Identification of a novel protein interaction motif in the regulatory subunit of casein kinase 2

Molecular and Cellular Biology

Volumn 34, Issue 2, 2014, Pages 246-258

  Cao, Jennifer Yinuo ^a   Shire, Kathy ^a   Landry, Cameron ^a   Gish, Gerald D ^b   Pawson, Tony ^b   Frappier, Lori ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; ARKL1 PROTEIN; CASEIN KINASE II; CELL PROTEIN; EPSTEIN BARR VIRUS ANTIGEN 1; GLUTATHIONE; MYC PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR DISTRIBUTION; CRYSTAL STRUCTURE; DIMERIZATION; DNA SEQUENCE; IMMUNOFLUORESCENCE MICROSCOPY; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEOMICS; VIRUS REPLICATION; WESTERN BLOTTING; WILD TYPE;

EID: 84891425783     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00968-13     Document Type: Article

References (73)

1. Pinna LA. 2002. Protein kinase CK2: a challenge to canons. J. Cell Sci. 115:3873-3878. http://dx.doi.org/10.1242/jcs.00074.
2. Pinna LA, Allende JE. 2009. Protein kinase CK2 in health and disease: protein kinase CK2: an ugly duckling in the kinome pond. Cell. Mol. Life Sci. 66:1795-1799. http://dx.doi.org/10.1007/s00018-009-9148-9.
3. Meggio F, Pinna LA. 2003. One-thousand-and-one substrates of proteinkinase CK2? FASEB J. 17:349-368. http://dx.doi.org/10.1096/fj.02-0473rev.
4. Ruzzene M, Pinna LA. 2010. Addiction to protein kinase CK2: a common denominator of diverse cancer cells? Biochim. Biophys. Acta 1804:499-504. http://dx.doi.org/10.1016/j.bbapap.2009.07.018.
5. Duncan JS, Litchfield DW. 2008. Too much of a good thing: the role of protein kinase CK2 in tumorigenesis and prospects for therapeutic inhibition of CK2. Biochim. Biophys. Acta 1784:33-47. http://dx.doi.org/10.1016/j.bbapap.2007.08.017.
6. Seldin DC, Leder P. 1995. Casein kinase II alpha transgene-induced murine lymphoma: relation to theileriosis in cattle. Science 267:894-897. http://dx.doi.org/10.1126/science.7846532.
7. Kelliher MA, Seldin DC, Leder P. 1996. Tal-1 induces T cell acute lymphoblastic leukemia accelerated by casein kinase IIalpha. EMBO J. 15:5160-5166.
8. Landesman-Bollag E, Romieu-Mourez R, Song DH, Sonenshein GE, CardiffRD, Seldin DC. 2001. Protein kinase CK2 in mammary gland tumorigenesis. Oncogene 20:3247-3257. http://dx.doi.org/10.1038/sj.onc.1204411.
9. Keller DM, Lu H. 2002. p53 serine 392 phosphorylation increases after UV through induction of the assembly of the CK2.hSPT16.SSRP1 complex. J. Biol. Chem. 277:50206-50213. http://dx.doi.org/10.1074/jbc. M209820200.
10. Cox ML, Meek DW. 2009. Phosphorylation of serine 392 in p53 is a common and integral event during p53 induction by diverse stimuli. Cell. Signal. 22:564-571.
11. Kapoor M, Lozano G. 1998. Functional activation of p53 via phosphorylation following DNA damage by UV but not gamma radiation. Proc. Natl. Acad. Sci. U. S. A. 95:2834-2837. http://dx.doi.org/10.1073/pnas.95.6.2834.
12. Scaglioni PP, Yung TM, Cai LF, Erdjument-Bromage H, Kaufman AJ, Singh B, Teruya-Feldstein J, Tempst P, PandolfiPP. 2006. A CK2-dependent mechanism for degradation of thePMLtumor suppressor. Cell 126:269-283. http://dx.doi.org/10.1016/j.cell.2006.05.041.
13. Al-Khouri AM, Ma Y, Togo SH, Williams S, Mustelin T. 2005. Cooperative phosphorylation of the tumor suppressor phosphatase and tensin homologue (PTEN) by casein kinases and glycogen synthase kinase 3beta. J. Biol. Chem. 280:35195-35202. http://dx.doi.org/10.1074/jbc. M503045200.
