Isoform specific phosphorylation of p53 by protein kinase CK1

Cellular and Molecular Life Sciences

Volumn 67, Issue 7, 2010, Pages 1105-1118

  Venerando, Andrea ^a,b   Marin, Oriano ^a,b   Cozza, Giorgio ^b   Bustos, Victor H ^a,c   Sarno, Stefania ^a,b   Pinna, Lorenzo Alberto ^a,b  

^a VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Casein kinase 1; CK1; CKI; p53 phosphorylation; p53 Ser20

Indexed keywords

CASEIN KINASE I; ISOENZYME; PROTEIN P53; RECOMBINANT PROTEIN; SYNTHETIC PEPTIDE; CASEIN KINASE IALPHA; CASEIN KINASE IDELTA; ZEBRAFISH PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CONSENSUS SEQUENCE; CONTROLLED STUDY; ENZYME SUBSTRATE; MOLECULAR DOCKING; MUTATIONAL ANALYSIS; NONHUMAN; PROTEIN PHOSPHORYLATION; STATISTICAL MODEL; ANIMAL; BINDING SITE; CHEMISTRY; COMPUTER SIMULATION; KINETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PHOSPHORYLATION;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CASEIN KINASE I; CASEIN KINASE IALPHA; CASEIN KINASE IDELTA; COMPUTER SIMULATION; ISOENZYMES; KINETICS; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHORYLATION; TUMOR SUPPRESSOR PROTEIN P53; ZEBRAFISH PROTEINS;

EID: 77950601544     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-009-0236-7     Document Type: Article

References (65)

