Abstract
CPEB, a cytoplasmic polyadenylation element-binding protein, plays an important role in translational control of maternal mRNAs in early animal development. During Xenopus oocyte maturation, CPEB undergoes a Cdc2-mediated phosphorylation- and ubiquitin-dependent degradation that is required for proper entry into meiosis II. However, the precise mechanism of CPEB degradation, including the identity of the responsible E3 ubiquitin ligase, is not known. Here, we show that the SCF(beta-TrCP) E3 ubiquitin ligase complex targets CPEB for degradation during Xenopus oocyte maturation. beta-TrCP, the F-box protein of SCF(beta-TrCP), specifically binds to a sequence (190)TSGFSS(195) (termed here the TSG motif) of CPEB, thereby targeting CPEB for degradation. beta-TrCP binding depends on phosphorylation of Thr-190, Ser-191, and Ser-195 in the TSG motif. Among these residues, Ser-191 is phosphorylated by the Polo-like kinase Plx1, which binds CPEB at a specific Thr-125 residue prephosphorylated by Cdc2. Finally, Cdc2-mediated phosphorylation of other multiple Ser residues, previously implicated in CPEB degradation, is required for both Thr-125 phosphorylation and beta-TrCP binding, presumably causing conformational changes of CPEB. We propose that Cdc2 and Plx1 sequentially phosphorylate CPEB and target it for SCF(beta-TrCP)-dependent degradation in Xenopus oocytes. We suggest that many other proteins carrying the TSG-like motif may be targeted by SCF(beta-TrCP).
MeSH Terms
Amino Acid Sequence
Animals
Binding Sites
Hydrolysis
Molecular Sequence Data
Oocytes/cytology
Phosphorylation
SKP Cullin F-Box Protein Ligases/metabolism
Transcription Factors/chemistry,metabolism
Xenopus
Xenopus Proteins/chemistry,metabolism
mRNA Cleavage and Polyadenylation Factors/chemistry,metabolism
Chemicals
Cpeb1 protein, Xenopus
Transcription Factors
Xenopus Proteins
mRNA Cleavage and Polyadenylation Factors
SKP Cullin F-Box Protein Ligases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Setoyama Daiki
Department of Biology, Graduate School of Sciences, Kyushu University, Hakozaki 6-10-1, Fukuoka 812-8581, Japan.
Yamashita Masakane
Sagata Noriyuki
References (34)
34 references, click to expand
-
Beta-TrCP recognizes a previously undescribed nonphosphorylated destruction motif in Cdc25A and Cdc25B phosphatases.
Proc Natl Acad Sci U S A. 2005 May 3;102(18):6279-84
PMID: 15845771
-
Meiotic regulation of the CDK activator RINGO/Speedy by ubiquitin-proteasome-mediated processing and degradation.
Nat Cell Biol. 2006 Oct;8(10):1084-94
PMID: 16964245
-
Poly(A) and translation: development control.
Curr Opin Cell Biol. 1993 Dec;5(6):950-4
PMID: 7907491
-
CPEB is a specificity factor that mediates cytoplasmic polyadenylation during Xenopus oocyte maturation.
Cell. 1994 Nov 18;79(4):617-27
PMID: 7954828
-
CPEB degradation during Xenopus oocyte maturation requires a PEST domain and the 26S proteasome.
Dev Biol. 2001 Mar 15;231(2):447-58
PMID: 11237472
-
Role of cdc2 kinase phosphorylation and conserved N-terminal proteolysis motifs in cytoplasmic polyadenylation-element-binding protein (CPEB) complex dissociation and degradation.
Biochem J. 2003 Feb 15;370(Pt 1):91-100
PMID: 12401129
-
CPEB, maskin, and cyclin B1 mRNA at the mitotic apparatus: implications for local translational control of cell division.
Cell. 2000 Oct 27;103(3):435-47
PMID: 11081630
-
Translational control by CPEB: a means to the end.
Nat Rev Mol Cell Biol. 2001 Jul;2(7):521-9
PMID: 11433366
-
The polo box is required for multiple functions of Plx1 in mitosis.
