Neuropeptide receptors provide a signalling pathway for trigeminal modulation of olfactory transduction

European Journal of Neuroscience

Volumn 37, Issue 4, 2013, Pages 572-582

  Daiber, Philipp ^a   Genovese, Federica ^a   Schriever, Valentin A ^b   Hummel, Thomas ^b   Möhrlen, Frank ^a   Frings, Stephan ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

Author keywords

Bimodal; CGRP; Irritants; Odorants

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CARBON DIOXIDE; DEODORANT AGENT; NEUROPEPTIDE RECEPTOR; PHENETHYL ALCOHOL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROGRAPHY; ELECTROOLFACTOGRAPHY; EVOKED RESPONSE; FEMALE; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; MALE; NEUROMODULATION; NOCICEPTIVE STIMULATION; NONHUMAN; NORMAL HUMAN; NUCLEOTIDE SEQUENCE; ODOR; OLFACTORY DISCRIMINATION; OLFACTORY NERVE; OLFACTORY RECEPTOR; PERCEPTION; PRIORITY JOURNAL; PSYCHOPHYSICS; RAT; SENSORY NERVE; SIGNAL TRANSDUCTION; TRIGEMINAL NERVE;

ADULT; ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; ELECTROOCULOGRAPHY; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IRRITANTS; MALE; ODORS; OLFACTORY MUCOSA; OLFACTORY PERCEPTION; OLFACTORY RECEPTOR NEURONS; RATS; RECEPTORS, ODORANT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRIGEMINAL NERVE; YOUNG ADULT;

EID: 84873987636     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12066     Document Type: Article

References (69)

