Nucleocytoplasmic shuttling of human inositol phosphate multikinase is influenced by CK2 phosphorylation

Biological Chemistry

Volumn 393, Issue 3, 2012, Pages 149-160

  Meyer, Rüdiger ^a   Nalaskowski, Marcus M ^a   Ehm, Patrick ^a   Schröder, Constantin ^a   Naj, Xenia ^a   Brehm, Maria A ^a   Mayr, Georg W ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

IPMK; Nuclear export signal; Nuclear import signal; Protein phosphorylation

Indexed keywords

CASEIN KINASE II; INOSITOL PHOSPHATE; INOSITOL PHOSPHATE MULTIKINASE; NUCLEAR PROTEIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NUCLEAR EXPORT SIGNAL; NUCLEAR IMPORT SIGNAL; NUCLEAR LOCALIZATION SIGNAL; PHOSPHATE METABOLISM; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SEQUENCE; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CASEIN KINASE II; CELL LINE; CELL NUCLEUS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOPLASM; HUMANS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN SORTING SIGNALS; SEQUENCE ALIGNMENT;

RAPTORES;

EID: 84859863112     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2011-0209     Document Type: Article

References (50)

1. Back, J.H. and Kim, A.L. (2011). The expanding relevance of nuclear mTOR in carcinogenesis. Cell Cycle 10, 3849-3852.
2. Bercy, J., Dubois, E., and Messenguy, F. (1987). Regulation of arginine metabolism in Saccharomyces cerevisiae: expression of the three ARGR regulatory genes and cellular localization of their products. Gene 55, 277-285.
3. Blom, N., Sicheritz-Ponten, T., Gupta, R., Gammeltoft, S., and Brunak S. (2004). Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4, 1633-1649. (Pubitemid 38738322)
4. Bontems, S., Di Valentin, E., Baudoux, L., Rentier, B., Sadzot-Delvaux, C., and Piette, J. (2002). Phosphorylation of varicella-zoster virus IE63 protein by casein kinases influences its cellular localization and gene regulation activity. J. Biol. Chem. 277, 21050-21060. (Pubitemid 34967416)
5. Brehm, M.A., Schenk, T.M., Zhou, X., Fanick, W., Lin, H., Windhorst, S., Nalaskowski, M.M., Kobras, M., Shears, S.B., and Mayr, G.W. (2007). Intracellular localization of human Ins(1,3,4,5,6) P5 2-kinase. Biochem. J. 408, 335-345.
6. Cantley, L.C. (2002). The phosphoinositide 3-kinase pathway. Science 296, 1655-1657. (Pubitemid 34579158)
7. Chakraborty, A., Werner, J.K. Jr., Koldobskiy, M.A., Mustafa, A.K., Juluri, K.R., Pietropaoli, J., Snowman, A.M., and Snyder, S.H. (2011). Casein kinase-2 mediates cell survival through phosphorylation and degradation of inositol hexakisphosphate kinase-2. Proc. Natl. Acad. Sci. USA 108, 2205-2209.
8. Chang, S.C. and Majerus, P.W. (2006). Inositol polyphosphate multikinase regulates inositol 1,4,5,6-tetrakisphosphate. Biochem. Biophys. Res. Commun. 339, 209-216. (Pubitemid 41697537)
9. Foster, K.G. and Fingar, D.C. (2010). Mammalian target of rapamycin (mTOR): conducting the cellular signaling symphony. J. Biol. Chem. 285, 14071-14077.
10. Frederick, J.P., Mattiske, D., Wofford, J.A., Megosh, L.C., Drake, L.Y., Chiou, S.T., Hogan, B.L., and York, J.D. (2005). An essential role for an inositol polyphosphate multikinase, Ipk2, in mouse embryogenesis and second messenger production. Proc. Natl. Acad. Sci. USA 102, 8454-8459. (Pubitemid 40862757)
11. Fujii, M. and York, J.D. (2005). A role for rat inositol polyphosphate kinases rIPK2 and rIPK1 in inositol pentakisphosphate and inositol hexakisphosphate production in rat-1 cells. J. Biol. Chem. 280, 1156-1164.
12. Hanakahi, L.A., Bartlet-Jones, M., Chappell, C., Pappin, D., and West, S.C. (2000). Binding of inositol phosphate to DNA-PK and stimulation of double-strand break repair. Cell 102, 721-729.
13. Harreman, M.T., Kline, T.M., Milford, H.G., Harben, M.B., Hodel, A.E., and Corbett, A.H. (2004). Regulation of nuclear import by phosphorylation adjacent to nuclear localization signals. J. Biol. Chem. 279, 20613-20621. (Pubitemid 38656455)
14. Irvine, R.F. and Schell, M.J. (2001). Back in the water: the return of the inositol phosphates. Nat. Rev. Mol. Cell Biol. 2, 327-338. (Pubitemid 33674045)
