Isoform Specific Phosphorylation Of P53 By Protein Kinase CK1
A. Venerando, O. Marin, G. Cozza, Victor H. Bustos, S. Sarno, Lorenzo Alberto Pinna
Published 2009 · Medicine, Biology
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The ability of three isoforms of protein kinase CK1 (α, γ1, and δ) to phosphorylate the N-terminal region of p53 has been assessed using either recombinant p53 or a synthetic peptide reproducing its 1–28 sequence. Both substrates are readily phosphoylated by CK1δ and CK1α, but not by the γ isoform. Affinity of full size p53 for CK1 is 3 orders of magnitude higher than that of its N-terminal peptide (Km 0.82 μM vs 1.51 mM). The preferred target is S20, whose phosphorylation critically relies on E17, while S6 is unaffected despite displaying the same consensus (E-x-x-S). Our data support the concept that non-primed phosphorylation of p53 by CK1 is an isoform-specific reaction preferentially affecting S20 by a mechanism which is grounded both on a local consensus and on a remote docking site mapped to the K221RQK224 loop according to modeling and mutational analysis.
This paper references
Large scale molecular analysis identifies genes with altered expression in salivary adenoid cystic carcinoma.
H. Frierson (2002)
A dual-kinase mechanism for Wnt co-receptor phosphorylation and activation
X. Zeng (2005)
Crystal structure of a beta-catenin/APC complex reveals a critical role for APC phosphorylation in APC function.
Y. C. Xing (2004)
A role for ATR in the DNA damage-induced phosphorylation of p53.
R. Tibbetts (1999)
Post-translational modification of p53 in tumorigenesis
A. Bode (2004)
A synthetic β‐casein phosphopeptide and analogues as model substrates for casein kinase‐1, a ubiquitous, phosphate directed protein kinase
F. Meggio (1991)
A Mutant-p53/Smad Complex Opposes p63 to Empower TGFβ-Induced Metastasis
M. Adorno (2009)
Human casein kinase Iδ phosphorylation of human circadian clock proteins period 1 and 2
F. Camacho (2001)
Integration of TGF-beta and Ras/MAPK signaling through p53 phosphorylation.
M. Cordenonsi (2007)
Metastatic tumor antigen 1 short form (MTA1s) associates with casein kinase I-γ2, an estrogen-responsive kinase
S. Mishra (2004)
Phosphate groups as substrate determinants for casein kinase I action.
H. Flotow (1990)
Solid phase peptide synthesis utilizing 9-fluorenylmethoxycarbonyl amino acids.
G. Fields (1990)
Integration of TGF-ß and Ras/MAPK Signaling Through p53 Phosphorylation
M. Cordenonsi (2007)
The first armadillo repeat is involved in the recognition and regulation of β-catenin phosphorylation by protein kinase CK1
Victor H Bustos (2006)
Casein kinase 1 delta is associated with pathological accumulation of tau in several neurodegenerative diseases
C. Schwab (2000)
Casein Kinase-1 Phosphorylates the p75 Tumor Necrosis Factor Receptor and Negatively Regulates Tumor Necrosis Factor Signaling for Apoptosis (*)
R. Beyaert (1995)
Cooperation between JNK1 and JNK2 in activation of p53 apoptotic pathway
N. Oleinik (2007)
Multisite and hierarchal protein phosphorylation.
P. Roach (1991)
Three-dimensional structure of mammalian casein kinase I: molecular basis for phosphate recognition.
K. Longenecker (1996)
Control of β-Catenin Phosphorylation/Degradation by a Dual-Kinase Mechanism
C. Liu (2002)
Dopamine- and cAMP-regulated phosphoprotein DARPP-32: phosphorylation of Ser-137 by casein kinase I inhibits dephosphorylation of Thr-34 by calcineurin.
F. Desdouits (1995)
Studies on the structural requirements of a microsomal cAMP‐independent protein kinase
F. Meggio (1979)
Keesler GA (2001) Human casein kinase I delta phosphorylation of human circadian clock proteins period 1 and 2
F Camacho (2001)
IC261, a specific inhibitor of the protein kinases casein kinase 1-delta and -epsilon, triggers the mitotic checkpoint and induces p53-dependent postmitotic effects
L. Behrend (2000)
Design and synthesis of two new peptide substrates for the specific and sensitive monitoring of casein kinases-1 and -2.
O. Marin (1994)
p53 and breast cancer, an update.
M. Lacroix (2006)
Role of MAP kinases in UVB-induced phosphorylation of p53 at serine 20
Qing-Bai She (2002)
Post-translational modifications and activation of p53 by genotoxic stresses.
