Differential inhibitor sensitivity between human kinases VRK1 and VRK2

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Vázquez Cedeira, Marta ^a   Barcia Sanjurjo, Iria ^b   Sanz García, Marta ^a   Barcia, Ramiro ^b   Lazo, Pedro A ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

2 [1 (3 AMIDINOTHIOPROPYL) 1H INDOL 3 YL] 3 (1 METHYL 1H INDOL 3 YL)MALEIMIDE; 2 MORPHOLINO 6 (1 THIANTHRENYL) 4 PYRANONE; ATM PROTEIN; AZD 7762; B RAF KINASE; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; CYCLIN DEPENDENT KINASE INHIBITOR 1; DNA DEPENDENT PROTEIN KINASE; IC 261; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHOTRANSFERASE; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN B1R; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; STAUROSPORINE; STRESS ACTIVATED PROTEIN KINASE; TDZD 8; UNCLASSIFIED DRUG; VACCINIA RELATED KINASE 1; VACCINIA RELATED KINASE 2; VIRUS PROTEIN;

ARTICLE; CHEMOSENSITIVITY; ENZYME INHIBITION; PROTEIN TARGETING; SENSITIVITY ANALYSIS;

VACCINIA VIRUS;

EID: 79961147773     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023235     Document Type: Article

References (63)

