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PMID: 18337466 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Apical accumulation of Rho in the neural plate is important for neural plate cell shape change and neural tube formation.

Molecular biology of the cell ·Vol. 19 ·No. 5 ·2008-05-00 ·Pages 2289-99

Kinoshita N, Sasai N, Misaki K, Yonemura S

Abstract

Although Rho-GTPases are well-known regulators of cytoskeletal reorganization, their in vivo distribution and physiological functions have remained elusive. In this study, we found marked apical accumulation of Rho in developing chick embryos undergoing folding of the neural plate during neural tube formation, with similar accumulation of activated myosin II. The timing of accumulation and biochemical activation of both Rho and myosin II was coincident with the dynamics of neural tube formation. Inhibition of Rho disrupted its apical accumulation and led to defects in neural tube formation, with abnormal morphology of the neural plate. Continuous activation of Rho also altered neural tube formation. These results indicate that correct spatiotemporal regulation of Rho is essential for neural tube morphogenesis. Furthermore, we found that a key morphogenetic signaling pathway, the Wnt/PCP pathway, was implicated in the apical accumulation of Rho and regulation of cell shape in the neural plate, suggesting that this signal may be the spatiotemporal regulator of Rho in neural tube formation.

MeSH Terms
Actomyosin/metabolism Animals Cell Adhesion Cell Polarity Cell Shape Chick Embryo Embryo, Nonmammalian/cytology,ultrastructure Enzyme Activation Myosin Type II/metabolism Neural Plate/cytology,embryology,enzymology,ultrastructure Neural Tube/cytology,embryology,enzymology,ultrastructure Neurulation Protein Transport Wnt Proteins/metabolism Xenopus/embryology rho GTP-Binding Proteins/metabolism
Chemicals
Wnt Proteins Actomyosin Myosin Type II rho GTP-Binding Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Kinoshita Nagatoki
Electron Microscope Laboratory and Organogenesis and Neurogenesis Group, RIKEN Center for Developmental Biology, Kobe 650-0047, Japan.
Sasai Noriaki
Misaki Kazuyo
Yonemura Shigenobu
References (45)
45 references, click to expand
  1. Rac1 is required for the formation of three germ layers during gastrulation.
    Oncogene. 1998 Dec 31;17(26):3427-33 PMID: 10030666
  2. Rho localization in cells and tissues.
    Exp Cell Res. 2004 May 1;295(2):300-14 PMID: 15093731
  3. An early marker of axial pattern in the chick embryo and its respecification by retinoic acid.
    Development. 1992 Apr;114(4):841-52 PMID: 1352239
  4. Shroom regulates epithelial cell shape via the apical positioning of an actomyosin network.
    J Cell Sci. 2005 Nov 15;118(Pt 22):5191-203 PMID: 16249236
  5. Convergent extension, planar-cell-polarity signalling and initiation of mouse neural tube closure.
    Development. 2007 Feb;134(4):789-99 PMID: 17229766
  6. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications.
    Nat Biotechnol. 2002 Jan;20(1):87-90 PMID: 11753368
  7. Neurulation: coming to closure.
    Trends Neurosci. 1997 Nov;20(11):510-7 PMID: 9364665
  8. ADP-ribosylation of rho p21 inhibits lysophosphatidic acid-induced protein tyrosine phosphorylation and phosphatidylinositol 3-kinase activation in cultured Swiss 3T3 cells.
    J Biol Chem. 1993 Nov 25;268(33):24535-8 PMID: 8227009
  9. Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation.
    Nature. 2004 Jun 10;429(6992):667-71 PMID: 15190355
  10. Non-canonical Wnt signalling and regulation of gastrulation movements.
    Semin Cell Dev Biol. 2002 Jun;13(3):251-60 PMID: 12137734
  11. Cdc42 is required for PIP(2)-induced actin polymerization and early development but not for cell viability.
    Curr Biol. 2000 Jun 29;10(13):758-65 PMID: 10898977
  12. Rho as a regulator of the cytoskeleton.
    Trends Biochem Sci. 1995 Jun;20(6):227-31 PMID: 7543224
  13. Rho kinases play an obligatory role in vertebrate embryonic organogenesis.
    Development. 2001 Aug;128(15):2953-62 PMID: 11532918
  14. Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton.
    Cell. 2001 Apr 6;105(1):81-91 PMID: 11301004
  15. Exoenzyme Tat-C3 inhibits association of zymosan particles, phagocytosis, adhesion, and complement binding in macrophage cells.
    Mol Cells. 2003 Oct 31;16(2):216-23 PMID: 14651264
  16. BMP4 induces EMT and Rho GTPase activation in human ovarian cancer cells.
    Carcinogenesis. 2007 Jun;28(6):1153-62 PMID: 17272306
  17. PAK and other Rho-associated kinases--effectors with surprisingly diverse mechanisms of regulation.
