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PMID: 15699213 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

DRhoGEF2 regulates actin organization and contractility in the Drosophila blastoderm embryo.

The Journal of cell biology ·Vol. 168 ·No. 4 ·2005-02-14 ·Pages 575-85

Padash Barmchi M, Rogers S, Häcker U

Abstract

Morphogenesis of the Drosophila melanogaster embryo is associated with a dynamic reorganization of the actin cytoskeleton that is mediated by small GTPases of the Rho family. Often, Rho1 controls different aspects of cytoskeletal function in parallel, requiring a complex level of regulation. We show that the guanine triphosphate (GTP) exchange factor DRhoGEF2 is apically localized in epithelial cells throughout embryogenesis. We demonstrate that DRhoGEF2, which has previously been shown to regulate cell shape changes during gastrulation, recruits Rho1 to actin rings and regulates actin distribution and actomyosin contractility during nuclear divisions, pole cell formation, and cellularization of syncytial blastoderm embryos. We propose that DRhoGEF2 activity coordinates contractile actomyosin forces throughout morphogenesis in Drosophila by regulating the association of myosin with actin to form contractile cables. Our results support the hypothesis that specific aspects of Rho1 function are regulated by specific GTP exchange factors.

MeSH Terms
Actins/metabolism Actomyosin/physiology Animals Blastoderm/cytology,metabolism Cell Cycle Proteins Cell Division/physiology Cell Polarity/physiology Cell Shape/physiology Cytoskeleton/physiology Drosophila Proteins/metabolism Drosophila melanogaster/embryology,genetics,metabolism Embryo, Nonmammalian/cytology,metabolism Embryonic Development/physiology Microfilament Proteins/metabolism Mutation/genetics rho GTP-Binding Proteins/metabolism
Chemicals
Actins Cell Cycle Proteins Drosophila Proteins Microfilament Proteins bnk protein, Drosophila sav protein, Drosophila Actomyosin rho GTP-Binding Proteins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Padash Barmchi Mojgan
Department of Cell and Molecular Biology, Lund Strategic Research Center for Stem Cell Biology and Cell Therapy, Lund University, BMC B13, 22184 Lund, Sweden.
Rogers Stephen
Häcker Udo
References (41)
41 references, click to expand
  1. Mutations in the Rho1 small GTPase disrupt morphogenesis and segmentation during early Drosophila development.
    Development. 1999 Dec;126(23):5353-64 PMID: 10556060
  2. A putative exchange factor for Rho1 GTPase is required for initiation of cytokinesis in Drosophila.
    Genes Dev. 1999 Sep 1;13(17):2301-14 PMID: 10485851
  3. Genetic analysis demonstrates a direct link between rho signaling and nonmuscle myosin function during Drosophila morphogenesis.
    Genetics. 2000 Jul;155(3):1253-65 PMID: 10880486
  4. Rho-Rho-kinase pathway in smooth muscle contraction and cytoskeletal reorganization of non-muscle cells.
    Trends Pharmacol Sci. 2001 Jan;22(1):32-9 PMID: 11165670
  5. 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
  6. Rac 'n Rho: the music that shapes a developing embryo.
    Dev Cell. 2001 Sep;1(3):321-31 PMID: 11702944
  7. Drosophila myosin phosphatase and its role in dorsal closure.
    Development. 2002 Mar;129(5):1215-23 PMID: 11874917
  8. Rho1 interacts with p120ctn and alpha-catenin, and regulates cadherin-based adherens junction components in Drosophila.
    Development. 2002 Aug;129(16):3771-82 PMID: 12135916
  9. How one becomes many: blastoderm cellularization in Drosophila melanogaster.
    Bioessays. 2002 Nov;24(11):1012-22 PMID: 12386932
  10. Roles of myosin phosphatase during Drosophila development.
    Development. 2003 Feb;130(4):671-81 PMID: 12505998
  11. Phosphorylation of myosin II regulatory light chain is necessary for migration of HeLa cells but not for localization of myosin II at the leading edge.
    Biochem J. 2003 Mar 1;370(Pt 2):551-6 PMID: 12429016
  12. piggyBac-based insertional mutagenesis in the presence of stably integrated P elements in Drosophila.
    Proc Natl Acad Sci U S A. 2003 Jun 24;100(13):7720-5 PMID: 12802016
  13. Balancing different types of actin polymerization at distinct sites: roles for Abelson kinase and Enabled.
    J Cell Biol. 2003 Dec 22;163(6):1267-79 PMID: 14676307
  14. Reassessing the role and dynamics of nonmuscle myosin II during furrow formation in early Drosophila embryos.