14. Eddy SF, Guo S, Demicco EG, Romieu-Mourez R, Landesman-Bollag E, Seldin DC, Sonenshein GE. 2005. Inducible IkappaB kinase/IkappaB kinase epsilon expression is induced by CK2 and promotes aberrant nuclear factor-kappaB activation in breast cancer cells. Cancer Res. 65: 11375-11383. http://dx.doi.org/10.1158/0008-5472.CAN-05-1602.
15. Romieu-Mourez R, Landesman-Bollag E, Seldin DC, Sonenshein GE. 2002. Protein kinase CK2 promotes aberrant activation of nuclear factorkappaB, transformed phenotype, and survival of breast cancer cells. Cancer Res. 62:6770-6778.
16. Torres J, Pulido R. 2001. The tumor suppressor PTEN is phosphorylated by the protein kinase CK2 at its C terminus. Implications for PTEN stability to proteasome-mediated degradation. J. Biol. Chem. 276:993-998.
17. Lallemand-Breitenbach V, de The H. 2010. PML nuclear bodies. Cold Spring Harb. Perspect. Biol. 2:a000661. http://dx.doi.org/10.1101/cshperspect.a000661.
18. St-Denis NA, Litchfield DW. 2009. Protein kinase CK2 in health and disease: from birth to death: the role of protein kinase CK2 in the regulation of cell proliferation and survival. Cell. Mol. Life Sci. 66:1817-1829. http://dx.doi.org/10.1007/s00018-009-9150-2.
19. Koffa MD, Kean J, Zachos G, Rice SA, Clements JB. 2003. CK2 protein kinase is stimulated and redistributed by functional herpes simplex virus ICP27 protein. J. Virol. 77:4315-4325. http://dx.doi.org/10.1128/JVI.77.7.4315-4325.2003.
20. Franck N, Le Seyec J, Guguen-Guillouzo C, Erdtmann L. 2005. Hepatitis C virus NS2 protein is phosphorylated by the protein kinase CK2 and targeted for degradation to the proteasome. J. Virol. 79:2700-2708. http://dx.doi.org/10.1128/JVI.79.5.2700-2708.2005.
21. El-Guindy AS, Miller G. 2004. Phosphorylation of Epstein-Barr virus ZEBRA protein at its casein kinase 2 sites mediates its ability to repress activation of a viral lytic cycle late gene by Rta. J. Virol. 78:7634-7644. http://dx.doi.org/10.1128/JVI.78.14.7634-7644.2004.
22. Meggio F, D'Agostino DM, Ciminale V, Chieco-Bianchi L, Pinna LA. 1996. Phosphorylation of HIV-1 Rev protein: implication of protein kinase CK2 and pro-directed kinases. Biochem. Biophys. Res. Commun. 226:547-554. http://dx.doi.org/10.1006/bbrc.1996.1392.
23. O'Reilly D, Hanscombe O, O'Hare P. 1997. A single serine residue at position 375 of VP16 is critical for complex assembly with Oct-1 and HCF and is a target of phosphorylation by casein kinase II. EMBO J. 16:2420-2430. http://dx.doi.org/10.1093/emboj/16.9.2420.
24. Zhi Y, Sandri-Goldin RM. 1999. Analysis of the phosphorylation sites of herpes simplex virus type 1 regulatory protein ICP27. J. Virol. 73:3246-3257.
25. Holowaty MN, Zeghouf M, Wu H, Tellam J, Athanasopoulos V, Greenblatt J, Frappier L. 2003. Protein profiling with Epstein-Barr nuclear antigen-1 reveals an interaction with the herpesvirus-associated ubiquitin-specific protease HAUSP/USP7. J. Biol. Chem. 278:29987-29994. http://dx.doi.org/10.1074/jbc. M303977200.
26. Malik-Soni N, Frappier L. 2012. Proteomic profiling of EBNA1-host protein interactions in latent and lytic Epstein-Barr virus infections. J. Virol. 86:6999-7002. http://dx.doi.org/10.1128/JVI.00194-12.
27. Frappier L. 2012. EBNA1 and host factors in Epstein-Barr virus latent DNA replication. Curr. Opin. Virol. 2:733-739. http://dx.doi.org/10.1016/j.coviro.2012.09.005.
28. Frappier L. 2011. Role of EBNA1 in NPC tumourigenesis. Semin. Cancer Biol. 22:154-161. http://dx.doi.org/10.1016/j.semcancer.2011.12.002.
