Phosphorylation by casein kinase 2 regulates Nap1 localization and function

Molecular and Cellular Biology

Volumn 28, Issue 4, 2008, Pages 1313-1325

  Calvert, Meredith E K ^a   Keck, Kristin M ^a   Ptak, Celeste ^a   Shabanowitz, Jeffrey ^a   Hunt, Donald F ^a   Pemberton, Lucy F ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; PROTEIN; PROTEIN NAP1; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; ENZYME PHOSPHORYLATION; ENZYME REGULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; STRUCTURE ANALYSIS;

ACTIVE TRANSPORT, CELL NUCLEUS; CASEIN KINASE II; CELL CYCLE; CELL CYCLE PROTEINS; CELL NUCLEUS; CYCLIN B; HISTONES; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 38949106130     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01035-07     Document Type: Article

References (60)

1. Adachi, Y., G. N. Pavlakis, and T. D. Copeland. 1994. Identification and characterization of SET, a nuclear phosphoprotein encoded by the translocation break point in acute undifferentiated leukemia. J. Biol. Chem. 269:2258-2262.
2. Adachi, Y., G. N. Pavlakis, and T. D. Copeland. 1994. Identification of in vivo phosphorylation sites of SET, a nuclear phosphoprotein encoded by the translocation breakpoint in acute undifferentiated leukemia. FEBS Lett. 340:231-235.
3. Aitchison, J. D., M. P. Rout, M. Marelli, G. Blobel, and R. W. Wozniak. 1995. Two novel related yeast nucleoporins Nup170p and Nup157p: complementation with the vertebrate homologue Nup155p and functional interactions with the yeast nuclear pore-membrane protein Pom152p. J. Cell Biol. 131:1133-1148.
4. Akada, R., J. Yamamoto, and I. Yamashita. 1997. Screening and identification of yeast sequences that cause growth inhibition when overexpressed. Mol. Gen. Genet. 254:267-274.
5. Altman, R., and D. Kellogg. 1997. Control of mitotic events by Nap1 and the Gin4 kinase. J. Cell Biol. 138:119-130.
6. Arnaoutov, A., and M. Dasso. 2003. The Ran GTPase regulates kinetochore function. Dev. Cell 5:99-111.
7. Blom, N., S. Gammeltoft, and S. Brunak. 1999. Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 294:1351-1362.
8. Carazo-Salas, R. E., G. Guarguaglini, O. J. Gruss, A. Segref, E. Karsenti, and I. W. Mattaj. 1999. Generation of GTP-bound Ran by RCC1 is required for chromatin-induced mitotic spindle formation. Nature 400:178-181.
9. Dong, A., Z. Liu, Y. Zhu, F. Yu, Z. Li, K. Cao, and W. H. Shen. 2005. Interacting proteins and differences in nuclear transport reveal specific functions for the NAP1 family proteins in plants. Plant Physiol. 138:1446-1456.
10. Faust, M., J. Gunther, E. Morgenstern, M. Montenarh, and C. Gotz. 2002. Specific localization of the catalytic subunits of protein kinase CK2 at the centrosomes. Cell. Mol. Life Sci. 59:2155-2164.
11. Faust, M., N. Schuster, and M. Montenarh. 1999. Specific binding of protein kinase CK2 catalytic subunits to tubulin. FEBS Lett. 462:51-56.
12. Fernandez, J., L. Andrews, and S. M. Mische. 1994. An improved procedure for enzymatic digestion of polyvinylidene difluoride-bound proteins for internal sequence analysis. Anal. Biochem. 218:112-117.
13. Fornerod, M., J. Boer, S. van Baal, M. Jaegle, M. von Lindern, K. G. Murti, D. Davis, J. Bonten, A. Buijs, and G. Grosveld. 1995. Relocation of the carboxyterminal part of CAN from the nuclear envelope to the nucleus as a result of leukemia-specific chromosome rearrangements. Oncogene 10:1739-1748.
