The subcellular localization of vaccinia-related kinase-2 (VRK2) isoforms determines their different effect on p53 stability in tumour cell lines

FEBS Journal

Volumn 273, Issue 11, 2006, Pages 2487-2504

  Blanco, Sandra ^a   Klimcakova, Lucia ^a   Vega, Francisco M ^a   Lazo, Pedro A ^a,b  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b CSIC   (Spain)

Author keywords

p53; Phosphorylation; Ser Thr kinase; VRK2

Indexed keywords

CALNEXIN; CALRETICULIN; CELL PROTEIN; PACLITAXEL; PROTEIN P53; THREONINE; UNCLASSIFIED DRUG; VACCINIA RELATED KINASE 2; VACCINIA RELATED KINASE 2A; VACCINIA RELATED KINASE 2B;

ACETYLATION; ALTERNATIVE RNA SPLICING; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; MITOCHONDRION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STABILITY; TRANSCRIPTION INITIATION; TUMOR CELL LINE; UBIQUITINATION;

AMINO ACID SEQUENCE; BREAST NEOPLASMS; CELL CYCLE; CELL LINE, TUMOR; COLONIC NEOPLASMS; FEMALE; HUMANS; LIVER NEOPLASMS; LUNG NEOPLASMS; MOLECULAR SEQUENCE DATA; PROTEIN-SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEIN P53; VACCINIA VIRUS;

EID: 33646680749     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2006.05256.x     Document Type: Article

References (72)

