Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
Detection of Near-Atmospheric Concentrations of CO2 by an Olfactory Subsystem in the Mouse
Ji Hu,1,2*
Chun Zhong,1,2*
Cheng Ding,1
Qiuyi Chi,3
Andreas Walz,4
Peter Mombaerts,4
Hiroaki Matsunami,3
Minmin Luo1
Abstract:
Carbon dioxide (CO2) is an important environmental cue for manyorganisms but is odorless to humans. It remains unclear whetherthe mammalian olfactory system can detect CO2 at concentrationsaround the average atmospheric level (0.038%). We demonstratedthe expression of carbonic anhydrase type II (CAII), an enzymethat catabolizes CO2, in a subset of mouse olfactory neuronsthat express guanylyl cyclase D (GC-D+ neurons) and projectaxons to necklace glomeruli in the olfactory bulb. Exposureto CO2 activated these GC-D+ neurons, and exposure of a mouseto CO2 activated bulbar neurons associated with necklace glomeruli.Behavioral tests revealed CO2 detection thresholds of 0.066%,and this sensitive CO2 detection required CAII activity. Weconclude that mice detect CO2 at near-atmospheric concentrationsthrough the olfactory subsystem of GC-D+ neurons.
1 National Institute of Biological Sciences, Beijing, 102206, China. 2 Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China. 3 Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710, USA. 4 The Rockefeller University, 1230 York Avenue, New York, NY 10021, USA.
* These authors contributed equally to this work.
To whom correspondence should be addressed. E-mail: luominmin{at}nibs.ac.cn
The editors suggest the following Related Resources on Science sites:
In Science Signaling
EDITORS' CHOICE
L. Bryan Ray (21 August 2007) Sci. STKE2007 (400), tw304.
[DOI: 10.1126/stke.4002007tw304] |Abstract »
THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
The Receptor Guanylyl Cyclase Type D (GC-D) Ligand Uroguanylin Promotes the Acquisition of Food Preferences in Mice.
H. Arakawa, K. R. Kelliher, F. Zufall, and S. D. Munger (2013)
Chem Senses
38, 391-397
|Abstract »|Full Text »|PDF »
Glutamatergic Signaling from the Parabrachial Nucleus Plays a Critical Role in Hypercapnic Arousal.
S. Kaur, N. P. Pedersen, S. Yokota, E. E. Hur, P. M. Fuller, M. Lazarus, N. L. Chamberlin, and C. B. Saper (2013)
J. Neurosci.
33, 7627-7640
|Abstract »|Full Text »|PDF »
Examining the Role of Carbonation and Temperature on Water Swallowing Performance: A Swallowing Reaction-Time Study.
E. Michou, A. Mastan, S. Ahmed, S. Mistry, and S. Hamdy (2012)
Chem Senses
37, 799-807
|Abstract »|Full Text »|PDF »
Natriuretic peptides block synaptic transmission by activating phosphodiesterase 2A and reducing presynaptic PKA activity.
F. Hu, J. Ren, J.-e. Zhang, W. Zhong, and M. Luo (2012)
PNAS
109, 17681-17686
|Abstract »|Full Text »|PDF »
Electrophysiological characterization of Grueneberg ganglion olfactory neurons: spontaneous firing, sodium conductance, and hyperpolarization-activated currents.
C. Y. Liu, C. Xiao, S. E. Fraser, H. A. Lester, and D. S. Koos (2012)
J Neurophysiol
108, 1318-1334
|Abstract »|Full Text »|PDF »
The wiring of Grueneberg ganglion axons is dependent on neuropilin 1.
T. Matsuo, D. A. Rossier, C. Kan, and I. Rodriguez (2012)
Development
139, 2783-2791
|Abstract »|Full Text »|PDF »
Stimulus Selection for Intranasal Sensory Isolation: Eugenol Is an Irritant.
P. M. Wise, C. J. Wysocki, and J. N. Lundstrom (2012)
Chem Senses
37, 509-514
|Abstract »|Full Text »|PDF »
Differentiation of Carbon Dioxide-Sensing Neurons in Caenorhabditis elegans Requires the ETS-5 Transcription Factor.
M. L. Guillermin, M. L. Castelletto, and E. A. Hallem (2011)
Genetics
189, 1327-1339
|Abstract »|Full Text »|PDF »
Redefining the components of central CO2 chemosensitivity - towards a better understanding of mechanism.