    Mol Biol Cell. 2004 Feb;15(2):838-50 PMID: 14657248
  15. Identification of a novel sequence in PDZ-RhoGEF that mediates interaction with the actin cytoskeleton.
    Mol Biol Cell. 2004 Apr;15(4):1760-75 PMID: 14742719
  16. The RhoGEF Pebble is required for cell shape changes during cell migration triggered by the Drosophila FGF receptor Heartless.
    Development. 2004 Jun;131(11):2631-40 PMID: 15128660
  17. The epithelial-mesenchymal transition of the Drosophila mesoderm requires the Rho GTP exchange factor Pebble.
    Development. 2004 Jun;131(11):2641-51 PMID: 15128661
  18. A Rho GTPase signaling pathway is used reiteratively in epithelial folding and potentially selects the outcome of Rho activation.
    Curr Biol. 2004 Oct 26;14(20):1822-6 PMID: 15498489
  19. Drosophila RhoGEF2 associates with microtubule plus ends in an EB1-dependent manner.
    Curr Biol. 2004 Oct 26;14(20):1827-33 PMID: 15498490
  20. Pole cell formation in Drosophila melanogaster.
    Dev Biol. 1980 Mar 15;75(2):419-30 PMID: 6768631
  21. Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis.
    J Cell Sci. 1983 May;61:31-70 PMID: 6411748
  22. The Drosophila gastrulation gene concertina encodes a G alpha-like protein.
    Cell. 1991 Jan 25;64(2):447-58 PMID: 1899050
  23. The pebble gene is required for cytokinesis in Drosophila.
    J Cell Sci. 1992 Dec;103 ( Pt 4):1021-30 PMID: 1487486
  24. bottleneck acts as a regulator of the microfilament network governing cellularization of the Drosophila embryo.
    Cell. 1993 Oct 22;75(2):373-85 PMID: 8402919
  25. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes.
    Development. 1993 Jun;118(2):401-15 PMID: 8223268
  26. The Drosophila peanut gene is required for cytokinesis and encodes a protein similar to yeast putative bud neck filament proteins.
    Cell. 1994 May 6;77(3):371-9 PMID: 8181057
  27. Actin cytoskeleton. Through the bottleneck.
    Curr Biol. 1994 Jan 1;4(1):76-8 PMID: 7922320
  28. Beta heavy-spectrin has a restricted tissue and subcellular distribution during Drosophila embryogenesis.
    Development. 1994 Jul;120(7):2039-50 PMID: 7925008
  29. The nullo protein is a component of the actin-myosin network that mediates cellularization in Drosophila melanogaster embryos.
    J Cell Sci. 1994 Jul;107 ( Pt 7):1863-73 PMID: 7983153
  30. Evidence for engrailed-independent wingless autoregulation in Drosophila.
    Dev Biol. 1995 Aug;170(2):636-50 PMID: 7649390
  31. Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex.
    J Cell Biol. 1995 Oct;131(1):165-78 PMID: 7559773
  32. Septins may form a ubiquitous family of cytoskeletal filaments.
    J Cell Biol. 1996 Sep;134(6):1345-8 PMID: 8830765
  33. The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster.
    Genetics. 1996 Dec;144(4):1673-9 PMID: 8978054
  34. Caenorhabditis elegans LET-502 is related to Rho-binding kinases and human myotonic dystrophy kinase and interacts genetically with a homolog of the regulatory subunit of smooth muscle myosin phosphatase to affect cell shape.
    Genes Dev. 1997 Feb 15;11(4):409-22 PMID: 9042856
  35. The role of RhoA in tissue polarity and Frizzled signalling.
    Nature. 1997 May 15;387(6630):292-5 PMID: 9153394
  36. Rho GTPases and signaling networks.
    Genes Dev. 1997 Sep 15;11(18):2295-322 PMID: 9308960
  37. The Rho GTPase and a putative RhoGEF mediate a signaling pathway for the cell shape changes in Drosophila gastrulation.
    Cell. 1997 Dec 26;91(7):905-15 PMID: 9428514
  38. DRhoGEF2 encodes a member of the Dbl family of oncogenes and controls cell shape changes during gastrulation in Drosophila.
    Genes Dev. 1998 Jan 15;12(2):274-84 PMID: 9436986
  39. Cellularization in Drosophila melanogaster is disrupted by the inhibition of rho activity and the activation of Cdc42 function.
    Dev Biol. 1998 Dec 1;204(1):151-64 PMID: 9851849
  40. 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
  41. Functional analysis of the Drosophila diaphanous FH protein in early embryonic development.
    Development. 2000 May;127(9):1887-97 PMID: 10751177
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
2005-02-14
Epub
2005-00-07
Pages
575-85
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2171764
Subset
IM
Grants
NIGMS NIH HHS · F32 GM064966 · United States
NIGMS NIH HHS · 5F32GM064966 · United States
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