Home LiteratureArticle Details
PMID: 15998801 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, P.H.S.

A microtubule-dependent zone of active RhoA during cleavage plane specification.

The Journal of cell biology ·Vol. 170 ·No. 1 ·2005-07-04 ·Pages 91-101

Bement WM, Benink HA, von Dassow G

Abstract

Cytokinesis in animal cells results from the assembly and constriction of a circumferential array of actin filaments and myosin-2. Microtubules of the mitotic apparatus determine the position at which the cytokinetic actomyosin array forms, but the molecular mechanisms by which they do so remain unknown. The small GTPase RhoA has previously been implicated in cytokinesis. Using four-dimensional microscopy and a probe for active RhoA, we show that active RhoA concentrates in a precisely bounded zone before cytokinesis and is independent of actin assembly. Cytokinetic RhoA activity zones are common to four echinoderm species, the vertebrate Xenopus laevis, and the highly asymmetric cytokinesis accompanying meiosis. Microtubules direct the formation and placement of the RhoA activity zone, and the zone is repositioned after physical spindle displacement. We conclude that microtubules specify the cytokinetic apparatus via a dynamic zone of local RhoA activity.

MeSH Terms
Actin Cytoskeleton/metabolism Animals Cleavage Stage, Ovum/cytology,physiology Cytokinesis/physiology Embryo, Nonmammalian/cytology,metabolism Female Intracellular Signaling Peptides and Proteins/metabolism Meiosis/physiology Microtubules/metabolism Myosins/metabolism Recombinant Fusion Proteins/genetics,metabolism Sea Urchins Species Specificity Spindle Apparatus/metabolism Starfish Strongylocentrotus purpuratus Xenopus laevis rhoA GTP-Binding Protein/metabolism
Chemicals
Intracellular Signaling Peptides and Proteins Recombinant Fusion Proteins Myosins rhoA GTP-Binding Protein
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Bement William M
Center for Cell Dynamics, Friday Harbor Laboratories, University of Washington, Friday Harbor, WA 98250, USA. [email protected]
Benink Hélène A
von Dassow George
References (39)
39 references, click to expand
  1. Human ECT2 is an exchange factor for Rho GTPases, phosphorylated in G2/M phases, and involved in cytokinesis.
    J Cell Biol. 1999 Nov 29;147(5):921-8 PMID: 10579713
  2. Microtubules continuously dictate distribution of actin filaments and positioning of cell cleavage in grasshopper spermatocytes.
    J Cell Sci. 2004 Mar 15;117(Pt 8):1591-602 PMID: 15020685
  3. CYK-4: A Rho family gtpase activating protein (GAP) required for central spindle formation and cytokinesis.
    J Cell Biol. 2000 Jun 26;149(7):1391-404 PMID: 10871280
  4. The role of Mg2+ cofactor in the guanine nucleotide exchange and GTP hydrolysis reactions of Rho family GTP-binding proteins.
    J Biol Chem. 2000 Aug 18;275(33):25299-307 PMID: 10843989
  5. MgcRacGAP is involved in cytokinesis through associating with mitotic spindle and midbody.
    J Biol Chem. 2001 Feb 23;276(8):5821-8 PMID: 11085985
  6. Contraction and polymerization cooperate to assemble and close actomyosin rings around Xenopus oocyte wounds.
    J Cell Biol. 2001 Aug 20;154(4):785-97 PMID: 11502762
  7. Rho-dependent transfer of Citron-kinase to the cleavage furrow of dividing cells.
    J Cell Sci. 2001 Sep;114(Pt 18):3273-84 PMID: 11591816
  8. Central spindle assembly and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity.
    Dev Cell. 2002 Jan;2(1):41-54 PMID: 11782313
  9. A RhoGEF and Rho family GTPase-activating protein complex links the contractile ring to cortical microtubules at the onset of cytokinesis.
    Dev Cell. 2003 Jan;4(1):29-39 PMID: 12530961
  10. Direct evidence for a critical role of myosin II in budding yeast cytokinesis and the evolvability of new cytokinetic mechanisms in the absence of myosin II.
    Mol Biol Cell. 2003 Feb;14(2):798-809 PMID: 12589071
  11. Centrosome separation and central spindle assembly act in redundant pathways that regulate microtubule density and trigger cleavage furrow formation.
    Dev Cell. 2003 Mar;4(3):333-44 PMID: 12636915
  12. Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor.
