Microvillous cells expressing IP3 receptor type 3 in the olfactory epithelium of mice

European Journal of Neuroscience

Volumn 32, Issue 10, 2010, Pages 1632-1645

  Hegg, Colleen C ^a   Jia, Cuihong ^a   Chick, Wallace S ^b   Restrepo, Diego ^b   Hansen, Anne ^b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Calcium imaging; Immunohistochemistry; Rodents

Indexed keywords

CALCIUM; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; INOSITOL TRISPHOSPHATE; INOSITOL TRISPHOSPHATE RECEPTOR TYPE 3; PURINERGIC P2X3 RECEPTOR; SUBSTANCE P; TAU PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MICROVILLUS; MOUSE; NONHUMAN; OLFACTORY BULBECTOMY; OLFACTORY EPITHELIUM; OLFACTORY NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BIOLOGICAL MARKERS; CALCIUM; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OLFACTORY MUCOSA; RECOMBINANT FUSION PROTEINS; TAU PROTEINS;

EID: 78349283008     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07449.x     Document Type: Article

References (49)

1. Andres, K.H. (1969) Der olfaktorische Saum der Katze. Z. Zellforsch., 96, 250-274.
2. Asan, E. & Drenckhahn, D. (2005) Immunocytochemical characterization of two types of microvillar cells in rodent olfactory epithelium. Histochem. Cell Biol., 123, 157-168.
3. Berridge, M.J. (2009) Inositol trisphosphate and calcium signaling mechanisms. Biochim. Biophys. Acta, 1793, 933-940.
4. Bojsen-Moller, F. (1975) Demonstration of terminalis, olfactory, trigeminal and perivascular nerves in the rat nasal septum. J. Comp. Neurol., 159, 245-256.
5. Braun, N. & Zimmermann, H. (1998) Association of ecto-5'-nucleotidase with specific cell types in the adult and developing rat olfactory organ. J. Comp. Neurol., 393, 528-537.
6. Carr, V.M., Farbman, A.I., Colletti, L.M. & Morgan, J.I. (1991) Identification of a new non-neuronal cell type in rat olfactory epithelium. Neuroscience, 45, 433-449.
7. Chick, W.S., Mentzer, S.E., Carpenter, D.A., Rinchik, E.M., Johnson, D. & You, Y. (2005) X-ray-induced deletion complexes in embryonic stem cells on mouse chromosome 15. Mamm. Genome, 16, 661-671.
8. Cunningham, A.M., Ryugo, D.K., Sharp, A.H., Reed, R.R., Snyder, S.H. & Ronnett, G.V. (1993) Neuronal inositol 1, 4, 5-trisphosphate receptor localized to the plasma membrane of olfactory cilia. Neuroscience, 57, 339-352.
9. DellaCorte, C., Restrepo, D., Menco, B.Ph.M., Andreini, I. & Kalinoski, D.L. (1996) Gαq/Gα11: immunolocalization in the olfactory epithelium of the rat (Rattus rattus) and the channel catfish (Ictalurus punctatus). Neuroscience, 74, 261-273.
10. Di, V.F., Steinberg, T.H. & Silverstein, S.C. (1990) Inhibition of Fura-2 sequestration and secretion with organic anion transport blockers. Cell Calcium, 11, 57-62.
11. Elsaesser, R. & Paysan, J. (2007) The sense of smell, its signalling pathways, and the dichotomy of cilia and microvilli in olfactory sensory cells. BMC Neurosci., 8, S1.
12. Elsaesser, R., Montani, G., Tirindelli, R. & Paysan, J. (2005) Phosphatidyl-inositide signaling proteins in a novel class of sensory cells in the mammalian olfactory epithelium. Eur. J. Neurosci., 21, 2692-2700.
13. Fadool, D.A. & Ache, B.W. (1992) Plasma membrane inositol 1, 4, 5-trisphosphate-activated channels mediate signal transduction in lobster olfactory receptor neurons. Neuron, 9, 907-918.