15. Jans, D.A. and Hubner, S. (1996). Regulation of protein transport to the nucleus: central role of phosphorylation. Physiol. Rev. 76, 651-685. (Pubitemid 26286075)
16. Jeganathan, S., Hascher, A., Chinnathambi, S., Biernat, J., Mandelkow, E.M., and Mandelkow, E. (2008). Proline-directed pseudo-phosphorylation at AT8 and PHF1 epitopes induces a compaction of the paperclip folding of Tau and generates a pathological (MC-1) conformation. J. Biol. Chem. 283, 32066-32076.
17. Kaffman, A. and O'Shea, E.K. (1999). Regulation of nuclear localization: a key to a door. Annu. Rev. Cell Dev. Biol. 15, 291-339. (Pubitemid 32250378)
18. Kim, S., Kim, S.F., Maag, D., Maxwell, M.J., Resnick, A.C., Juluri, K.R., Chakraborty, A., Koldobskiy, M.A., Cha, S.H., Barrow, R., et al. (2011). Amino acid signaling to mTOR mediated by inositol polyphosphate multikinase. Cell Metab. 13, 215-221.
19. la Cour, T., Kiemer, L., Molgaard, A., Gupta, R., Skriver, K., and Brunak, S. (2004). Analysis and prediction of leucine-rich nuclear export signals. Protein Eng. Des. Sel. 17, 527-536. (Pubitemid 39487532)
20. Litchfield, D.W. (2003). Protein kinase CK2: structure, regulation and role in cellular decisions of life and death. Biochem. J. 369, 1-15. (Pubitemid 36174119)
21. Litchfield, D.W. and Luscher, B. (1993). Casein kinase II in signal transduction and cell cycle regulation. Mol. Cell. Biochem. 127-128, 187-199. (Pubitemid 24032665)
22. Luo, H.R., Huang, Y.E., Chen, J.C., Saiardi, A., Iijima, M., Ye, K., Huang, Y., Nagata, E., Devreotes, P., and Snyder, S.H. (2003). Inositol pyrophosphates mediate chemotaxis in Dictyostelium via pleckstrin homology domain-PtdIns(3,4,5)P3 interactions. Cell 114, 559-572. (Pubitemid 37159253)
23. Maag, D., Maxwell, M.J., Hardesty, D.A., Boucher, K.L., Choudhari, N., Hanno, A.G., Ma, J.F., Snowman, A.S., Pietropaoli, J.W., Xu, R., et al. (2011). Inositol polyphosphate multikinase is a physiologic PI3-kinase that activates Akt/PKB. Proc. Natl. Acad. Sci. USA 108, 1391-1396.
24. Mayr, G.W., Windhorst, S., and Hillemeier, K. (2005). Antiproliferative plant and synthetic polyphenolics are specific inhibitors of vertebrate inositol-1,4,5-trisphosphate 3-kinases and inositol polyphosphate multikinase. J. Biol. Chem. 280, 13229-13240. (Pubitemid 40517206)
25. Montenarh, M. (2010). Cellular regulators of protein kinase CK2. Cell Tissue Res. 342, 139-146.
26. Morgan-Lappe, S., Woods, K.W., Li, Q., Anderson, M.G., Schurdak, M.E., Luo, Y., Giranda, V.L., Fesik, S.W., and Leverson, J.D. (2006). RNAi-based screening of the human kinome identifies Akt-cooperating kinases: a new approach to designing efficacious multitargeted kinase inhibitors. Oncogene 25, 1340-1348. (Pubitemid 43336462)
27. Nalaskowski, M.M., Deschermeier, C., Fanick, W., and Mayr, G.W. (2002). The human homologue of yeast ArgRIII protein is an inositol phosphate multikinase with predominantly nuclear localization. Biochem. J. 366, 549-556. (Pubitemid 35001699)
28. Odom, A.R., Stahlberg, A., Wente, S.R., and York, J.D. (2000). A role for nuclear inositol 1,4,5-trisphosphate kinase in transcriptional control. Science 287, 2026-2029. (Pubitemid 30158681)
29. Poon, I.K. and Jans, D.A. (2005). Regulation of nuclear transport: central role in development and transformation? Traffic 6, 173-186. (Pubitemid 40298152)
30. Remus, T.P., Zima, A.V., Bossuyt, J., Bare, D.J., Martin, J.L., Blatter, L.A., Bers, D.M., and Mignery, G.A. (2006). Biosensors to measure inositol 1,4,5-trisphosphate concentration in living cells with spatiotemporal resolution. J. Biol. Chem. 281, 608-616. (Pubitemid 43671224)
31. Resnick, A.C., Snowman, A.M., Kang, B.N., Hurt, K.J., Snyder, S.H., and Saiardi, A. (2005). Inositol polyphosphate multikinase is a nuclear PI3-kinase with transcriptional regulatory activity. Proc. Natl. Acad. Sci. USA 102, 12783-12788. (Pubitemid 41279443)
32. Rihs, H.P., Jans, D.A., Fan, H., and Peters, R. (1991). The rate of nuclear cytoplasmic protein transport is determined by the casein kinase II site flanking the nuclear localization sequence of the SV40 T-antigen. EMBO J. 10, 633-639. (Pubitemid 21905517)
