Abstract
Wee1, the inhibitory kinase of cyclin B/Cdc2, undergoes a phosphorylation-dependent catalytic inactivation at M phase of the mitotic cell cycle, but the precise mechanism for this inactivation is not known. Using Xenopus egg and extract systems, we show here that the kinase activity of Xenopus somatic Wee1 (XeWee1B) is regulated by its N-terminal, small, well conserved region, termed here the Wee-box. The Wee-box is essential for the normal kinase activity of XeWee1B during interphase, acting positively on the C-terminal catalytic domain, which alone cannot efficiently phosphorylate Cdc2. Significantly, a Thr-186-Pro (TP) motif within the Wee-box is phosphorylated by Cdc2 at M phase and specifically binds the cis/trans prolyl isomerase Pin1. This Pin1 binding is required for the inactivation of XeWee1B at M phase, presumably causing isomerization of the phospho-TP motif and thereby impairing the function of the Wee-box. These results provide important insights into the mechanism of Wee1 inactivation at M phase.
MeSH Terms
Amino Acid Motifs
Amino Acid Sequence
Animals
Catalytic Domain
Cell Cycle Proteins/genetics,metabolism
Cell Division
Gene Expression Regulation
Insecta
Mitosis
Molecular Sequence Data
NIMA-Interacting Peptidylprolyl Isomerase
Oocytes/metabolism
Peptidylprolyl Isomerase/metabolism
Phosphorylation
Protein Binding
Protein-Tyrosine Kinases/genetics,metabolism
Xenopus
Xenopus Proteins/genetics,metabolism
Chemicals
Cell Cycle Proteins
NIMA-Interacting Peptidylprolyl Isomerase
Xenopus Proteins
Wee2 protein, Xenopus
Protein-Tyrosine Kinases
Peptidylprolyl Isomerase
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Okamoto Kengo
Department of Biology, Graduate School of Sciences, Kyushu University, Hakozaki 6-10-1, Fukuoka 812-8581, Japan.
Sagata Noriyuki
References (29)
29 references, click to expand
-
The existence of two distinct Wee1 isoforms in Xenopus: implications for the developmental regulation of the cell cycle.
EMBO J. 2002 May 15;21(10):2472-84
PMID: 12006499
-
New pathways from PKA to the Cdc2/cyclin B complex in oocytes: Wee1B as a potential PKA substrate.
Cell Cycle. 2006 Feb;5(3):227-31
PMID: 16418576
-
A signalling pathway controlling c-Myc degradation that impacts oncogenic transformation of human cells.
Nat Cell Biol. 2004 Apr;6(4):308-18
PMID: 15048125
-
M-phase kinases induce phospho-dependent ubiquitination of somatic Wee1 by SCFbeta-TrCP.
Proc Natl Acad Sci U S A. 2004 Mar 30;101(13):4419-24
PMID: 15070733
-
Pinning down cell signaling, cancer and Alzheimer's disease.
Trends Biochem Sci. 2004 Apr;29(4):200-9
PMID: 15082314
-
Chk1, but not Chk2, inhibits Cdc25 phosphatases by a novel common mechanism.
EMBO J. 2004 Aug 18;23(16):3386-96
PMID: 15272308
-
The protein kinase family: conserved features and deduced phylogeny of the catalytic domains.
Science. 1988 Jul 1;241(4861):42-52
PMID: 3291115
-
Cell cycle extracts.
Methods Cell Biol. 1991;36:581-605
PMID: 1839804
-
Phosphorylation and inactivation of the mitotic inhibitor Wee1 by the nim1/cdr1 kinase.
Nature. 1993 Jun 24;363(6431):736-8
PMID: 8515817
-
Nim1 kinase promotes mitosis by inactivating Wee1 tyrosine kinase.
Nature. 1993 Jun 24;363(6431):738-41
PMID: 8515818
-
Two distinct mechanisms for negative regulation of the Wee1 protein kinase.
EMBO J. 1993 Sep;12(9):3427-36
PMID: 7504624
-
Principles of CDK regulation.
Nature. 1995 Mar 9;374(6518):131-4
PMID: 7877684
-
Cdc2 regulatory factors.
Curr Opin Cell Biol. 1994 Dec;6(6):877-82
PMID: 7880537
-
Regulation of the human WEE1Hu CDK tyrosine 15-kinase during the cell cycle.
EMBO J. 1995 May 1;14(9):1878-91
PMID: 7743995
-
Cell cycle regulation of a Xenopus Wee1-like kinase.
Mol Biol Cell. 1995 Jan;6(1):119-34
PMID: 7749193
-
Cell cycle regulation of human WEE1.
EMBO J. 1995 May 15;14(10):2166-75
PMID: 7774574
-
Regulation of Schizosaccharomyces pombe Wee1 tyrosine kinase.
J Biol Chem. 1997 May 16;272(20):13320-5
PMID: 9148953
-
The essential mitotic peptidyl-prolyl isomerase Pin1 binds and regulates mitosis-specific phosphoproteins.
Genes Dev. 1998 Mar 1;12(5):706-20
PMID: 9499405
-
Control of Swe1p degradation by the morphogenesis checkpoint.
EMBO J. 1998 Nov 16;17(22):6678-88
PMID: 9822611
-
The Polo-like kinase Plx1 interacts with and inhibits Myt1 after fertilization of Xenopus eggs.
EMBO J. 2005 Mar 9;24(5):1057-67
PMID: 15692562
-
Structure and inhibition of the human cell cycle checkpoint kinase, Wee1A kinase: an atypical tyrosine kinase with a key role in CDK1 regulation.
Structure. 2005 Apr;13(4):541-50
PMID: 15837193
-
Phosphorylation-specific prolyl isomerization: is there an underlying theme?
Nat Cell Biol. 2005 May;7(5):435-41
PMID: 15867923
-
Concerted mechanism of Swe1/Wee1 regulation by multiple kinases in budding yeast.
EMBO J. 2005 Jun 15;24(12):2194-204
PMID: 15920482
-
Akt/protein kinase B-dependent phosphorylation and inactivation of WEE1Hu promote cell cycle progression at G2/M transition.
Mol Cell Biol. 2005 Jul;25(13):5725-37
PMID: 15964826
-
Cdk1-dependent regulation of the mitotic inhibitor Wee1.
Cell. 2005 Aug 12;122(3):407-20
PMID: 16096060
-
Cyclin-dependent kinase (CDK) phosphorylation destabilizes somatic Wee1 via multiple pathways.
Proc Natl Acad Sci U S A. 2005 Aug 16;102(33):11663-8
PMID: 16085715
-
Systems-level dissection of the cell-cycle oscillator: bypassing positive feedback produces damped oscillations.
Cell. 2005 Aug 26;122(4):565-78
PMID: 16122424
-
Multisite M-phase phosphorylation of Xenopus Wee1A.
Mol Cell Biol. 2005 Dec;25(23):10580-90
PMID: 16287869
-
Wee1-dependent mechanisms required for coordination of cell growth and cell division.
J Cell Sci. 2003 Dec 15;116(Pt 24):4883-90
PMID: 14625382