Protein array identification of substrates of the Epstein-Barr virus protein kinase BGLF4

Journal of Virology

Volumn 83, Issue 10, 2009, Pages 5219-5231

  Zhu, Jian ^a   Liao, Gangling ^a,b   Shan, Liang ^a   Zhang, Jun ^a   Chen, Mei Ru ^c   Hayward, Gary S ^a,b   Hayward, S Diane ^a,b   Desai, Prashant ^a,b   Zhu, Heng ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

BGLF4 PROTEIN; CYCLIN B; CYCLIN DEPENDENT KINASE; EPSTEIN BARR VIRUS ANTIGEN; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS ENZYME; BGLF4 PROTEIN, EPSTEIN BARR VIRUS; BGLF4 PROTEIN, EPSTEIN-BARR VIRUS; EBV ENCODED NUCLEAR ANTIGEN 1; EBV-ENCODED NUCLEAR ANTIGEN 1; PROTEIN SERINE THREONINE KINASE; VIRUS PROTEIN;

ARTICLE; BINDING SITE; CELL CYCLE PROGRESSION; CONTROLLED STUDY; DNA REPLICATION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME SUBSTRATE; EPISOME; EPSTEIN BARR VIRUS; GENE VECTOR; GENETIC TRANSFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MICROARRAY; PROTEIN PHOSPHORYLATION; VIRION; VIRUS GENOME; VIRUS LATENCY; VIRUS REPLICATION; ENZYME SPECIFICITY; GENETICS; HUMAN; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; TUMOR CELL LINE;

HERPESVIRIDAE; HUMAN HERPESVIRUS 4;

CELL LINE, TUMOR; DNA REPLICATION; DNA, VIRAL; EPSTEIN-BARR VIRUS NUCLEAR ANTIGENS; HERPESVIRUS 4, HUMAN; HUMANS; PHOSPHORYLATION; PROTEIN ARRAY ANALYSIS; PROTEIN-SERINE-THREONINE KINASES; SUBSTRATE SPECIFICITY; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 65349113014     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02378-08     Document Type: Article

References (52)

