Home LiteratureArticle Details
PMID: 12719470 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores.

The Journal of cell biology ·Vol. 161 ·No. 2 ·2003-04-28 ·Pages 267-80

Ditchfield C, Johnson VL, Tighe A, Ellston R, Haworth C, Johnson T, Mortlock A, Keen N, Taylor SS

Abstract

The Aurora/Ipl1 family of protein kinases plays multiple roles in mitosis and cytokinesis. Here, we describe ZM447439, a novel selective Aurora kinase inhibitor. Cells treated with ZM447439 progress through interphase, enter mitosis normally, and assemble bipolar spindles. However, chromosome alignment, segregation, and cytokinesis all fail. Despite the presence of maloriented chromosomes, ZM447439-treated cells exit mitosis with normal kinetics, indicating that the spindle checkpoint is compromised. Indeed, ZM447439 prevents mitotic arrest after exposure to paclitaxel. RNA interference experiments suggest that these phenotypes are due to inhibition of Aurora B, not Aurora A or some other kinase. In the absence of Aurora B function, kinetochore localization of the spindle checkpoint components BubR1, Mad2, and Cenp-E is diminished. Furthermore, inhibition of Aurora B kinase activity prevents the rebinding of BubR1 to metaphase kinetochores after a reduction in centromeric tension. Aurora B kinase activity is also required for phosphorylation of BubR1 on entry into mitosis. Finally, we show that BubR1 is not only required for spindle checkpoint function, but is also required for chromosome alignment. Together, these results suggest that by targeting checkpoint proteins to kinetochores, Aurora B couples chromosome alignment with anaphase onset.

