Centrioles are amplified in cycling progenitors of olfactory sensory neurons

Kaitlin Ching,Tim Stearns,Piali Sengupta

doi:10.1371/journal.pbio.3000852

Abstract

Olfaction in most animals is mediated by neurons bearing cilia that are accessible to the environment. Olfactory sensory neurons (OSNs) in chordates usually have multiple cilia, each with a centriole at its base. OSNs differentiate from stem cells in the olfactory epithelium, and how the epithelium generates cells with many centrioles is not yet understood. We show that centrioles are amplified via centriole rosette formation in both embryonic development and turnover of the olfactory epithelium in adult mice, and rosette-bearing cells often have free centrioles in addition. Cells with amplified centrioles can go on to divide, with centrioles clustered at each pole. Additionally, we found that centrioles are amplified in immediate neuronal precursors (INPs) concomitant with elevation of mRNA for polo-like kinase 4 (Plk4) and SCL/Tal1-interrupting locus gene (Stil), key regulators of centriole duplication. These results support a model in which centriole amplification occurs during a transient state characterized by elevated Plk4 and Stil in early INP cells. These cells then go on to divide at least once to become OSNs, demonstrating that cell division with amplified centrioles, known to be tolerated in disease states, can occur as part of a normal developmental program.

Highlights

Olfaction, the primary way that animals sense their chemical environment, begins in olfactory sensory neurons (OSNs)
We considered the potential means by which cells amplify centriole number during differentiation from stem cells to OSNs
Building on a previous observation of centriole rosettes in the olfactory epithelium of embryonic mice [16], we have found that centrioles in both adult and embryonic olfactory epithelium can be amplified from the centrosome of the progenitor cell via centriole rosettes prior to cell division

Summary

Introduction

The primary way that animals sense their chemical environment, begins in olfactory sensory neurons (OSNs). Each OSN has multiple cilia, which protrude from the end of a dendrite at the apical surface of the olfactory epithelium. Odorants contact receptors on the surface of cilia, initiating a signaling event in the OSN. At the base of each cilium, a centriole organizes the structure (Fig 1A). Cilia are necessary for olfaction, as are the centrioles that organize their microtubule structures [1,2]. Each OSN must have multiple centrioles, raising the question: How are these many centrioles made?

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Conclusion