Planar cell polarity in the <i>C. elegans</i> embryo emerges by differential retention of aPARs at cell-cell contacts

Dutta, Priyanka; Odedra, Devang; Pohl, Christian

doi:10.1101/576777

Cited by 2 publications

(2 citation statements)

References 67 publications

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“…We would also like to thank Michael Glotzer for providing the strain MG644. This manuscript has been released as a Pre-Print at bioarxiv.org (Dutta et al, 2019).…”

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confidence: 99%

Planar Asymmetries in the C. elegans Embryo Emerge by Differential Retention of aPARs at Cell-Cell Contacts

Dutta

Odedra

Pohl

2019

Front. Cell Dev. Biol.

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Formation of the anteroposterior and dorsoventral body axis in Caenorhabditis elegans depends on cortical flows and advection of polarity determinants. The role of this patterning mechanism in tissue polarization after formation of cell-cell contacts is not fully understood. Here, we demonstrate that planar asymmetries are established during left-right symmetry breaking: Centripetal cortical flows asymmetrically and differentially advect anterior polarity determinants (aPARs) from contacts to the medial cortex, resulting in their unmixing from apical myosin. Contact localization and advection of PAR-6 requires balanced CDC-42 activation, while asymmetric retention and advection of PAR-3 can occur independently of PAR-6. Concurrent asymmetric retention of PAR-3, E-cadherin/HMR-1 and opposing retention of antagonistic CDC-42 and Wnt pathway components leads to planar asymmetries. The most obvious mark of planar asymmetry, retention of PAR-3 at a single cell-cell contact, is required for proper cytokinetic cell intercalation. Hence, our data uncover how planar polarity is established in a system without the canonical planar cell polarity pathway through planar asymmetric retention of aPARs.

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“…We would also like to thank Michael Glotzer for providing the strain MG644. This manuscript has been released as a Pre-Print at bioarxiv.org (Dutta et al, 2019).…”

mentioning

confidence: 99%

Planar Asymmetries in the C. elegans Embryo Emerge by Differential Retention of aPARs at Cell-Cell Contacts

Dutta

Odedra

Pohl

2019

Front. Cell Dev. Biol.

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“…Embryos were mounted as described by (Dutta, P. et al, 2019), thereby either embryos were collected directly from OP50 seeded NGM-plates with an eyelash pick and washed in a drop of M9 buffer or they were dissected from gravid hermaphrodites. Imaging was performed during early lima-bean to 1.5-fold stages.…”

Section: Cgc B Mounting Of Embryosmentioning

confidence: 99%

Coupling between epidermis and amphid morphogenesis during embryonic development of C. elegans

Kunz¹

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Sensory organs are fundamental for survival of animal populations, since the detection of environmental stimuli is crucial for localization of nourishment, predators or mating partners. In nematodes, the amphid (AM) sensilla are the largest sensory organs for detection of chemical compounds. This study investigates how the AM sensilla acquire their special elongated shape during lima-bean to 1.5-fold embryonic stages of C. elegans head development. The dissertation also examines events facilitating the morphogenesis of other head sensilla (IL/OL/CEP) and addresses aspects of general embryonic head morphogenesis. Using high resolution live-cell imaging techniques with different combinations of markers highlighting specific tissues, this study shows that epidermal head enclosure, migration of AM socket cells (pores) and translocation of AM dendrite tips are coupled processes, facilitating the elongation of AM dendrites. Importantly, during AM dendrite elongation the AM neural cell bodies are staying stationary. Manipulation through conducting UV-Laser ablation (epidermis close to pore/pore) and RPN-6.1 dsRNA interference resulted in compromised AM pore migration and impaired dendrite elongation. This leads to the conclusion that AM pores need to be physically attached (through C. elegans apical junctions, CeAJ) to the migrating epidermal sheet and to AM dendrite tips for successful AM morphogenesis. This study infers that RPN-6.1 plays an important role for correct AM pore morphogenesis and AM pore to AM dendrite tip attachment. Our results lead to the conclusion that head enclosure drives AM pore migration and AM dendrite elongation with AM neural cell bodies staying stationary. Thereby, CeAJ are interconnecting AM dendrite tips to AM pores and CeAJ link the sensillar ending to the migrating epidermis. Thus, migration of attached target tissue (pore), with neural cell bodies staying stationary (constituting an abutment), creates a pulling force facilitating AM dendrite elongation. This passive neurite elongation procedure is coined dendrite towing in this study. Additionally, this study discovers that translocation of IL, OL and CEP head sensilla pores is influenced by apical constriction. This conclusion was made based on the findings that IL/OL/CEP pores migrate towards the prospective mouth anterior to the epidermal leading edge, separated from AM pores and irrespective of highly impaired AM sensilla morphogenesis after strong RPN-6.1 depletion. Also, concurrent with translocation of IL/OL/CEP pores, bottle-shaped cells occur and non-muscle-myosin and apical polarity factors are getting enriched at the anterior most part of the head, indicating de-novo manifestation of apical constriction. It is furthermore assumed that apical constriction in arcade cells might contribute to early pharynx development. All in all, this study reveals two force-generating events: Head enclosure-driven AM sensilla morphogenesis via dendrite towing and, otherwise, apical constriction-facilitated translocation of IL/OL/CEP sensilla pores. These events can get separated by graded depletion of the proteasome activator RPN-6.1.

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Planar cell polarity in the C. elegans embryo emerges by differential retention of aPARs at cell-cell contacts

Cited by 2 publications

References 67 publications

Planar Asymmetries in the C. elegans Embryo Emerge by Differential Retention of aPARs at Cell-Cell Contacts

Planar Asymmetries in the C. elegans Embryo Emerge by Differential Retention of aPARs at Cell-Cell Contacts

Coupling between epidermis and amphid morphogenesis during embryonic development of C. elegans

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