33. Ruzzene, M., Penzo, D., and Pinna, L.A. (2002). Protein kinase CK2 inhibitor 4,5,6,7-tetrabromobenzotriazole (TBB) induces apoptosis and caspase-dependent degradation of haematopoietic lineage cell-specific protein 1 (HS1) in Jurkat cells. Biochem. J. 364, 41-47. (Pubitemid 34538944)
34. Saiardi, A., Caffrey, J.J., Snyder, S.H., and Shears, S.B. (2000). Inositol polyphosphate multikinase (ArgRIII) determines nuclear mRNA export in Saccharomyces cerevisiae. FEBS Lett. 468, 28-32. (Pubitemid 30101676)
35. Saiardi, A., Nagata, E., Luo, H.R., Sawa, A., Luo, X., Snowman, A.M., and Snyder, S.H. (2001a). Mammalian inositol polyphosphate multikinase synthesizes inositol 1,4,5-trisphosphate and an inositol pyrophosphate. Proc. Natl. Acad. Sci. USA 98, 2306-2311. (Pubitemid 32209478)
36. Saiardi, A., Nagata, E., Luo, H.R., Snowman, A.M., and Snyder, S.H. (2001b). Identification and characterization of a novel inositol hexakisphosphate kinase. J. Biol. Chem. 276, 39179-39185.
37. Saiardi, A., Resnick, A.C., Snowman, A.M., Wendland, B., and Snyder, S.H. (2005). Inositol pyrophosphates regulate cell death and telomere length through phosphoinositide 3-kinase-related protein kinases. Proc. Natl. Acad. Sci. USA 102, 1911-1914. (Pubitemid 40261986)
38. Seeds, A.M., Sandquist, J.C., Spana, E.P., and York, J.D. (2004). A molecular basis for inositol polyphosphate synthesis in Drosophila melanogaster. J. Biol. Chem. 279, 47222-47232. (Pubitemid 39518379)
39. Shen, X., Xiao, H., Ranallo, R., Wu, W.H., and Wu, C. (2003). Modulation of ATP-dependent chromatin-remodeling complexes by inositol polyphosphates. Science 299, 112-114. (Pubitemid 36042414)
40. Sorokin, A.V., Kim, E.R., and Ovchinnikov, L.P. (2007). Nucleocytoplasmic transport of proteins. Biochemistry (Mosc) 72, 1439-1457.
41. Steger, D.J., Haswell, E.S., Miller, A.L., Wente, S.R., and O'Shea, E.K. (2003). Regulation of chromatin remodeling by inositol polyphosphates. Science 299, 114-116. (Pubitemid 36042415)
42. Streb, H., Irvine, R.F., Berridge, M.J., and Schulz, I. (1983). Release of Ca 2 + from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol-1,4,5-trisphosphate. Nature 306, 67-69. (Pubitemid 13022768)
43. Verbsky, J. and Majerus, P.W. (2005). Increased levels of inositol hexakisphosphate (InsP6) protect HEK293 cells from tumor necrosis factor α- and Fas-induced apoptosis. J. Biol. Chem. 280, 29263-29268. (Pubitemid 41161380)
44. von Knethen, A., Tzieply, N., Jennewein, C., and Brune, B. (2009). Casein-kinase-II-dependent phosphorylation of PPARgamma provokes CRM1-mediated shuttling of PPARgamma from the nucleus to the cytosol. J. Cell Sci. 123, 192-201.
45. Wang, W. and Malcolm, B.A. (1999). Two-stage PCR protocol allowing introduction of multiple mutations, deletions and insertions using QuikChange site-directed mutagenesis. Biotechniques 26, 680-682.
46. Wolff, B., Sanglier, J.J., and Wang, Y. (1997). Leptomycin B is an inhibitor of nuclear export: inhibition of nucleo-cytoplasmic translocation of the human immunodeficiency virus type 1 (HIV-1) Rev protein and Rev-dependent mRNA. Chem. Biol. 4, 139-147. (Pubitemid 27161752)
47. Wright, C.S., van Steensel, M.A., Hodgins, M.B., and Martin, P.E. (2009). Connexin mimetic peptides improve cell migration rates of human epidermal keratinocytes and dermal fibroblasts in vitro. Wound Repair Regen. 17, 240-249.
48. Wright, C.S., Pollok, S., Flint, D.J., Brandner, J.M., and Martin, P.E. (2011). The connexin mimetic peptide Gap27 increases human dermal fibroblast migration in hyperglycemic and hyperinsulinemic conditions in vitro. J. Cell. Physiol. 227, 77-87.
49. Xia, H.J., Brearley, C., Elge, S., Kaplan, B., Fromm, H., and Mueller- Roeber, B. (2003). Arabidopsis inositol polyphosphate 6-/3- kinase is a nuclear protein that complements a yeast mutant lacking a functional ArgR-Mcm1 transcription complex. Plant Cell 15, 449-463. (Pubitemid 36229997)
50. York, J.D., Odom, A.R., Murphy, R., Ives, E.B., and Wente, S.R. (1999). A phospholipase C-dependent inositol polyphosphate kinase pathway required for efficient messenger RNA export. Science 285, 96-100. (Pubitemid 29307573)