1. Ambinder, R. F., M. A. Mullen, Y. N. Chang, G. S. Hayward, and S. D. Hayward. 1991. Functional domains of Epstein-Barr virus nuclear antigen EBNA-1. J. Virol. 65:1466-1478.
2. Asai, R., A. Kato, K. Kato, M. Kanamori-Koyama, K. Sugimoto, T. Sairenji, Y. Nishiyama, and Y. Kawaguchi. 2006. Epstein-Barr virus protein kinase BGLF4 is a virion tegument protein that dissociates from virions in a phosphorylation- dependent process and phosphorylates the viral immediate-early protein BZLF1. J. Virol. 80:5125-5134. (Pubitemid 43752758)
3. Biron, K. K., R. J. Harvey, S. C. Chamberlain, S. S. Good, A. A. Smith III, M. G. Davis, C. L. Talarico, W. H. Miller, R. Ferris, R. E. Dornsife, S. C. Stanat, J. C. Drach, L. B. Townsend, and G. W. Koszalka. 2002. Potent and selective inhibition of human cytomegalovirus replication by 1263W94, a benzimidazole L-riboside with a unique mode of action. Antimicrob. Agents Chemother. 46:2365-2372.
4. Bornkamm, G. W., U. Behrends, and J. Mautner. 2006. The infectious kiss: newly infected B cells deliver Epstein-Barr virus to epithelial cells. Proc. Natl. Acad. Sci. USA 103:7201-7202.
5. Calderwood, M. A., K. Venkatesan, L. Xing, M. R. Chase, A. Vazquez, A. M. Holthaus, A. E. Ewence, N. Li, T. Hirozane-Kishikawa, D. E. Hill, M. Vidal, E. Kieff, and E. Johannsen. 2007. Epstein-Barr virus and virus human protein interaction maps. Proc. Natl. Acad. Sci. USA 104:7606-7611.
6. Chaudhuri, B., H. Xu, I. Todorov, A. Dutta, and J. L. Yates. 2001. Human DNA replication initiation factors, ORC and MCM, associate with oriP of Epstein-Barr virus. Proc. Natl. Acad. Sci. USA 98:10085-10089.
7. Chen, C. S., E. Korobkova, H. Chen, J. Zhu, X. Jian, S. C. Tao, C. He, and H. Zhu. 2008. A proteome chip approach reveals new DNA damage recognition activities in Escherichia coli. Nat. Methods 5:69-74.
8. Chen, M. R., S. J. Chang, H. Huang, and J. Y. Chen. 2000. A protein kinase activity associated with Epstein-Barr virus BGLF4 phosphorylates the viral early antigen EA-D in vitro. J. Virol. 74:3093-3104. (Pubitemid 30143732)
9. Chen, M. R., J. M. Middeldorp, and S. D. Hayward. 1993. Separation of the complex DNA binding domain of EBNA-1 into DNA recognition and dimerization subdomains of novel structure. J. Virol. 67:4875-4885. (Pubitemid 23215969)
10. Chiu, Y. F., C. P. Tung, Y. H. Lee, W. H. Wang, C. Li, J. Y. Hung, C. Y. Wang, Y. Kawaguchi, and S. T. Liu. 2007. A comprehensive library of mutations of Epstein Barr virus. J. Gen. Virol. 88:2463-2472. (Pubitemid 47323891)
11. Crawford, D. H., and I. Ando. 1986. EB virus induction is associated with B-cell maturation. Immunology 59:405-409.
12. Daikoku, T., A. Kudoh, M. Fujita, Y. Sugaya, H. Isomura, and T. Tsurumi. 2004. In vivo dynamics of EBNA1-oriP interaction during latent and lytic replication of Epstein-Barr virus. J. Biol. Chem. 279:54817-54825.
13. Fixman, E. D., G. S. Hayward, and S. D. Hayward. 1992. trans-acting requirements for replication of Epstein-Barr virus ori-Lyt. J. Virol. 66:5030-5039.
14. Gardella, T., P. Medveczky, T. Sairenji, and C. Mulder. 1984. Detection of circular and linear herpesvirus DNA molecules in mammalian cells by gel electrophoresis. J. Virol. 50:248-254. (Pubitemid 14165314)
15. Gershburg, E., M. Marschall, K. Hong, and J. S. Pagano. 2004. Expression and localization of the Epstein-Barr virus-encoded protein kinase. J. Virol. 78:12140-12146. (Pubitemid 39458733)
16. Gershburg, E., and J. S. Pagano. 2007. Conserved herpesvirus protein kinases. Biochim. Biophys. Acta 1784:2003-2012.
17. Gershburg, E., and J. S. Pagano. 2002. Phosphorylation of the Epstein-Barr virus (EBV) DNA polymerase processivity factor EA-D by the EBV-encoded protein kinase and effects of the L-riboside benzimidazole 1263W94. J. Virol. 76:998-1003. (Pubitemid 34070632)
18. Gershburg, E., S. Raffa, M. R. Torrisi, and J. S. Pagano. 2007. Epstein-Barr virus-encoded protein kinase (BGLF4) is involved in production of infectious virus. J. Virol. 81:5407-5412. (Pubitemid 46744449)
