 |
Previous Article | Next Article 
The Journal of Neuroscience, July 1, 1999, 19(13):5332-5347
The Native Rat Olfactory Cyclic Nucleotide-Gated Channel Is
Composed of Three Distinct Subunits
Wolfgang
Bönigk1,
Jonathan
Bradley2,
Frank
Müller1,
Federico
Sesti1,
Ingrid
Boekhoff3,
Gabriele V.
Ronnett4,
U. Benjamin
Kaupp1, and
Stephan
Frings1
1 Forschungszentrum Jülich, Institut für
Biologische Informationsverarbeitung, 52425 Jülich, Germany,
2 Ecole Normale Supérieure, Laboratoire de
Neurobiologie, 75005 Paris, France, 3 Universität
Hohenheim, Institut für Physiologie, 70574 Stuttgart, Germany,
and 4 Department of Neurosciences and Neurology, Johns
Hopkins University School of Medicine, Baltimore, Maryland 21205
Cyclic nucleotide-gated (CNG) channels play central roles in visual
and olfactory signal transduction. In the retina, rod photoreceptors
express the subunits CNC 1 and CNC 1a. In cone photoreceptors, only
CNC 2 expression has been demonstrated so far. Rat olfactory sensory
neurons (OSNs) express two homologous subunits, here designated CNC 3
and CNC 4. This paper describes the characterization of CNC 1b, a
third subunit expressed in OSNs and establishes it as a component of
the native channel. CNC 1b is an alternate splice form of the rod
photoreceptor CNC 1a subunit. Analysis of mRNA and protein expression
together suggest co-expression of all three subunits in sensory cilia
of OSNs. From single-channel analyses of native rat olfactory channels
and of channels expressed heterologously from all possible combinations
of the CNC 3, - 4, and - 1b subunits, we conclude that the native
CNG channel in OSNs is composed of all three subunits. Thus, CNG
channels in both rod photoreceptors and olfactory sensory neurons
result from coassembly of specific subunits with various forms of
an alternatively spliced subunit.
Key words:
cAMP; cGMP; sensory transduction; olfaction; ion
channels; channel structure; subunit
Copyright © 1999 Society for Neuroscience 0270-6474/99/19135332-16$05.00/0
This article has been cited by other articles:

|
 |

|
 |
 
Y. Zhang, L. L. Molday, R. S. Molday, S. S. Sarfare, M. L. Woodruff, G. L. Fain, T. W. Kraft, and S. J. Pittler
Knockout of GARPs and the {beta}-subunit of the rod cGMP-gated channel disrupts disk morphogenesis and rod outer segment structural integrity
J. Cell Sci.,
April 15, 2009;
122(8):
1192 - 1200.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Biel
Cyclic Nucleotide-regulated Cation Channels
J. Biol. Chem.,
April 3, 2009;
284(14):
9017 - 9021.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Krannich and M. Stengl
Cyclic Nucleotide-Activated Currents in Cultured Olfactory Receptor Neurons of the Hawkmoth Manduca sexta
J Neurophysiol,
November 1, 2008;
100(5):
2866 - 2877.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. J. Kleene
The Electrochemical Basis of Odor Transduction in Vertebrate Olfactory Cilia
Chem Senses,
November 1, 2008;
33(9):
839 - 859.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K.-T. Cheng, Y.-K. Leung, B. Shen, Y.-C. Kwok, C.-O. Wong, H.-Y. Kwan, Y.-B. Man, X. Ma, Y. Huang, and X. Yao
CNGA2 Channels Mediate Adenosine-Induced Ca2+ Influx in Vascular Endothelial Cells
Arterioscler. Thromb. Vasc. Biol.,
May 1, 2008;
28(5):
913 - 918.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Wunder, A. Rebmann, A. Geerts, and B. Kalthof
Pharmacological and Kinetic Characterization of Adrenomedullin 1 and Calcitonin Gene-Related Peptide 1 Receptor Reporter Cell Lines
Mol. Pharmacol.,
April 1, 2008;
73(4):
1235 - 1243.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
U. Mayer, N. Ungerer, D. Klimmeck, U. Warnken, M. Schnolzer, S. Frings, and F. Mohrlen
Proteomic Analysis of a Membrane Preparation from Rat Olfactory Sensory Cilia
Chem Senses,
February 1, 2008;
33(2):
145 - 162.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Feldmesser, D. Bercovich, N. Avidan, S. Halbertal, L. Haim, R. Gross-Isseroff, S. Goshen, and D. Lancet
Mutations in Olfactory Signal Transduction Genes Are Not a Major Cause of Human Congenital General Anosmia
Chem Senses,
January 1, 2007;
32(1):
21 - 30.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Michalakis, J. Reisert, H. Geiger, C. Wetzel, X. Zong, J. Bradley, M. Spehr, S. Huttl, A. Gerstner, A. Pfeifer, et al.
