Differential Thresholds of Proteasome Activation Reveal Two Separable Mechanisms of Sensory Organ Polarization in C. elegans.

Patricia Kunz,Christian Pohl,Christina Lehmann

doi:10.3389/fcell.2021.619596

Patricia Kunz, Christian Pohl + Show 1 more

Open Access

https://doi.org/10.3389/fcell.2021.619596

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Abstract

Cephalization is a major innovation of animal evolution and implies a synchronization of nervous system, mouth, and foregut polarization to align alimentary tract and sensomotoric system for effective foraging. However, the underlying integration of morphogenetic programs is poorly understood. Here, we show that invagination of neuroectoderm through de novo polarization and apical constriction creates the mouth opening in the Caenorhabditis elegans embryo. Simultaneously, all 18 juxta-oral sensory organ dendritic tips become symmetrically positioned around the mouth: While the two bilaterally symmetric amphid sensilla endings are towed to the mouth opening, labial and cephalic sensilla become positioned independently. Dendrite towing is enabled by the pre-polarized sensory amphid pores intercalating into the leading edge of the anteriorly migrating epidermal sheet, while apical constriction-mediated cell–cell re-arrangements mediate positioning of all other sensory organs. These two processes can be separated by gradual inactivation of the 26S proteasome activator, RPN-6.1. Moreover, RPN-6.1 also shows a dose-dependent requirement for maintenance of coordinated apical polarization of other organs with apical lumen, the pharynx, and the intestine. Thus, our data unveil integration of morphogenetic programs during the coordination of alimentary tract and sensory organ formation and suggest that this process requires tight control of ubiquitin-dependent protein degradation.

Highlights

Through sensory organs, animals can receive stimuli and transduce these to the nervous system to bring about a physiological change or behavioral response (Schmidt-Rhaesa, 2007)
For all other head sensory organs, cell shape changes through de novo apical polarization, and subsequent apical constriction mediates their centripetal movement and symmetric placement of their juxta-oral, anterior endings. We show that these two processes occur through different morphogenetic mechanisms, we uncover that they show a differential sensitivity to reduced proteasome activity
They comprise sensilla, symmetrically positioned around the mouth: A bilateral pair of amphid (AM) sensilla, the fourfold symmetric cephalic (CEP), and the six-fold symmetric inner (IL) and outer labial sensilla. Since all these sensilla require an apical lumen for the dendrite endings of sensory neurons to integrate into or penetrate through the cuticle, we reasoned that apical polarity factors should highlight them

Summary

Introduction

Animals can receive stimuli and transduce these to the nervous system to bring about a physiological change or behavioral response (Schmidt-Rhaesa, 2007). It has been initially suggested that “anterior neurons move toward the tip of the head, and the rudiments of the sensilla are formed; the neurons move posteriorly again, sensory cell bodies laying down their dendritic processes as they go” (Sulston et al, 1983) This idea has been revisited a decade ago, and the morphogenetic mechanism of retrograde extension has been coined to describe this presumably particular mode of dendrite morphogenesis utilized here (Heiman and Shaham, 2009). It has been shown that a tight interaction between glia, their associated neurons and the surrounding epidermis is possible since both glia and neurons exhibit properties of epithelial cells that allow them to integrate into the surrounding epithelium (Low et al, 2019) This mechanism was proposed for the amphid sensilla, a bilateral pair of sensory organs both containing 12 sensory neuron dendrites (Altun and Hall, 2010). This has later been confirmed by time-lapse imaging and has been coined axon towing (Gilmour et al, 2004)

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