The native rat olfactory cyclic nucleotide-gated channel is composed of three distinct subunits

Journal of Neuroscience

Volumn 19, Issue 13, 1999, Pages 5332-5347

  Bönigk, Wolfgang ^a   Bradley, Jonathan ^b   Müller, Frank ^a   Sesti, Federico ^a,e   Boekhoff, Ingrid ^c   Ronnett, Gabriele V ^d   Kaupp, U Benjamin ^a   Frings, Stephan ^a  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

^b ECOLE NORMALE SUPÉRIEURE   (France)

^c UNIVERSITY OF HOHENHEIM   (Germany)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

cAMP; cGMP; Channel structure; Ion channels; Olfaction; Sensory transduction; Subunit

Indexed keywords

CYCLIC AMP; CYCLIC GMP; ION CHANNEL; MEMBRANE PROTEIN; MESSENGER RNA; PROTEIN KINASE C;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; IMMUNOBLOTTING; IN SITU HYBRIDIZATION; MALE; NONHUMAN; OLFACTORY EPITHELIUM; OLFACTORY NERVE; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETINA ROD; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 0242302894     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-13-05332.1999     Document Type: Article

References (71)

1. Anholt RRH, Aebi U, Snyder SH (1986) A partially purified preparation of isolated chemosensory cilia from the olfactory epithelium of the bullfrog, Rana catesbeiana. J Neurosci 6:1962-1965.
2. Ardell MD, Aragon I, Oliveira L, Porche GE, Burke E, Pittler SJ (1996) The β subunit of human rod photoreceptor cGMP-gated cation channel is generated from a complex transcription unit. FEBS Lett 389:213-218.
3. Bakalyar HA, Reed RR (1990) Identification of a specialized adenylyl cyclase that may mediate odorant detection. Science 250:1403-1406.
4. Balasubramanian S, Lynch JW, Barry PH (1996) Calcium-dependent modulation of the agonist affinity of the mammalian olfactory cyclic nucleotide-gated channel by calmodulin and a novel endogenous factor. J Membr Biol 152:13-23.
5. Baumann A, Frings S, Godde M, Seifert R, Kaupp UB (1994) Primary structure and functional expression of a Drosophila cyclic nucleotide-gated channel present in eyes and antennae. EMBO J 13:5040-5050.
6. Bönigk W, Altenhofen W, Müller F, Dose A, Illing M, Molday RS, Kaupp UB (1993) Rod and cone photoreceptor cells express distinct genes for cGMP-gated channels. Neuron 10:865-877.
7. Bradley J, Li J, Davidson N, Lester HA, Zinn K (1994) Heteromeric olfactory cyclic nucleotide-gated channels: a new subunit that confers increased sensitivity to cAMP. Proc Natl Acad Sci USA 91:8890-8894.
8. Bradley J 1996. Molecular analysis of olfactory signal transduction. PhD thesis, Caltech.
9. Bradley J, Zhang Y, Bakin R, Lester HA, Ronnett GV, Zinn K (1997) Functional expression of the heteromeric "olfactory" cyclic nucleotide-gated channel in the hippocampus: a potential effector of synaptic plasticity in brain neurons. J Neurosci 17:1993-2005.
10. 2+ channel. Neuron 18:951-958.
11. Bucossi G, Eismann E, Sesti F, Nizzari M, Seri M, Kaupp UB, Torre V (1996) Time-dependent current decline in cyclic GMP-gated bovine channels caused by point mutations in the pore region expressed in Xenopus oocytes. J Physiol (Lond) 493:409-418.
12. Bucossi G, Nizzari M, Torre V (1997) Single-channel properties of ionic channels gated by cyclic nucleotides. Biophys J 72:1165-1181.
13. 2+-calmodulin of cyclic nucleotide-activated channel of rat olfactory receptor neurons. Nature 368:545-548.
14. Chen Z, Pace U, Heldman J, Shapira A, Lancet D (1986) Isolated frog olfactory cilia: a preparation of dendritic membranes from chemosensory neurons. J Neurosci 6:2146-2154.
15. Chen T-Y, Peng Y-W, Dhallan RS, Ahamed B, Reed RR, Yau K-W (1993) A new subunit of the cyclic nucleotide-gated cation channel in retinal rods. Nature 362:764-767.
16. 2+-calmodulin modulation. Proc Natl Acad Sci USA 91:11757-11761.
17. Cook NJ, Hanke W, Kaupp UB (1987) Identification, purification, and functional reconstitution of the cyclic GMP-dependent channel from rod photoreceptors. Proc Natl Acad Sci USA 84:585-589.
18. Dhallan RS, Yau K-W, Schrader KA, Reed RR (1990) Primary structure and functional expression of a cyclic nucleotide-activated channel from olfactory neurons. Nature 347:184-187.
