Summary
Cyclic 3′,5′-nucleotide phosphodiesterase activity was demonstrated cytochemically in the rat olfactory mucosa using cyclic AMP as substrate. Strong activity was observed on the plasma membrane of the cilia, dendritic knob and axon of olfactory cells; weak activity was apparent on the membrane of the dendritic shaft and cell body. This suggests that the cyclic AMP produced by odorant-sensitive adenylate cyclase in the dendritic terminal acts mainly in its original site and to a lesser extent in the dendritic shaft and cell body. The enzyme also hydrolysed cyclic GMP but the hydrolysis was not as great as in the case of cyclic AMP. Besides its presence in olfactory cells, enzymatic activity was also observed on the plasma membrane of basal cells and certain supporting cells with an astrocyte-like morphology.
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References
Anholt, R. R. H., Farmer, R. W. & Karavanich, C. A. (1989) Excitation by odorants of olfactory receptor cells: molecular interactions at the ciliary membrane. In Chemical Senses (edited by Brand, J. G., Teeter, J. H., Cagan, R. H. & Kare, M. R.) Vol. 1. pp. 347–61. New York, Basel: Marcel Dekker.
Asanuma, N. & Nomura, H. (1990) Cyclic nucleotide phosphodiesterase activity in rat olfactory mucosa (cytochemical study). Chem. Senses 15, 389.
Asanuma, N. & Nomura, H. (1991) Cytochemical localization of adenylate cyclase activity in rat olfactory cells. Histochem. J. 23, 83–90.
Ashcroft, S. J. H., Randle, P. J. & Taljedal, I.-B. (1972) Cyclic nucleotide phosphodiesterase activity in normal mouse pancreatic islets. FEBS Lett. 20, 263–6.
Boekhoff, I., Tareilus, E., Strotmann, J. & Breer, H. (1990) Rapid activation of alternative second messenger pathways in olfactory cilia from rats by different odorants. EMBO J. 9, 2453–8.
Borgers, M. (1973) The cytochemical application of new potent inhibitors of alkaline phosphatases. J. Histochem. Cytochem. 21, 812–24.
Breer, H., Boekhoff, I. & Tareilus, E. (1990) Rapid kinetics of second messenger formation in olfactory transduction. Nature 345, 65–8.
Cheung, W. Y. (1967) Cyclic 3′,5′-nucleotide phosphodiesterase: pronounced stimulation by snake venom. Biochem. Biophys. Res. Commun. 29, 478–82.
Cheung, W. Y. (1969) Cyclic 3′,5′-nucleotide phosphodiesterase: preparation of a partially inactive enzyme and its subsequent stimulation by snake venom. Biochim. Biophys. Acta 191, 303–15.
Dhallan, R. S., Yau, K.-W., Schrader, K. A. & Reed, R. R. (1990) Primary structure and functional expression of a cyclic nucleotide-activated channel from olfactory neurons. Nature 347, 184–7.
Firestein, S., Darrow, B. & Shepherd, G. M. (1991a) Activation of the sensory current in salamander olfactory receptor neurons depends on a G protein-mediated cAMP second messenger system. Neuron 6, 825–35.
Firestein, S., Zufall, F. & Shepherd, G. M. (199lb) Single odorsensitive channels in olfactory receptor neurons are also gated by cyclic nucleotides. J. Neurosci. 11, 3565–72.
Florendo, N. T., Barrnett, R. J. & Greengard, P. (1971) Cyclic 3′,5′-nucleotide phosphodiesterase: cytochemical localization in cerebral cortex. Science 173, 745–7.
Frings, S. & Lindemann, B. (1991) Current recording from sensory cilia of olfactory receptor cells in situ. I. The neuronal response to cyclic nucleotides. J. Gen. Physiol. 97, 1–16.
Getchell, T. V. (1977) Analysis of intracellular recordings from salamander olfactory epithelium. Brain Res. 123, 275–86.
Gold, G. H., Lowe, G. & Nakamura, T. (1989) A role for cyclic AMP in olfactory transduction. In Chemical Senses (edited by Brand, J. G., Teeter, J. H., Cagan, R. H. & Kare, M. R.) Vol. 1. pp. 311–7. New York, Basel: Marcel Dekker.
Graziadei, P. P. C. (1971) The olfactory mucosa of vertebrates. In Handbook of Sensory Physiology (edited by Beidler, L. M.) Vol. 4, Pt 1. pp. 27–58. Berlin: Springer-Verlag.
Graziadei, P. P. C. (1973) Cell dynamics in the olfactory mucosa. Tissue Cell 5, 113–31.
Hidaka, H., Shibuya, M., Asano, T. & Hara, F. (1975) Cyclic nucleotide phosphodiesterase of human cerebrospinal fluid. J. Neurochem. 25, 49–53.