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. Zhang J, Yang PL, Gray NS, (2009) Targeting cancer with small molecule kinase inhibitors. Nat Rev Cancer 9: 28-39.
3. Cohen P, (2001) The role of protein phosphorylation in human health and disease. Eur J Biochem 268: 5001-5010.
4. Yang H, Higgins B, Kolinsky K, Packman K, Go Z, et al. (2010) RG7204 (PLX4032), a selective BRAFV600E inhibitor, displays potent antitumor activity in preclinical melanoma models. Cancer Res 70: 5518-5527.
5. Bain J, McLauchlan H, Elliott M, Cohen P, (2003) The specificities of protein kinase inhibitors: an update. Biochem J 371: 199-204.
6. Davies SP, Reddy H, Caivano M, Cohen P, (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351: 95-105.
7. Fedorov O, Marsden B, Pogacic V, Rellos P, Muller S, et al. (2007) A systematic interaction map of validated kinase inhibitors with Ser/Thr kinases. Proc Natl Acad Sci U S A 104: 20523-20528.
8. Banham AH, Smith GL, (1992) Vaccinia virus gene B1R encodes a 34-kDa serine/threonine protein kinase that localizes in cytoplasmic factories and is packaged into virions. Virology 191: 803-812.
9. 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.
10. Gorjanacz M, Klerkx EP, Galy V, Santarella R, Lopez-Iglesias C, et al. (2008) Caenorhabditis elegans BAF-1 and its kinase VRK-1 participate directly in post-mitotic nuclear envelope assembly. Embo J 26: 132-143.
11. Aihara H, Nakagawa T, Yasui K, Ohta T, Hirose S, et al. (2004) Nucleosomal histone kinase-1 phosphorylates H2A Thr 119 during mitosis in the early Drosophila embryo. Genes Dev 18: 877-888.
12. Khoury MP, Bourdon J-C, (2010) The Isoforms of the p53 Protein. Cold Spring Harbor Perspecti Biol 2: a000927.
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. Klerkx EP, Lazo PA, Askjaer P, (2009) Emerging biological functions of the vaccinia-related kinase (VRK) family. Histol Histopathol 24: 749-759.
15. Scheeff ED, Eswaran J, Bunkoczi G, Knapp S, Manning G, (2009) Structure of the pseudokinase VRK3 reveals a degraded catalytic site, a highly conserved kinase fold, and a putative regulatory binding site. Structure 17: 128-138.
16. Vega FM, Sevilla A, Lazo PA, (2004) p53 Stabilization and accumulation induced by human vaccinia-related kinase 1. Mol Cell Biol 24: 10366-10380.
17. Neumann B, Walter T, Heriche JK, Bulkescher J, Erfle H, et al. (2010) Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes. Nature 464: 721-727.
18. Valbuena A, Sanz-Garcia M, Lopez-Sanchez I, Vega FM, Lazo PA, (2011) Roles of VRK1 as a new player in the control of biological processes required for cell division. Cell Signal 23: 1267-1272.
19. 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.
20. 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.
21. 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.
22. Blanco S, Klimcakova L, Vega FM, Lazo PA, (2006) The subcellular localization of vaccinia-related kinase-2 (VRK2) isoforms determines their different effect on p53 stability in tumour cell lines. Febs J 273: 2487-2504.
23. Sanz-Garcia M, Lopez-Sanchez I, Lazo PA, (2008) Proteomics identification of nuclear Ran GTPase as an inhibitor of human VRK1 and VRK2 (vaccinia-related kinase) activities. Mol Cell Proteomics 7: 2199-2214.
24. Scott JD, Pawson T, (2009) Cell signaling in space and time: where proteins come together and when they're apart. Science 326: 1220-1224.
25. Valbuena A, Suarez-Gauthier A, Lopez-Rios F, Lopez-Encuentra A, Blanco S, et al. (2007) Alteration of the VRK1-p53 autoregulatory loop in human lung carcinomas. Lung Cancer 58: 303-309.
26. Finetti P, Cervera N, Charafe-Jauffret E, Chabannon C, Charpin C, et al. (2008) Sixteen-kinase gene expression identifies luminal breast cancers with poor prognosis. Cancer Res 68: 767-776.
27. Fournier MV, Martin KJ, Kenny PA, Xhaja K, Bosch I, et al. (2006) Gene expression signature in organized and growth-arrested mammary acini predicts good outcome in breast cancer. Cancer Res 66: 7095-7102.
28. Kang TH, Park DY, Kim W, Kim KT, (2008) VRK1 phosphorylates CREB and mediates CCND1 expression. J Cell Sci 121: 3035-3041.
29. Kang TH, Park DY, Choi YH, Kim KJ, Yoon HS, et al. (2007) Mitotic histone H3 phosphorylation by vaccinia-related kinase 1 in mammalian cells. Mol Cell Biol 27: 8533-8546.
30. Kilpinen S, Ojala K, Kallioniemi O, (2010) Analysis of kinase gene expression patterns across 5681 human tissue samples reveals functional genomic taxonomy of the kinome. PLoS ONE 5: e15068.
31. Karaman MW, Herrgard S, Treiber DK, Gallant P, Atteridge CE, et al. (2008) A quantitative analysis of kinase inhibitor selectivity. Nat Biotechnol 26: 127-132.
32. Andreani A, Cavalli A, Granaiola M, Leoni A, Locatelli A, et al. (2000) Imidazo[2,1-b]thiazolylmethylene- and indolylmethylene-2-indolinones: a new class of cyclin-dependent kinase inhibitors. Design, synthesis, and CDK1/cyclin B inhibition. Anticancer Drug Des 15: 447-452.
33. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, et al. (2007) The selectivity of protein kinase inhibitors: a further update. Biochem J 408: 297-315.
34. De Azevedo WF, Leclerc S, Meijer L, Havlicek L, Strnad M, et al. (1997) Inhibition of cyclin-dependent kinases by purine analogues: crystal structure of human cdk2 complexed with roscovitine. Eur J Biochem 243: 518-526.
35. Gautschi O, Heighway J, Mack PC, Purnell PR, Lara PN Jr, et al. (2008) Aurora kinases as anticancer drug targets. Clin Cancer Res 14: 1639-1648.