14. Finger, T.E., Silver, W.L. & Restrepo, D. (2000) The Neurobiology of Taste and Smell. Wiley-Liss, New York.
15. Futatsugi, A., Nakamura, T., Yamada, M.K., Ebisui, E., Nakamura, K., Uchida, K., Kitaguchi, T., Takahashi-Iwanaga, H., Noda, T., Aruga, J. & Mikoshiba, K. (2005) IP3 receptor types 2 and 3 mediate exocrine secretion underlying energy metabolism. Science, 309, 2232-2234.
16. Gimelbrant, A., Hutchinson, J.N., Thompson, B.R. & Chess, A. (2007) Widespread monoallelic expression on human autosomes. Science, 318, 1136-1140.
17. 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.
18. 2+ signaling. J. Biol. Chem., 279, 11967-11975.
19. Hegg, C.C., Irwin, M. & Lucero, M.T. (2009) Calcium store-mediated signaling in sustentacular cells of the mouse olfactory epithelium. Glia, 57, 634-644.
20. Johnson, E.W., Eller, P.M. & Jafek, B.W. (1993) An immuno-electron microscopic comparison of olfactory marker protein localization in the supranuclear regions of the rat olfactory epithelium and vomeronasal organ neuroepithelium. Acta Otolaryngol. Stockholm, 113, 766-771.
21. Jourdan, F. (1975) Ultrastructure de l'épithélium olfactif du rat: polymorphisme des récepteurs. C. R. Acad. Sci., 280, 443-446.
22. Juilfs, D.M., Fülle, H.J., Zhao, A.Z., Houslay, M.D. & Garbers, D.L. (1997) A subset of olfactory neurons that selectively express cGMP-stimulated phosphodiesterase (PDE2) and guanylyl cyclase-D define a unique olfactory signal transduction pathway. Proc. Natl Acad. Sci. USA, 94, 3388-3395.
23. Liman, E.R., Corey, D.P. & Dulac, C. (1999) TRP2: a candidate transduction channel for mammalian pheromone sensory signaling. Proc. Natl Acad. Sci. USA, 96, 5791-5796.
24. Lin, W., Ezekwe, E.A.D., Jr., Zhao, Z., Liman, E.R. & Restrepo, D. (2008a) TRPM5-expressing microvillous cells in the main olfactory epithelium. BMC Neurosci., 9, 114.
25. Lin, W., Ogura, T., Margolskee, R.F., Finger, T.E. & Restrepo, D. (2008b) TRPM5-expressing solitary chemosensory cells respond to odorous irritants. J. Neurophysiol., 99, 1451-1460.
26. Manzini, I., Schweers, T.S. & Schild, D. (2008) Improved fluorescent (calcium indicator) dye uptake in brain slices by blocking multidrug resistance transporters. J. Neurosci. Methods, 167, 140-147.
27. Maxwell, I.H., Harrison, G.S., Wood, W.M. & Maxwell, F. (1989) A DNS cassette containing a trimerized SV40 polyadenylation signal which efficiently blocks spurious plasmid-initiated transcription. BioTechniques, 7, 276-280.
28. Menco, B.P. (1988) Tight-junctional strands first appear in regions where three cells meet in differentiating olfactory epithelium: a freeze-fracture study. J. Cell Sci., 89, 495-505.
29. Miragall, F., Hwang, T.-K., Traub, O., Hertzberg, E.L. & Dermietzel, R. (1992) Expression of connexins in the developing olfactory system of the mouse. J. Comp. Neurol., 325, 359-378.
30. 2+ signals by differential expression of IP3 receptor subtypes. EMBO J., 18, 1303-1308.
31. Mombaerts, P. (2008) TrpC2: expression outside the mouse VNO. Chem. Senses, 33, ISOT Abstr. S28.
32. Moran, D.T., Rowley, C. III & Jafek, B.W. (1982) Electron microscopy of human olfactory epithelium reveals a new cell type: the microvillar cell. Brain Res., 253, 39-46.
33. Mousley, A., Polese, G., Marks, N.J. & Eisthen, H.L. (2006) Terminal nerve-derived neuropeptide Y modulates physiological responses in the olfactory epithelium of hungry axolotls (Ambystoma mexicanum). J. Neurosci., 26, 7707-7717.