1. Manning G Whyte DB Martinez R Hunter T Sudarsanam S 2002 The protein kinase complement of the human genome Science 298 1912 1934
2. Kamath RS Fraser AG Dong Y Poulin G Durbin R Gotta M Kanapin A Le Bot N Moreno S Sohrmann M et al. 2003 Systematic functional analysis of the Caenorhabditis elegans genome using RNAi Nature 421 231 237
3. Morrison DK Murakami MS Cleghon V 2000 Protein kinases and phosphatases in the Drosophila genome J Cell Biol 150 F57 F62
4. Dhillon N Hoekstra MF 1994 Characterization of two protein kinases from Schizosaccharomyces pombe involved in the regulation of DNA repair EMBO J 13 2777 2788
5. Hoekstra MF Liskay RM Ou AC DeMaggio AJ Burbee DG Heffron F 1991 HRR25, a putative protein kinase from budding yeast: association with repair of damaged DNA Science 253 1031 1034
6. Ho Y Mason S Kobayashi R Hoekstra M Andrews B 1997 Role of the casein kinase I isoform, Hrr25, and the cell cycle-regulatory transcription factor, SBF, in the transcriptional response to DNA damage in Saccharomyces cerevisiae Proc Natl Acad Sci USA 94 581 586
7. Nezu J Oku A Jones MH Shimane M 1997 Identification of two novel human putative serine/threonine kinases, VRK1 and VRK2, with structural similarity to vaccinia virus B1R kinase Genomics 45 327 331
8. Lin S Chen W Broyles SS 1992 The vaccinia virus B1R gene product is a serine/threonine protein kinase J Virol 66 2717 2723
9. Banham AH Smith GL 1992 Vaccinia virus B1R encodes a 34-kDa serine/threonine protein kinase that localizes in cytoplasmic factories and is packaged into virions Virology 191 803 812
10. Rempel RE Traktman P 1992 Vaccinia virus B1 kinase: phenotypic analysis of temperature-sensitive mutants and enzymatic characterization of recombinant proteins J Virol 66 4413 4426
11. Lopez-Borges S Lazo PA 2000 The human vaccinia-related kinase 1 (VRK1) phosphorylates threonine-18 within the mdm-2 binding site of the p53 tumour suppressor protein Oncogene 19 3656 3664
12. Barcia R Lopez-Borges S Vega FM Lazo PA 2002 Kinetic properties of p53 phosphorylation by the human vaccinia-related kinase Arch Biochem Biophys 399 1 5
13. Nichols RJ Traktman P 2004 Characterization of three paralogous members of the mammalian vaccinia related kinase family J Biol Chem 279 7934 7946
14. Lazo PA Vega FM Sevilla A 2005 Vaccinia-related kinase-1 AfCS-Nature Molecule Pages 10.1038/mp.a003025.003001
15. Vega FM Sevilla A Lazo PA 2004 p53 stabilization and accumulation induced by human vaccinia-related kinase Mol Cell Biol 24 10366 10380
16. Sevilla A Santos CR Barcia R Vega FM Lazo PA 2004 c-Jun phosphorylation by the human vaccinia-related kinase 1 (VRK1) and its cooperation with the N-terminal kinase of c-Jun (JNK) Oncogene 23 8950 8958
17. Sevilla A Santos CR Vega FM Lazo PA 2004 Human vaccinia-related kinase 1 (VRK1) activates the ATF2 transcriptional activity by novel phosphorylation on Thr-73 and Ser-62 and cooperates with JNK J Biol Chem 279 27458 27465
18. Vega FM Gonzalo P Gaspar ML Lazo PA 2003 Expression of the VRK (vaccinia-related kinase) gene family of p53 regulators in murine hematopoietic development FEBS Lett 544 176 180
19. Dorrell MI Aguilar E Weber C Friedlander M 2004 Global gene expression analysis of the developing postnatal mouse retina Invest Ophthalmol Vis Sci 45 1009 1019
20. Santos CR Rodriguez-Pinilla M Vega FM Rodriguez-Peralto JL Blanco S Sevilla A Valbuena A Hernandez T van Wijnen AJ Li F et al. 2006 VRK1 signaling pathway in the context of the proliferation phenotype in head and neck squamous cell carcinoma Mol Cancer Res 4 177 185
21. McLean LA Gathmann I Capdeville R Polymeropoulos MH Dressman M 2004 Pharmacogenomic analysis of cytogenetic response in chronic myeloid leukemia patients treated with imatinib Clin Cancer Res 10 155 165
22. Shiio Y Eisenman RN Yi EC Donohoe S Goodlett DR Aebersold R 2003 Quantitative proteomic analysis of chromatin-associated factors J Am Soc Mass Spectrom 14 696 703
