Checkpoint inhibition of the APC/C in HeLa cells is mediated by a complex of BUBR1, BUB3, CDC20, and MAD2

doi:10.1083/jcb.200102093

Published 3 September 2001. doi:10.1083/jcb.200102093

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© The Rockefeller University Press, 0021-9525/2001/9/925 $5.00
The Journal of Cell Biology, Volume 154, Number 5, September 3, 2001 925-936

Article

Checkpoint inhibition of the APC/C in HeLa cells is mediated by a complex of BUBR1, BUB3, CDC20, and MAD2

Valery Sudakin, Gordon K.T. Chan and Tim J. Yen

Institute for Cancer Research, The Fox Chase Cancer Center, Philadelphia, PA 19111

Address correspondence to Tim Yen, Institute for Cancer Research, The Fox Chase Cancer Center, 7701 Burholme Ave., Philadelphia, PA 19111. Tel.: (215) 728-2590. Fax: (215) 728-2412. E-mail: tj_yen{at}fccc.edu

The mitotic checkpoint prevents cells with unaligned chromosomesfrom prematurely exiting mitosis by inhibiting the anaphase-promotingcomplex/cyclosome (APC/C) from targeting key proteins for ubiquitin-mediatedproteolysis. We have examined the mechanism by which the checkpointinhibits the APC/C by purifying an APC/C inhibitory factor fromHeLa cells. We call this factor the mitotic checkpoint complex(MCC) as it consists of hBUBR1, hBUB3, CDC20, and MAD2 checkpointproteins in near equal stoichiometry. MCC inhibitory activityis 3,000-fold greater than that of recombinant MAD2, which hasalso been shown to inhibit APC/C in vitro. Surprisingly, MCCis not generated from kinetochores, as it is also present andactive in interphase cells. However, only APC/C isolated frommitotic cells was sensitive to inhibition by MCC. We found thatthe majority of the APC/C in mitotic lysates is associated withthe MCC, and this likely contributes to the lag in ubiquitinligase activity. Importantly, chromosomes can suppress the reactivationof APC/C. Chromosomes did not affect the inhibitory activityof MCC or the stimulatory activity of CDC20. We propose thatthe preformed interphase pool of MCC allows for rapid inhibitionof APC/C when cells enter mitosis. Unattached kinetochores thentarget the APC/C for sustained inhibition by the MCC.

Key Words: kinetochore; hBUBR1; anaphase promoting complex; MAD2; mitotic checkpoint

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