1. Knippschild U, Gocht A, Wolff S, Huber N, Löhler J, Stöter M (2005) The casein kinase 1 family: participation in multiple cellular processes in eukaryotes. Cell Signal 17(6):675-689 (Pubitemid 40250168)
2. Longenecker KL, Roach PJ, Hurley TD (1996) Three-dimensional structure of mammalian casein kinase I: molecular basis for phosphate recognition. J Mol Biol 257:618-631
3. Xu RM, Carmel G, Sweet RM, Kuret J, Cheng X (1995) Crystal structure of casein kinase-1, a phosphate-directed protein kinase. EMBO J 14:1015-1023
4. Brockman JL, Gross SD, Sussman MR, Anderson RA (1992) Cell cycle-dependent localization of casein kinase I to mitotic spindles. Proc Natl Acad Sci USA 89:9454-9458
5. Milne DM, Looby P, Meek DW (2001) Catalytic activity of protein kinase CK1 delta (casein kinase 1 delta) is essential for its normal subcellular localization. Exp Cell Res 263:43-54 (Pubitemid 32989105)
6. Petronczki M, Matos J, Mori S, Gregan J, Bogdanova A, Schwickart M, Mechtler K, Shirahige K, Zachariae W, Nasmyth K (2006) Monopolar attachment of sister kinetochores at meiosis I requires casein kinase 1. Cell 126:1049-1064 (Pubitemid 44380290)
7. Behrend L, Milne DM, Stoter M, Deppert W, Campbell LE, Meek DW, Knippschild U (2000) IC261, a specific inhibitor of the protein kinases casein kinase 1-delta and -epsilon, triggers the mitotic checkpoint and induces p53-dependent postmitotic effects. Oncogene 19:5303-5313
8. Behrend L, Stoter M, Kurth M, Rutter G, Heukeshoven J, Deppert W, Knippschild U (2000) Interaction of casein kinase 1 delta (CK1delta) with post-Golgi structures, microtubules and the spindle apparatus. Eur J Cell Biol 79:240-251 (Pubitemid 30232569)
9. Camacho F, Cilio M, Guo Y, Virshup DM, Patel K, Khorkova O, Styren S, Morse B, Yao Z, Keesler GA (2001) Human casein kinase I delta phosphorylation of human circadian clock proteins period 1 and 2. FEBS Lett 489:159-165 (Pubitemid 32126401)
10. Zhu J, Shibasaki F, Price R, Guillemot JC, Yano T, Dotsch V, Wagner G, Ferrara P, McKeon F (1998) Intramolecular masking of nuclear import signal on NF-AT4 by casein kinase I and MEKK1. Cell 93:851-861 (Pubitemid 28257590)
11. Peters JM, McKay RM, McKay JP, Graff JM (1999) Casein kinase I transduces Wnt signals. Nature 401:345-350
12. Zeng X, Tamai K, Doble B, Li S, Huang H, Habas R, Okamura H, Woodgett J, He X (2005) A dual-kinase mechanism for Wnt co-receptor phosphorylation and activation. Nature 438:873-877 (Pubitemid 41753071)
13. Davidson G, Wu W, Shen J, Bilic J, Fenger U, Stannek P, Glinka A, Niehrs C (2005) Casein kinase 1 gamma couples Wnt receptor activation to cytoplasmic signal transduction. Nature 438:867-872 (Pubitemid 41753070)
14. Hämmerlein A, Weiske J, Huber O (2005) A second protein kinase CK1-mediated step negatively regulates Wnt signalling by disrupting the lymphocyte enhancer factor-1/beta-catenin complex. Cell Mol Life Sci 62(5):606-618 (Pubitemid 40386338)
15. Swiatek W, Kang H, Garcia BA, Shabanowitz J, Coombs GS, Hunt DF, Virshup DM (2006) Negative regulation of LRP6 function by casein kinase I epsilon phosphorylation. J Biol Chem 281:12233-12241 (Pubitemid 43855306)
16. Price MA (2006) CKI, there's more than one: casein kinase I family members in Wnt and Hedgehog signaling. Genes Dev 20(4):399-410
17. Bryja V, Schulte G, Rawal N, Grahn A, Arenas E (2007) Wnt-5a induces Dishevelled phosphorylation and dopaminergic differentiation via a CK1-dependent mechanism. J Cell Sci 120(4):586-595 (Pubitemid 46437893)
18. Beyaert R, Vanhaesebroeck B, Declercq W, Van Lint J, Vandenabele P, Agostinis P, Vandenheede JR, Fiers W (1995) Casein kinase-1 phosphorylates the p75 tumor necrosis factor receptor and negatively regulates tumor necrosis factor signaling for apoptosis. J Biol Chem 270:23293-23299
19. Desagher S, Osen-Sand A, Montessuit S, Magnenat E, Vilbois F, Hochmann A, Journot L, Antonsson B, Martinou JC (2001) Phosphorylation of bid by casein kinases I and II regulates its cleavage by caspase 8. Mol Cell 8:601-611 (Pubitemid 32946937)
20. Schwab C, DeMaggio AJ, Ghoshal N, Binder LI, Kuret J, McGeer PL (2000) Casein kinase 1 delta is associated with pathological accumulation of tau in several neurodegenerative diseases. Neurobiol Aging 21:503-510 (Pubitemid 30621488)
21. Yasojima K, Kuret J, DeMaggio AJ, McGeer E, McGeer PL (2000) Casein kinase 1 delta mRNA is upregulated in Alzheimer disease brain. Brain Res 865:116-120 (Pubitemid 30256215)
22. Xu Y, Padiath QS, Shapiro RE, Jones CR, Wu SC, Saigon N, Saigon K, Ptacek LJ, Fu YH (2005) Functional consequences of a CKI delta mutation causing familial advanced sleep phase syndrome. Nature 434:640-644 (Pubitemid 40488555)