14. Fornerod, M., J. Boer, S. van Baal, H. Morreau, and G. Grosveld. 1996. Interaction of cellular proteins with the leukemia specific fusion proteins DEK-CAN and SET-CAN and their normal counterpart, the nucleoporin CAN. Oncogene 13:1801-1808.
15. Fujii-Nakata, T., Y. Ishimi, A. Okuda, and A. Kikuchi. 1992. Functional analysis of nucleosome assembly protein, NAP-1. The negatively charged COOH-terminal region is not necessary for the intrinsic assembly activity. J. Biol. Chem. 267:20980-20986.
16. Gal, T. Z., I. Glazer, A. Sherman, and H. Koltai. 2005. Protein interaction of nucleosome assembly protein 1 and casein kinase 2 during desiccation response in the insect-killing nematode Steinernema feltiae IS-6. J. Parasitol. 91:691-693.
17. Gavin, A. C., M. Bosche, R. Krause, P. Grandi, M. Marzioch, A. Bauer, J. Schultz, J. M. Rick, A. M. Michon, C. M. Cruciat, M. Remor, C. Hofert, M. Schelder, M. Brajenovic, H. Ruffner, A. Merino, K. Klein, M. Hudak, D. Dickson, T. Rudi, V. Gnau, A. Bauch, S. Bastuck, B. Huhse, C. Leutwein, M. A. Heurtier, R. R. Copley, A. Edelmann, E. Querfurth, V. Rybin, G. Drewes, M. Raida, T. Bouwmeester, P. Bork, B. Seraphin, B. Kuster, G. Neubauer, and G. Superti-Furga. 2002. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415:141-147.
18. Gharahdaghi, F., M. Kirchner, J. Fernandez, and S. M. Mische. 1996. Peptide-mass profiles of polyvinylidene difluoride-bound proteins by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry in the presence of nonionic detergents. Anal. Biochem. 233:94-99.
19. 2/M in Saccharomyces cerevisiae. J. Biol. Chem. 270:25905-25914.
20. Hosaka, K., T. Kodaki, and S. Yamashita. 1989. Cloning and characterization of the yeast CKI gene encoding choline kinase and its expression in Escherichia coli. J. Biol. Chem. 264:2053-2059.
21. Ishimi, Y., J. Hirosumi, W. Sato, K. Sugasawa, S. Yokota, F. Hanaoka, and M. Yamada. 1984. Purification and initial characterization of a protein which facilitates assembly of nucleosome-like structure from mammalian cells. Eur. J. Biochem. 142:431-439.
22. Ishimi, Y., W. Sato, M. Kojima, K. Sugasawa, F. Hanaoka, and M. Yamada. 1985. Rapid purification of nucleosome assembly protein (AP-I) and production of monoclonal antibodies against it. Cell Struct. Funct. 10:373-382.
23. Ito, T., M. Bulger, R. Kobayashi, and J. T. Kadonaga. 1996. Drosophila NAP-1 is a core histone chaperone that functions in ATP-facilitated assembly of regularly spaced nucleosomal arrays. Mol. Cell. Biol. 16:3112-3124.
24. Iwase, M., and A. Toh-e. 2001. Nis1 encoded by YNL078W: a new neck protein of Saccharomyces cerevisiae. Genes Genet. Syst. 76:335-343.
25. Kellogg, D. R., and A. W. Murray. 1995. NAP1 acts with Clb2 to perform mitotic functions and to suppress polar bud growth in budding yeast. J. Cell Biol. 130:675-685.
26. Krek, W., G. Maridor, and E. A. Nigg. 1992. Casein kinase II is a predominantly nuclear enzyme. J. Cell Biol. 116:43-55.
27. Krick, R., A. Aschrafi, D. Hasgun, and J. Arnemann. 2006. CK2-dependent C-terminal phosphorylation at T300 directs the nuclear transport of TSPY protein. Biochem. Biophys. Res. Commun. 341:343-350.
