Human Bubr1 Is a Mitotic Checkpoint Kinase That Monitors Cenp-E Functions at Kinetochores and Binds the Cyclosome/APC

doi:10.1083/jcb.146.5.941

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© The Rockefeller University Press, 0021-9525/1999//941 $5.00
The Journal of Cell Biology, Volume 146, Number 5, , 1999 941-954

Original Article

Human Bubr1 Is a Mitotic Checkpoint Kinase That Monitors Cenp-E Functions at Kinetochores and Binds the Cyclosome/APC

G.K.T. Chan^a, S.A. Jablonski^a, V. Sudakin^a, J.C. Hittle^a, and T.J. Yen^a

^a Institute for Cancer Research, Fox Chase Cancer Center, Philadelphia, Pennsylvania 19111
Fox Chase Cancer Center, 7701 Burholme Avenue, Philadelphia, PA 19111.(215) 728-2412(215) 728-2590

TJ_Yen{at}fccc.edu

Human cells express two kinases that are related to the yeastmitotic checkpoint kinase BUB1. hBUB1 and hBUBR1 bind to kinetochoreswhere they are postulated to be components of the mitotic checkpointthat monitors kinetochore activities to determine if chromosomeshave achieved alignment at the spindle equator (Jablonski, S.A.,G.K.T. Chan, C.A. Cooke, W.C. Earnshaw, and T.J. Yen. 1998.Chromosoma. 107:386–396). In support of this, hBUB1 andthe homologous mouse BUB1 have been shown to be important forthe mitotic checkpoint (Cahill, D.P., C. Lengauer, J. Yu, G.J.Riggins, J.K. Willson, S.D. Markowitz, K.W. Kinzler, and B.Vogelstein. 1998. Nature. 392:300–303; Taylor, S.S., andF. McKeon. 1997. Cell. 89:727–735). We now demonstratethat hBUBR1 is also an essential component of the mitotic checkpoint.hBUBR1 is required by cells that are exposed to microtubuleinhibitors to arrest in mitosis. Additionally, hBUBR1 is essentialfor normal mitotic progression as it prevents cells from prematurelyentering anaphase. We establish that one of hBUBR1's checkpointfunctions is to monitor kinetochore activities that depend onthe kinetochore motor CENP-E. hBUBR1 is expressed throughoutthe cell cycle, but its kinase activity is detected after cellshave entered mitosis. hBUBR1 kinase activity was rapidly stimulatedwhen the spindle was disrupted in mitotic cells. Finally, hBUBR1was associated with the cyclosome/anaphase-promoting complex(APC) in mitotically arrested cells but not in interphase cells.The combined data indicate that hBUBR1 can potentially providetwo checkpoint functions by monitoring CENP-E–dependentactivities at the kinetochore and regulating cyclosome/APC activity.

Key Words: kinetochore • hBUBR1 • mitotic checkpoint •anaphase-promoting complex • CENP-E

1.used in this paper: ACA, anticentromere autoimmune antibodies;APC, anaphase-promoting complex; CENP-E, centromere proteinE; DAPI, 4',6-diamidino-2-phenylindole

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