title: Non-centrosomal epidermal microtubules act in parallel to LET-502/ROCK to promote C. elegans elongation.
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.
authors.affiliation: 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.
authors.forename: Sophie
authors.initials: S
authors.lastname: Quintin
authors.affiliation: Ludwig Institute for Cancer Research, Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92037, USA.
authors.forename: Shahoe
authors.initials: S
authors.lastname: Wang
authors.affiliation: IGBMC - CNRS UMR 7104 - INSERM U964 - Université de Strasbourg, 1 rue Laurent Fries, BP 10142, Illkirch 67404, Cedex, France.
authors.forename: Julien
authors.initials: J
authors.lastname: Pontabry
authors.affiliation: IGBMC - CNRS UMR 7104 - INSERM U964 - Université de Strasbourg, 1 rue Laurent Fries, BP 10142, Illkirch 67404, Cedex, France.
authors.forename: Ambre
authors.initials: A
authors.lastname: Bender
authors.affiliation: Institut de Biologie Paris Seine, IBPS FR3631, Université Pierre et Marie Curie, 7-9 Quai Saint Bernard, Paris 75005, France.
authors.forename: François
authors.initials: F
authors.lastname: Robin
authors.affiliation: IGBMC - CNRS UMR 7104 - INSERM U964 - Université de Strasbourg, 1 rue Laurent Fries, BP 10142, Illkirch 67404, Cedex, France.
authors.forename: Vincent
authors.initials: V
authors.lastname: Hyenne
authors.affiliation: IGBMC - CNRS UMR 7104 - INSERM U964 - Université de Strasbourg, 1 rue Laurent Fries, BP 10142, Illkirch 67404, Cedex, France.
authors.forename: Frédéric
authors.initials: F
authors.lastname: Landmann
authors.affiliation: IGBMC - CNRS UMR 7104 - INSERM U964 - Université de Strasbourg, 1 rue Laurent Fries, BP 10142, Illkirch 67404, Cedex, France.
authors.forename: Christelle
authors.initials: C
authors.lastname: Gally
authors.affiliation: Ludwig Institute for Cancer Research, Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92037, USA.
authors.forename: Karen
authors.initials: K
authors.lastname: Oegema
authors.affiliation: 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.
authors.forename: Michel
authors.initials: M
authors.lastname: Labouesse
mesh_terms: D000205:Actomyosin / Q000378:metabolism; D022005:Adherens Junctions / Q000378:metabolism; D000818:Animals; D015820:Cadherins / Q000378:metabolism; D017173:Caenorhabditis elegans / Q000196:embryology* / Q000254:growth & development; D029742:Caenorhabditis elegans Proteins / Q000378:metabolism*; D003598:Cytoskeletal Proteins; D003599:Cytoskeleton / Q000378:metabolism; D000078404:Epidermal Cells; D004817:Epidermis / Q000378:metabolism; D022002:Hemidesmosomes / Q000378:metabolism; D008870:Microtubules / Q000378:metabolism*; D009024:Morphogenesis / Q000502:physiology; D009124:Muscle Proteins / Q000378:metabolism; D024462:Myosin Type II / Q000378:metabolism; D009687:Nuclear Proteins; D021381:Protein Transport / Q000235:genetics; D050765:Qa-SNARE Proteins / Q000378:metabolism; D034622:RNA Interference; D034741:RNA, Small Interfering / Q000235:genetics; D014404:Tubulin / Q000378:metabolism; D054460:rho-Associated Kinases / Q000378:metabolism*
chemical_list: D015820:Cadherins; D029742:Caenorhabditis elegans Proteins; D003598:Cytoskeletal Proteins; D009124:Muscle Proteins; C000608701:NOCA-1 protein, C elegans; D009687:Nuclear Proteins; D050765:Qa-SNARE Proteins; D034741:RNA, Small Interfering; D014404:Tubulin; C120778:let-805 protein, C elegans; D000205:Actomyosin; C515856:LET-502 protein, C elegans; D054460:rho-Associated Kinases; D024462:Myosin Type II
keywords: Caenorhabditis elegans; Morphogenesis; Non-centrosomal microtubules