19. Gupta, R., B. Kus, C. Fladd, J. Wasmuth, R. Tonikian, S. Sidhu, N. J. Krogan, J. Parkinson, and D. Rotin. 2007. Ubiquitination screen using protein microarrays for comprehensive identification of Rsp5 substrates in yeast. Mol. Syst. Biol. 3:116. (Pubitemid 46878941)
20. Han, Z., E. Marendy, Y. D. Wang, J. Yuan, J. T. Sample, and S. Swaminathan. 2007. Multiple roles of Epstein-Barr virus SM protein in lytic replication. J. Virol. 81:4058-4069. (Pubitemid 46586901)
21. Hume, A. J., J. S. Finkel, J. P. Kamil, D. M. Coen, M. R. Culbertson, and R. F. Kalejta. 2008. Phosphorylation of retinoblastoma protein by viral protein with cyclin-dependent kinase function. Science 320:797-799.
22. Hutt-Fletcher, L. M. 2007. Epstein-Barr virus entry. J. Virol. 81:7825-7832. (Pubitemid 47101468)
23. Johannsen, E., M. Luftig, M. R. Chase, S. Weicksel, E. Cahir-McFarland, D. Illanes, D. Sarracino, and E. Kieff. 2004. Proteins of purified Epstein-Barr virus. Proc. Natl. Acad. Sci. USA 101:16286-16291.
24. Kato, K., Y. Kawaguchi, M. Tanaka, M. Igarashi, A. Yokoyama, G. Matsuda, M. Kanamori, K. Nakajima, Y. Nishimura, M. Shimojima, H. T. Phung, E. Takahashi, and K. Hirai. 2001. Epstein-Barr virus-encoded protein kinase BGLF4 mediates hyperphosphorylation of cellular elongation factor 1 (EF-1): EF-1δ is universally modified by conserved protein kinases of herpesviruses in mammalian cells. J. Gen. Virol. 82:1457-1463.
25. Kato, K., A. Yokoyama, Y. Tohya, H. Akashi, Y. Nishiyama, and Y. Kawaguchi. 2003. Identification of protein kinases responsible for phosphorylation of Epstein-Barr virus nuclear antigen leader protein at serine-35, which regulates its coactivator function. J. Gen. Virol. 84:3381-3392.
26. Kawaguchi, Y., K. Kato, M. Tanaka, M. Kanamori, Y. Nishiyama, and Y. Yamanashi. 2003. Conserved protein kinases encoded by herpesviruses and cellular protein kinase cdc2 target the same phosphorylation site in eukaryotic elongation factor 1δ. J. Virol. 77:2359-2368. (Pubitemid 36222759)
27. Koszalka, G. W., N. W. Johnson, S. S. Good, L. Boyd, S. C. Chamberlain, L. B. Townsend, J. C. Drach, and K. K. Biron. 2002. Preclinical and toxicology studies of 1263W94, a potent and selective inhibitor of human cytomegalovirus replication. Antimicrob. Agents Chemother. 46:2373-2380.
28. Kudoh, A., T. Daikoku, Y. Ishimi, Y. Kawaguchi, N. Shirata, S. Iwahori, H. Isomura, and T. Tsurumi. 2006. Phosphorylation of MCM4 at sites inactivating DNA helicase activity of the MCM4-MCM6-MCM7 complex during Epstein-Barr virus productive replication. J. Virol. 80:10064-10072. (Pubitemid 44522600)
29. Laichalk, L. L., and D. A. Thorley-Lawson. 2005. Terminal differentiation into plasma cells initiates the replicative cycle of Epstein-Barr virus in vivo. J. Virol. 79:1296-1307. (Pubitemid 40053911)
30. Lake, C. M., S. J. Molesworth, and L. M. Hutt-Fletcher. 1998. The Epstein- Barr virus (EBV) gN homolog BLRF1 encodes a 15-kilodalton glycoprotein that cannot be authentically processed unless it is coexpressed with the EBV gM homolog BBRF3. J. Virol. 72:5559-5564. (Pubitemid 28283339)
31. Lalezari, J. P., J. A. Aberg, L. H. Wang, M. B. Wire, R. Miner, W. Snowden, C. L. Talarico, S. Shaw, M. A. Jacobson, and W. L. Drew. 2002. Phase I dose escalation trial evaluating the pharmacokinetics, anti-human cytomegalovirus (HCMV) activity, and safety of 1263W94 in human immunodeficiency virus-infected men with asymptomatic HCMV shedding. Antimicrob. Agents Chemother. 46:2969-2976.
32. Lee, C. P., J. Y. Chen, J. T. Wang, K. Kimura, A. Takemoto, C. C. Lu, and M. R. Chen. 2007. Epstein-Barr virus BGLF4 kinase induces premature chromosome condensation through activation of condensin and topoisomerase II. J. Virol. 81:5166-5180. (Pubitemid 46744427)
33. Lee, C. P., Y. H. Huang, S. F. Lin, Y. Chang, Y. H. Chang, K. Takada, and M. R. Chen. 2008. Epstein-Barr virus BGLF4 kinase induces disassembly of the nuclear lamina to facilitate virion production. J. Virol. 82:11913-11926.
34. Leight, E. R., and B. Sugden. 2001. Establishment of an oriP replicon is dependent upon an infrequent, epigenetic event. Mol. Cell. Biol. 21:4149-4161.