E. Appella (2001)
Solid Phase Peptide Synthesis Utilizing 9-Fluorenylmethoxycarbonylamino Acids
G. Fields (1990)
Biochemical and cellular characteristics of the four splice variants of protein kinase CK1α from zebrafish (Danio rerio)
V. Burzio (2002)
Role of phosphorylated aminoacyl residues in generating atypical consensus sequences which are recognized by casein kinase-2 but not by casein kinase-1.
J. W. Perich (1992)
Casein kinase 1 γ couples Wnt receptor activation to cytoplasmic signal transduction
G. Davidson (2005)
Cyclic adenosine 3':5'-monophosphate-dependent and -independent protein kinase in acute myeloblastic leukemia.
L. Elias (1981)
Negative regulation of LRP6 function by casein kinase I epsilon phosphorylation.
W. Świątek (2006)
Negative Regulation of LRP6 Function by Casein Kinase I ϵ Phosphorylation*
W. Świa̧tek (2006)
Phosphorylation of Ser-20 mediates stabilization of human p53 in response to DNA damage.
N. Chehab (1999)
Mechanism of Phosphorylation-Dependent Binding of APC to β-Catenin and Its Role in β-Catenin Degradation
Nam-Chul Ha (2004)
Damage-mediated Phosphorylation of Human p53 Threonine 18 through a Cascade Mediated by a Casein 1-like Kinase
K. Sakaguchi (2000)
ATM Mediates Phosphorylation at Multiple p53 Sites, Including Ser46, in Response to Ionizing Radiation*
S. Saito (2002)
Elucidation of the ribonuclease A aggregation process mediated by 3D domain swapping: a computational approach reveals possible new multimeric structures.
G. Cozza (2008)
p53 is phosphorylated in vitro and in vivo by the delta and epsilon isoforms of casein kinase 1 and enhances the level of casein kinase 1 delta in response to topoisomerase-directed drugs
U. Knippschild (1997)
Critical role for Ser20 of human p53 in the negative regulation of p53 by Mdm2
T. Unger (1999)
Cell cycle-dependent localization of casein kinase I to mitotic spindles.
J. L. Brockman (1992)
A Central Role for CK1 in Catalyzing Phosphorylation of the p53 Transactivation Domain at Serine 20 after HHV-6B Viral Infection*
Nicola J. Maclaine (2008)
The regulatory beta subunit of protein kinase CK2 contributes to the recognition of the substrate consensus sequence. A study with an eIF2 beta-derived peptide.
Giorgia Poletto (2008)
ERKs and p38 Kinase Phosphorylate p53 Protein at Serine 15 in Response to UV Radiation*
Q. She (2000)
Casein kinase 1 delta mRNA is upregulated in Alzheimer disease brain
K. Yasojima (2000)
Axin-mediated CKI phosphorylation of beta-catenin at Ser 45: a molecular switch for the Wnt pathway.
S. Amit (2002)
Casein kinase I transduces Wnt signals
John M. Peters (1999)
CKI, there's more than one: casein kinase I family members in Wnt and Hedgehog signaling.
M. Price (2006)
The casein kinase 1 family: participation in multiple cellular processes in eukaryotes.
U. Knippschild (2005)
Phosphorylation of bid by casein kinases I and II regulates its cleavage by caspase 8.
S. Desagher (2001)
Catalytic Activity of Protein Kinase CK1δ (Casein Kinase 1δ) Is Essential for Its Normal Subcellular Localization
D. Milne (2001)
Monopolar Attachment of Sister Kinetochores at Meiosis I Requires Casein Kinase 1
Mark Petronczki (2006)
Functional consequences of a CKIδ mutation causing familial advanced sleep phase syndrome
Y. Xu (2005)
A second protein kinase CK1-mediated step negatively regulates Wnt signalling by disrupting the lymphocyte enhancer factor-1/β-catenin complex
A. Hämmerlein (2005)
Wnt-5a induces Dishevelled phosphorylation and dopaminergic differentiation via a CK1-dependent mechanism
V. Bryja (2007)
Crystal structure of casein kinase‐1, a phosphate‐directed protein kinase.
R. Xu (1995)
Catalytic activity of protein kinase CK1 delta (casein kinase 1delta) is essential for its normal subcellular localization.
D. Milne (2001)
Somatic Mutations and Altered Expression of the Candidate Tumor Suppressors CSNK1ε, DLG1, and EDD/hHYD in Mammary Ductal Carcinoma
Tannin J Fuja (2004)
Intramolecular Masking of Nuclear Import Signal on NF-AT4 by Casein Kinase I and MEKK1
J. Zhu (1998)
Casein kinase 1 gamma couples Wnt receptor activation to cytoplasmic signal transduction.
G. Davidson (2005)
Optimal sequences for non-phosphate-directed phosphorylation by protein kinase CK1 (casein kinase-1)--a re-evaluation.
