The human adenovirus type 5 E1B 55-kilodalton protein is phosphorylated by protein kinase CK2

Journal of Virology

Volumn 86, Issue 5, 2012, Pages 2400-2415

  Ching, Wilhelm ^a   Dobner, Thomas ^a   Koyuncu, Emre ^a,b  

^a LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

^b PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 DIMETHYLAMINO 4,5,6,7 TETRABROMO 1H BENZIMIDAZOLE; 4,5,6,7 TETRABROMOBENZOTRIAZOLE; CASEIN KINASE II; CASEIN KINASE IIALPHA; E1B 55K PROTEIN; E1B PROTEIN; GLUTATHIONE TRANSFERASE; PROTEIN SERINE THREONINE KINASE INHIBITOR; UNCLASSIFIED DRUG;

ADENOVIRUS INFECTION; ARTICLE; CONTROLLED STUDY; DNA REPLICATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME LOCALIZATION; HUMAN; HUMAN ADENOVIRUS 5; HUMAN CELL; IN VITRO STUDY; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; VIRUS REPLICATION; WILD TYPE;

ADENOVIRIDAE INFECTIONS; ADENOVIRUS E1B PROTEINS; ADENOVIRUSES, HUMAN; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CASEIN KINASE II; CELL LINE; HUMANS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN BINDING;

HUMAN ADENOVIRUS TYPE 5;

EID: 84857846180     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.06066-11     Document Type: Article

References (71)