    Science. 2003 Mar 14;299(5613):1743-7 PMID: 12637748
  13. Phosphorylation by aurora B converts MgcRacGAP to a RhoGAP during cytokinesis.
    Dev Cell. 2003 Apr;4(4):549-60 PMID: 12689593
  14. Closing the GAP: a role for a RhoA GAP in cytokinesis.
    Mol Cell. 2003 Apr;11(4):846-8 PMID: 12718869
  15. Activity of Rho-family GTPases during cell division as visualized with FRET-based probes.
    J Cell Biol. 2003 Jul 21;162(2):223-32 PMID: 12860967
  16. Working with Xenopus spinal neurons in live cell culture.
    Methods Cell Biol. 2003;71:129-56 PMID: 12884690
  17. Determining the position of the cell division plane.
    Nature. 2003 Aug 28;424(6952):1074-8 PMID: 12904818
  18. p190RhoGAP is cell cycle regulated and affects cytokinesis.
    J Cell Biol. 2003 Nov 10;163(3):571-82 PMID: 14610059
  19. Rho localization in cells and tissues.
    Exp Cell Res. 2004 May 1;295(2):300-14 PMID: 15093731
  20. Formation and function of the polar body contractile ring in Spisula.
    Dev Biol. 2004 May 15;269(2):421-32 PMID: 15110710
  21. Cell type-specific regulation of RhoA activity during cytokinesis.
    J Biol Chem. 2004 Oct 22;279(43):44756-62 PMID: 15308673
  22. Mutations in alpha- and beta-tubulin affect spindle formation in Chinese hamster ovary cells.
    J Cell Biol. 1983 Oct;97(4):1055-61 PMID: 6619186
  23. Simulation testing of mechanisms for inducing the formation of the contractile ring in cytokinesis.
    J Cell Biol. 1989 Nov;109(5):2215-23 PMID: 2808525
  24. A model for astral stimulation of cytokinesis in animal cells.
    J Cell Biol. 1989 Nov;109(5):2225-32 PMID: 2808526
  25. Regulation of cytoplasmic division of Xenopus embryo by rho p21 and its inhibitory GDP/GTP exchange protein (rho GDI).
    J Cell Biol. 1993 Mar;120(5):1187-95 PMID: 8436590
  26. A rho-like protein is involved in the organisation of the contractile ring in dividing sand dollar eggs.
    Zygote. 1993 Nov;1(4):325-31 PMID: 8081830
  27. Translocation of activated Rho from the cytoplasm to membrane ruffling area, cell-cell adhesion sites and cleavage furrows.
    Oncogene. 1995 Jul 6;11(1):39-48 PMID: 7624130
  28. Signals from the spindle midzone are required for the stimulation of cytokinesis in cultured epithelial cells.
    Mol Biol Cell. 1996 Feb;7(2):225-32 PMID: 8688554
  29. A requirement for Rho and Cdc42 during cytokinesis in Xenopus embryos.
    Curr Biol. 1997 Jan 1;7(1):12-23 PMID: 8999996
  30. Myosin II-independent processes in mitotic cells of Dictyostelium discoideum: redistribution of the nuclei, re-arrangement of the actin system and formation of the cleavage furrow.
    J Cell Sci. 1997 Jan;110 ( Pt 2):123-37 PMID: 9044043
  31. Inhibition of myosin light chain kinase by p21-activated kinase.
    Science. 1999 Mar 26;283(5410):2083-5 PMID: 10092231
  32. 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
  33. Cell division without mitotic apparatus in sea urchin eggs.
    Exp Cell Res. 1956 Dec;11(3):630-6 PMID: 13384430
  34. Experiments concerning the cleavage stimulus in sand dollar eggs.
    J Exp Zool. 1961 Oct;148:81-9 PMID: 14490383
  35. AN EXPERIMENTAL ANALYSIS OF UNILATERAL CLEAVAGE IN INVERTEBRATE EGGS.
    J Exp Zool. 1963 Jul;153:99-112 PMID: 14051860
  36. Concentric zones of active RhoA and Cdc42 around single cell wounds.
    J Cell Biol. 2005 Jan 31;168(3):429-39 PMID: 15684032
  37. MgcRacGAP regulates cortical activity through RhoA during cytokinesis.
    Exp Cell Res. 2004 Feb 15;293(2):275-82 PMID: 14729465
  38. Designing biosensors for Rho family proteins--deciphering the dynamics of Rho family GTPase activation in living cells.
    J Cell Sci. 2004 Mar 15;117(Pt 8):1313-8 PMID: 15020671
  39. Microtubule-actomyosin interactions in cortical flow and cytokinesis.
    Cell Motil Cytoskeleton. 2000 Feb;45(2):87-92 PMID: 10658205
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
2005-07-04
Pages
91-101
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2171391
Subset
IM
Grants
NIGMS NIH HHS · P50 GM066050 · United States
NIGMS NIH HHS · R01 GM052932 · United States
NIGMS NIH HHS · GM52932 · United States
NIGMS NIH HHS · GM66050 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]