Kurahashi, T. (1990) The response induced by intracellular cyclic AMP in isolated olfactory receptor cells of the newt. J. Physiol. 430, 355–71.
Kurahashi, T. & Kaneko, A. (1991) High density cAMP-gated channels at the ciliary membrane in the olfactory receptor cell. NeuroReport 2, 5–8.
Lowe, G., Nakamura, T. & Gold, G. H. (1989) Adenylate cyclase mediates olfactory transduction for a wide variety of odorants. Proc. Natl Acad. Sci. USA 86, 5641–5.
Nakamura, T. & Gold, G. H. (1987) A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature 325, 442–4.
Nomura, H. (1978) Histochemical localization of adenylate cyclase and phosphodiesterase activities in the foliate papillae of the rabbit. I. Light microscopic observations. Chem. Senses Flavour 3, 319–24.
Pace, U. & Lancet, D. (1986) Olfactory GTP-binding protein: signal-transducing polypeptide of vertebrate chemosensory neurons. Proc. Natl Acad. Sci. USA 83, 4947–51.
Pace, U., Hanski, E., Salomon, Y. & Lancet, D. (1985) Odorantsensitive adenylate cyclase may mediate olfactory reception. Nature 316, 255–8.
Peytremann, A., Nicholson, W. E., Liddle, G. W., Hardman, J. G. & Sutherland, E. W. (1973) Effects of methylxanthines on adenosine 3′,5′-monophosphate and corticosterone in the rat adrenal. Endocrinology 92, 525–30.
Poeggel, G., Luppa, H., & Ludwig, A. (1987a) Histochemistry of cyclic nucleotide phosphodiesterase in nervous tissue. I. Enzymehistochemical investigations. Acta Histochem. Cytochem. 20, 375–80.
Poeggel, G., Luppa, H. & Ludwig, A. (1987b) Histochemistry of cyclic nucleotide phosphodiesterase in nervous tissue. II. Immunohistochemical investigations. Acta Histochem. Cytochem. 20, 381–6.
Poeggel, G., Luppa, H. & Schmidt, A. (1988) Histochemistry of cyclic nucleotide phosphodiesterase in nervous tissue. III. Enzyme cytochemical investigations. Acta Histochem. Cytochem. 21, 473–80.
Rafols, J. A. & Getchell, T. V. (1983) Morphological relations between the receptor neurons, sustentacular cells and Schwann cells in the olfactory mucosa of the salamander. Anat. Rec. 206, 87–101.
Ronnett, G. V., Parfitt, D. J., Hester, L. D. & Snyder, S. H. (1991) Odorant-sensitive adenylate cyclase: rapid, potent activation and desensitization in primary olfactory neuronal cultures. Proc. Natl Acad. Sci. USA 88, 2366–9.
Shanta, T. R., Woods, W. D., Waitzman, M. B. & Bourne, G. H. (1966) Histochemical method for localization of cyclic 3′,5′-nucleotide phosphodiesterase. Histochemie 7, 177–90.
Shirley, S. G., Robinson, C. J., Dickinson, K., Aujla, R. & Dodd, G. H. (1986) Olfactory adenylate cyclase of the rat: stimulation by odorants and inhibition by Ca2+. Biochem. J. 240, 605–7.
Sklar, P. B., Anholt, R. R. H. & Snyder, S. H. (1986) The odorant-sensitive adenylate cyclase of olfactory receptor cells: differential stimulation by distinct classes of odorants. J. Biol. Chem. 261, 15538–43.
Snyder, S. H., Sklar, P. B. & Pevsner, J. (1988) Molecular mechanisms of olfaction. J. Biol. Chem. 263, 13971–4.
Steinlen, S., Klumpp, S. & Schultz, J. E. (1990) Guanylate cyclase in olfactory cilia from rat and pig. Biochim. Biophys. Acta 1054, 69–72.
Suzuki, N. (1989) Voltage- and cyclic nucleotide-gated currents in isolated olfactory receptor cells. In Chemical Senses (edited by Brand, J. G., Teeter, J. H., Cagan, R. H. & Kare, M. R.) Vol. 1. p. 469–93. New York, Basel: Marcel Dekker.
Trotier, D. & Macleod, P. (1987) The amplification process in olfactory receptor cells. Ann. N.Y. Acad. Sci. 510, 677–9.
Vodyanoy, V. & Vodyanoy, I. (1987) ATP and GTP are essential for olfactory response. Neurosci. Lett. 73, 253–8.
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Asanuma, N., Nomura, H. Cytochemical localization of cyclic 3′,5′-nucleotide phosphodiesterase activity in the rat olfactory mucosa. Histochem J 25, 348–356 (1993). https://doi.org/10.1007/BF00159499
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DOI: https://doi.org/10.1007/BF00159499