29. Sivachandran N, Sarkari F, Frappier L. 2008. Epstein-Barr nuclear antigen 1 contributes to nasopharyngeal carcinoma through disruption of PML nuclear bodies. PLoS Pathog. 4:e1000170. http://dx.doi.org/10.1371/journal.ppat.1000170.
30. Everett RD, Chelbi-Alix MK. 2007. PML and PML nuclear bodies: implications in antiviral defence. Biochimie 89:819-830. http://dx.doi.org/10.1016/j.biochi.2007.01.004.
31. Sivachandran N, Wang X, Frappier L. 2012. Functions of the Epstein-Barr virus EBNA1 protein in viral reactivation and lytic infection. J. Virol. 86:6146-6158. http://dx.doi.org/10.1128/JVI.00013-12.
32. Sivachandran N, Dawson CW, Young LS, Liu FF, Middeldorp J, Frappier L. 2011. Contributions of the Epstein-Barr virus EBNA1 protein to gastric carcinoma. J. Virol. 86:60-68. http://dx.doi.org/10.1128/JVI.06776-11.
33. Sivachandran N, Cao JY, Frappier L. 2010. Epstein-Barr virus nuclear antigen 1 hijacks the host kinase CK2 to disrupt PML nuclear bodies. J. Virol. 84:11113-11123. http://dx.doi.org/10.1128/JVI.01183-10.
34. Sarno S, Marin O, Boschetti M, Pagano MA, Meggio F, Pinna LA. 2000. Cooperative modulation of protein kinase CK2 by separate domains of its regulatory beta-subunit. Biochemistry 39:12324-12329. http://dx.doi.org/10.1021/bi0011431.
35. Canton DA, Zhang C, Litchfield DW. 2001. Assembly of protein kinase CK2: investigation of complex formation between catalytic and regulatory subunits using a zinc-finger-deficient mutant of CK2beta. Biochem. J. 358:87-94. http://dx.doi.org/10.1042/0264-6021:3580087.
36. Bibby AC, Litchfield DW. 2005. The multiple personalities of the regulatory subunit of protein kinase CK2: CK2 dependent and CK2 independent roles reveal a secret identity for CK2beta. Int. J. Biol. Sci. 1:67-79. http://dx.doi.org/10.7150/ijbs.1.67.
37. Bojanowski K, Filhol O, Cochet C, Chambaz EM, Larsen AK. 1993. DNA topoisomerase II and casein kinase II associate in a molecular complex that is catalytically active. J. Biol. Chem. 268:22920-22926.
38. Appel K, Wagner P, BoldyreffB, Issinger OG, Montenarh M. 1995. Mapping of the interaction sites of the growth suppressor protein p53 with the regulatory beta-subunit of protein kinase CK2. Oncogene 11:1971-1978.
39. Sun Y, Hegamyer G, Cheng YJ, Hildesheim A, Chen JY, Chen IH, Cao Y, Yao KT, Colburn NH. 1992. An infrequent point mutation of the p53 gene in human nasopharyngeal carcinoma. Proc. Natl. Acad. Sci. U. S. A. 89:6516-6520. http://dx.doi.org/10.1073/pnas.89.14.6516.
40. Menezes J, Leibold W, Klein G, Clements G. 1975. Establishment and characterization of an Epstein-Barr virus (EBC)-negative lymphoblastoid B cell line (BJA-B) from an exceptional, EBV-genome-negative African Burkitt's lymphoma. Biomedicine 22:276-284.
41. Shire K, Ceccarelli DF, Avolio-Hunter TM, Frappier L. 1999. EBP2, a human protein that interacts with sequences of the Epstein-Barr virus nuclear antigen 1 important for plasmid maintenance. J. Virol. 73:2587-2595.
42. Shire K, Kapoor P, Jiang K, Hing MN, Sivachandran N, Nguyen T, Frappier L. 2006. Regulation of the EBNA1 Epstein-Barr virus protein by serine phosphorylation and arginine methylation. J. Virol. 80:5261-5272. http://dx.doi.org/10.1128/JVI.02682-05.
43. Bosc DG, Slominski E, Sichler C, Litchfield DW. 1995. Phosphorylationof casein kinase II by p34cdc2. Identification of phosphorylation sites using phosphorylation site mutants in vitro. J. Biol. Chem. 270:25872-25878.
44. Holowaty MN, Sheng Y, Nguyen T, Arrowsmith C, Frappier L. 2003. Protein interaction domains of the ubiquitin-specific protease, USP7/HAUSP. J. Biol. Chem. 278:47753-47761. http://dx.doi.org/10.1074/jbc. M307200200.
