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Development. 2016 Jan 1;143(1):160-73. doi: 10.1242/dev.126615. Epub 2015 Nov 19.

Non-centrosomal epidermal microtubules act in parallel to LET-502/ROCK to promote C. elegans elongation.

Author information

1
IGBMC - CNRS UMR 7104 - INSERM U964 - Université de Strasbourg, 1 rue Laurent Fries, BP 10142, Illkirch 67404, Cedex, France quintin@igbmc.fr michel.labouesse@upmc.fr.
2
Ludwig Institute for Cancer Research, Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92037, USA.
3
IGBMC - CNRS UMR 7104 - INSERM U964 - Université de Strasbourg, 1 rue Laurent Fries, BP 10142, Illkirch 67404, Cedex, France.
4
Institut de Biologie Paris Seine, IBPS FR3631, Université Pierre et Marie Curie, 7-9 Quai Saint Bernard, Paris 75005, France.
5
IGBMC - CNRS UMR 7104 - INSERM U964 - Université de Strasbourg, 1 rue Laurent Fries, BP 10142, Illkirch 67404, Cedex, France Institut de Biologie Paris Seine, IBPS FR3631, Université Pierre et Marie Curie, 7-9 Quai Saint Bernard, Paris 75005, France quintin@igbmc.fr michel.labouesse@upmc.fr.

Abstract

C. elegans embryonic elongation is a morphogenetic event driven by actomyosin contractility and muscle-induced tension transmitted through hemidesmosomes. A role for the microtubule cytoskeleton has also been proposed, but its contribution remains poorly characterized. Here, we investigate the organization of the non-centrosomal microtubule arrays present in the epidermis and assess their function in elongation. We show that the microtubule regulators γ-tubulin and NOCA-1 are recruited to hemidesmosomes and adherens junctions early in elongation. Several parallel approaches suggest that microtubule nucleation occurs from these sites. Disrupting the epidermal microtubule array by overexpressing the microtubule-severing protein Spastin or by inhibiting the C. elegans ninein homolog NOCA-1 in the epidermis mildly affected elongation. However, microtubules were essential for elongation when hemidesmosomes or the activity of the Rho kinase LET-502/ROCK were partially compromised. Imaging of junctional components and genetic analyses suggest that epidermal microtubules function together with Rho kinase to promote the transport of E-cadherin to adherens junctions and myotactin to hemidesmosomes. Our results indicate that the role of LET-502 in junctional remodeling is likely to be independent of its established function as a myosin II activator, but requires a microtubule-dependent pathway involving the syntaxin SYX-5. Hence, we propose that non-centrosomal microtubules organized by epidermal junctions contribute to elongation by transporting junction remodeling factors, rather than having a mechanical role.

KEYWORDS:

Caenorhabditis elegans; Morphogenesis; Non-centrosomal microtubules

PMID:
26586219
PMCID:
PMC6514414
DOI:
10.1242/dev.126615
[Indexed for MEDLINE]
Free PMC Article

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