1. Anderson CW, Schmitt RC, Smart JE, Lewis JB. 1984. Early region 1B of adenovirus 2 encodes two coterminal proteins of 495 and 155 amino acid residues. J. Virol. 50:387-396.
2. Arrigoni G, et al. 2004. Phosphorylation of calmodulin fragments by protein kinase CK2: mechanistic aspects and structural consequences. Biochemistry 43:12788-12798.
3. Babiss LE, Ginsberg HS. 1984. Adenovirus type 5 early region 1b gene product is required for efficient shutoff of host protein synthesis. J. Virol. 50:202-212.
4. Babiss LE, Ginsberg HS, Darnell JE, Jr. 1985. Adenovirus E1B proteins are required for accumulation of late viral mRNA and for effects on cellular mRNA translation and transport. Mol. Cell. Biol. 5:2552-2558.
5. Baker A, Rohleder KJ, Hanakahi LA, Ketner G. 2007. Adenovirus E4 34k and E1b 55k oncoproteins target host DNA ligase IV for proteasomal degradation. J. Virol. 81:7034-7040.
6. Blackford AN, Grand RJ. 2009. Adenovirus E1B 55-kilodalton protein: multiple roles in viral infection and cell transformation. J. Virol. 83:4000-4012.
7. Blanchette P, et al. 2004. Both BC-box motifs of adenovirus protein E4orf6 are required to efficiently assemble an E3 ligase complex that degrades p53. Mol. Cell. Biol. 24:9619-9629.
8. Blanchette P, et al. 2008. Control of mRNA export by adenovirus E4orf6 and E1B55K proteins during productive infection requires E4orf6 ubiquitin ligase activity. J. Virol. 82:2642-2651.
9. Boivin D, Morrison MR, Marcellus RC, Querido E, Branton PE. 1999. Analysis of synthesis, stability, phosphorylation, and interacting polypeptides of the 34-kilodalton product of open reading frame 6 of the early region 4 protein of human adenovirus type 5. J. Virol. 73:1245-1253.
10. Buchou T, et al. 2003. Disruption of the regulatory beta subunit of protein kinase CK2 in mice leads to a cell-autonomous defect and early embryonic lethality. Mol. Cell. Biol. 23:908-915.
11. Cathomen T, Weitzman MD. 2000. A functional complex of adenovirus proteins E1B-55kDa and E4orf6 is necessary to modulate the expression level of p53 but not its transcriptional activity. J. Virol. 74:11407-11412.
12. Chemnitz J, Pieper D, Gruttner C, Hauber J. 2009. Phosphorylation of the HuR ligand APRIL by casein kinase 2 regulates CD83 expression. Eur. J. Immunol. 39:267-279.
13. Dallaire F, Blanchette P, Groitl P, Dobner T, Branton PE. 2009. Identification of integrin α3 as a new substrate of the adenovirus E4orf6/E1B 55-kilodalton E3 ubiquitin ligase complex. J. Virol. 83:5329-5338.
14. Desagher S, et al. 2001. Phosphorylation of bid by casein kinases I and II regulates its cleavage by caspase 8. Mol. Cell 8:601-611.
15. Doble BW, Woodgett JR. 2003. GSK-3: tricks of the trade for a multitasking kinase. J. Cell Sci. 116:1175-1186.
16. Dobner T, Kzhyshkowska J. 2001. Nuclear export of adenovirus RNA. Curr. Top. Microbiol. Immunol. 259:25-54.
17. 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.
18. Filhol O, Cochet C, Wedegaertner P, Gill GN, Chambaz EM. 1991. Coexpression of both alpha and beta subunits is required for assembly of regulated casein kinase II. Biochemistry 30:11133-11140.
19. Filhol O, et al. 2003. Live-cell fluorescence imaging reveals the dynamics of protein kinase CK2 individual subunits. Mol. Cell. Biol. 23:975-987.
20. Flint SJ, Gonzalez RA. 2003. Regulation of mRNA production by the adenoviral E1B 55-kDa and E4 Orf6 proteins. Curr. Top. Microbiol. Immunol. 272:287-330.
21. 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.
22. Gonzalez RA, Flint SJ. 2002. Effects of mutations in the adenoviral E1B 55-kilodalton protein coding sequence on viral late mRNA metabolism. J. Virol. 76:4507-4519.
23. 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.
24. Grasser FA, et al. 1992. Phosphorylation of the Epstein-Barr virus nuclear antigen 2. Biochem. Biophys. Res. Commun. 186:1694-1701.
25. Groitl P, Dobner T. 2006. Construction of adenovirus type 5 early region 1 and 4 virus mutants, p 29-39. In Wold WS, Tollefson AE (ed), Adenovirus methods and protocols, 2nd ed, vol 1. Humana Press, Inc, Totowa, NJ.
26. Harlow E, Franza BR, Jr, Schley C. 1985. Monoclonal antibodies specific for adenovirus early region 1A proteins: extensive heterogeneity in early region 1A products. J. Virol. 55:533-546.
27. Kindsmuller K, et al. 2007. Intranuclear targeting and nuclear export of the adenovirus E1B-55K protein are regulated by SUMO1 conjugation. Proc. Natl. Acad. Sci. U. S. A. 104:6684-6689.
28. Kindsmuller K, et al. 2009. A 49-kilodalton isoform of the adenovirus type 5 early region 1B 55-kilodalton protein is sufficient to support virus replication. J. Virol. 83:9045-9056.
29. 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.
30. Kzhyshkowska J, Kremmer E, Hofmann M, Wolf H, Dobner T. 2004. Protein arginine methylation during lytic adenovirus infection. Biochem. J. 383:259-265.
31. Landesman-Bollag E, et al. 2001. Protein kinase CK2: signaling and tumorigenesis in the mammary gland. Mol. Cell. Biochem. 227:153-165.
32. Lilley CE, Schwartz RA, Weitzman MD. 2007. Using or abusing: viruses and the cellular DNA damage response. Trends Microbiol. 15:119-126.
33. Malette P, Yee SP, Branton PE. 1983. Studies on the phosphorylation of the 58,000 Dalton early region 1B protein of human adenovirus type 5. J. Gen. Virol. 64:1069-1078.
34. Malik P, Clements JB. 2004. Protein kinase CK2 phosphorylation regulates the interaction of Kaposi's sarcoma-associated herpesvirus regulatory protein ORF57 with its multifunctional partner hnRNP K. Nucleic Acids Res. 32:5553-5569.
35. Medina-Palazon C, et al. 2007. Protein kinase CK2 phosphorylation of EB2 regulates its function in the production of Epstein-Barr virus infectious viral particles. J. Virol. 81:11850-11860.
