Click here to close
Hello! We notice that you are using Internet Explorer, which is not supported by Xenbase and may cause the site to display incorrectly.
We suggest using a current version of Chrome,
FireFox, or Safari.
J Cell Sci
2018 Jun 28;13112:. doi: 10.1242/jcs.212647.
Show Gene links
Show Anatomy links
Septin-dependent remodeling of cortical microtubule drives cell reshaping during epithelial wound healing.
Shindo A, Audrey A, Takagishi M, Takahashi M, Wallingford JB, Kinoshita M.
???displayArticle.abstract???
Wounds in embryos heal rapidly through contraction of the wound edges. Despite well-recognized significance of the actomyosin purse string for wound closure, roles for other cytoskeletal components are largely unknown. Here, we report that the septin cytoskeleton cooperates with actomyosin and microtubules to coordinate circumferential contraction of the wound margin and concentric elongation of wound-proximal cells in Xenopus laevis embryos. Microtubules reoriented radially, forming bundles along lateral cell cortices in elongating wound-proximal cells. Depletion of septin 7 (Sept7) slowed wound closure by attenuating the wound edge contraction and cell elongation. ROCK/Rho-kinase inhibitor-mediated suppression of actomyosin contractility enhanced the Sept7 phenotype, whereas the Sept7 depletion did not affect the accumulation of actomyosin at the wound edge. The cortical microtubule bundles were reduced in wound-proximal cells in Sept7 knockdown (Sept7-KD) embryos, but forced bundling of microtubules mediated by the microtubule-stabilizing protein Map7 did not rescue the Sept7-KD phenotype. Nocodazole-mediated microtubule depolymerization enhanced the Sept7-KD phenotype, suggesting that Sept7 is required for microtubule reorganization during cell elongation. Our findings indicate that septins are required for the rapid wound closure by facilitating cortical microtubule reorganization and the concentric elongation of surrounding cells.
Abreu-Blanco,
Drosophila embryos close epithelial wounds using a combination of cellular protrusions and an actomyosin purse string.
2012, Pubmed
Abreu-Blanco,
Drosophila embryos close epithelial wounds using a combination of cellular protrusions and an actomyosin purse string.
2012,
Pubmed Abreu-Blanco,
Cell wound repair in Drosophila occurs through three distinct phases of membrane and cytoskeletal remodeling.
2011,
Pubmed Ageta-Ishihara,
Septins promote dendrite and axon development by negatively regulating microtubule stability via HDAC6-mediated deacetylation.
2013,
Pubmed Bai,
Novel septin 9 repeat motifs altered in neuralgic amyotrophy bind and bundle microtubules.
2013,
Pubmed Bement,
Wound-induced assembly and closure of an actomyosin purse string in Xenopus oocytes.
1999,
Pubmed
,
Xenbase Bertin,
Phosphatidylinositol-4,5-bisphosphate promotes budding yeast septin filament assembly and organization.
2010,
Pubmed Bowen,
Septin GTPases spatially guide microtubule organization and plus end dynamics in polarizing epithelia.
2011,
Pubmed Brock,
Healing of incisional wounds in the embryonic chick wing bud: characterization of the actin purse-string and demonstration of a requirement for Rho activation.
1996,
Pubmed Brock,
Transcriptional regulation of Profilin during wound closure in Drosophila larvae.
2012,
Pubmed Brooks,
In vivo investigation of cilia structure and function using Xenopus.
2015,
Pubmed
,
Xenbase Cordeiro,
The role of transcription-independent damage signals in the initiation of epithelial wound healing.
2013,
Pubmed Davidson,
Embryonic wound healing by apical contraction and ingression in Xenopus laevis.
2002,
Pubmed
,
Xenbase Gong,
Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation.
2004,
Pubmed Haigo,
Shroom induces apical constriction and is required for hingepoint formation during neural tube closure.
2003,
Pubmed
,
Xenbase Hu,
Septin-driven coordination of actin and microtubule remodeling regulates the collateral branching of axons.
2012,
Pubmed Hunter,
Polarized E-cadherin endocytosis directs actomyosin remodeling during embryonic wound repair.
2015,
Pubmed Joo,
Mammalian SEPT2 is required for scaffolding nonmuscle myosin II and its kinases.
2007,
Pubmed Kieserman,
High-magnification in vivo imaging of Xenopus embryos for cell and developmental biology.
2010,
Pubmed
,
Xenbase Kim,
Planar cell polarity acts through septins to control collective cell movement and ciliogenesis.