1. Bakalyar, H.A. & Reed, R.R. (1990) Identification of a specialized adenylyl cyclase that may mediate odorant detection. Science, 250, 1403-1406.
2. Bensafi, M., Iannilli, E., Gerber, J. & Hummel, T. (2008) Neural coding of stimulus concentration in the human olfactory and intranasal trigeminal systems. Neuroscience, 154, 832-838.
3. 2+-activated Cl- currents are dispensable for olfaction. Nat. Neurosci., 14, 763-769.
4. - currents in isolated mouse olfactory sensory neurons. J. Neurophysiol., 98, 153-160.
5. Bouvet, J.F., Delaleu, J.C. & Holley, A. (1987) Olfactory receptor cell function is affected by trigeminal nerve activity. Neurosci. Lett., 77, 181-186.
6. Bouvet, J.F., Delaleu, J.C. & Holley, A. (1988) The activity of olfactory receptor cells is affected by acetylcholine and substance P. Neurosci. Res., 5, 214-223.
7. Brand, G. (2006) Olfactory/trigeminal interactions in nasal chemoreception. Neurosci. Biobehav. Rev., 30, 908-917.
8. Bungay, P.M., Sumbria, R.K. & Bickel, U. (2011) Unifying the mathematical modeling of in vivo and in vitro microdialysis. J. Pharm. Biomed. Anal., 55, 54-63.
9. Cain, W.S. (1977) Bilateral interaction in olfaction. Nature, 268, 50-52.
10. Cain, W.S. & Murphy, C.L. (1980) Interaction between chemoreceptive modalities of odour and irritation. Nature, 284, 255-257.
11. Coates, E.L. (2001) Olfactory CO(2) chemoreceptors. Respir. Physiol., 129, 219-229.
12. Cometto-Muniz, J.E. & Hernandez, S.M. (1990) Odorous and pungent attributes of mixed and unmixed odorants. Percept. Psychophys., 47, 391-399.
13. Croy, I., Negoias, S., Novakova, L., Landis, B.N. & Hummel, T. (2012) Learning about the functions of the olfactory system from people without a sense of smell. PLoS ONE, 7, e33365.
14. Dauner, K., Lissmann, J., Jeridi, S., Frings, S. & Mohrlen, F. (2012) Expression patterns of anoctamin 1 and anoctamin 2 chloride channels in the mammalian nose. Cell Tiss. Res., 347, 327-341.
15. Doty, R.L., Brugger, W.E., Jurs, P.C., Orndorff, M.A., Snyder, P.J. & Lowry, L.D. (1978) Intranasal trigeminal stimulation from odorous volatiles: psychometric responses from anosmic and normal humans. Physiol. Behav., 20, 175-185.
16. Evans, B.N., Rosenblatt, M.I., Mnayer, L.O., Oliver, K.R. & Dickerson, I.M. (2000) CGRP-RCP, a novel protein required for signal transduction at calcitonin gene-related peptide and adrenomedullin receptors. J. Biol. Chem., 275, 31438-31443.
17. Ferris, K.E., Clark, R.D. & Coates, E.L. (2007) Topical inhibition of nasal carbonic anhydrase affects the CO2 detection threshold in rats. Chem. Senses, 32, 263-271.
18. Finger, T.E. & Bottger, B. (1993) Peripheral peptidergic fibers of the trigeminal nerve in the olfactory bulb of the rat. J. Comp. Neurol., 334, 117-124.
19. Finger, T.E., St Jeor, V.L., Kinnamon, J.C. & Silver, W.L. (1990) Ultrastructure of substance P- and CGRP-immunoreactive nerve fibers in the nasal epithelium of rodents. J. Comp. Neurol., 294, 293-305.
20. Frasnelli, J., Schuster, B. & Hummel, T. (2007) Interactions between olfaction and the trigeminal system: what can be learned from olfactory loss. Cereb. Cortex, 17, 2268-2275.
21. Getchell, M.L., Bouvet, J.F., Finger, T.E., Holley, A. & Getchell, T.V. (1989) Peptidergic regulation of secretory activity in amphibian olfactory mucosa: immunohistochemistry, neural stimulation, and pharmacology. Cell Tiss. Res., 256, 381-389.
22. Hansen, A. & Finger, T.E. (2008) Is TrpM5 a reliable marker for chemosensory cells? Multiple types of microvillous cells in the main olfactory epithelium of mice. BMC Neurosci., 9, 115.
23. Hengl, T., Kaneko, H., Dauner, K., Vocke, K., Frings, S. & Mohrlen, F. (2010) Molecular components of signal amplification in olfactory sensory cilia. Proc. Natl. Acad. Sci. USA, 107, 6052-6057.
24. Hu, J., Zhong, C., Ding, C., Chi, Q., Walz, A., Mombaerts, P., Matsunami, H. & Luo, M. (2007) Detection of near-atmospheric concentrations of CO2 by an olfactory subsystem in the mouse. Science, 317, 953-957.