35. Levitskaya, J., A. Sharipo, A. Leonchiks, A. Ciechanover, and M. G. Masucci. 1997. Inhibition of ubiquitin/proteasome-dependent protein degradation by the Gly-Ala repeat domain of the Epstein-Barr virus nuclear antigen 1. Proc. Natl. Acad. Sci. USA 94:12616-12621.
36. Lu, J. Y., Y. Y. Lin, J. Qian, S. C. Tao, J. Zhu, C. Pickart, and H. Zhu. 2008. Functional Dissection of a HECT ubiquitin E3 ligase. Mol. Cell Proteomics 7:35-45.
37. Michel, D., and T. Mertens. 2004. The UL97 protein kinase of human cytomegalovirus and homologues in other herpesviruses: impact on virus and host. Biochim. Biophys. Acta 1697:169-180.
38. Ptacek, J., G. Devgan, G. Michaud, H. Zhu, X. Zhu, J. Fasolo, H. Guo, G. Jona, A. Breitkreutz, R. Sopko, R. R. McCartney, M. C. Schmidt, N. Rachidi, S. J. Lee, A. S. Mah, L. Meng, M. J. Stark, D. F. Stern, C. De Virgilio, M. Tyers, B. Andrews, M. Gerstein, B. Schweitzer, P. F. Predki, and M. Snyder. 2005. Global analysis of protein phosphorylation in yeast. Nature 438:679-684.
39. Romaker, D., V. Schregel, K. Maurer, S. Auerochs, A. Marzi, H. Sticht, and M. Marschall. 2006. Analysis of the structure-activity relationship of four herpesviral UL97 subfamily protein kinases reveals partial but not full functional conservation. J. Med. Chem. 49:7044-7053.
40. Semmes, O. J., L. Chen, R. T. Sarisky, Z. Gao, L. Zhong, and S. D. Hayward. 1998. Mta has properties of an RNA export protein and increases cytoplasmic accumulation of Epstein-Barr virus replication gene mRNA. J. Virol. 72:9526-9534. (Pubitemid 28520815)
41. Tanner, J., J. Weis, D. Fearon, Y. Whang, and E. Kieff. 1987. Epstein-Barr virus gp350/220 binding to the B lymphocyte C3d receptor mediates adsorption, capping, and endocytosis. Cell 50:203-213.
42. Tarakanova, V. L., V. Leung-Pineda, S. Hwang, C. W. Yang, K. Matatall, M. Basson, R. Sun, H. Piwnica-Worms, B. P. Sleckman, and H. W. Virgin. 2007. Gamma-herpesvirus kinase actively initiates a DNA damage response by inducing phosphorylation of H2AX to foster viral replication. Cell Host Microbe 1:275-286.
43. Thorley-Lawson, D. A. 2001. Epstein-Barr virus: exploiting the immune system. Nat. Rev. Immunol. 1:75-82.
44. Tsurumi, T., M. Fujita, and A. Kudoh. 2005. Latent and lytic Epstein-Barr virus replication strategies. Rev. Med. Virol. 15:3-15. (Pubitemid 40070039)
45. Wang, J., and B. Sugden. 2005. Origins of bidirectional replication of Epstein-Barr virus: models for understanding mammalian origins of DNA synthesis. J. Cell Biochem. 94:247-256.
46. Wang, J. T., P. W. Yang, C. P. Lee, C. H. Han, C. H. Tsai, and M. R. Chen. 2005. Detection of Epstein-Barr virus BGLF4 protein kinase in virus replication compartments and virus particles. J. Gen. Virol. 86:3215-3225. (Pubitemid 41685153)
47. Wang, L. H., R. W. Peck, Y. Yin, J. Allanson, R. Wiggs, and M. B. Wire. 2003. Phase I safety and pharmacokinetic trials of 1263W94, a novel oral anti-human cytomegalovirus agent, in healthy and human immunodeficiency virus-infected subjects. Antimicrob. Agents Chemother. 47:1334-1342.
48. Yang, K., A. P. Poon, B. Roizman, and J. D. Baines. 2008. Temperature-sensitive mutations in the putative herpes simplex virus type 1 terminase subunits pUL15 and pUL33 preclude viral DNA cleavage/packaging and interaction with pUL28 at the nonpermissive temperature. J. Virol. 82:487-494. (Pubitemid 350309162)
49. Young, L. S., and A. B. Rickinson. 2004. Epstein-Barr virus: 40 years on. Nat. Rev. Cancer 4:757-768.
50. Yue, W., E. Gershburg, and J. S. Pagano. 2005. Hyperphosphorylation of EBNA2 by Epstein-Barr virus protein kinase suppresses transactivation of the LMP1 promoter. J. Virol. 79:5880-5885. (Pubitemid 40548259)
51. Zhou, J., C. M. Chau, Z. Deng, R. Shiekhattar, M. P. Spindler, A. Schepers, and P. M. Lieberman. 2005. Cell cycle regulation of chromatin at an origin of DNA replication. EMBO J. 24:1406-1417. (Pubitemid 40593061)
52. Zhu, H., J. F. Klemic, S. Chang, P. Bertone, A. Casamayor, K. G. Klemic, D. Smith, M. Gerstein, M. A. Reed, and M. Snyder. 2000. Analysis of yeast protein kinases using protein chips. Nat. Genet. 26:283-289.