19. 2+ permeation in cyclic nucleotide-gated channels. EMBO J 18:131-144.
20. 2+ blockage and ionic selectivity. Proc Natl Acad Sci USA 91:1109-1113.
21. Finn JT, Grunwald ME, Yau K-W (1996) Cyclic nucleotide-gated ion channels: an extended family with diverse functions. Annu Rev Physiol 58:395-426.
22. Frings S, Lynch JW, Lindemann B (1992) Properties of cyclic nucleotide-gated channels mediating olfactory transduction: activation, selectivity, and blockage. J Gen Physiol 100:45-67.
23. Frings S, Seifert R, Godde M, Kaupp UB (1995) Profoundly different calcium permeation and blockage determine the specific function of distinct cyclic nucleotide-gated channels. Neuron 15:169-179.
24. Frohman MA, Dush MK, Martin GR (1988) Rapid production of fulllength cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci USA 85:8998-9002.
25. Gordon SE, Oakley JC, Varnum MD, Zagotta WN (1996) Altered ligand specificity by protonation in the ligand binding domain of cyclic nucleotide-gated channels. Biochemistry 35:3994-4001.
26. Goulding EH, Ngai J, Kramer RH, Colicos S, Axel R, Siegelbaum SA, Chess A (1992) Molecular cloning and single-channel properties of the cyclic nucleotide-gated channel from catfish olfactory neurons. Neuron 8:45-58.
27. Grunwald ME, Yu W-P, Yu H-H, Yau K-W (1998) Identification of a domain on the β-subunit of the rod cGMP-gated cation channel that mediates inhibition by calcium-calmodulin. J Biol Chem 273:9148-9157.
28. Hallani M, Lynch JW, Barry PH (1998) Characterization of calcium-activated chloride channels in patches excised from the dendritic knob of mammalian olfactory receptor neurons. J Membr Biol 161:163-171.
29. 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. Pflügers Arch 391:85-100.
30. Henn DK, Baumann A, Kaupp UB (1995) Probing the transmembrane topology of cyclic nucleotide-gated ion channels with a gene fusion approach. Proc Natl Acad Sci USA 92:7425-7429.
31. Hsu Y-T, Molday RS (1993) Modulation of the cGMP-gated channel of rod photoreceptor cells by calmodulin. Nature 361:76-79.
32. Jan LY, Jan YN (1990) A superfamily of ion channels. Nature 345:672.
33. 6 subunits. J Neurosci 18:2449-2457.
34. Kaprielian Z, Cho KO, Hadjargyrou M, Patterson PH (1995) CD9, a major platelet cell surface glycoprotein, is a ROCA antigen and is expressed in the nervous system. J Neurosci 15:565-573.
35. Kaupp UB (1995) Family of cyclic nucleotide gated ion channels. Curr Opin Neurobiol 5:434-442.
36. Kaupp UB, Niidome T, Tanabe T, Terada S, Bönigk W, Stühmer W, Cook NJ, Kangawa K, Matsuo H, Hirose T, Miyata T, Numa S (1989) Primary structure and functional expression from complementary DNA of the rod photoreceptor cyclic GMP-gated channel. Nature 342:762-766.
37. Kleene SJ (1997) High-gain, low-noise amplification in olfactory transduction. Biophys J 73:1110-1117.
38. Kleene SJ, Gesteland RC (1991) Calcium-activated chloride conductance in frog olfactory cilia. J Neurosci 11:3624-3629.
39. Kleene SJ, Gesteland RC, Bryant SH (1994) An electrophysiological survey of frog olfactory cilia. J Exp Biol 195:307-328.
40. Körschen HG, Illing M, Seifert R, Sesti F, Williams A, Gotzes S, Colville C, Müller F, Dosé A, Godde M, Molday L, Kaupp UB, Molday RS (1995) A 240 kDa protein represents the complete β subunit of the cyclic nucleotide-gated channel from rod photoreceptor. Neuron 15:627-636.
41. Kurahashi T, Kaneko A (1991) High density cAMP-gated channels at the ciliary membrane in the olfactory receptor cell. NeuroReport 2:5-8.
42. Kurahashi T, Menini A (1997) Mechanism of odorant adaptation in the olfactory receptor cell. Nature 385:725-729.
43. Kurahashi T, Yau K-W (1993) Co-existence of cationic and chloride components in odorant-induced current of vertebrate olfactory receptor cells. Nature 363:71-74.
44. Leinders-Zufall T, Rand MN, Shepherd GM, Greer CA, Zufall F (1997) Calcium entry through cyclic nucleotide-gated channels in individual cilia of olfactory receptor cells: spatiotemporal dynamics. J Neurosci 17:4136-4148.
45. Leinders-Zufall T, Greer CA, Shepherd GM, Zufall F (1998) Imaging odor-induced calcium transients in single olfactory cilia: specificity of activation and role in transduction. J Neurosci 18:5630-5639.