Loss of CNGB1 Protein Leads to Olfactory Dysfunction and Subciliary Cyclic Nucleotide-gated Channel Trapping
J. Biol. Chem.,
November 17, 2006;
281(46):
35156 - 35166.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. D. Brady, E. D. Rich, J. R. Martens, J. W. Karpen, M. D. Varnum, and R. L. Brown
Interplay between PIP3 and calmodulin regulation of olfactory cyclic nucleotide-gated channels
PNAS,
October 17, 2006;
103(42):
15635 - 15640.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T.-Y. Chen, H. Takeuchi, and T. Kurahashi
Odorant Inhibition of the Olfactory Cyclic Nucleotide-gated Channel with a Native Molecular Assembly
J. Gen. Physiol.,
August 28, 2006;
128(3):
365 - 371.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Kaneko, F. Mohrlen, and S. Frings
Calmodulin Contributes to Gating Control in Olfactory Calcium-activated Chloride Channels
J. Gen. Physiol.,
May 30, 2006;
127(6):
737 - 748.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. E. Contreras and M. Holmgren
Access of Quaternary Ammonium Blockers to the Internal Pore of Cyclic Nucleotide-gated Channels: Implications for the Location of the Gate
J. Gen. Physiol.,
April 24, 2006;
127(5):
481 - 494.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Qu, A. J. Moorhouse, M. Chandra, K. D. Pierce, T. M. Lewis, and P. H. Barry
A Single P-loop Glutamate Point Mutation to either Lysine or Arginine Switches the Cation-Anion Selectivity of the CNGA2 Channel
J. Gen. Physiol.,
March 27, 2006;
127(4):
375 - 389.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Batra-Safferling, K. Abarca-Heidemann, H. G. Korschen, C. Tziatzios, M. Stoldt, I. Budyak, D. Willbold, H. Schwalbe, J. Klein-Seetharaman, and U. B. Kaupp
Glutamic Acid-rich Proteins of Rod Photoreceptors Are Natively Unfolded
J. Biol. Chem.,
January 20, 2006;
281(3):
1449 - 1460.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Nache, E. Schulz, T. Zimmer, J. Kusch, C. Biskup, R. Koopmann, V. Hagen, and K. Benndorf
Activation of olfactory-type cyclic nucleotide-gated channels is highly cooperative
J. Physiol.,
November 15, 2005;
569(1):
91 - 102.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Seino and T. Shibasaki
PKA-Dependent and PKA-Independent Pathways for cAMP-Regulated Exocytosis
Physiol Rev,
October 1, 2005;
85(4):
1303 - 1342.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Liu and M. D. Varnum
Functional consequences of progressive cone dystrophy-associated mutations in the human cone photoreceptor cyclic nucleotide-gated channel CNGA3 subunit
Am J Physiol Cell Physiol,
July 1, 2005;
289(1):
C187 - C198.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. R. Henion, D. Raitcheva, R. Grosholz, F. Biellmann, W. C. Skarnes, T. Hennet, and G. A. Schwarting
{beta}1,3-N-Acetylglucosaminyltransferase 1 Glycosylation Is Required for Axon Pathfinding by Olfactory Sensory Neurons
J. Neurosci.,
February 23, 2005;
25(8):
1894 - 1903.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Huttl, S. Michalakis, M. Seeliger, D.-G. Luo, N. Acar, H. Geiger, K. Hudl, R. Mader, S. Haverkamp, M. Moser, et al.
