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Molecular and Cellular Biology, October 1999, p. 6929-6939, Vol. 19, No. 10
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
The Morphogenesis Checkpoint in Saccharomyces
cerevisiae: Cell Cycle Control of Swe1p Degradation by Hsl1p
and Hsl7p
John N.
McMillan,1
Mark S.
Longtine,2
Rey A. L.
Sia,1
Chandra L.
Theesfeld,1
Elaine S. G.
Bardes,1
John R.
Pringle,2 and
Daniel
J.
Lew1,*
Department of Pharmacology and Cancer
Biology, Duke University Medical Center, Durham, North Carolina
27710,1 and Biology Department,
University of North Carolina, Chapel Hill, North Carolina
275992
Received 7 June 1999/Returned for modification 13 July
1999/Accepted 26 July 1999
In Saccharomyces cerevisiae, the Wee1 family kinase
Swe1p is normally stable during G1 and S phases but is
unstable during G2 and M phases due to ubiquitination and
subsequent degradation. However, perturbations of the actin
cytoskeleton lead to a stabilization and accumulation of Swe1p. This
response constitutes part of a morphogenesis checkpoint that couples
cell cycle progression to proper bud formation, but the basis for the
regulation of Swe1p degradation by the morphogenesis checkpoint remains
unknown. Previous studies have identified a protein kinase, Hsl1p, and
a phylogenetically conserved protein of unknown function, Hsl7p, as
putative negative regulators of Swe1p. We report here that Hsl1p and
Hsl7p act in concert to target Swe1p for degradation. Both proteins are
required for Swe1p degradation during the unperturbed cell cycle, and
excess Hsl1p accelerates Swe1p degradation in the G2-M
phase. Hsl1p accumulates periodically during the cell cycle and
promotes the periodic phosphorylation of Hsl7p. Hsl7p can be detected
in a complex with Swe1p in cell lysates, and the overexpression of
Hsl7p or Hsl1p produces an effective override of the G2
arrest imposed by the morphogenesis checkpoint. These findings suggest
that Hsl1p and Hsl7p interact directly with Swe1p to promote its
recognition by the ubiquitination complex, leading ultimately to its destruction.
*
Corresponding author. Mailing address: Department of
Pharmacology and Cancer Biology, Box 3686, Duke University Medical
Center, Durham, NC 27710. Phone: (919) 613-8627. Fax: (919) 613-8642. E-mail: daniel.lew{at}duke.edu.
Molecular and Cellular Biology, October 1999, p. 6929-6939, Vol. 19, No. 10
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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-
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