Elevated CO2 Levels Cause Mitochondrial Dysfunction and Impair Cell Proliferation.
C. U. Vohwinkel, E. Lecuona, H. Sun, N. Sommer, I. Vadasz, N. S. Chandel, and J. I. Sznajder (2011)
J. Biol. Chem.
286, 37067-37076
|Abstract »|Full Text »|PDF »
Role for the Membrane Receptor Guanylyl Cyclase-C in Attention Deficiency and Hyperactive Behavior.
R. Gong, C. Ding, J. Hu, Y. Lu, F. Liu, E. Mann, F. Xu, M. B. Cohen, and M. Luo (2011)
Science
333, 1642-1646
|Abstract »|Full Text »|PDF »
Comparison of the Orthonasal and Retronasal Detection Thresholds for Carbon Dioxide in Humans.
J. Melzner, T. Bitter, O. Guntinas-Lichius, R. Gottschall, M. Walther, and H. Gudziol (2011)
Chem Senses
36, 435-441
|Abstract »|Full Text »|PDF »
Different Profiles of Main and Accessory Olfactory Bulb Mitral/Tufted Cell Projections Revealed in Mice Using an Anterograde Tracer and a Whole-Mount, Flattened Cortex Preparation.
Phosphoinositide 3-Kinase-Dependent Antagonism in Mammalian Olfactory Receptor Neurons.
K. Ukhanov, D. Brunert, E. A. Corey, and B. W. Ache (2011)
J. Neurosci.
31, 273-280
|Abstract »|Full Text »|PDF »
Receptor-type guanylate cyclase is required for carbon dioxide sensation by Caenorhabditis elegans.
E. A. Hallem, W. C. Spencer, R. D. McWhirter, G. Zeller, S. R. Henz, G. Ratsch, D. M. Miller III, H. R. Horvitz, P. W. Sternberg, and N. Ringstad (2011)
PNAS
108, 254-259
|Abstract »|Full Text »|PDF »
Downregulation of Fzd6 and Cthrc1 and upregulation of olfactory receptors and protocadherins by dietary beta-carotene in lungs of Bcmo1-/- mice.
Y. G. J. van Helden, R. W. Godschalk, S. G. Heil, A. Bunschoten, S. Hessel, J. Amengual, M. L. Bonet, J. von Lintig, F. J. van Schooten, and J. Keijer (2010)
Carcinogenesis
31, 1329-1337
|Abstract »|Full Text »|PDF »
Elevated CO2 suppresses specific Drosophila innate immune responses and resistance to bacterial infection.
I. T. Helenius, T. Krupinski, D. W. Turnbull, Y. Gruenbaum, N. Silverman, E. A. Johnson, P. H. S. Sporn, J. I. Sznajder, and G. J. Beitel (2009)
PNAS
106, 18710-18715
|Abstract »|Full Text »|PDF »
The Taste of Carbonation.
J. Chandrashekar, D. Yarmolinsky, L. von Buchholtz, Y. Oka, W. Sly, N. J. P. Ryba, and C. S. Zuker (2009)
Science
326, 443-445
|Abstract »|Full Text »|PDF »
From Pheromones to Behavior.
R. Tirindelli, M. Dibattista, S. Pifferi, and A. Menini (2009)
Physiol Rev
89, 921-956
|Abstract »|Full Text »|PDF »
Guanylyl cyclase-D in the olfactory CO2 neurons is activated by bicarbonate.
L. Sun, H. Wang, J. Hu, J. Han, H. Matsunami, and M. Luo (2009)
PNAS
106, 2041-2046
|Abstract »|Full Text »|PDF »
Stimulation of Mammalian G-protein-responsive Adenylyl Cyclases by Carbon Dioxide.
P. D. Townsend, P. M. Holliday, S. Fenyk, K. C. Hess, M. A. Gray, D. R. W. Hodgson, and M. J. Cann (2009)
J. Biol. Chem.
284, 784-791
|Abstract »|Full Text »|PDF »
V-ATPase expression in the mouse olfactory epithelium.
T. G. Paunescu, A. C. Jones, R. Tyszkowski, and D. Brown (2008)
Am J Physiol Cell Physiol
295, C923-C930
|Abstract »|Full Text »|PDF »
Grueneberg Ganglion Cells Mediate Alarm Pheromone Detection in Mice.