36. Han Z, Pantazis P, Lange TS, Wyche JH, Hendrickson EA, (2000) The staurosporine analog, Ro-31-8220, induces apoptosis independently of its ability to inhibit protein kinase C. Cell Death Differ 7: 521-530.
37. Kojima I, Mogami H, Shibata H, Ogata E, (1993) Role of calcium entry and protein kinase C in the progression activity of insulin-like growth factor-I in Balb/c 3T3 cells. J Biol Chem 268: 10003-10006.
38. Yeo EJ, Provost JJ, Exton JH, (1997) Dissociation of tyrosine phosphorylation and activation of phosphoinositide phospholipase C induced by the protein kinase C inhibitor Ro-31-8220 in Swiss 3T3 cells treated with platelet-derived growth factor. Biochim Biophys Acta 1356: 308-320.
39. Keller HU, Niggli V, (1993) The PKC-inhibitor Ro 31-8220 selectively suppresses PMA- and diacylglycerol-induced fluid pinocytosis and actin polymerization in PMNs. Biochem Biophys Res Commun 194: 1111-1116.
40. Mahon TM, Matthews JS, O'Neill LA, (1997) Staurosporine, but not Ro 31-8220, induces interleukin 2 production and synergizes with interleukin 1alpha in EL4 thymoma cells. Biochem J 325 (Pt 1): 39-45.
41. Alessi DR, (1997) The protein kinase C inhibitors Ro 318220 and GF 109203X are equally potent inhibitors of MAPKAP kinase-1beta (Rsk-2) and p70 S6 kinase. FEBS Lett 402: 121-123.
42. Deak M, Clifton AD, Lucocq LM, Alessi DR, (1998) Mitogen- and stress-activated protein kinase-1 (MSK1) is directly activated by MAPK and SAPK2/p38, and may mediate activation of CREB. Embo J 17: 4426-4441.
43. Tamaoki T, Nomoto H, Takahashi I, Kato Y, Morimoto M, et al. (1986) Staurosporine, a potent inhibitor of phospholipid/Ca++dependent protein kinase. Biochem Biophys Res Commun 135: 397-402.
44. Zabludoff SD, Deng C, Grondine MR, Sheehy AM, Ashwell S, et al. (2008) AZD7762, a novel checkpoint kinase inhibitor, drives checkpoint abrogation and potentiates DNA-targeted therapies. Mol Cancer Ther 7: 2955-2966.
45. Mitchell JB, Choudhuri R, Fabre K, Sowers AL, Citrin D, et al. (2010) In vitro and in vivo radiation sensitization of human tumor cells by a novel checkpoint kinase inhibitor, AZD7762. Clin Cancer Res 16: 2076-2084.
46. Behrend L, Milne DM, Stoter M, Deppert W, Campbell LE, et al. (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.
47. Cheong JK, Hung NT, Wang H, Tan P, Voorhoeve PM, et al. (2011) IC261 induces cell cycle arrest and apoptosis of human cancer cells via CK1delta/varepsilon and Wnt/beta-catenin independent inhibition of mitotic spindle formation. Oncogene.
48. Stoter M, Bamberger AM, Aslan B, Kurth M, Speidel D, et al. (2005) Inhibition of casein kinase I delta alters mitotic spindle formation and induces apoptosis in trophoblast cells. Oncogene 24: 7964-7975.
49. Martinez A, Alonso M, Castro A, Perez C, Moreno FJ, (2002) First non-ATP competitive glycogen synthase kinase 3 beta (GSK-3beta) inhibitors: thiadiazolidinones (TDZD) as potential drugs for the treatment of Alzheimer's disease. J Med Chem 45: 1292-1299.
50. Savage MJ, Gingrich DE, (2009) Advances in the Development of Kinase Inhibitor Therapeutics for Alzheimer's Disease. Drug Develop Res 70: 125-144.
51. Santos CR, Vega FM, Blanco S, Barcia R, Lazo PA, (2004) The vaccinia virus B1R kinase induces p53 downregulation by an Mdm2-dependent mechanism. Virology 328: 254-265.
52. Knight ZA, Lin H, Shokat KM, (2010) Targeting the cancer kinome through polypharmacology. Nat Rev Cancer 10: 130-137.
53. MacKeigan JP, Murphy LO, Blenis J, (2005) Sensitized RNAi screen of human kinases and phosphatases identifies new regulators of apoptosis and chemoresistance. Nat Cell Biol 7: 591-600.
54. Valbuena A, Lopez-Sanchez I, Lazo PA, (2008) Human VRK1 is an early response gene and its loss causes a block in cell cycle progression. PLoS ONE 3: e1642.
55. Blanco S, Santos C, Lazo PA, (2007) Vaccinia-related kinase 2 modulates the stress response to hypoxia mediated by TAK1. Mol Cell Biol 27: 7273-7283.
56. Blanco S, Sanz-Garcia M, Santos CR, Lazo PA, (2008) Modulation of interleukin-1 transcriptional response by the interaction between VRK2 and the JIP1 scaffold protein. PLoS ONE 3: e1660.
57. Fernandez IF, Blanco S, Lozano J, Lazo PA, (2010) VRK2 Inhibits Mitogen-Activated Protein Kinase Signaling and Inversely Correlates with ErbB2 in Human Breast Cancer. Mol Cell Biol 30: 4687-4697.
58. Morgan MA, Parsels LA, Zhao L, Parsels JD, Davis MA, et al. (2010) Mechanism of radiosensitization by the Chk1/2 inhibitor AZD7762 involves abrogation of the G2 checkpoint and inhibition of homologous recombinational DNA repair. Cancer Res 70: 4972-4981.
59. Nishijo K, Chen QR, Zhang L, McCleish AT, Rodriguez A, et al. (2009) Credentialing a preclinical mouse model of alveolar rhabdomyosarcoma. Cancer Res 69: 2902-2911.
60. Martin KJ, Patrick DR, Bissell MJ, Fournier MV, (2008) Prognostic breast cancer signature identified from 3D culture model accurately predicts clinical outcome across independent datasets. PLoS ONE 3: e2994.
61. Lochhead PA, (2009) Protein kinase activation loop autophosphorylation in cis: overcoming a Catch-22 situation. Sci Signal 2: pe4.
62. Eswaran J, Knapp S, (2010) Insights into protein kinase regulation and inhibition by large scale structural comparison. Biochim Biophys Acta 1804: 429-432.
63. Valbuena A, Lopez-Sanchez I, Vega FM, Sevilla A, Sanz-Garcia M, et al. (2007) Identification of a dominant epitope in human vaccinia-related kinase 1 (VRK1) and detection of different intracellular subpopulations. Arch Biochem Biophys 465: 219-226.