45. Chen GI, Gingras AC. 2007. Affinity-purification mass spectrometry (AP-MS) of serine/threonine phosphatases. Methods 42:298-305. http://dx.doi.org/10.1016/j.ymeth.2007.02.018.
46. Saridakis V, Sheng Y, Sarkari F, Holowaty MN, Shire K, Nguyen T, Zhang RG, Liao J, Lee W, Edwards AM, Arrowsmith CH, Frappier L. 2005. Structure of the p53 binding domain of HAUSP/USP7 bound to Epstein-Barr nuclear antigen 1: implications for EBV-mediated immortalization. Mol. Cell 18:25-36. http://dx.doi.org/10.1016/j.molcel.2005.02.029.
47. Duellman SJ, Thompson KL, Coon JJ, Burgess RR. 2009. Phosphorylation sites of Epstein-Barr virus EBNA1 regulate its function. J. Gen. Virol. 90:2251-2259. http://dx.doi.org/10.1099/vir.0.012260-0.
48. Kang MS, Lee EK, Soni V, Lewis TA, Koehler AN, Srinivasan V, KieffE. 2011. Roscovitine inhibits EBNA1 serine 393 phosphorylation, nuclear localization, transcription, and episome maintenance. J. Virol. 85:2859-2868. http://dx.doi.org/10.1128/JVI.01628-10.
49. Niefind K, Guerra B, Ermakowa I, Issinger OG. 2001. Crystal structure of human protein kinase CK2: insights into basic properties of the CK2 holoenzyme. EMBO J. 20:5320-5331. http://dx.doi.org/10.1093/emboj/20.19.5320.
50. Raaf J, Brunstein E, Issinger OG, Niefind K. 2008. The interaction of CK2alpha and CK2beta, the subunits of protein kinase CK2, requires CK2beta in a preformed conformation and is enthalpically driven. Protein Sci. 17:2180-2186. http://dx.doi.org/10.1110/ps.037770.108.
51. Pickard BS, Malloy MP, Clark L, Lehellard S, Ewald HL, Mors O, Porteous DJ, Blackwood DH, Muir WJ. 2005. Candidate psychiatric illness genes identified in patients with pericentric inversions of chromosome Psychiatr. Genet. 15:37-44. http://dx.doi.org/10.1097/00041444-200503000-00007.
52. Sun H, Hunter T. 2012. Poly-small ubiquitin-like modifier (Poly-SUMO)-binding proteins identified through a string search. J. Biol. Chem. 287:42071-42083. http://dx.doi.org/10.1074/jbc. M112.410985.
53. Erker Y, Neyret-Kahn H, Seeler JS, Dejean A, AtfiA, Levy L. 2013. Arkadia, a novel SUMO-targeted ubiquitin ligase involved in PML degradation. Mol. Cell. Biol. 33:2163-2177. http://dx.doi.org/10.1128/MCB.01019-12.
54. Maridor G, Park W, Krek W, Nigg EA. 1991. Casein kinase II. cDNA sequences, developmental expression, and tissue distribution of mRNAs for alpha, alpha', and beta subunits of the chicken enzyme. J. Biol. Chem. 266:2362-2368.
55. Graham KC, Litchfield DW. 2000. The regulatory beta subunit of protein kinase CK2 mediates formation of tetrameric CK2 complexes. J. Biol. Chem. 275:5003-5010. http://dx.doi.org/10.1074/jbc.275.7.5003.
56. Filhol O, Martiel JL, Cochet C. 2004. Protein kinase CK2: a new view of an old molecular complex. EMBO Rep. 5:351-355. http://dx.doi.org/10.1038/sj.embor.7400115.
57. Bolanos-Garcia VM, Fernandez-Recio J, Allende JE, Blundell TL. 2006. Identifying interaction motifs in CK2beta-a ubiquitous kinase regulatory subunit. Trends Biochem. Sci. 31:654-661. http://dx.doi.org/10.1016/j.tibs.2006.10.005.
58. Chen M, Li D, Krebs EG, Cooper JA. 1997. The casein kinase II beta subunit binds to Mos and inhibits Mos activity. Mol. Cell. Biol. 17:1904-1912.
59. Hagemann C, Kalmes A, Wixler V, Wixler L, Schuster T, Rapp UR. 1997. The regulatory subunit of protein kinase CK2 is a specific A-Raf activator. FEBS Lett. 403:200-202. http://dx.doi.org/10.1016/S0014-5793(97)00011-2.