MeSH Terms
Anaphase/drug effects,genetics Aurora Kinase B Aurora Kinases Benzamides/pharmacology Calcium-Binding Proteins/genetics,metabolism Cell Cycle Proteins Chromosomal Proteins, Non-Histone/genetics,metabolism Chromosome Segregation/drug effects,genetics DNA Replication/drug effects,genetics Enzyme Inhibitors/pharmacology Eukaryotic Cells/drug effects,enzymology,ultrastructure Genes, cdc/drug effects HeLa Cells Humans Kinetochores/drug effects,metabolism Mad2 Proteins Mitosis/drug effects,genetics Paclitaxel/pharmacology Phosphorylation/drug effects Protein Kinases/genetics,metabolism Protein Serine-Threonine Kinases/antagonists & inhibitors,genetics Quinazolines/pharmacology Repressor Proteins/drug effects,genetics Spindle Apparatus/drug effects,genetics Tumor Suppressor Protein p53/drug effects,genetics
Chemicals
4-(4-(N-benzoylamino)anilino)-6-methoxy-7-(3-(1-morpholino)propoxy)quinazoline Benzamides Calcium-Binding Proteins Cell Cycle Proteins Chromosomal Proteins, Non-Histone Enzyme Inhibitors MAD2L1 protein, human Mad2 Proteins Quinazolines Repressor Proteins Tumor Suppressor Protein p53 centromere protein E Protein Kinases AURKB protein, human Aurora Kinase B Aurora Kinases BUB1 protein, human Bub1 spindle checkpoint protein Protein Serine-Threonine Kinases Paclitaxel
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Ditchfield Claire
School of Biological Sciences, University of Manchester, 2.205 Stopford Building, Oxford Rd., Manchester M13 9PT, UK.
Johnson Victoria L
Tighe Anthony
Ellston Rebecca
Haworth Carolyn
Johnson Trevor
Mortlock Andrew
Keen Nicholas
Taylor Stephen S
References (35)
35 references, click to expand
  1. Inhibition of Src kinases by a selective tyrosine kinase inhibitor causes mitotic arrest.
    Cancer Res. 1999 Dec 15;59(24):6145-52 PMID: 10626805
  2. Human BUBR1 is a mitotic checkpoint kinase that monitors CENP-E functions at kinetochores and binds the cyclosome/APC.
    J Cell Biol. 1999 Sep 6;146(5):941-54 PMID: 10477750
  3. Evidence that the Ipl1-Sli15 (Aurora kinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections.
    Cell. 2002 Feb 8;108(3):317-29 PMID: 11853667
  4. The kinase activity of aurora B is required for kinetochore-microtubule interactions during mitosis.
    Curr Biol. 2002 Jun 4;12(11):894-9 PMID: 12062052
  5. Inhibition of aurora B kinase blocks chromosome segregation, overrides the spindle checkpoint, and perturbs microtubule dynamics in mitosis.
    Curr Biol. 2002 Jun 4;12(11):900-5 PMID: 12062053
  6. Mitogen-activated protein kinase kinase activity is required for the G(2)/M transition of the cell cycle in mammalian fibroblasts.
    Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11335-40 PMID: 10500177
  7. The Aurora/Ipl1p kinase family: regulators of chromosome segregation and cytokinesis.
    Trends Cell Biol. 1999 Nov;9(11):454-9 PMID: 10511710
  8. Aurora/Ipl1p-related kinases, a new oncogenic family of mitotic serine-threonine kinases.
    J Cell Sci. 1999 Nov;112 ( Pt 21):3591-601 PMID: 10523496
  9. CENP-E forms a link between attachment of spindle microtubules to kinetochores and the mitotic checkpoint.
    Nat Cell Biol. 2000 Aug;2(8):484-91 PMID: 10934468
  10. Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes.
    Cell. 2000 Aug 4;102(3):279-91 PMID: 10975519
  11. Chromosomal passengers and the (aurora) ABCs of mitosis.
    Trends Cell Biol. 2001 Feb;11(2):49-54 PMID: 11166196
  12. Mammalian mad2 and bub1/bubR1 recognize distinct spindle-attachment and kinetochore-tension checkpoints.
    Proc Natl Acad Sci U S A. 2001 Apr 10;98(8):4492-7 PMID: 11274370
  13. Essential roles of Drosophila inner centromere protein (INCENP) and aurora B in histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction, and chromosome segregation.
    J Cell Biol. 2001 May 14;153(4):865-80 PMID: 11352945
  14. Tetraploid state induces p53-dependent arrest of nontransformed mammalian cells in G1.
    Mol Biol Cell. 2001 May;12(5):1315-28 PMID: 11359924
  15. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells.
    Nature. 2001 May 24;411(6836):494-8 PMID: 11373684
  16. Mitotic kinases as regulators of cell division and its checkpoints.
    Nat Rev Mol Cell Biol. 2001 Jan;2(1):21-32 PMID: 11413462
  17. Human INCENP colocalizes with the Aurora-B/AIRK2 kinase on chromosomes and is overexpressed in tumour cells.
    Chromosoma. 2001 May;110(2):65-74 PMID: 11453556
  18. Bir1/Cut17 moving from chromosome to spindle upon the loss of cohesion is required for condensation, spindle elongation and repair.
    Genes Cells. 2001 Sep;6(9):743-63 PMID: 11554922
  19. The budding yeast protein kinase Ipl1/Aurora allows the absence of tension to activate the spindle checkpoint.
    Genes Dev. 2001 Dec 1;15(23):3118-29 PMID: 11731476
  20. Aurora-A kinase is required for centrosome maturation in Caenorhabditis elegans.
    J Cell Biol. 2001 Dec 24;155(7):1109-16 PMID: 11748251
  21. Kinetochore localisation and phosphorylation of the mitotic checkpoint components Bub1 and BubR1 are differentially regulated by spindle events in human cells.
    J Cell Sci. 2001 Dec;114(Pt 24):4385-95 PMID: 11792804
  22. The spindle checkpoint: structural insights into dynamic signalling.
    Nat Rev Mol Cell Biol. 2002 Oct;3(10):731-41 PMID: 12360190
  23. Mad2 and BubR1 function in a single checkpoint pathway that responds to a loss of tension.
    Mol Biol Cell. 2002 Oct;13(10):3706-19 PMID: 12388768
  24. Chromosome micromanipulation. 3. Spindle fiber tension and the reorientation of mal-oriented chromosomes.
    J Cell Biol. 1969 Oct;43(1):40-50 PMID: 5824068
  25. The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by an inhibitory signal produced by unattached kinetochores.
    J Cell Biol. 1995 Aug;130(4):941-8 PMID: 7642709
  26. How cells get the right chromosomes.
    Science. 1997 Jan 31;275(5300):632-7 PMID: 9005842
  27. Kinetochore localization of murine Bub1 is required for normal mitotic timing and checkpoint response to spindle damage.
    Cell. 1997 May 30;89(5):727-35 PMID: 9182760
  28. AIM-1: a mammalian midbody-associated protein required for cytokinesis.
    EMBO J. 1998 Feb 2;17(3):667-76 PMID: 9450992
  29. A homologue of Drosophila aurora kinase is oncogenic and amplified in human colorectal cancers.
    EMBO J. 1998 Jun 1;17(11):3052-65 PMID: 9606188
  30. Localization of Mad2 to kinetochores depends on microtubule attachment, not tension.
    J Cell Biol. 1998 Jun 1;141(5):1181-91 PMID: 9606210
  31. The vertebrate cell kinetochore and its roles during mitosis.
    Trends Cell Biol. 1998 Aug;8(8):310-8 PMID: 9704407
  32. Tumour amplified kinase STK15/BTAK induces centrosome amplification, aneuploidy and transformation.
    Nat Genet. 1998 Oct;20(2):189-93 PMID: 9771714
  33. Multinuclearity and increased ploidy caused by overexpression of the aurora- and Ipl1-like midbody-associated protein mitotic kinase in human cancer cells.
    Cancer Res. 1998 Nov 1;58(21):4811-6 PMID: 9809983
  34. The conserved protein kinase Ipl1 regulates microtubule binding to kinetochores in budding yeast.
    Genes Dev. 1999 Mar 1;13(5):532-44 PMID: 10072382
  35. Aurora-A overexpression reveals tetraploidization as a major route to centrosome amplification in p53-/- cells.
    EMBO J. 2002 Feb 15;21(4):483-92 PMID: 11847097
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
2003-04-28
Pages
267-80
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2172902
Subset
IM
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: product@genelibs.com