J Biol Chem. 2004 May 14;279(20):21367-73
PMID: 15016807
-
Structure of a beta-TrCP1-Skp1-beta-catenin complex: destruction motif binding and lysine specificity of the SCF(beta-TrCP1) ubiquitin ligase.
Mol Cell. 2003 Jun;11(6):1445-56
PMID: 12820959
-
Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates.
Science. 2003 Feb 21;299(5610):1228-31
PMID: 12595692
-
Differential mRNA translation and meiotic progression require Cdc2-mediated CPEB destruction.
EMBO J. 2002 Apr 2;21(7):1833-44
PMID: 11927567
-
The SCF ubiquitin ligase: insights into a molecular machine.
Nat Rev Mol Cell Biol. 2004 Sep;5(9):739-51
PMID: 15340381
-
Calcium triggers exit from meiosis II by targeting the APC/C inhibitor XErp1 for degradation.
Nature. 2005 Oct 13;437(7061):1048-52
PMID: 16127448
-
Translational regulation in development.
Cell. 1995 Apr 21;81(2):171-8
PMID: 7736569
-
A clean start: degradation of maternal proteins at the oocyte-to-embryo transition.
Trends Cell Biol. 2004 Aug;14(8):420-6
PMID: 15308208
-
Control of translation initiation in animals.
Annu Rev Cell Dev Biol. 1998;14:399-458
PMID: 9891789
-
Nuclear envelope breakdown may deliver an inhibitor of protein phosphatase 1 which triggers cyclin B translation in starfish oocytes.
Dev Biol. 2005 Sep 1;285(1):200-10
PMID: 16081061
-
Polo-like kinases and the orchestration of cell division.
Nat Rev Mol Cell Biol. 2004 Jun;5(6):429-40
PMID: 15173822
-
CPEB: a life in translation.
Trends Biochem Sci. 2007 Jun;32(6):279-85
PMID: 17481902
-
What does Mos do in oocytes and somatic cells?
Bioessays. 1997 Jan;19(1):13-21
PMID: 9008413
-
PEST sequences and regulation by proteolysis.
Trends Biochem Sci. 1996 Jul;21(7):267-71
PMID: 8755249
-
The many faces of beta-TrCP E3 ubiquitin ligases: reflections in the magic mirror of cancer.
Oncogene. 2004 Mar 15;23(11):2028-36
PMID: 15021890
-
Phosphorylation of CPE binding factor by Eg2 regulates translation of c-mos mRNA.
Nature. 2000 Mar 16;404(6775):302-7
PMID: 10749216
-
MAPK interacts with XGef and is required for CPEB activation during meiosis in Xenopus oocytes.
J Cell Sci. 2007 Mar 15;120(Pt 6):1093-103
PMID: 17344432
-
Facilitation of dendritic mRNA transport by CPEB.
Genes Dev. 2003 Mar 1;17(5):638-53
PMID: 12629046
-
Translational unmasking of Emi2 directs cytostatic factor arrest in meiosis II.
Cell Cycle. 2007 Mar 15;6(6):725-31
PMID: 17361107
-
SCFbeta-TRCP controls clock-dependent transcription via casein kinase 1-dependent degradation of the mammalian period-1 (Per1) protein.
J Biol Chem. 2005 Jul 22;280(29):26863-72
PMID: 15917222
-
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
-
Control of meiotic and mitotic progression by the F box protein beta-Trcp1 in vivo.
Dev Cell. 2003 Jun;4(6):799-812
PMID: 12791266
-
Regulation of the meiotic cell cycle in oocytes.
Curr Opin Cell Biol. 2000 Dec;12(6):666-75
PMID: 11063930
-
Emerging roles for ubiquitin and protein degradation in neuronal function.
Pharmacol Rev. 2007 Mar;59(1):14-39
PMID: 17329546
-
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
-
Role of Polo-like kinase in the degradation of early mitotic inhibitor 1, a regulator of the anaphase promoting complex/cyclosome.
Proc Natl Acad Sci U S A. 2004 May 25;101(21):7937-42
PMID: 15148369