An olfactory cilia pattern in the mammalian nose ensures high sensitivity to odors

Rosemary C. Challis, Huikai Tian, Jue Wang, Jiwei He, Jianbo Jiang, Xuanmao Chen, Wenbin Yin, Timothy Connelly, Limei Ma, C. Ron Yu, Jennifer L. Pluznick, Daniel R. Storm, Liquan Huang, Kai Zhao, Minghong Ma

Research output: Contribution to journalArticle

Abstract

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.

Original languageEnglish (US)
Pages (from-to)2503-2512
Number of pages10
JournalCurrent Biology
Volume25
Issue number19
DOIs
StatePublished - Oct 5 2015

Keywords

  • airflow
  • computational fluid dynamics model
  • odorant absorption
  • olfactory cilia
  • patch clamp
  • type III adenylyl cyclase

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

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  • Cite this

    Challis, R. C., Tian, H., Wang, J., He, J., Jiang, J., Chen, X., Yin, W., Connelly, T., Ma, L., Yu, C. R., Pluznick, J. L., Storm, D. R., Huang, L., Zhao, K., & Ma, M. (2015). An olfactory cilia pattern in the mammalian nose ensures high sensitivity to odors. Current Biology, 25(19), 2503-2512. https://doi.org/10.1016/j.cub.2015.07.065