Sensitivity of the kinase activity of human vaccinia-related kinase proteins to toxic metals

Journal of Biological Inorganic Chemistry

Volumn 18, Issue 4, 2013, Pages 473-482

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

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^b UNIVERSITY OF SALAMANCA   (Spain)

^c HOSPITAL UNIVERSITARIO DE SALAMANCA   (Spain)

Author keywords

B1R; Kinase inhibition; Phosphorylation; VRK1; VRK2

Indexed keywords

CADMIUM; COBALT; COPPER; GROWTH FACTOR; HISTONE H3; HUMAN VACCINIA RELATED KINASE; HUMAN VACCINIA RELATED KINASE 1; HUMAN VACCINIA RELATED KINASE 2; LEAD; MERCURY; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN P53; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG;

ARTICLE; ASSAY; AUTOPHOSPHORYLATION; BIOACCUMULATION; CELL CYCLE REGULATION; CELL STRESS; CHEMOSENSITIVITY; CONTROLLED STUDY; DEGENERATIVE DISEASE; DISEASE ASSOCIATION; DNA DAMAGE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; INTOXICATION; NEOPLASM; PATHOGENESIS; PHOSPHORYLATION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VACCINIA; WILSON DISEASE;

DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; HUMANS; INHIBITORY CONCENTRATION 50; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; METALS, HEAVY; PROTEIN-SERINE-THREONINE KINASES;

EID: 84876502231     PISSN: 09498257     EISSN: 14321327     Source Type: Journal    
DOI: 10.1007/s00775-013-0992-6     Document Type: Article

References (62)

