Journal Article

Olfactory sensory neurons transiently express multiple olfactory receptors during development

Li, Qian, Tan, Longzhi, Xie, X Sunney

2015

Overview

In mammals, each olfactory sensory neuron randomly expresses one, and only one, olfactory receptor (OR)—a phenomenon called the “one‐neuron‐one‐receptor” rule. Although extensively studied, this rule was never proven for all ~1,000 OR genes in one cell at once, and little is known about its dynamics. Here, we directly tested this rule by single‐cell transcriptomic sequencing of 178 cells from the main olfactory epithelium of adult and newborn mice. To our surprise, a subset of cells expressed multiple ORs. Most of these cells were developmentally immature. Our results illustrated how the “one‐neuron‐one‐receptor” rule may have been established: At first, a single neuron temporarily expressed multiple ORs—seemingly violating the rule—and then all but one OR were eliminated. This work provided experimental evidence that epigenetic regulation in the olfactory system selects a single OR by suppressing a few transiently expressed ORs in a single cell during development. Synopsis Single‐cell transcriptomic analyses of mouse olfactory sensory neurons reveal co‐expression of multiple olfactory receptors at an early developmental stage and provide insights into how the “one‐neuron‐one‐receptor” rule is established during neurogenesis. Olfactory sensory neurons co‐express multiple olfactory receptors at an immature stage, while mature neurons express only one olfactory receptor. New splicing isoforms of olfactory receptors and other previously undetected characteristics of their expression are identified by single‐cell RNA sequencing. RNA in situ hybridization reveals co‐expression of trace amine‐associated receptors in olfactory sensory neurons during development. Graphical Abstract Single‐cell transcriptomic analyses of mouse olfactory sensory neurons reveal co‐expression of multiple olfactory receptors at an early developmental stage and provide insights into how the “one‐neuron‐one‐receptor” rule is established during neurogenesis.

• Publisher: Nature Publishing Group UK,EMBO Press,John Wiley and Sons Inc,Springer Nature
• Subject: Animals / EMBO09 / EMBO17 / EMBO27 / Epigenesis, Genetic / Epigenetics / Epithelium / Gene expression / Gene Expression Profiling - methods / Gene Expression Regulation, Developmental / Hybridization / immature and mature olfactory sensory neurons / Mice / Neurons / odorant receptor / Odorant receptors / Olfactory epithelium / Olfactory receptor neurons / Olfactory Receptor Neurons - cytology / Olfactory Receptor Neurons - metabolism / Olfactory system / Quality / Receptors / Receptors, Odorant - genetics / Scholarships & fellowships / Sensory neurons / Sequence Analysis, RNA - methods / Single-Cell Analysis - methods / single‐cell RNA‐Seq / Standard deviation / trace amine‐associated receptor (TAAR)