gordon SE (2004) State-dependent block of CNG channels by dequalinium. J Gen Physiol 123(3):295–304

    Article  CAS  Google Scholar 

  69. Fodor AA, Gordon SE, Zagotta WN (1997) Mechanism of tetracaine block of cyclic nucleotide-gated channels. J Gen Physiol 109(1):3–14

    Article  CAS  Google Scholar 

  70. Brown RL, Haley TL, West KA, Crabb JW (1999) Pseudechetoxin: a peptide blocker of cyclic nucleotide-gated ion channels. Proc Natl Acad Sci U S A 96(2):754–759

    Article  CAS  Google Scholar 

  71. Brown RL, Lynch LL, Haley TL, Arsanjani R (2003) Pseudechetoxin binds to the pore turret of cyclic nucleotide-gated ion channels. J Gen Physiol 122(6):749–760

    Article  CAS  Google Scholar 

  72. Brown RL, Strassmaier T, Brady JD, Karpen JW (2006) The pharmacology of cyclic nucleotide-gated channels: emerging from the darkness. Curr Pharm Des 12(28):3597–3613

    Article  CAS  Google Scholar 

  73. Buser HR, Zanier C, Tanner H (1982) Identification of 2,4,6-trichloroanisole as a potent compound causing cork taint in wine. J Agric Food Chem 30(2):359–362

    Article  CAS  Google Scholar 

  74. Lundbaek JA (2008) Lipid bilayer-mediated regulation of ion channel function by amphiphilic drugs. J Gen Physiol 131(5):421–429

    Article  CAS  Google Scholar 

  75. Kawai F, Kurahashi T, Kaneko A (1997) Nonselective suppression of voltage-gated currents by odorants in the newt olfactory receptor cells. J Gen Physiol 109(2):265–272

    Article  CAS  Google Scholar 

  76. Kishino Y, Kato H, Kurahashi T, Takeuchi H (2011) Chemical structures of odorants that suppress ion channels in the olfactory receptor cell. J Physiol Sci 61(3):231–245

    Article  CAS  Google Scholar 

  77. Sanhueza M, Bacigalupo J (1999) Odor suppression of voltage-gated currents contributes to the odor-induced response in olfactory neurons. Am J Physiol 277(6 Pt 1):C1086–C1099

    CAS  Google Scholar 

  78. Stotz SC, Vriens J, Martyn D, Clardy J, Clapham DE (2008) Citral sensing by Transient [corrected] receptor potential channels in dorsal root ganglion neurons. PLoS One 3(5), e2082

    Article  Google Scholar 

  79. Pevsner J, Hou V, Snowman AM, Snyder SH (1990) Odorant-binding protein. Characterization of ligand binding. J Biol Chem 265(11):6118–6125

    CAS  Google Scholar 

  80. Weiss T, Snitz K, Yablonka A, Khan RM, Gafsou D, Schneidman E, Sobel N (2012) Perceptual convergence of multi-component mixtures in olfaction implies an olfactory white. Proc Natl Acad Sci U S A 109(49):19959–19964

    Article  CAS  Google Scholar 

  81. Curtis RF, Land DG, Griffiths NM, Gee M, Robinson D, Peel JL, Dennis C, Gee JM (1972) 2,3,4,6-Tetrachloroanisole association with musty taint in chickens and microbiological formation. Nature 235(5335):223–224

    Article  CAS  Google Scholar 

  82. Engel C, de Groot AP, Weurman C (1966) Tetrachloroanisole: a source of musty taste in eggs and broilers. Science 154(3746):270–271

    Article  CAS  Google Scholar 

  83. Miki A, Isogai A, Utsunomiya H, Iwata H (2005) Identification of 2,4,6-trichloroanisole (TCA) causing a musty/muddy off-flavor in sake and its production in rice koji and moromi mash. J Biosci Bioeng 100(2):178–183

    Article  CAS  Google Scholar 

  84. Qi F, Xu B, Chen Z, Ma J, Sun D, Zhang L, Wu F (2009) Ozonation catalyzed by the raw bauxite for the degradation of 2,4,6-trichloroanisole in drinking water. J Hazard Mater 168(1):246–252

    Article  CAS  Google Scholar 

  85. Spadone JC, Takeoka G, Liardon R (1990) Analytical investigation of Rio off-flavor in green coffee. J Agric Food Chem 38(1):226–233

    Article  CAS  Google Scholar 

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Takeuchi, H., Kurahashi, T. (2016). Olfactory Transduction Channels and Their Modulation by Varieties of Volatile Substances. In: Krautwurst, D. (eds) Taste and Smell. Topics in Medicinal Chemistry, vol 23. Springer, Cham. https://doi.org/10.1007/7355_2015_100

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