23. Elias L, Li AP, Longmire J (1981) Cyclic adenosine 3':5'-monophosphate- dependent and -independent protein kinase in acute myeloblastic leukemia. Cancer Res 41:2182-2188 (Pubitemid 11111413)
24. Mishra SK, Yang Z, Mazumdar A, Talukder AH, Larose L, Kumar R (2004) Metastatic tumor antigen 1 short form (MTA1 s) associates with casein kinase I-gamma2, an estrogen-responsive kinase. Oncogene 23:4422-4429 (Pubitemid 38850421)
25. Frierson HF Jr, El-Naggar AK, Welsh JB, Sapinoso LM, Su AI, Cheng J, Saku T, Moskaluk CA, Hampton GM (2002) Large scale molecular analysis identifies genes with altered expression in salivary adenoid cystic carcinoma Am J Pathol 161:1315-1323
26. Fuja TJ, Lin F, Osann KE, Bryant PJ (2004) Somatic mutations and altered expression of the candidate tumor suppressors CSNK1 epsilon, DLG1, and EDD/hHYD in mammary ductal carcinoma. Cancer Res 64:942-951
27. Adorno M, Cordenonsi M, Montagner M, Dupont S, Wong C, Hann B, Solari A, Bobisse S, Rondina MB, Guzzardo V, Parenti AR, Rosato A, Bicciato S, Balmain A, Piccolo S (2009) A Mutant-p53/Smad complex opposes p63 to empower TGFbetainduced metastasis. Cell 137:87-98
28. Meggio F, Donella-Deana A, Pinna LA (1979) Studies on the structural requirements of a microsomal cAMP-independent protein kinase. FEBS Lett 106(1):76-80
29. Flotow H, Graves PR, Wang AQ, Fiol CJ, Roeske RW, Roach PJ (1990) Phosphate groups as substrate determinants for casein kinase I action. J Biol Chem 265(24): 14264-14269 (Pubitemid 20281799)
30. Meggio F, Perich JW, Reynolds EC, Pinna LA (1991) A synthetic beta-casein phosphopeptide and analogues as model substrates for casein kinase-1, a ubiquitous, phosphate directed protein kinase. FEBS Lett 283(2):303-306
31. Roach PJ (1991) Multisite and hierarchal protein phosphorylation. J Biol Chem 266(22): 14139-14142
32. Amit S, Hatzubai A, Birman Y, Andersen JS, Ben-Shushan E, Mann M, Ben-Neriah Y, Alkalay I (2002) Axin mediated CKI phosphorylation of β-catenin at Ser 45: a molecular switch for the Wnt pathway. Genes Dev 16:1066-1076 (Pubitemid 34507196)
33. Liu C, Li Y, Semenov M, Han C, Baeg GH, Tan Y, Zhang Z, Lin X, He X (2002) Control of β-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108:837-847 (Pubitemid 34327534)
34. Ha NC, Tonozuka T, Stamos JL, Choi WI, Weis WI (2004) Mechanism of phosphorylation-dependent binding of APC to β-catenin and its role in β-catenin degradation. Mol Cell 15:511-521 (Pubitemid 39141779)
35. Xing Y, Clements WK, Le Trong I, Hinds TR, Stenkamp R, Kimelman D, Xu W (2004) Crystal structure of a β-catenin/APC complex reveals a critical role for APC phosphorylation in APC function. Mol Cell 15:523-533 (Pubitemid 39141780)
36. Ferrarese A, Marin O, Bustos VH, Venerando A, Antonelli M, Allende JE, Pinna LA (2007) Chemical dissection of the APC Repeat 3 multistep phosphorylation by the concerted action of protein kinases CK1 and GSK3. Biochemistry 46(42): 11902-11910 (Pubitemid 47623758)
37. Desdouits F, Siciliano JC, Greengard P, Girault JA (1995) Dopamine- and cAMP-regulated phosphoprotein DARPP-32: phosphorylation of Ser-137 by casein kinase I inhibits dephosphorylation of Thr-34 by calcineurin. Proc Natl Acad Sci USA 92(7):2682-2685
38. Pulgar V, Marin O, Meggio F, Allende CC, Allende JE, Pinna LA (1999) Optimal sequences for non-phosphate-directed phosphorylation by protein kinase CK1 (casein kinase-1)-a re-evaluation. Eur J Biochem 260(2):520-526 (Pubitemid 29122551)
39. Marin O, Burzio V, Boschetti M, Meggio F, Allende CC, Allende JE, Pinna LA (2002) Structural features underlying the multisite phosphorylation of the A domain of the NF-AT4 transcription factor by protein kinase CK1. Biochemistry 41(2):618-627 (Pubitemid 34062033)
40. Marin O, Bustos VH, Cesaro L, Meggio F, Pagano MA, Antonelli M, Allende CC, Pinna LA, Allende JE (2003) A noncanonical sequence phosphorylated by casein kinase 1 in beta-catenin may play a role in casein kinase 1 targeting of important signaling proteins. Proc Natl Acad Sci USA 100(18): 10193-10200 (Pubitemid 37071855)
41. Bustos VH, Ferrarese A, Venerando A, Marin O, Allende JE, Pinna LA (2006) The first armadillo repeat is involved in the recognition and regulation of beta-catenin phosphorylation by protein kinase CK1. Proc Natl Acad Sci USA 103(52):19725-19730 (Pubitemid 46043311)
42. Bode AM, Dong Z (2004) Post-translational modification of p53 in tumorigenesis. Nat Rev Cancer 4:793-805