Impaired Channel Targeting and Retinal Degeneration in Mice Lacking the Cyclic Nucleotide-Gated Channel Subunit CNGB1
J. Neurosci.,
January 5, 2005;
25(1):
130 - 138.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Kusch, V. Nache, and K. Benndorf
Effects of permeating ions and cGMP on gating and conductance of rod-type cyclic nucleotide-gated (CNGA1) channels
J. Physiol.,
November 1, 2004;
560(3):
605 - 616.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. H. Yu and W. A. Catterall
The VGL-Chanome: A Protein Superfamily Specialized for Electrical Signaling and Ionic Homeostasis
Sci. Signal.,
October 5, 2004;
2004(253):
re15 - re15.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Delay and D. Restrepo
Odorant Responses of Dual Polarity Are Mediated by cAMP in Mouse Olfactory Sensory Neurons
J Neurophysiol,
September 1, 2004;
92(3):
1312 - 1319.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. C. Trudeau and W. N. Zagotta
Dynamics of Ca2+-Calmodulin-dependent Inhibition of Rod Cyclic Nucleotide-gated Channels Measured by Patch-clamp Fluorometry
J. Gen. Physiol.,
August 30, 2004;
124(3):
211 - 223.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. D. Brady, T. C. Rich, X. Le, K. Stafford, C. J. Fowler, L. Lynch, J. W. Karpen, R. L. Brown, and J. R. Martens
Functional Role of Lipid Raft Microdomains in Cyclic Nucleotide-Gated Channel Activation
Mol. Pharmacol.,
March 1, 2004;
65(3):
503 - 511.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Trankner, H. Jagle, S. Kohl, E. Apfelstedt-Sylla, L. T. Sharpe, U. B. Kaupp, E. Zrenner, R. Seifert, and B. Wissinger
Molecular Basis of an Inherited Form of Incomplete Achromatopsia
J. Neurosci.,
January 7, 2004;
24(1):
138 - 147.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Hofmann, M. Biel, and U. B. Kaupp
International Union of Pharmacology. XLII. Compendium of Voltage-Gated Ion Channels: Cyclic Nucleotide-Modulated Channels
Pharmacol. Rev.,
December 1, 2003;
55(4):
587 - 589.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. L. Brown, L. L. Lynch, T. L. Haley, and R. Arsanjani
Pseudechetoxin Binds to the Pore Turret of Cyclic Nucleotide-gated Ion Channels
J. Gen. Physiol.,
November 24, 2003;
122(6):
749 - 760.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Much, C. Wahl-Schott, X. Zong, A. Schneider, L. Baumann, S. Moosmang, A. Ludwig, and M. Biel
Role of Subunit Heteromerization and N-Linked Glycosylation in the Formation of Functional Hyperpolarization-activated Cyclic Nucleotide-gated Channels
J. Biol. Chem.,
October 31, 2003;
278(44):
43781 - 43786.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Zheng, M. D. Varnum, and W. N. Zagotta
Disruption of an Intersubunit Interaction Underlies Ca2+-Calmodulin Modulation of Cyclic Nucleotide-Gated Channels
J. Neurosci.,
September 3, 2003;
23(22):
8167 - 8175.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Peng, E. D. Rich, C. A. Thor, and M. D. Varnum
Functionally Important Calmodulin-binding Sites in Both NH2- and COOH-terminal Regions of the Cone Photoreceptor Cyclic Nucleotide-gated Channel CNGB3 Subunit
J. Biol. Chem.,
June 27, 2003;
278(27):
24617 - 24623.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. C. Trudeau and W. N. Zagotta
Calcium/Calmodulin Modulation of Olfactory and Rod Cyclic Nucleotide-gated Ion Channels
J. Biol. Chem.,
May 23, 2003;
278(21):
18705 - 18708.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. R. Kelliher, J. Ziesmann, S. D. Munger, R. R. Reed, and F. Zufall
Importance of the CNGA4 channel gene for odor discrimination and adaptation in behaving mice
PNAS,
April 1, 2003;
100(7):
4299 - 4304.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Rosenbaum, L. D. Islas, A. E. Carlson, and S. E. Gordon