25. Hummel, T. & Livermore, A. (2002) Intranasal chemosensory function of the trigeminal nerve and aspects of its relation to olfaction. Int. Arch. Occup. Environ. Health, 75, 305-313.
26. Hummel, T., Sekinger, B., Wolf, S.R., Pauli, E. & Kobal, G. (1997) 'Sniffin' sticks': olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chem. Senses, 22, 39-52.
27. Hummel, T., Mohammadian, P., Marchl, R., Kobal, G. & Lotsch, J. (2003) Pain in the trigeminal system: irritation of the nasal mucosa using short- and long-lasting stimuli. Int. J. Psychophysiol., 47, 147-158.
28. Iannilli, E., Gerber, J., Frasnelli, J. & Hummel, T. (2007) Intranasal trigeminal function in subjects with and without an intact sense of smell. Brain Res., 1139, 235-244.
29. Iannilli, E., Bitter, T., Gudziol, H., Burmeister, H.P., Mentzel, H.J., Chopra, A.P. & Hummel, T. (2011) Differences in anosmic and normosmic group in bimodal odorant perception: a functional- MRI study. Rhinology, 49, 458-463.
30. Inokuchi, A., Kimmelman, C.P. & Snow, J.B. Jr. (1993) Convergence of olfactory and nasotrigeminal inputs and possible trigeminal contributions to olfactory responses in the rat thalamus. Eur. Arch. Otorhinolaryngol., 249, 473-477.
31. Jacquot, L., Monnin, J. & Brand, G. (2004) Influence of nasal trigeminal stimuli on olfactory sensitivity. C. R. Biol., 327, 305-311.
32. Jordt, S.E., Bautista, D.M., Chuang, H.H., McKemy, D.D., Zygmunt, P.M., Hogestatt, E.D., Meng, I.D. & Julius, D. (2004) Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature, 427, 260-265.
33. Kimoto, M., Iwai, S., Maeda, T., Yura, Y., Fernley, R.T. & Ogawa, Y. (2004) Carbonic anhydrase VI in the mouse nasal gland. J. Histochem. Cytochem., 52, 1057-1062.
34. Kleene, S.J. (2008) The electrochemical basis of odor transduction in vertebrate olfactory cilia. Chem. Senses, 33, 839-859.
35. Kobal, G. & Hummel, C. (1988) Cerebral chemosensory evoked potentials elicited by chemical stimulation of the human olfactory and respiratory nasal mucosa. Electroencephalogr. Clin. Neurophysiol., 71, 241-250.
36. Kratskin, I., Hummel, T., Hastings, L. & Doty, R. (2000) 3-Methylindole alters both olfactory and trigeminal nasal mucosal potentials in rats. NeuroReport, 11, 2195-2197.
37. Leopold, D.A., Hummel, T., Schwob, J.E., Hong, S.C., Knecht, M. & Kobal, G. (2000) Anterior distribution of human olfactory epithelium. Laryngoscope, 110, 417-421.
38. Liberles, S.D. & Buck, L.B. (2006) A second class of chemosensory receptors in the olfactory epithelium. Nature, 442, 645-650.
39. Lin, W., Ogura, T., Margolskee, R.F., Finger, T.E. & Restrepo, D. (2008) TRPM5-expressing solitary chemosensory cells respond to odorous irritants. J. Neurophysiol., 99, 1451-1460.
40. Livermore, A., Hummel, T. & Kobal, G. (1992) Chemosensory event-related potentials in the investigation of interactions between the olfactory and the somatosensory (trigeminal) systems. Electroencephalogr. Clin. Neurophysiol., 83, 201-210.
41. Luo, M. (2008) The necklace olfactory system in mammals. J. Neurogenet., 22, 229-238.
42. Ma, M. (2007) Encoding olfactory signals via multiple chemosensory systems. Crit. Rev. Biochem. Mol. Biol., 42, 463-480.
43. Ma, M. (2010) Multiple olfactory subsystems convey various sensory signals. In Menini, A. (Ed.), Neurobiology of Olfaction. CRC Press, Boca Raton, FL, pp. 225-240.
44. McLatchie, L.M., Fraser, N.J., Main, M.J., Wise, A., Brown, J., Thompson, N., Solari, R., Lee, M.G. & Foord, S.M. (1998) RAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor. Nature, 393, 333-339.
45. Munger, S.D., Leinders-Zufall, T. & Zufall, F. (2009) Subsystem organization of the mammalian sense of smell. Ann. Rev. Physiol., 71, 115-140.
46. Nickell, W.T., Kleene, N.K. & Kleene, S.J. (2007) Mechanisms of neuronal chloride accumulation in intact mouse olfactory epithelium. J. Physiol., 583, 1005-1020.
47. Pfeuffer, E., Mollner, S., Lancet, D. & Pfeuffer, T. (1989) Olfactory adenylyl cyclase. Identification and purification of a novel enzyme form. J. Biol. Chem., 264, 18803-18807.