23. Tien ES Gray JP Peters JM Vanden Heuvel JP 2003 Comprehensive gene expression analysis of peroxisome proliferator-treated immortalized hepatocytes: identification of peroxisome proliferator-activated receptor {alpha}-dependent growth regulatory genes Cancer Res 63 5767 5780
24. Vernell R Helin K Muller H 2003 Identification of target genes of the p16INK4A-pRB-E2F pathway J Biol Chem 278 46124 46137
25. Boldrick JC Alizadeh AA Diehn M Dudoit S Liu CL Belcher CE Botstein D Staudt LM Brown PO Relman DA 2002 Stereotyped and specific gene expression programs in human innate immune responses to bacteria Proc Natl Acad Sci USA 99 972 977
26. Diehn M Alizadeh AA Rando OJ Liu CL Stankunas K Botstein D Crabtree GR Brown PO 2002 Genomic expression programs and the integration of the CD28 costimulatory signal in T cell activation Proc Natl Acad Sci USA 99 11796 11801
27. Prives C Hall PA 1999 The p53 pathway J Pathol 187 112 126
28. Vousden KH Lu X 2002 Live or let die: the cell's response to p53 Nat Rev Cancer 2 594 604
29. Garcia-Cao I Garcia-Cao M Martin-Caballero J Criado LM Klatt P Flores JM Weill JC Blasco MA Serrano M 2002 'Super p53' mice exhibit enhanced DNA damage response, are tumor resistant and age normally EMBO J 21 6225 6235
30. Hemann MT Fridman JS Zilfou JT Hernando E Paddison PJ Cordon-Cardo C Hannon GJ Lowe SW 2003 An epi-allelic series of p53 hypomorphs created by stable RNAi produces distinct tumor phenotypes in vivo Nat Genet 33 396 400
31. Alarcon-Vargas D Ronai Z 2002 p53-Mdm2 - the affair that never ends Carcinogenesis 23 541 547
32. Woods DB Vousden KH 2001 Regulation of p53 function Exp Cell Res 264 56 66
33. Saito S Yamaguchi H Higashimoto Y Chao C Xu Y Fornace AJ Jr. Appella E Anderson CW 2003 Phosphorylation site interdependence of human p53 post-translational modifications in response to stress J Biol Chem 278 37536 37544
34. Meek DW 1998 Multisite phosphorylation and the integration of stress signals at p53 Cell Signal 10 159 166
35. Bode AM Dong Z 2004 Post-translational modification of p53 in tumorigenesis Nat Rev Cancer 4 793 805
36. Siliciano JD Canman CE Taya Y Sakaguchi K Appella E Kastan MB 1997 DNA damage induces phosphorylation of the amino terminus of p53 Genes Dev 11 3471 3481
37. de Rozieres S Maya R Oren M Lozano G 2000 The loss of mdm2 induces p53-mediated apoptosis Oncogene 19 1691 1697
38. Ljungman M 2000 Dial 9-1-1 for p53: mechanisms of p53 activation by cellular stress Neoplasia 2 208 225
39. Appella E Anderson CW 2001 Post-translational modifications and activation of p53 by genotoxic stresses Eur J Biochem 268 2764 2772
40. Brooks CL Gu W 2003 Ubiquitination, phosphorylation and acetylation: the molecular basis for p53 regulation Curr Opin Cell Biol 15 164 171
41. Ashcroft M Taya Y Vousden KH 2000 Stress signals utilize multiple pathways to stabilize p53 Mol Cell Biol 20 3224 3233
42. Dumaz N Milne DM Jardine LJ Meek DW 2001 Critical roles for the serine 20, but not the serine 15, phosphorylation site and for the polyproline domain in regulating p53 turnover Biochem J 359 459 464
43. Dumaz N Meek DW 1999 Serine 15 phosphorylation stimulates p53 transactivation but does not directly influence interaction with HDM2 EMBO J 18 7002 7010
44. Lambert PF Kashanchi F Radonovich MF Shiekhattar R Brady JN 1998 Phosphorylation of p53 serine 15 increases interaction with CBP J Biol Chem 273 33048 33053
45. Shieh SY Ahn J Tamai K Taya Y Prives C 2000 The human homologs of checkpoint kinases Chk1 and Cds1 (Chk2) phosphorylate p53 at multiple DNA damage-inducible sites Genes Dev 14 289 300
46. Jackson MW Agarwal MK Agarwal ML Agarwal A Stanhope-Baker P Williams BR Stark GR 2004 Limited role of N-terminal phosphoserine residues in the activation of transcription by p53 Oncogene 23 4477 4487
47. Sluss HK Armata H Gallant J Jones SN 2004 Phosphorylation of serine 18 regulates distinct p53 functions in mice Mol Cell Biol 24 976 984
48. Knights CD Liu Y Appella E Kulesz-Martin M 2003 Defective p53 post-translational modification required for wild type p53 inactivation in malignant epithelial cells with mdm2 gene amplification J Biol Chem 278 52890 52900
