TY - JOUR
T1 - An olfactory cilia pattern in the mammalian nose ensures high sensitivity to odors
AU - Challis, Rosemary C.
AU - Tian, Huikai
AU - Wang, Jue
AU - He, Jiwei
AU - Jiang, Jianbo
AU - Chen, Xuanmao
AU - Yin, Wenbin
AU - Connelly, Timothy
AU - Ma, Limei
AU - Yu, C. Ron
AU - Pluznick, Jennifer L.
AU - Storm, Daniel R.
AU - Huang, Liquan
AU - Zhao, Kai
AU - Ma, Minghong
N1 - Funding Information:
We are grateful to Drs. Yoshihiro Yoshihara and Gilad Barnea for generously providing the antibodies against mOR-EG and MOR28, respectively. We thank Penn Vet Imaging Core (supported by the National Center for Research Resources 1S10RR024583) for obtaining microCT scans of the mouse nasal cavity and Drs. Dewight Williams and Ray Meade at the Penn Electron Microscopy Resource Laboratory for performing scanning EM experiments. We thank Hugh Huang and Marina Zhang for their help in quantification of cilia lengths and Dr. Wenqin Luo’s lab for helpful discussions. This work was supported by grants from the NIDCD, NIH (F31DC013945 to R.C.C.; R01DC011554 and R01DC006213 to M.M.; R03DC008187 to K.Z.; and R21DC013177 to L.H.).
Publisher Copyright:
© 2015 Elsevier Ltd All rights reserved.
PY - 2015/10/5
Y1 - 2015/10/5
N2 - In many sensory organs, specialized receptors are strategically arranged to enhance detection sensitivity and acuity. It is unclear whether the olfactory system utilizes a similar organizational scheme to facilitate odor detection. Curiously, olfactory sensory neurons (OSNs) in the mouse nose are differentially stimulated depending on the cell location. We therefore asked whether OSNs in different locations evolve unique structural and/or functional features to optimize odor detection and discrimination. Using immunohistochemistry, computational fluid dynamics modeling, and patch clamp recording, we discovered that OSNs situated in highly stimulated regions have much longer cilia and are more sensitive to odorants than those in weakly stimulated regions. Surprisingly, reduction in neuronal excitability or ablation of the olfactory G protein in OSNs does not alter the cilia length pattern, indicating that neither spontaneous nor odor-evoked activity is required for its establishment. Furthermore, the pattern is evident at birth, maintained into adulthood, and restored following pharmacologically induced degeneration of the olfactory epithelium, suggesting that it is intrinsically programmed. Intriguingly, type III adenylyl cyclase (ACIII), a key protein in olfactory signal transduction and ubiquitous marker for primary cilia, exhibits location-dependent gene expression levels, and genetic ablation of ACIII dramatically alters the cilia pattern. These findings reveal an intrinsically programmed configuration in the nose to ensure high sensitivity to odors.
AB - In many sensory organs, specialized receptors are strategically arranged to enhance detection sensitivity and acuity. It is unclear whether the olfactory system utilizes a similar organizational scheme to facilitate odor detection. Curiously, olfactory sensory neurons (OSNs) in the mouse nose are differentially stimulated depending on the cell location. We therefore asked whether OSNs in different locations evolve unique structural and/or functional features to optimize odor detection and discrimination. Using immunohistochemistry, computational fluid dynamics modeling, and patch clamp recording, we discovered that OSNs situated in highly stimulated regions have much longer cilia and are more sensitive to odorants than those in weakly stimulated regions. Surprisingly, reduction in neuronal excitability or ablation of the olfactory G protein in OSNs does not alter the cilia length pattern, indicating that neither spontaneous nor odor-evoked activity is required for its establishment. Furthermore, the pattern is evident at birth, maintained into adulthood, and restored following pharmacologically induced degeneration of the olfactory epithelium, suggesting that it is intrinsically programmed. Intriguingly, type III adenylyl cyclase (ACIII), a key protein in olfactory signal transduction and ubiquitous marker for primary cilia, exhibits location-dependent gene expression levels, and genetic ablation of ACIII dramatically alters the cilia pattern. These findings reveal an intrinsically programmed configuration in the nose to ensure high sensitivity to odors.
KW - airflow
KW - computational fluid dynamics model
KW - odorant absorption
KW - olfactory cilia
KW - patch clamp
KW - type III adenylyl cyclase
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U2 - 10.1016/j.cub.2015.07.065
DO - 10.1016/j.cub.2015.07.065
M3 - Article
C2 - 26365258
AN - SCOPUS:84943456951
SN - 0960-9822
VL - 25
SP - 2503
EP - 2512
JO - Current Biology
JF - Current Biology
IS - 19
ER -