60. Lieberman SL, Ruderman JV. 2004. CK2 beta, which inhibits Mos function, binds to a discrete domain in the N-terminus of Mos. Dev. Biol. 268:271-279. http://dx.doi.org/10.1016/j.ydbio.2003.12.009.
61. Guerra B, Issinger OG, Wang JY. 2003. Modulation of human checkpoint kinase Chk1 by the regulatory beta-subunit of protein kinase CK2. Oncogene 22:4933-4942. http://dx.doi.org/10.1038/sj.onc.1206721.
62. Li D, Meier UT, Dobrowolska G, Krebs EG. 1997. Specific interaction between casein kinase 2 and the nucleolar protein Nopp140. J. Biol. Chem. 272:3773-3779. http://dx.doi.org/10.1074/jbc.272.6.3773.
63. Ahn BH, Lee JH, Bae YS. 2003. Identification of mutations in protein kinase CKIIbeta subunit that affect its binding to ribosomal protein L41 and homodimerization. J. Biochem. Mol. Biol. 36:344-348. http://dx.doi.org/10.5483/BMBRep.2003.36.4.344.
64. Raman C, Kuo A, Deshane J, Litchfield DW, Kimberly RP. 1998. Regulation of casein kinase 2 by direct interaction with cell surface receptor CD5. J. Biol. Chem. 273:19183-19189. http://dx.doi.org/10.1074/jbc.273.30.19183.
65. Romero-Oliva F, Allende JE. 2001. Protein p21(WAF1/CIP1) is phosphorylated by protein kinase CK2 in vitro and interacts with the amino terminal end of the CK2 beta subunit. J. Cell. Biochem. 81:445-452. http://dx.doi.org/10.1002/1097-4644(20010601)81:3_445::AID-JCB10583.0.CO;2-2.
66. Akten B, Tangredi MM, Jauch E, Roberts MA, Ng F, Raabe T, Jackson FR. 2009. Ribosomal s6 kinase cooperates with casein kinase 2 to modulate the Drosophila circadian molecular oscillator. J. Neurosci. 29:466-475. http://dx.doi.org/10.1523/JNEUROSCI.4034-08.2009.
67. Olsen BB, Wang SY, Svenstrup TH, Chen BP, Guerra B. 2012. Protein kinase CK2 localizes to sites of DNA double-strand break regulating the cellular response to DNA damage. BMC Mol. Biol. 13:7. http://dx.doi.org/10.1186/1471-2199-13-7.
68. Olsen BB, Issinger OG, Guerra B. 2010. Regulation of DNA-dependent protein kinase by protein kinase CK2 in human glioblastoma cells. Oncogene 29:6016-6026. http://dx.doi.org/10.1038/onc.2010.337.
69. Episkopou V, Arkell R, Timmons PM, Walsh JJ, Andrew RL, Swan D. 2001. Induction of the mammalian node requires Arkadia function in the extraembryonic lineages. Nature 410:825-830. http://dx.doi.org/10.1038/35071095.
70. Hecker CM, Rabiller M, Haglund K, Bayer P, Dikic I. 2006. Specification of SUMO1-and SUMO2-interacting motifs. J. Biol. Chem. 281: 16117-16127. http://dx.doi.org/10.1074/jbc. M512757200.
71. Briones-Orta MA, Levy L, Madsen CD, Das D, Erker Y, Sahai E, Hill CS. 2013. Arkadia regulates tumor metastasis by modulation of the TGFbeta pathway. Cancer Res. 73:1800-1810. http://dx.doi.org/10.1158/0008-5472.CAN-12-1916.
72. Ma T, Chen Y, Zhang F, Yang CY, Wang S, Yu X. 2013. RNF111-dependent neddylation activates DNA damage-induced ubiquitination. Mol. Cell 49:897-907. http://dx.doi.org/10.1016/j.molcel.2013.01.006.
73. Poulsen SL, Hansen RK, Wagner SA, van Cuijk L, van Belle GJ, Streicher W, Wikstrom M, Choudhary C, Houtsmuller AB, Marteijn JA, Bekker-Jensen S, Mailand N. 2013. RNF111/Arkadia is a SUMOtargeted ubiquitin ligase that facilitates the DNA damage response. J. Cell Biol. 201:797-807. http://dx.doi.org/10.1083/jcb.201212075.