28. Lew, D. J., and S. I. Reed. 1993. Morphogenesis in the yeast cell cycle: regulation by Cdc28 and cyclins. J. Cell Biol. 120:1305-1320.
29. Li, H. Y., and Y. Zheng. 2004. Phosphorylation of RCC1 in mitosis is essential for producing a high RanGTP concentration on chromosomes and for spindle assembly in mammalian cells. Genes Dev. 18:512-527.
30. Li, M., A. Makkinje, and Z. Damuni. 1996. The myeloid leukemia-associated protein SET is a potent inhibitor of protein phosphatase 2A. J. Biol. Chem. 271:11059-11062.
31. Li, M., D. Strand, A. Krehan, W. Pyerin, H. Heid, B. Neumann, and B. M. Mechler. 1999. Casein kinase 2 binds and phosphorylates the nucleosome assembly protein-1 (NAP1) in Drosophila melanogaster. J. Mol. Biol. 293:1067-1084.
32. Litchfield, D. W. 2003. Protein kinase CK2: structure, regulation and role in cellular decisions of life and death. Biochem. J. 369:1-15.
33. Longhese, M. P., M. Clerici, and G. Lucchini. 2003. The S-phase checkpoint and its regulation in Saccharomyces cerevisiae Mutat. Res. 532:41-58.
34. Longtine, M. S., C. L. Theesfeld, J. N. McMillan, E. Weaver, J. R. Pringle, and D. J. Lew. 2000. Septin-dependent assembly of a cell cycle-regulatory module in Saccharomyces cerevisiae. Mol. Cell. Biol. 20:4049-4061.
35. Lorch, Y., B. Maier-Davis, and R. D. Kornberg. 2006. Chromatin remodeling by nucleosome disassembly in vitro. Proc. Natl. Acad. Sci. USA 103:3090-3093.
36. McMillan, J. N., M. S. Longtine, R. A. Sia, C. L. Theesfeld, E. S. Bardes, J. R. Pringle, and D. J. Lew. 1999. The morphogenesis checkpoint in Saccharomyces cerevisiae: cell cycle control of Swe1p degradation by Hsl1p and Hsl7p. Mol. Cell. Biol. 19:6929-6939.
37. Miyaji-Yamaguchi, M., K. Kato, R. Nakano, T. Akashi, A. Kikuchi, and K. Nagata. 2003. Involvement of nucleocytoplasmic shuttling of yeast Nap1 in mitotic progression. Mol. Cell. Biol. 23:6672-6684.
38. Mortensen, E. M., H. McDonald, J. Yates III, and D. R. Kellogg. 2002. Cell cycle-dependent assembly of a Gin4-septin complex. Mol. Biol. Cell 13:2091-2105.
39. Mosammaparast, N., B. D. del Rosario, and L. F. Pemberton. 2005. Modulation of histone deposition by the karyopherin Kap114p. Mol. Cell. Biol. 25:1764-1778.
40. Mosammaparast, N., C. S. Ewart, and L. F. Pemberton. 2002. A role for nucleosome assembly protein 1 in the nuclear transport of histones H2A and H2B. EMBO J. 21:6527-6538.
41. Mosammaparast, N., K. R. Jackson, Y. Guo, C. J. Brame, J. Shabanowitz, D. F. Hunt, and L. F. Pemberton. 2001. Nuclear import of histone H2A and H2B is mediated by a network of karyopherins. J. Cell Biol. 153:251-262.
42. Nemergut, M. E., C. A. Mizzen, T. Stukenberg, C. D. Allis, and I. G. Macara. 2001. Chromatin docking and exchange activity enhancement of RCC1 by histones H2A and H2B. Science 292:1540-1543.
43. Ohkuni, K., K. Shirahige, and A. Kikuchi. 2003. Genome-wide expression analysis of NAP1 in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 306:5-9.
44. Okuzaki, D., and H. Nojima. 2001. Kcc4 associates with septin proteins of Saccharomyces cerevisiae. FEBS Lett. 489:197-201.