46. Liman ER, Buck LB (1994) A second subunit of the olfactory cyclic nucleotide-gated channel confers high sensitivity to cAMP. Neuron 13:611-621.
47. Liu DT, Tibbs GR, Siegelbaum SA (1996) Subunit stoichiometry of cyclic nucleotide-gated channels and effects of subunit order on channel function. Neuron 16:983-990.
48. Liu M, Chen T-Y, Ahamed B, Li J, Yau K-W (1994) Calcium-calmodulin modulation of the olfactory cyclic nucleotide-gated cation channel. Science 266:1348-1354.
49. Lowe G, Gold GH (1993) Nonlinear amplification by calcium-dependent chloride channels in olfactory receptor cells. Nature 366:283-286.
50. Ludwig J, Margalit T, Eismann E, Lancet D, Kaupp UB (1990) Primary structure of cAMP-gated channel from bovine olfactory epithelium. FEBS Lett 270:24-29.
51. olfα and type III adenylyl cyclase. Neuron 8:441-453.
52. Molday LL, Cook NJ, Kaupp UB, Molday RS (1990) The cGMP-gated cation channel of bovine rod photoreceptor cells is associated with a 240-kDa protein exhibiting immunochemical cross-reactivity with spectrin. J Biol Chem 265:18690-18695.
53. Müller F, Bönigk W, Sesti F, Frings S (1998) Phosphorylation of mammalian olfactory cyclic nucleotide-gated channels increases ligand sensitivity. J Neurosci 18:164-173.
54. Pace U, Hanski E, Salomon Y, Lancet D (1985) Odorant-sensitive adenylate cyclase may mediate olfactory reception. Nature 316:255-258.
55. Pfeuffer E, Mollner S, Lancet D, Pfeuffer T (1989) Olfactory adenylyl cyclase. J Biol Chem 264:18803-18807.
56. Reuter D, Zierold K, Schröder W, Frings S (1998) A depolarizing chloride current contributes to chemo-electrical transduction in olfactory sensory neurons in situ. J Neurosci 18:6623-6630.
57. Root MJ, MacKinnon R (1993) Identification of an external divalent cation-binding site in the pore of a cGMP-activated channel. Neuron 11:459-466.
58. Sautter A, Zong X, Hofmann F, Biel M (1998) An isoform of the rod photoreceptor cyclic nucleotide-gated channel β subunit expressed in olfactory neurons. Proc Natl Acad Sci USA 95:4696-4701.
59. Schaeren-Wiemers N, Gerfin-Moser A (1993) A single protocol to detect transcripts of various types and expression levels in neural tissues and cultured cells: in situ hybridization using digoxigenin-labeled cRNA probes. Histochemistry 100:431-440.
60. Schaffner W, Weissmann C (1973) A rapid, sensitive, and specific method for the determination of protein in dilute solution. Anal Biochem 56:502-514.
61. 2+-binding site in the pore of cyclic nucleotide-gated channels: S5/S6 segments control affinity of intrapore glutamates. EMBO J 18:119-130.
62. Sesti F, Straforini M, Lamb TD, Torre V (1994) Gating, selectivity and blockage of single channels activated by cyclic GMP in retinal rods of the tiger salamander. J Physiol (Lond) 474:203-222.
63. Sesti F, Eismann E, Kaupp UB, Nizzari M, Torre V (1995) The multiion nature of cGMP-gated channel from vertebrate rods. J Physiol (Lond) 487:17-36.
64. + channel Kv1 subtypes in synaptic membranes from bovine brain. Biochemistry 36:8195-8201.
65. Torre V, Straforini M, Sesti F, Lamb TD (1992) Different channel-gating properties of two classes of cyclic GMP-activated channel in vertebrate photoreceptors. Proc R Soc Lond B Biol Sci 250:209-215.
66. A receptor subtype. J Neurosci 17:2728-2737.
67. Vasser R, Ngai J, Axel R (1993) Spatial segregation of odorant-receptor expression in the mammalian olfactory epithelium. Cell 74:309-318.
68. Weitz D, Zoche M, Müller F, Beyermann M, Körschen HG, Kaupp UB, Koch K-W (1998) Calmodulin controls the rod photoreceptor CNG channel through an unconventional binding site in the N-terminus of the β-subunit. EMBO J 17:2273-2284.
69. Weyand I, Godde M, Frings S, Weiner J, Müller F, Altenhofen W, Hatt H, Kaupp UB (1994) Cloning and functional expression of a cyclic-nucleotide-gated channel from mammalian sperm. Nature 368:859-863.
70. 2+ entry into sperm. J Cell Biol 142:473-484.
71. Zagotta WN, Siegelbaum SA (1996) Structure and function of cyclic nucleotide-gated channels. Annu Rev Neurosci 19:235-263.