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Long-range migration of centrioles to the apical surface of the olfactory epithelium

Kaitlin Ching, Jennifer T. Wang, Tim Stearns

Preprint posted on October 13, 2021 https://www.biorxiv.org/content/10.1101/2021.10.12.464082v1

Shuttling centrioles down the nose – local maturation for multiple sensory cilia formation

Selected by Mafalda Pimentel

Background

Our sense of smell depends on odorant detection by olfactory sensory neurons (OSNs) in the olfactory epithelium. The dendrite of these neurons extends all the way to the apical surface, where it forms a knob exposing multiple cilia with odorant receptors (Fig 1).

 

Figure 1 – Schematics depicting olfactory epithelium organization. Progenitor cells (white) are at the base of the epithelium, and nuclei migrate towards the apical side along OSN differentiation and dendrite extension. Source: Ching et al. 2021 bioRxiv, Fig 1

Since there is one centriole at the base of each cilium and cells typically have two centrioles, these need to be amplified to form multiple cilia. Interestingly, this amplification takes place in dividing precursor cells located at the base of the olfactory epithelium1. This implies that OSN centrioles need to migrate tens of microns to the apical surface, a process uncovered by Ching et al. in this preprint.

 

Key findings

To resolve the number of centrioles during OSN differentiation, the authors used expansion microscopy and eGFP-centrin2 adult mice.  Progenitor cells had on average 26.4 centrioles. These kept amplifying to reach an average of 36.46 centrioles per knob in mature OSNs. Surprisingly, the average number of cilia was slightly lower (30.54) and did not correlate with centriole number, suggesting that cilia number might be regulated by additional mechanisms.

Using an ex vivo live imaging system the authors observed that centrioles moved slowly (0.18um/min) in clusters along the growing dendrite of immature OSNs. The aggregation of migrating centrioles is probably independent of cohesion fibers (CROOC/rootletin) since these were not detected in the dendritic shaft.

Centriole composition normally changes with cell cycle progression – the early proteins used as scaffold are lost, and new proteins necessary for centrosome and cilia function are recruited. This centriole maturation process was also observed in OSNs, since centrioles at the knob lack the biogenesis proteins SAS6 and STIL, but have gamma-tubulin and the pericentriolar component CDK5RAP2. In early knobs, only the parental centriole has distal appendages and thus the capacity to ciliate. The remaining centrioles eventually acquire basal feet and form multiple cilia for olfactory function.

To perturb microtubule dynamics, the authors developed an explant culture system in which dissected epithelia were placed in transwell filters positioned at an air-liquid interface mimicking the olfactory environment. Treatment of explants with the microtubule stabilizer paclitaxel led to an accumulation of centrioles below the apical surface, suggesting that dynamic microtubules are necessary to efficiently transport centrioles to the knob.

 

Figure 2 – Summary of the different steps for olfactory cilia formation. Centrioles are amplified in progenitors before the last round of cell division and differentiation. Centrioles migrate in groups along the extending dendrite. At the tip, the parental centriole is the first to form a cilium, followed by the ciliation of amplified centrioles once these mature.  Source: Ching et al. 2021 bioRxiv, Fig 6

 

What I like about this work

It is challenging to study subcellular structures in complex vertebrate tissues, due to the lack of 3D resolution and temporal control. The authors successfully implemented the necessary technological advancements to dissect centriole biology in the olfactory epithelium. These methods will be useful to study this important external surface, on which olfaction and pathogen exposure take place. This pioneer work also opens many interesting questions, discussed below.

 

Standing questions for the future

  1. It is very interesting to see centrioles maturing in the knob, similarly to local translation for dendritic spine development. This “local maturation” could be necessary to ensure that cilia are not misplaced. Are basal foot and rootletin mRNAs enriched in the dendritic knob?
  2. Another fascinating observation is the apparent “capping” of cilia number around 35, independently of the presence of excess centrioles. It could be that cilia number is limited by knob surface area and tissue mechanics, although the knob itself could also be regulated by the number of centrioles. Are the centrioles without cilia often missing basal feet?
  3. Regarding the migration itself, one could also imagine centrioles hitchhiking on other organelles such as Golgi (through PCM). Do centriole groups often co-localize with other organelles?
  4. The explant culture system is just so cool and has such potential! Could it be that the air interface is necessary for efficient centriole migration? Would ablation of the parental centriole affect the ciliation of the remaining centrioles?

 

References

  1. Ching, K. & Stearns, T. Centrioles are amplified in cycling progenitors of olfactory sensory neurons. PLOS Biology 18, e3000852 (2020).

Tags: centrosomes, cilia, cytoskeleton, microtubules, neurons, olfactory, sensory

Posted on: 3rd November 2021

doi: https://doi.org/10.1242/prelights.30970

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