Dequalinium: A Novel, High-affinity Blocker of CNGA1 Channels
J. Gen. Physiol.,
December 30, 2002;
121(1):
37 - 47.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Holmgren
Influence of Permeant Ions on Gating in Cyclic Nucleotide-gated Channels
J. Gen. Physiol.,
December 30, 2002;
121(1):
61 - 72.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
U. B. Kaupp and R. Seifert
Cyclic Nucleotide-Gated Ion Channels
Physiol Rev,
July 1, 2002;
82(3):
769 - 824.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. C. Trudeau and W. N. Zagotta
Mechanism of calcium/calmodulin inhibition of rod cyclic nucleotide-gated channels
PNAS,
June 11, 2002;
99(12):
8424 - 8429.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. B. Kuzmiski and B. A. MacVicar
Cyclic Nucleotide-Gated Channels Contribute to the Cholinergic Plateau Potential in Hippocampal CA1 Pyramidal Neurons
J. Neurosci.,
November 15, 2001;
21(22):
8707 - 8714.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Boyer, J. J. Art, C. J. Dechesne, J. Lehouelleur, J. Vautrin, and A. Sans
Contribution of the Plasmalemma to Ca2+ Homeostasis in Hair Cells
J. Neurosci.,
April 15, 2001;
21(8):
2640 - 2650.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Muller, M. Vantler, D. Weitz, E. Eismann, M. Zoche, K.-W. Koch, and U B. Kaupp
Ligand sensitivity of the {alpha}2 subunit from the bovine cone cGMP-gated channel is modulated by protein kinase C but not by calmodulin
J. Physiol.,
April 15, 2001;
532(2):
399 - 409.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. R. Meyer, A. Angele, E. Kremmer, U. B. Kaupp, and F. Muller
A cGMP-signaling pathway in a subset of olfactory sensory neurons
PNAS,
September 12, 2000;
97(19):
10595 - 10600.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M.-C. Broillet
A Single Intracellular Cysteine Residue Is Responsible for the Activation of the Olfactory Cyclic Nucleotide-gated Channel by NO
J. Biol. Chem.,
May 12, 2000;
275(20):
15135 - 15141.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Gerstner, X. Zong, F. Hofmann, and M. Biel
Molecular Cloning and Functional Characterization of a New Modulatory Cyclic Nucleotide-Gated Channel Subunit from Mouse Retina
J. Neurosci.,
February 15, 2000;
20(4):
1324 - 1332.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. He, M. Ruiz, and J. W. Karpen
Constraining the subunit order of rod cyclic nucleotide-gated channels reveals a diagonal arrangement of like subunits
PNAS,
January 18, 2000;
97(2):
895 - 900.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. E. Grunwald, H. Zhong, J. Lai, and K.-W. Yau
Molecular determinants of the modulation of cyclic nucleotide-activated channels by calmodulin
PNAS,
November 9, 1999;
96(23):
13444 - 13449.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Baker, Diana. M. Cummings, S. D. Munger, J. W. Margolis, L. Franzen, R. R. Reed, and F. L. Margolis
Targeted Deletion of a Cyclic Nucleotide-Gated Channel Subunit (OCNC1): Biochemical and Morphological Consequences in Adult Mice
J. Neurosci.,
November 1, 1999;
19(21):
9313 - 9321.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. R. Murrell and D. D. Hunter
An Olfactory Sensory Neuron Line, Odora, Properly Targets Olfactory Proteins and Responds to Odorants
J. Neurosci.,
October 1, 1999;
19(19):
8260 - 8270.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. A. Vitalis, J. L. Costantin, P.-S. Tsai, H. Sakakibara, S. Paruthiyil, T. Iiri, J.-F. Martini, M. Taga, A. L. H. Choi, A. C. Charles, et al.
Role of the cAMP signaling pathway in the regulation of gonadotropin-releasing hormone secretion in GT1 cells
PNAS,
February 15, 2000;
97(4):
1861 - 1866.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|