43. Lacroix M, Toillon RA, Leclercq G (2006) p53 and breast cancer, an update. Endocr Relat Cancer 13(2):293-325
44. Appella E, Anderson CW (2001) Post-translational modifications and activation of p53 by genotoxic stresses. Eur J Biochem 268(10):2764-2772 (Pubitemid 32862957)
45. Knippschild U, Milne DM, Campbell LE, DeMaggio AJ, Christenson E, Hoekstra MF, Meek DW (1997) 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. Oncogene 15(14): 1727-1736 (Pubitemid 27466713)
46. Higashimoto Y, Saito S, Tong XH, Hong A, Sakaguchi K, Appella E, Anderson CW (2000) Human p53 is phosphorylated on serines 6 and 9 in response to DNA damage-inducing agents. J Biol Chem 275(30):23199-23203 (Pubitemid 30646216)
47. Cordenonsi M, Montagner M, Adorno M, Zacchigna L, Martello G, Mamidi A, Soligo S, Dupont S, Piccolo S (2007) Integration of TGF-beta and Ras/MAPK signaling through p53 phosphorylation. Science 315(5813):840-843 (Pubitemid 46255835)
48. Dumaz N, Milne DM, Meek DW (1999) Protein kinase CK1 is a p53-threonine 18 kinase which requires prior phosphorylation of serine 15. FEBS Lett 463(3):312-316 (Pubitemid 30001941)
49. Sakaguchi K, Saito S, Higashimoto Y, Roy S, Anderson CW, Appella E (2000) Damage-mediated phosphorylation of human p53 threonine 18 through a cascade mediated by a casein 1-like kinase. Effect on Mdm2 binding. J Biol Chem 275(13):9278-9283 (Pubitemid 30185148)
50. Shieh SY, Ikeda M, Taya Y, Prives C (1997) DNA damage induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 91:325-334 (Pubitemid 27467963)
51. Saito S, Goodarzi AA, Higashimoto Y, Noda Y, Lees-Miller SP, Appella E, Anderson CW (2002) ATM mediates phosphorylation at multiple p53 sites, including Ser(46), in response to ionizing radiation. J Biol Chem 277:12491-12494 (Pubitemid 34952604)
52. Tibbetts RS, Brumbaugh KM, Williams JM, Sarkaria JM, Cliby WA, Shieh SY, Taya Y, Prives C, Abraham RT (1999) A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev 13:152-157 (Pubitemid 29061945)
53. She QB, Chen N, Dong Z (2000) ERKs and p38 kinase phosphorylate p53 protein at serine 15 in response to UV radiation. J Biol Chem 275:20444-20449 (Pubitemid 30457622)
54. MacLaine NJ, Oster B, Bundgaard B, Fraser JA, Buckner C, Lazo PA, Meek DW, Höllsberg P, Hupp TR (2008) A central role for CK1 in catalyzing phosphorylation of the p53 transactivation domain at serine 20 after HHV-6B viral infection. J Biol Chem 283(42):28563-28573
55. Chehab NH, Malikzay A, Stavridi ES, Halazonetis TD (1999) Phosphorylation of Ser-20 mediates stabilization of human p53 in response to DNA damage. Proc Natl Acad Sci USA 96:13777-13782
56. Unger T, Juven-Gershon T, Moallem E, Berger M, Vogt Sionov R, Lozano G, Oren M, Haupt Y (1999) Critical role for Ser20 of human p53 in the negative regulation of p53 by Mdm2. EMBO J 18:1805-1814 (Pubitemid 29158524)
57. She QB, Ma WY, Dong Z (2002) Role of MAP kinases in UVB-induced phosphorylation of p53 at serine 20. Oncogene 21:1580-1589
58. Fields GB, Noble RL (1990) Solid phase peptide synthesis utilizing 9- fluorenylmethoxycarbonyl amino acids. Int J Pept Protein Res 35:161-214 (Pubitemid 20126875)
59. Burzio V, Antonelli M, Allende CC, Allende JE (2002) Biochemical and cellular characteristics of the four splice variants of protein kinase CK1α from zebrafish (Danio rerio). J Cell Biochem 86:805-814 (Pubitemid 34839981)
60. Marin O, Meggio F, Pinna LA (1994) Design and synthesis of two new peptide substrates for the specific and sensitive monitoring of casein kinases-1 and -2. Biochem Biophys Res Commun 198:898-905 (Pubitemid 24172782)
61. Perich JW, Meggio F, Reynolds EC, Marin O, Pinna LA (1992) Role of phosphorylated aminoacyl residues in generating atypical consensus sequences which are recognized by casein kinase-2 but not by casein kinase-1. Biochemistry 31:5893-5897
62. Molecular operating environment (MOE 2008.10), C.C.G., Inc., 1255 University St., Suite 1600, Montreal, Quebec, Canada H3B 3X3
63. Cozza G, Moro S, Gotte G (2008) Elucidation of the ribonuclease A aggregation process mediated by 3D domain swapping: a computational approach reveals possible new multimeric structures. Biopolymers 89:26-39
64. Poletto G, Vilardell J, Marin O, Pagano MA, Cozza G, Sarno S, Falqués A, Itarte E, Pinna LA, Meggio F (2008) The regulatory beta subunit of protein kinase CK2 contributes to the recognition of the substrate consensus sequence. A study with an eIF2 betaderived peptide. Biochemistry 47:8317-8325
65. Oleinik NV, Krupenko NI, Krupenko SA (2007) Cooperation between JNK1 and JNK2 in activation of p53 apoptotic pathway. Oncogene 26:7222-7230