2010,
Pubmed
,
Xenbase Kinoshita,
Nedd5, a mammalian septin, is a novel cytoskeletal component interacting with actin-based structures.
1997,
Pubmed Kofron,
Plakoglobin is required for maintenance of the cortical actin skeleton in early Xenopus embryos and for cdc42-mediated wound healing.
2002,
Pubmed
,
Xenbase Kremer,
Mammalian septins regulate microtubule stability through interaction with the microtubule-binding protein MAP4.
2005,
Pubmed Lawson,
Surface ectodermal wound healing in the chick embryo.
1998,
Pubmed Lee,
Uncorking gastrulation: the morphogenetic movement of bottle cells.
2012,
Pubmed
,
Xenbase Levayer,
Oscillation and polarity of E-cadherin asymmetries control actomyosin flow patterns during morphogenesis.
2013,
Pubmed Mandato,
Actomyosin transports microtubules and microtubules control actomyosin recruitment during Xenopus oocyte wound healing.
2003,
Pubmed
,
Xenbase Martin,
Actin cables and epidermal movement in embryonic wound healing.
1992,
Pubmed Martin,
Wound healing--aiming for perfect skin regeneration.
1997,
Pubmed Masson,
Identification and molecular characterization of E-MAP-115, a novel microtubule-associated protein predominantly expressed in epithelial cells.
1993,
Pubmed McCluskey,
Analysis of the tissue movements of embryonic wound healing--DiI studies in the limb bud stage mouse embryo.
1995,
Pubmed Megason,
Digitizing life at the level of the cell: high-performance laser-scanning microscopy and image analysis for in toto imaging of development.
2003,
Pubmed Mostowy,
Septins: the fourth component of the cytoskeleton.
2012,
Pubmed Nagata,
Filament formation of MSF-A, a mammalian septin, in human mammary epithelial cells depends on interactions with microtubules.
2003,
Pubmed Nandadasa,
N- and E-cadherins in Xenopus are specifically required in the neural and non-neural ectoderm, respectively, for F-actin assembly and morphogenetic movements.
2009,
Pubmed
,
Xenbase Nishimura,
Planar cell polarity links axes of spatial dynamics in neural-tube closure.
2012,
Pubmed Nölke,
Septins guide microtubule protrusions induced by actin-depolymerizing toxins like Clostridium difficile transferase (CDT).
2016,
Pubmed Sellin,
Mammalian SEPT9 isoforms direct microtubule-dependent arrangements of septin core heteromers.
2012,
Pubmed Shindo,
PCP and septins compartmentalize cortical actomyosin to direct collective cell movement.
2014,
Pubmed
,
Xenbase Shindo,
Coordination of cell polarity during Xenopus gastrulation.
2008,
Pubmed
,
Xenbase Sirajuddin,
Structural insight into filament formation by mammalian septins.
2007,
Pubmed Soto,
Inositol kinase and its product accelerate wound healing by modulating calcium levels, Rho GTPases, and F-actin assembly.
2013,
Pubmed
,
Xenbase Spiliotis,
Regulation of microtubule organization and functions by septin GTPases.
2010,
Pubmed Stanisstreet,
Scanning electron microscopy of wound healing in Xenopus and chicken embryos.
1980,
Pubmed
,
Xenbase Surka,
The mammalian septin MSF localizes with microtubules and is required for completion of cytokinesis.
2002,
Pubmed Suzuki,
Distinct intracellular Ca2+ dynamics regulate apical constriction and differentially contribute to neural tube closure.
2017,
Pubmed
,
Xenbase Wasik,
Septin 7 reduces nonmuscle myosin IIA activity in the SNAP23 complex and hinders GLUT4 storage vesicle docking and fusion.
2017,
Pubmed Weirich,
The septin family of GTPases: architecture and dynamics.
2008,
Pubmed Wühr,
A model for cleavage plane determination in early amphibian and fish embryos.
2010,
Pubmed
,
Xenbase Xie,
The GTP-binding protein Septin 7 is critical for dendrite branching and dendritic-spine morphology.
2007,
Pubmed Yu,
Local mechanical forces promote polarized junctional assembly and axis elongation in Drosophila.
2016,
Pubmed Zallen,
Patterned gene expression directs bipolar planar polarity in Drosophila.
2004,
Pubmed Zulueta-Coarasa,
Automated multidimensional image analysis reveals a role for Abl in embryonic wound repair.
2014,
Pubmed