• 2022 (Vol.36)
  • 1990 (Vol.4)
  • 1989 (Vol.3)
  • 1988 (Vol.2)
  • 1987 (Vol.1)

Mechanisms of transduction of olfactory signals: the possible role of the contractive apparatus of the olfactory ciliae

© 2017 V. M. Ganshin, E. P. Zinkevich

A.N. Severtzov Institute of Ecology and Evolution, RAS, 119071, Moscow Leninsky Prospekt, 33

Received 07 Jul 2016

A hypothesis is proposed whereby the activation of Cl-channels in the chain of olfactory transduction is activated indirectly with respect to the activation of the contractive apparatus of the olfactory cilia. At the rst stage, activation of the olfactory elements of the brils of the olfactory cilia with Са2+-ions provide smooth uctuations of the signals of the olfactory receptors, G-proteins, adenylatecyclase of type III and cation cATP-dependent channels. In this case, the Са2+ current signal is transformed integrally into mechanical stress of bril along the length of the olfactory cilium. At the second stage the integral change of bril contraction by mechanical effect on the sensory membrane caused activation of Cl-channels grouped in the membrane of the basal portion of the cilium directly in the zone of the development of the generator potential. The mechanism under discussion throws a new light on the role on the olfactory cilia in transduction of the olfactory signals and, as based on the integral function of their contractive apparatus, interpret rationally some fundamental and mutually contradictory properties of olfactory reception as rapidity of action, sensitivity and selectivity.

Key words: оolfactory receptor protein, G-protein, cATP-dependent cation channels, Са2+-controlled chlorine channels, potassium- sodium-chloride co-transport, olfactory cilia, olfactory sensitivity, selectivity, speed

Cite: Ganshin V. M., Zinkevich E. P. Mekhanizmy transduktsii obonyatelnykh signalov: vozmozhnaya rol sokratitelnogo apparata obonyatelnykh resnichek [Mechanisms of transduction of olfactory signals: the possible role of the contractive apparatus of the olfactory ciliae]. Sensornye sistemy [Sensory systems]. 2017. V. 31(1). P. 59-71 (in Russian).

References:

  • Bigday E.V. Biophysical mechanisms of olfactory reception // J. Evolutionary biochemistry and physiology. 2004 a. V.40. No 2. P. 112–117 [in Russian].
  • Bigday E.V. Geterogenity of olfactory reception // Diss... doctor biology. Sankt Petersburg. 2004 b. 264 p. [in Russian].
  • Bronshteine A.A. Vital observations on movement of the hairs of olfactory cilia // The reports of USSR Academy Sci.1962. V. 142. N 3. P. 715–718 [in Russian].
  • Bronstein A.A., Minor A.V. The importance of agella and motility for function of the olfactory receptors // The reports of USSR Academy Sci. 1973. V.213. No 4. P. 987– 989 [in Russian].
  • Ganshin B.M., Zinkevich E.P. Possible role of competition in the model of the olfactory receptor // Sensory Systems. 2012. V. 26. N 4. P. 331–341 [in Russian].
  • Gelfand V.I., Rosenblat V.A. Microtubes. Their structure, chemistry and functional role // Results of science and technology. A series of “Biological Chemistry”. M. VINITY. 1977. V.11. P. 78–143 [in Russian].
  • Zavarzin A.A., Rharazova A.D., Molitvin M.N. Cell biology: general cytology // SPb, Izd-vo SPbGU. 1992. 320 p. [in Russian].
  • Kalamkarov G.R., Ostrovsky M.A., Yunusov R.R., Shevchenko, T.F. Molecular mechanisms of the proteins interaction involved in photoreceptor signal transduction // Sensory systems. 2004. T. 18. No. 4. P. 275–280 [in Russian].
  • Minor A.V. Structural organization of the peripheral parts of the olfactory analyzer olfactory bulb // Physiology sensory systems. Part 2. 1972. P. 515– 549 [in Russian].
  • Minor A.V. Mechanism of the olfactory receptor potential generation // the Mechanisms of receptor elements of sensory organs. Leningrad: Nauka, 1973. P. 121–126 [in Russian].
  • Minor A.V., Kaissling K-E. “Dark” noise in the olfactory cells of the insect. Assessment of the frequency in the pheromone receptors spontaneous activation // Sensory systems. 2000. T. 20. No. 4. S. 325–327 [in Russian].
  • Ogneva I.V. Experimental analysis and modeling of the agella motor activity in the olfactory cells // Dis. kand. Fiz.-Mat. Sciences. SPb. 2005. 130 c. [in Russian].
  • Trushenkov V.G. Characteristics motility of the agella olfactory neuroreceptors in amphibians // Dis... Cand. Biol. Sciences. Vladivostok. 1995. 113 p. [in Russian].
  • Bhandawat V., Reisert J., Yau K-W. Elementary response of olfactory receptor neurons to odorants // Science. 2005. V. 308. P. 1931–1934.
  • Cleveland D.W., Sullivan K.F. Molecular biology and genetics of tubulin // Annu Rev. Biochem. 1985. V. 54. P. 331–365.
  • Derksen H.E. Axon membrane voltage uctuations. Acta Physiol. Pharmacol. Neerl. 1965. V.13. P. 373–466.
  • Dzeja C., Hagen V., Kaupp U.B., Frings S. Ca2+ permeation in cyclic nucleotide-gated channels // EMBO J. 1999. V.18. P. 131–144.
  • Flannery R.J., French D.A., Kleene S.J. Clustering of cyclic nucleotide-gated channels in olfactory cilia // Biophys J. 2006. V. 91. P. 179–188.
  • French D.A., Badamdorj D., Kleene S.J. Spatial Distribution of Calcium-Gated Chloride Channels in Olfactory Cilia // PLoS One. 2010. V. 5(12): e15676.
  • Haas M., Forbush B. The Na-K-Cl cotransporter of secretory epithelia // Annu. Rev. Physiol. 2000 V. 62. P. 515–534.
  • Kaneko H., Putzier I., Frings S., Kaupp U.B., Gensch T. Chloride accumulation in mammalian olfactory sensory neurons // J. Neurosci. 2004. V. 24 P. 7931–7938.
  • Kaupp U.B., Seifert R. Cyclic nucleotide-gated ion channels // Physiol. Rev. 2002. V. 82. P. 769–824.
  • Kleene S.J. Basal conductance of frog olfactory cilia // P ugers Arch. 1992. V. 421. P. 374–380.
  • Kleene S.J. Origin of the chloride current in olfactory transduction // Neuron. 1993. V.11. P. 123–132.
  • Kleene S.J. High-gain, low-noise ampli cation in olfactory transduction // Biophys. J. 1997. V.73. P. 1110–1117.
  • Kleene S.J. The electrochemical basis of odor transduction in vertebrate olfactory cilia // Chem. Senses. 2008. V.33. P. 839–859.
  • Kurahashi T., Yau K-W. Co-existence of cationic and chloride components in odorant-induced current of vertebrate olfactory receptor cells // Nature. 1993. V. 363. P. 71–74.