48. Pifferi, S., Dibattista, M. & Menini, A. (2009) TMEM16B induces chloride currents activated by calcium in mammalian cells. Pflugers Arch., 458, 1023-1038.
49. Potter, S.M., Zheng, C., Koos, D.S., Feinstein, P., Fraser, S.E. & Mombaerts, P. (2001) Structure and emergence of specific olfactory glomeruli in the mouse. J. Neurosci., 21, 9713-9723.
50. Schaefer, M.L., Bottger, B., Silver, W.L. & Finger, T.E. (2002) Trigeminal collaterals in the nasal epithelium and olfactory bulb: a potential route for direct modulation of olfactory information by trigeminal stimuli. J. Comp. Neurol., 444, 221-226.
51. Schaeren-Wiemers, N. & Gerfin-Moser, A. (1993) A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry, 100, 431-440.
52. Shusterman, D. & Avila, P.C. (2003) Real-time monitoring of nasal mucosal pH during carbon dioxide stimulation: implications for stimulus dynamics. Chem. Senses, 28, 595-601.
53. Silver, W.L. (1992) Neural and pharmacological basis for nasal irritation. Ann. NY Acad. Sci., 641, 152-163.
54. Silver, W.L. & Moulton, D.G. (1982) Chemosensitivity of rat nasal trigeminal receptors. Physiol. Behav., 28, 927-931.
55. Silverman, J.D. & Kruger, L. (1989) Calcitonin-gene-related-peptide-immunoreactive innervation of the rat head with emphasis on specialized sensory structures. J. Comp. Neurol., 280, 303-330.
56. Spehr, M., Wetzel, C.H., Hatt, H. & Ache, B.W. (2002) 3-phosphoinositides modulate cyclic nucleotide signaling in olfactory receptor neurons. Neuron, 33, 731-739.
57. Stephan, A.B., Shum, E.Y., Hirsh, S., Cygnar, K.D., Reisert, J. & Zhao, H. (2009) ANO2 is the cilial calcium-activated chloride channel that may mediate olfactory amplification. Proc. Natl. Acad. Sci. USA, 106, 11776-11781.
58. Tarun, A.S., Bryant, B., Zhai, W., Solomon, C. & Shusterman, D. (2003) Gene expression for carbonic anhydrase isoenzymes in human nasal mucosa. Chem. Senses, 28, 621-629.
59. Ukhanov, K., Corey, E.A., Brunert, D., Klasen, K. & Ache, B.W. (2010) Inhibitory odorant signaling in Mammalian olfactory receptor neurons. J. Neurophysiol., 103, 1114-1122.
60. Vause, C., Bowen, E., Spierings, E. & Durham, P. (2007) Effect of carbon dioxide on calcitonin gene-related peptide secretion from trigeminal neurons. Headache, 47, 1385-1397.
61. Walker, C.S., Conner, A.C., Poyner, D.R. & Hay, D.L. (2010) Regulation of signal transduction by calcitonin gene-related peptide receptors. Trends Pharmacol. Sci., 31, 476-483.
62. Wang, Y.Y., Chang, R.B., Waters, H.N., McKemy, D.D. & Liman, E.R. (2008) The nociceptor ion channel TRPA1 is potentiated and inactivated by permeating calcium ions. J. Biol. Chem., 283, 32691-32703.
63. Wang, Y.Y., Chang, R.B. & Liman, E.R. (2010) TRPA1 is a component of the nociceptive response to CO2. J. Neurosci., 30, 12958-12963.
64. Wang, Y.Y., Chang, R.B., Allgood, S.D., Silver, W.L. & Liman, E.R. (2011) A TRPA1-dependent mechanism for the pungent sensation of weak acids. J. Gen. Physiol., 137, 493-505.
65. Wetzel, C.H., Oles, M., Wellerdieck, C., Kuczkowiak, M., Gisselmann, G. & Hatt, H. (1999) Specificity and sensitivity of a human olfactory receptor functionally expressed in human embryonic kidney 293 cells and Xenopus Laevis oocytes. J. Neurosci., 19, 7426-7433.
66. Wise, P.M., Wysocki, C.J. & Radil, T. (2003) Time-intensity ratings of nasal irritation from carbon dioxide. Chem. Senses, 28, 751-760.
67. Yan, C., Zhao, A.Z., Bentley, J.K., Loughney, K., Ferguson, K. & Beavo, J.A. (1995) Molecular cloning and characterization of a calmodulin-dependent phosphodiesterase enriched in olfactory sensory neurons. Proc. Natl. Acad. Sci. USA, 92, 9677-9681.
68. Youngentob, S.L., Hornung, D.E. & Mozell, M.M. (1991) Determination of carbon dioxide detection thresholds in trained rats. Physiol. Behav., 49, 21-26.
69. Zielinski, B.S., Getchell, M.L. & Getchell, T.V. (1989) Ultrastructural evidence for peptidergic innervation of the apical region of frog olfactory epithelium. Brain Res., 492, 361-365.