36. Meggio F, Pinna LA. 2003. One-thousand-and-one substrates of protein kinase CK2? FASEB J. 17:349-368.
37. Mitsudomi T, et al. 1992. p53 gene mutations in non-small-cell lung cancer cell lines and their correlation with the presence of ras mutations and clinical features. Oncogene 7:171-180.
38. Munstermann U, et al. 1990. Casein kinase II is elevated in solid human tumours and rapidly proliferating non-neoplastic tissue. Eur. J. Biochem. 189:251-257.
39. Niefind K, Putter M, Guerra B, Issinger OG, Schomburg D. 1999. GTP plus water mimic ATP in the active site of protein kinase CK2. Nat. Struct. Biol. 6:1100-1103.
40. Pagano MA, et al. 2008. The selectivity of inhibitors of protein kinase CK2: an update. Biochem. J. 415:353-365.
41. Pagano MA, et al. 2004. 2-Dimethylamino-4,5,6,7-tetrabromo-1Hbenzimidazole: a novel powerful and selective inhibitor of protein kinase CK2. Biochem. Biophys. Res. Commun. 321:1040-1044.
42. Park JW, Bae YS. 1999. Phosphorylation of ribosomal protein L5 by protein kinase CKII decreases its 5S rRNA binding activity. Biochem. Biophys. Res. Commun. 263:475-481.
43. Pilder S, Moore M, Logan J, Shenk T. 1986. The adenovirus E1B-55K transforming polypeptide modulates transport or cytoplasmic stabilization of viral and host cell mRNAs. Mol. Cell. Biol. 6:470-476.
44. Pinna LA. 1990. Casein kinase 2: an "eminence grise" in cellular regulation? Biochim. Biophys. Acta 1054:267-284.
45. Pinna LA. 1997. Protein kinase CK2. Int. J. Biochem. Cell Biol. 29:551-554.
46. Pinna LA. 2002. Protein kinase CK2: a challenge to canons. J. Cell Sci. 115:3873-3878.
47. Pistorius K, Seitz G, Remberger K, Issinger O-G. 1991. Differential CKII activities in human colorectal mucosa, adenomas, and carcinomas. Onkologie 14:255-260.
48. Ponten J, Saksela E. 1967. Two established in vitro cell lines from human mesenchymal tumours. Int. J. Cancer 2:434-447.
49. Querido E, et al. 1997. Regulation of p53 levels by the E1B 55-kilodalton protein and E4orf6 in adenovirus-infected cells. J. Virol. 71:3788-3798.
50. Querido E, et al. 2001. Identification of three functions of the adenovirus e4orf6 protein that mediate p53 degradation by the E4orf6-E1B55K complex. J. Virol. 75:699-709.
51. Reich NC, Sarnow P, Duprey E, Levine AJ. 1983. Monoclonal antibodies which recognize native and denatured forms of the adenovirus DNAbinding protein. Virology 128:480-484.
52. Rojas S, Corbin-Lickfett KA, Escudero-Paunetto L, Sandri-Goldin RM. 2010. ICP27 phosphorylation site mutants are defective in herpes simplex virus 1 replication and gene expression. J. Virol. 84:2200-2211.
53. Salvi M, Sarno S, Cesaro L, Nakamura H, Pinna LA. 2009. Extraordinary pleiotropy of protein kinase CK2 revealed by weblogo phosphoproteome analysis. Biochim. Biophys. Acta 1793:847-859.
54. Sarnow P, Sullivan CA, Levine AJ. 1982. A monoclonal antibody detecting the adenovirus type 5-E1b-58Kd tumor antigen: characterization of the E1b-58Kd tumor antigen in adenovirus-infected and -transformed cells. Virology 120:510-517.
55. Schneider E, Kartarius S, Schuster N, Montenarh M. 2002. The cyclin H/cdk7/Mat1 kinase activity is regulated by CK2 phosphorylation of cyclin H. Oncogene 21:5031-5037.
56. Schreiner S, et al. 2010. Proteasome-dependent degradation of Daxx by the viral E1B-55K protein in human adenovirus-infected cells. J. Virol. 84:7029-7038.
57. Schwartz RA, et al. 2008. Distinct requirements of adenovirus E1b55K protein for degradation of cellular substrates. J. Virol. 82:9043-9055.
58. Seldin DC, Lou DY, Toselli P, Landesman-Bollag E, Dominguez I. 2008. Gene targeting of CK2 catalytic subunits. Mol. Cell. Biochem. 316:141-147.
59. Sieber T, Dobner T. 2007. Adenovirus type 5 early region 1B 156R protein promotes cell transformation independently of repression of p53- stimulated transcription. J. Virol. 81:95-105.
60. Slaton JW, Unger GM, Sloper DT, Davis AT, Ahmed K. 2004. Induction of apoptosis by antisense CK2 in human prostate cancer xenograft model. Mol. Cancer Res. 2:712-721.
61. Souquere-Besse S, et al. 2002. Adenovirus infection targets the cellular protein kinase CK2 and RNA-activated protein kinase (PKR) into viral inclusions of the cell nucleus. Microsc. Res. Technol. 56:465-478.
62. 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.
63. Stracker TH, Carson CT, Weitzman MD. 2002. Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex. Nature 418:348-352.
64. Teodoro JG, Branton PE. 1997. Regulation of p53-dependent apoptosis, transcriptional repression, and cell transformation by phosphorylation of the 55-kilodalton E1B protein of human adenovirus type 5. J. Virol. 71:3620-3627.
65. Teodoro JG, et al. 1994. Phosphorylation at the carboxy terminus of the 55-kilodalton adenovirus type 5 E1B protein regulates transforming activity. J. Virol. 68:776-786.
66. Trembley JH, Wang G, Unger G, Slaton J, Ahmed K. 2009. Protein kinase CK2 in health and disease: CK2: a key player in cancer biology. Cell. Mol. Life Sci. 66:1858-1867.
67. Ubersax JA, and Ferrell JE, Jr. 2007. Mechanisms of specificity in protein phosphorylation. Nat. Rev. Mol. Cell. Biol. 8:530-541.
68. Wang H, Davis A, Yu S, Ahmed K. 2001. Response of cancer cells to molecular interruption of the CK2 signal. Mol. Cell. Biochem. 227:167-174.
69. Weitzman MD, Ornelles DA. 2005. Inactivating intracellular antiviral responses during adenovirus infection. Oncogene 24:7686-7696.
70. Wimmer P, et al. 2010. SUMO modification of E1B-55K oncoprotein regulates isoform-specific binding to the tumour suppressor protein PML. Oncogene 29:5511-5522.
71. Yaron Y, McAdara JK, Lynch M, Hughes E, Gasson JC. 2001. Identification of novel functional regions important for the activity of HOXB7 in mammalian cells. J. Immunol. 166:5058-5067.