    Biochem J. 2005 Mar 1;386(Pt 2):201-14 PMID: 15548136
  18. Rho GTPases and signaling networks.
    Genes Dev. 1997 Sep 15;11(18):2295-322 PMID: 9308960
  19. Neural tube closure requires Dishevelled-dependent convergent extension of the midline.
    Development. 2002 Dec;129(24):5815-25 PMID: 12421719
  20. ROCK-I regulates closure of the eyelids and ventral body wall by inducing assembly of actomyosin bundles.
    J Cell Biol. 2005 Mar 14;168(6):941-53 PMID: 15753128
  21. Rhotekin, a new putative target for Rho bearing homology to a serine/threonine kinase, PKN, and rhophilin in the rho-binding domain.
    J Biol Chem. 1996 Jun 7;271(23):13556-60 PMID: 8662891
  22. Neural tube defects and abnormal brain development in F52-deficient mice.
    Proc Natl Acad Sci U S A. 1996 Mar 5;93(5):2110-5 PMID: 8700893
  23. Shroom, a PDZ domain-containing actin-binding protein, is required for neural tube morphogenesis in mice.
    Cell. 1999 Nov 24;99(5):485-97 PMID: 10589677
  24. A reexamination of the role of microfilaments in neurulation in the chick embryo.
    Anat Rec. 1988 Jan;220(1):87-102 PMID: 3348489
  25. Xenopus Zic-related-1 and Sox-2, two factors induced by chordin, have distinct activities in the initiation of neural induction.
    Development. 1998 Feb;125(4):579-87 PMID: 9435279
  26. Mena is required for neurulation and commissure formation.
    Neuron. 1999 Feb;22(2):313-25 PMID: 10069337
  27. Efficient selection for high-expression transfectants with a novel eukaryotic vector.
    Gene. 1991 Dec 15;108(2):193-9 PMID: 1660837
  28. Analysis of Dishevelled signalling pathways during Xenopus development.
    Curr Biol. 1996 Nov 1;6(11):1456-67 PMID: 8939601
  29. Shroom induces apical constriction and is required for hingepoint formation during neural tube closure.
    Curr Biol. 2003 Dec 16;13(24):2125-37 PMID: 14680628
  30. Multiplicity of the interactions of Wnt proteins and their receptors.
    Cell Signal. 2007 Apr;19(4):659-71 PMID: 17188462
  31. The adhesion signaling molecule p190 RhoGAP is required for morphogenetic processes in neural development.
    Development. 2000 Nov;127(22):4891-903 PMID: 11044403
  32. Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daam1.
    Cell. 2001 Dec 28;107(7):843-54 PMID: 11779461
  33. Dishevelled genes mediate a conserved mammalian PCP pathway to regulate convergent extension during neurulation.
    Development. 2006 May;133(9):1767-78 PMID: 16571627
  34. Early subdivisions in the neural plate define distinct competence for inductive signals.
    Development. 2002 Jan;129(1):83-93 PMID: 11782403
  35. Possible existence of common internalization mechanisms among arginine-rich peptides.
    J Biol Chem. 2002 Jan 25;277(4):2437-43 PMID: 11711547
  36. Planar cell polarity signalling couples cell division and morphogenesis during neurulation.
    Nature. 2006 Jan 12;439(7073):220-4 PMID: 16407953
  37. Vinculin knockout results in heart and brain defects during embryonic development.
    Development. 1998 Jan;125(2):327-37 PMID: 9486805
  38. Rho GTPases: biochemistry and biology.
    Annu Rev Cell Dev Biol. 2005;21:247-69 PMID: 16212495
  39. Role of frizzled 7 in the regulation of convergent extension movements during gastrulation in Xenopus laevis.
    Development. 2000 Jul;127(14):3091-100 PMID: 10862746
  40. Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway.
    Development. 2000 May;127(10):2227-38 PMID: 10769246
  41. Coactivation of Rac and Rho by Wnt/Frizzled signaling is required for vertebrate gastrulation.
    Genes Dev. 2003 Jan 15;17(2):295-309 PMID: 12533515
  42. A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling.
    Dev Cell. 2003 Sep;5(3):367-77 PMID: 12967557
  43. Regulation of ephexin1, a guanine nucleotide exchange factor of Rho family GTPases, by fibroblast growth factor receptor-mediated tyrosine phosphorylation.
    J Biol Chem. 2007 Oct 19;282(42):31103-12 PMID: 17702745
  44. Direct interaction of Rnd1 with FRS2 beta regulates Rnd1-induced down-regulation of RhoA activity and is involved in fibroblast growth factor-induced neurite outgrowth in PC12 cells.
    J Biol Chem. 2005 May 6;280(18):18418-24 PMID: 15738000
  45. Participation of small GTPases in dorsal closure of the Drosophila embryo: distinct roles for Rho subfamily proteins in epithelial morphogenesis.
    J Cell Sci. 1999 Feb;112 ( Pt 3):273-84 PMID: 9885281
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1939-4586
Published
2008-05-00
Epub
2008-00-12
Pages
2289-99
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC2366863
Subset
IM
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