1. Hu H (2012) Heavy metal poisoning. In: Longo D, Fauci A, Kasper D, Hauser S, Jameson J, Loscalzo J (eds) Harrison's principles of internal medicine. McGraw-Hill, New York
2. Manning G, Whyte DB, Martinez R et al (2002) The protein kinase complement of the human genome. Science 298:1912-1934
3. 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
4. Nichols RJ, Traktman P (2004) Characterization of three paralogous members of the mammalian vaccinia related kinase family. J Biol Chem 279:7934-7946
5. 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
6. 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
7. 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
8. Santos CR, Rodriguez-Pinilla M, Vega FM 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
9. 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
10. Sevilla A, Santos CR, Barcia R et al (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
11. 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
12. Kang TH, Park DY, Kim W, Kim KT (2008) VRK1 phosphorylates CREB and mediates CCND1 expression. J Cell Sci 121:3035-3041
13. Kang TH, Park DY, Choi YH et al (2007) Mitotic histone H3 phosphorylation by vaccinia-related kinase 1 in mammalian cells. Mol Cell Biol 27:8533-8546
14. 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
15. Kussie PH, Gorina S, Marechal V et al (1996) Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain. Science 274:948-953
16. Teufel DP, Bycroft M, Fersht AR (2009) Regulation by phosphorylation of the relative affinities of the N-terminal transactivation domains of p53 for p300 domains and Mdm2. Oncogene 28:2112-2118
17. Meek DW, Anderson CW (2009) Posttranslational Modification of p53: Cooperative Integrators of Function. Cold Spring Harb Perspect Biol 1:a000950
18. Valbuena A, Sanz-Garcia M, Lopez-Sanchez I et al (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-Sanchez I, Sanz-Garcia M, Lazo PA (2009) Plk3 interacts with and specifically phosphorylates VRK1 in Ser342, a downstream target in a pathway that induces Golgi fragmentation. Mol Cell Biol 29:1189-1201
20. Sanz-Garcia M, Monsalve DM, Sevilla A, Lazo PA (2012) Vaccinia-related Kinase 1 (VRK1) is an upstream nucleosomal kinase required for the assembly of 53BP1 foci in response to ionizing radiation-induced DNA damage. J Biol Chem 287:23757-23768
21. Renbaum P, Kellerman E, Jaron R et al (2009) Spinal muscular atrophy with pontocerebellar hypoplasia is caused by a mutation in the VRK1 gene. Am J Hum Genet 85:281-289
22. Nichols RJ, Wiebe MS, Traktman P (2006) The vaccinia-related kinases phosphorylate the N' terminus of BAF, regulating its interaction with DNA and its retention in the nucleus. Mol Biol Cell 17:2451-2464
23. Gorjanacz M, Klerkx EP, Galy V 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
24. Montes de Oca R, Shoemaker CJ, Gucek M et al (2009) Barrier-to- autointegration factor proteome reveals chromatin-regulatory partners. PLoS ONE 4:e7050
25. Dauer WT, Worman HJ (2009) The nuclear envelope as a signaling node in development and disease. Dev Cell 17:626-638
26. Rass U, Ahel I, West SC (2007) Defective DNA repair and neurodegenerative disease. Cell 130:991-1004
27. 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
28. 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
29. 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
30. Fernandez IF, Perez-Rivas LG, Blanco S et al (2012) VRK2 anchors KSR1-MEK1 to endoplasmic reticulum forming a macromolecular complex that compartmentalizes MAPK signaling. Cell Mol Life Sci 69:3881-3893
31. Steinberg S, de Jong S, Andreassen OA et al (2011) Common variants at VRK2 and TCF4 conferring risk of schizophrenia. Hum Mol Genet 20:4076-4081
32. Vazquez-Cedeira M, Lazo PA (2012) Human VRK2 (Vaccinia-related Kinase 2) modulates tumor cell invasion by hyperactivation of NFAT1 and expression of cyclooxygenase-2. J Biol Chem 287:42739-42750
33. Shin J, Chakraborty G, Bharatham N et al (2011) NMR solution structure of human vaccinia-related kinase 1 (VRK1) reveals the C-terminal tail essential for its structural stability and autocatalytic activity. J Biol Chem 286:22131-22138
34. Scheeff ED, Eswaran J, Bunkoczi G et al (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
35. Fedorov O, Marsden B, Pogacic V et al (2007) A systematic interaction map of validated kinase inhibitors with Ser/Thr kinases. Proc Natl Acad Sci USA 104:20523-20528
36. Fedorov O, Sundstrom M, Marsden B, Knapp S (2007) Insights for the development of specific kinase inhibitors by targeted structural genomics. Drug Discov Today 12:365-372
37. Vazquez-Cedeira M, Barcia-Sanjurjo I, Sanz-Garcia M et al (2011) Differential inhibitor sensitivity between human kinases VRK1 and VRK2. PLoS ONE 6:e23235
38. Santos CR, Vega FM, Blanco S et al (2004) The vaccinia virus B1R kinase induces p53 downregulation by an Mdm2-dependent mechanism. Virology 328:254-265
39. Valbuena A, Lopez-Sanchez I, Vega FM 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
40. Barcia R, Lopez-Borges S, Vega FM, Lazo PA (2002) Kinetic properties of p53 phosphorylation by the human vaccinia-related kinase 1. Arch Biochem Biophys 399:1-5
41. Monsalve DM, Merced T, Fernandez IF et al (2013) Cell Death Dis 4:e513. doi: 10.1038/cddis.2013.40
42. Foulkes EC (2000) Transport of toxic heavy metals across cell membranes. Proc Soc Exp Biol Med 223:234-240
43. Banham AH, Leader DP, Smith GL (1993) Phosphorylation of ribosomal proteins by the vaccinia virus B1R protein kinase. FEBS Lett 321:27-31
44. Speizer LA, Watson MJ, Kanter JR, Brunton LL (1989) Inhibition of phorbol ester binding and protein kinase C activity by heavy metals. J Biol Chem 264:5581-5585
45. Koga M, Zwaal R, Guan KL et al (2000) A Caenorhabditis elegans MAP kinase kinase, MEK-1, is involved in stress responses. EMBO J 19:5148-5156
46. Kim DH, Liberati NT, Mizuno T et al (2004) Integration of Caenorhabditis elegans MAPK pathways mediating immunity and stress resistance by MEK-1 MAPK kinase and VHP-1 MAPK phosphatase. Proc Natl Acad Sci USA 101:10990-10994
47. Wiebe MS, Nichols RJ, Molitor TP et al (2010) Mice deficient in the serine/threonine protein kinase VRK1 are infertile due to a progressive loss of spermatogonia. Biol Reprod 82:182-193
48. Schober CS, Aydiner F, Booth CJ et al (2011) The kinase VRK1 is required for normal meiotic progression in mammalian oogenesis. Mech Dev 128:178-190
49. Choi YH, Park CH, Kim W et al (2010) Vaccinia-related kinase 1 is required for the maintenance of undifferentiated spermatogonia in mouse male germ cells. PLoS ONE 5:e15254
50. Sanz-Garcia M, Vazquez-Cedeira M, Kellerman E et al (2011) Substrate profiling of human vaccinia-related kinases identifies coilin, a Cajal body nuclear protein, as a phosphorylation target with neurological implications. J Proteomics 75:548-560
51. Walker MP, Tian L, Matera AG (2009) Reduced viability, fertility and fecundity in mice lacking the cajal body marker protein, coilin. PLoS ONE 4:e6171
52. Brewer GJ (2008) Wilson′s disease. In: Fauci AS, Braunwald E, Kasper DL, Hauser SL, Longo DL, Jameson JL, Loscalzo J (eds) Harrison's principles of internal medicine. McGraw-Hill, New York, pp 2449-2452
53. Sharma HS, Muresanu DF, Patnaik R et al (2011) Superior neuroprotective effects of cerebrolysin in heat stroke following chronic intoxication of Cu or Ag engineered nanoparticles. A comparative study with other neuroprotective agents using biochemical and morphological approaches in the rat. J Nanosci Nanotechnol 11:7549-7569
54. O'Halloran TV, Culotta VC (2000) Metallochaperones, an intracellular shuttle service for metal ions. J Biol Chem 275:25057-25060
55. Xu F, Farkas S, Kortbeek S et al (2012) Mercury-induced toxicity of rat cortical neurons is mediated through N-methyl-D-aspartate receptors. Mol Brain 5:30
56. Korogi Y, Takahashi M, Shinzato J, Okajima T (1994) MR findings in seven patients with organic mercury poisoning (Minamata disease). Am J Neuroradiol 15:1575-1578
57. Vega FM, Sevilla A, Lazo PA (2004) p53 Stabilization and accumulation induced by human vaccinia-related kinase 1. Mol Cell Biol 24:10366-10380
58. Valbuena A, Blanco S, Vega FM, Lazo PA (2008) The C/H3 domain of p300 is required to protect VRK1 and VRK2 from their downregulation induced by p53. PLoS ONE 3:e2649
59. Valbuena A, Castro-Obregon S, Lazo PA (2011) Downregulation of VRK1 by p53 in response to DNA damage is mediated by the autophagic pathway. PLoS ONE 6:e17320
60. Valbuena A, Vega FM, Blanco S, Lazo PA (2006) p53 downregulates its activating vaccinia-related kinase 1, forming a new autoregulatory loop. Mol Cell Biol 26:4782-4793
61. Lee CW, Ferreon JC, Ferreon AC et al (2010) Graded enhancement of p53 binding to CREB-binding protein (CBP) by multisite phosphorylation. Proc Natl Acad Sci USA 107:19290-19295
62. Kim W, Chakraborty G, Kim S et al (2012) Macro histone H2A1.2 (macroH2A1) protein suppresses mitotic kinase VRK1 during interphase. J Biol Chem 287:5278-5289