34. Munger, S.D., Leinders-Zufall, T. & Zufall, F. (2009) Subsystem organization of the mammalian sense of smell. Annu. Rev. Physiol., 71, 115-140.
35. Nucifora, F.C. Jr, Sharp, A.H., Milgram, S.L. & Ross, C.A. (1996) Inositol 1, 4, 5-trisphosphate recetors in endocrine cells: localization and association in hetero- and homotetramers. Mol. Biol. Cell, 7, 949-960.
36. Patterson, R.L., Boehning, D. & Snyder, S.H. (2004) Inositol 1.4.5-trisphosphate receptors as signal integrators. Annu. Rev. Biochem., 73, 437-465.
37. Rash, J.E., Davidson, K.G.V., Kamasawa, N., Yasumura, T., Kamasawa, M., Zhang, C., Michaels, R., Restrepo, D., Ottersen, O.P., Olson, C.O. & Nagy, J.I. (2005) Ultrastructural localization of connexins (Cx36, Cx43, Cx45), glutamate receptors and aquaporin-4 in rodent olfactory mucosa, olfactory nerve and olfactory bulb. J. Neurocytol., 34, 307-341.
38. Restrepo, D., Miyamoto, T., Bryant, B.P. & Teeter, J.H. (1990) Odor stimuli induce rapid increase in intracellular calcium in olfactory neurons. Science, 249, 1166-1168.
39. Restrepo, D., Teeter, J.H., Honda, E., Boyle, A.G., Marecek, J.F., Prestwich, G.D. & Kalinoski, D.L. (1992) Evidence for an InsP3-gated channel protein in isolated rat olfactory cilia. Am. J. Physiol., 263, C667-C673.
40. Rodriguez, I., Feinstein, P. & Mombaerts, P. (1999) Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system. Cell, 97, 199-208.
41. Rowley, J.C. III, Moran, D.T. & Jafek, B.W. (1989) Peroxidase backfills suggest the mammalian olfactory epithelium contains a second morphologically distinct class of bipolar sensory neuron: the microvillar cell. Brain Res., 502, 387-400.
42. Sharp, A.H., Nucifora, F.C. Jr, Blondel, O., Sheppard, C.A., Zhang, C., Snyder, S.H., Russell, J.T., Ryugo, D.K. & Ross, C.A. (1999) Differential cellular expression of isoforms of inositol 1, 4, 5-triphosphate receptors in neurons and glia in brain. J. Comp. Neurol., 406, 207-220.
43. Silver, W.L., Farley, L.G. & Finger, T.E. (1991) The effects of neonatal capsaicin administration on trigeminal nerve chemoreceptors in the rat nasal cavity. Brain Res., 561, 212-216.
44. Smutzer, G., Zimmerman, J.E., Hahn, C.G., Ruscheinsky, D.D., Rodríguez, A., Han, L.Y. & Arnold, S.E. (1997) Inositol 1, 4, 5-trisphosphate receptor expression in mammalian olfactory tissue. Mol. Brain Res., 44, 347-354.
45. Tizzano, M., Dvoryanchikov, G., Barrows, J.K., Kim, S., Chaudhari, N. & Finger, T.E. (2008) Expression of Galpha14 in sweet-transducing taste cells of the posterior tongue. BMC Neurosci., 9, 110.
46. Tizzano, M., Gulbransen, B.D., Vandenbeuch, A., Clapp, T.R., Herman, J.P., Sibhatu, H.M., Churchill, M.E.A., Silver, W.L., Kinnamon, S.C. & Finger, T.E. (2010) Nasal chemosensory cells use bitter taste signaling to detect irritants and bacterial signals. Proc. Natl Acad. Sci. USA, 107, 3210-3215.
47. Young, J.T. (1981) Histopathologic examination of the rat nasal cavity. Fundam. Appl. Toxicol., 1, 309-312.
48. Zhang, C. & Restrepo, D. (2002) Expression of connexin 45 in the olfactory system. Brain Res., 929, 37-47.
49. Zufall, F. & Munger, S.D. (2001) From odor and pheromone transduction to the organization of the sense of smell. Trends Neurosci., 24, 191-193.