45. Okuzaki, D., S. Tanaka, H. Kanazawa, and H. Nojima. 1997. Gin4 of S. cerevisiae is a bud neck protein that interacts with the Cdc28 complex. Genes Cells 2:753-770.
46. Padmanabha, R., J. L. Chen-Wu, D. E. Hanna, and C. V. Glover. 1990. Isolation, sequencing, and disruption of the yeast CKA2 gene: casein kinase II is essential for viability in Saccharomyces cerevisiae. Mol. Cell. Biol. 10:4089-4099.
47. Park, Y. J., and K. Luger. 2006. Structure and function of nucleosome assembly proteins. Biochem. Cell Biol. 84:549-558.
48. Park, Y. J., and K. Luger. 2006. The structure of nucleosome assembly protein 1. Proc. Natl. Acad. Sci. USA 103:1248-1253.
49. Pemberton, L. F., M. P. Rout, and G. Blobel. 1995. Disruption of the nucleoporin gene NUP133 results in clustering of nuclear pore complexes. Proc. Natl. Acad. Sci. USA 92:1187-1191.
50. Rethinaswamy, A., M. J. Birnbaum, and C. V. Glover. 1998. Temperature-sensitive mutations of the CKA1 gene reveal a role for casein kinase II in maintenance of cell polarity in Saccharomyces cerevisiae. J. Biol. Chem. 273:5869-5877.
51. Rodriguez, P., J. Pelletier, G. B. Price, and M. Zannis-Hadjopoulos. 2000. NAP-2: histone chaperone function and phosphorylation state through the cell cycle. J. Mol. Biol. 298:225-238.
52. Selth, L., and J. Q. Svejstrup. 2007. Vps75, a new yeast member of the NAP histone chaperone family. J. Biol. Chem. 282:12358-12362.
53. Shim, E. Y., S. J. Hong, J. H. Oum, Y. Yanez, Y. Zhang, and S. E. Lee. 2007. RSC mobilizes nucleosomes to improve accessibility of repair machinery to the damaged chromatin. Mol. Cell. Biol. 27:1602-1613.
54. Spellman, P. T., G. Sherlock, M. Q. Zhang, V. R. Iyer, K. Anders, M. B. Eisen, P. O. Brown, D. Botstein, and B. Futcher. 1998. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol. Biol. Cell 9:3273-3297.
55. Tsuchiya, K., R. Reijo, D. C. Page, and C. M. Disteche. 1995. Gonadoblastoma: molecular definition of the susceptibility region on the Y chromosome. Am. J. Hum. Genet. 57:1400-1407.
56. Tyler, J. K., C. R. Adams, S. R. Chen, R. Kobayashi, R. T. Kamakaka, and J. T. Kadonaga. 1999. The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 402:555-560.
57. Ubersax, J. A., E. L. Woodbury, P. N. Quang, M. Paraz, J. D. Blethrow, K. Shah, K. M. Shokat, and D. O. Morgan. 2003. Targets of the cyclin-dependent kinase Cdk1. Nature 425:859-864.
58. Uetz, P., L. Giot, G. Cagney, T. A. Mansfield, R. S. Judson, J. R. Knight, D. Lockshon, V. Narayan, M. Srinivasan, P. Pochart, A. Qureshi-Emili, Y. Li, B. Godwin, D. Conover, T. Kalbfleisch, G. Vijayadamodar, M. Yang, M. Johnston, S. Fields, and J. M. Rothberg. 2000. A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403:623-627.
59. von Lindern, M., S. van Baal, J. Wiegant, A. Raap, A. Hagemeijer, and G. Grosveld. 1992. can, a putative oncogene associated with myeloid leukemogenesis, may be activated by fusion of its 3′ half to different genes: characterization of the set gene. Mol. Cell. Biol. 12:3346-3355.
60. Yu, I. J., D. L. Spector, Y. S. Bae, and D. R. Marshak. 1991. Immunocytochemical localization of casein kinase II during interphase and mitosis. J. Cell Biol. 114:1217-1232.