V. Pulgar (1999)
Interaction of casein kinase 1 delta (CK1delta) with post-Golgi structures, microtubules and the spindle apparatus.
L. Behrend (2000)
DNA Damage-Induced Phosphorylation of p53 Alleviates Inhibition by MDM2
S. Shieh (1997)
A noncanonical sequence phosphorylated by casein kinase 1 in β-catenin may play a role in casein kinase 1 targeting of important signaling proteins
O. Marin (2003)
Human p53 Is Phosphorylated on Serines 6 and 9 in Response to DNA Damage-inducing Agents*
Y. Higashimoto (2000)
Casein kinase 1 delta mRNA is upregulated in Alzheimer disease
K Yasojima (2000)
Chemical dissection of the APC Repeat 3 multistep phosphorylation by the concerted action of protein kinases CK1 and GSK3.
A. Ferrarese (2007)
Protein kinase CK1 is a p53‐threonine 18 kinase which requires prior phosphorylation of serine 15
N. Dumaz (1999)
Structural features underlying the multisite phosphorylation of the A domain of the NF-AT4 transcription factor by protein kinase CK1.
O. Marin (2002)
This paper is referenced by
Casein kinase 1α has a non-redundant and dominant role within the CK1 family in melanoma progression
Tobias Sinnberg (2016)
Molecular Imaging of GSK3β and CK1α kinases
Shyam Nyati (2010)
Casein kinase: the triple meaning of a misnomer.
A. Venerando (2014)
Superiority of PLK-2 as α-synuclein phosphorylating agent relies on unique specificity determinants.
M. Salvi (2012)
The kinase domain of CK1δ can be phosphorylated by Chk1
T. Boehm (2019)
The CK1 Family: Contribution to Cellular Stress Response and Its Role in Carcinogenesis
U. Knippschild (2014)
Molecular imaging of glycogen synthase kinase-3beta and casein kinase-1alpha kinases.
Shyam Nyati (2010)
Biological functions of casein kinase 1 isoforms and putative roles in tumorigenesis
B. Schittek (2014)
Exploiting the MDM2-CK1α Protein-Protein Interface to Develop Novel Biologics That Induce UBL-Kinase-Modification and Inhibit Cell Growth
Anne-Sophie Huart (2012)
Corrigendum: Site-specific NMR mapping and time-resolved monitoring of serine and threonine phosphorylation in reconstituted kinase reactions and mammalian cell extracts
François-Xavier Theillet (2015)
Inactivation of CK1α in multiple myeloma empowers drug cytotoxicity by affecting AKT and β-catenin survival signaling pathways
Sabrina Manni (2017)
Pyrvinium pamoate does not activate protein kinase CK1, but promotes Akt/PKB down-regulation and GSK3 activation.
A. Venerando (2013)
IC261, a specific inhibitor of CK1δ/ε, promotes aerobic glycolysis through p53-dependent mechanisms in colon cancer
M Liu (2020)
FBXW7-mutated colorectal cancer cells exhibit aberrant expression of phosphorylated-p53 at Serine-15
N. Li (2015)
Inhibition of protein kinase CK2 by flavonoids and tyrphostins. A structural insight.
G. Lolli (2012)
Differential abundance of CK1α provides selectivity for pharmacological CK1α activators to target WNT-dependent tumors
B. Li (2017)
Design, Synthesis, and Optimization of CK1δ Inhibitors
Jakob Halekotte (2016)
Detection of Phospho-Sites Generated by Protein Kinase CK2 in CFTR: Mechanistic Aspects of Thr1471 Phosphorylation
A. Venerando (2013)
Discovery of potential neurodegenerative inhibitors in Alzheimer’s disease by casein kinase 1 structure-based virtual screening
Ricardo P. Rodrigues (2017)
CK1δ activity is modulated by CDK2/E- and CDK5/p35-mediated phosphorylation
Chiara Ianes (2015)
Expression of casein kinase genes in glioma cell line U87: Effect of hypoxia and glucose or glutamine deprivation
Dmytro O. Minchenko (2012)
Structure, regulation, and (patho-)physiological functions of the stress-induced protein kinase CK1 delta (CSNK1D).
Pengfei Xu (2019)
Site-specific NMR mapping and time-resolved monitoring of serine and threonine phosphorylation in reconstituted kinase reactions and mammalian cell extracts
François-Xavier Theillet (2013)
New insights on thyroid hormone mediated regulation of herpesvirus infections
R. Figliozzi (2017)
Casein kinases as potential therapeutic targets
G. Cozza (2016)
Quantitative Phosphoproteomic Analysis Reveals Key Mechanisms of Cellular Proliferation in Liver Cancer Cells
B. Zhu (2017)