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 9278 9283
50. 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 463 312 316
51. Stoter M Bamberger AM Aslan B Kurth M Speidel D Loning T Frank HG Kaufmann P Lohler J Henne-Bruns D et al. 2005 Inhibition of casein kinase I delta alters mitotic spindle formation and induces apoptosis in trophoblast cells Oncogene 24 7964 7975
52. Chen J Marechal V Levine AJ 1993 Mapping of the p53 and mdm-2 interaction domains Mol Cell Biol 13 4107 4114
53. Schon O Friedler A Bycroft M Freund S Fersht A 2002 Molecular mechanism of the interaction between MDM2 and p53 J Mol Biol 323 491 501
54. Jabbur JR Tabor AD Cheng X Wang H Uesugi M Lozano G Zhang W 2002 Mdm-2 binding and TAF (II) 31 recruitment is regulated by hydrogen bond disruption between the p53 residues Thr18 and Asp21 Oncogene 21 7100 7113
55. Yuan ZM Huang Y Ishiko T Nakada S Utsugisawa T Shioya H Utsugisawa Y Yokoyama K Weichselbaum R Shi Y et al. 1999 Role for p300 in stabilization of p53 in the response to DNA damage J Biol Chem 274 1883 1886
56. Grossman SR 2001 p300/CBP/p53 interaction and regulation of the p53 response Eur J Biochem 268 2773 2778
57. Ito A Lai CH Zhao X Saito S Hamilton MH Appella E Yao TP 2001 p300/CBP-mediated p53 acetylation is commonly induced by p53-activating agents and inhibited by MDM2 EMBO J 20 1331 1340
58. Dornan D Shimizu H Perkins ND Hupp TR 2003 DNA-dependent acetylation of p53 by the transcription coactivator p300 J Biol Chem 278 13431 13441
59. Damia G Filiberti L Vikhanskaya F Carrassa L Taya Y D'Incalci M Broggini M 2001 Cisplatinum and taxol induce different patterns of p53 phosphorylation Neoplasia 3 10 16
60. Webley K Bond JA Jones CJ Blaydes JP Craig A Hupp T Wynford-Thomas D 2000 Posttranslational modifications of p53 in replicative senescence overlapping but distinct from those induced by dna damage Mol Cell Biol 20 2803 2808
61. Milne DM Palmer RH Campbell DG Meek DW 1992 Phosphorylation of the p53 tumour-suppressor protein at the three N-terminal sites by a novel casein kinase I-like enzyme Oncogene 7 1361 1369
62. Milne DM Campbell DG Caudwell FB Meek DW 1994 Phosphorylation of tumor suppressor protein p53 by mitogen-activated protein kinase J Biol Chem 269 9253 9260
63. Ashcroft M Kubbutat MH Vousden KH 1999 Regulation of p53 function and stability by phosphorylation Mol Cell Biol 19 1751 1758
64. Dornan D Hupp TR 2001 Inhibition of p53-dependent transcription by BOX-I phospho-peptide mimetics that bind to p300 EMBO Report 2 139 144
65. Ferguson M Luciani MG Finlan L Rankin EM Ibbotson S Fersht A Hupp TR 2004 The development of a CDK2-docking site peptide that inhibits p53 and sensitizes cells to death Cell Cycle 3 80 89
66. Kubbutat MHG Jones SN Vousden KH 1997 Regulation of p53 stability by mdm2 Nature 387 299 303
67. Stewart ZA Tang LJ Pietenpol JA 2001 Increased p53 phosphorylation after microtubule disruption is mediated in a microtubule inhibitor- and cell-specific manner Oncogene 20 113 124
68. Pospisilova S Brazda V Kucharikova K Luciani MG Hupp TR Skladal P Palecek E Vojtesek B 2004 Activation of the DNA-binding ability of latent p53 protein by protein kinase C is abolished by protein kinase CK2 Biochem J 378 939 947
69. Kussie PH Gorina S Marechal V Elenbaas B Moreau J Levine AJ Pavletich NP 1996 Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain Science 274 948 953
70. Li M Luo J Brooks CL Gu W 2002 Acetylation of p53 inhibits its ubiquitination by Mdm2 J Biol Chem 277 50607 50611
71. Agoulnik AI Lu B Zhu Q Truong C Ty MT Arango N Chada KK Bishop CE 2002 A novel gene, Pog, is necessary for primordial germ cell proliferation in the mouse and underlies the germ cell deficient mutation, gcd Hum Mol Genet 11 3047 3053
72. Lu B Bishop CE 2003 Late onset of spermatogenesis and gain of fertility in POG-deficient mice indicate that POG is not necessary for the proliferation of spermatogonia Biol Reprod 69 161 168