  • Leinders-Zufall T., Rand M.N., Shepherd G.M., Greer C.A., Zufall F. Calcium entry through cyclic nucleotide-gated channels in individual cilia of olfactory receptor cells: spatiotemporal dynamics // J. Neurosci. 1997. V.17. P. 4136–4148.
  • Leinders-Zufall T., Greer C.A., Shepherd G.M., Zufall F. I maging odorinduced calcium transients in single olfactory cilia: speci city of activation and role in transduction // J. Neurosci. 1998. V.18. P. 5630–5639.
  • Lowe G., Gold G.H. Nonlinear ampli cation by calciumdependent chloride channels in olfactory receptor cells // Nature. 1993. V. 366. P. 283–286.
  • Mammen A., Simpson J.P., Nighorn A., Imanishi Y., Palczewski K., Ronnett G.V., Moon C. Hippocalcin in the olfactory epithelium: a mediator of second messenger signaling // Biochem. Biophys. Res. Commun. 2004. V. 322. P. 1131–1139.
  • Matsuzaki O., Bakin R.E, Cai X., Menco B.P.M., Ronnett G.V. Localization of the olfactory cyclic nucleotide-gated channel subunit 1 in normal, embryonic and regenerating olfactory epithelium // Neuroscience. 1999. V. 94. P. 131–140.
  • Menco B. Ph.M. Qualitative and quantitative freeze-fracture studies of olfactory and nasal respiratory structures of frog, ox, rat, and dog. I. A general survey // Cell. Tissue. Res. 1980. V. 207. P. 183–209.
  • Menco B. Ph.M., Farbman A.I. Ultrastructural evidence for multiple mucous domains in frog olfactory epithelium // Cell. Tissue. Res. 1992. V.270. P. 47–56.
  • Menco B. Ph.M., Morrison E.E. Morphology of the mammalian olfactory epithelium: Form, ne structure, function, and pathology // Handbook of olfaction and gustation. 2nd edition. Ed. Doty R.L. New York: Marcel Dekker. 2003. P. 17–49.
  • Menini A. Calcium signalling and regulation in olfactory neurons // Curr. Opin. Neurobiol. 1999. V. 9. P. 419–426.
  • Mombaerts P. Molecular biology of odorant receptors in vertebrates // Annu. Rev. Physiol. 1999. V. 22. P. 487–509.
  • Pace U., Hanski E., Salomon Y., Lancet D. Odorant-sensitive adenylate cyclase may mediate olfactory reception // Nature. 1985. V. 316. P. 255–258.
  • Reisert J., Matthews H.R. Response properties of isolated mouse olfactory receptor cells // J. Physiol. 2001 a.V. 530. P. 113–122.
  • Reisert J., Matthews H.R. Responses to prolonged odour stimulation in frog olfactory receptor cells // J. Physiol. 2001 b. V. 534. P. 179–191.
  • Reisert J., Bauer P.J., Yau K-W., Frings S. The Ca-activated Cl channel and its control in rat olfactory receptor neurons // J. Gen. Physiol. 2003. V.122. P. 349–363.
  • Reisert J., Lai J., Yau K.W., Bradley J. Mechanism of the excitatory Cl– response in mouse olfactory receptor neurons // Neuron. 2005. V. 45. P. 553–561.
  • Reisert J., Restrepo D. Molecular tuning of odorant receptors and its implication for odor signal processing // Chem. Senses. 2009. V. 34. P. 535–545.
  • Reisert J. Origin of basal activity in mammalian olfactory receptor neurons // JGP. 2010. V. 136. No 5. P. 529– 540.
  • Reuter D., Zierold K., Schroder W.H., Frings S. A depolarizing chloride current contributes to chemoelectrical transduction in olfactory sensory neurons in situ // J. Neurosci. 1998. V.18. P. 6623–6630.
  • Ronnett G.V. Moon C. G-proteins and olfactory signal transduction // Annu. Rev. Physiol. 2002. V.64. P. 189–222.
  • Russell J.M. Sodium-potassium-chloride cotransport // Physiol. Rev. 2000. V. 80. P. 211–276.
  • Schild D., Restrepo D. Transduction mechanisms in vertebrate olfactory receptor cells // Physiol. Rev. 1998. V. 78. P. 429–466.
  • Takeuchi H., Kurahashi T. Distribution, amplification, and summation of cyclic nucleotide sensitivities within single olfactory sensory cilia // J. Neurosci. 2008. V. 28. P. 766–775.
  • Zhainazarov A.B., Ache B.W. Odor-induced currents in Xenopus olfactory receptor cells measured with perforated-patch recording // J. Neurophysiol. 1995. V. 74. P. 479–483.
  • Uebi T., Miwa N., Kawamura S. Comprehensive interaction of dicalcin with annexins in frog olfactory and respiratory cilia // FEBS J. 2007. V.274. P. 4863–4876.