JC virus agnoprotein enhances large T antigen binding to the origin of viral DNA replication: Evidence for its involvement in viral DNA replication

Virology

Volumn 433, Issue 1, 2012, Pages 12-26

  Saribas, A Sami ^a   White, Martyn K ^a   Safak, Mahmut ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Agnoprotein; BKV; DNA replication; Large T antigen; Polyomavirus JC; Progressive multifocal leukoencephalopathy; SV40; Transcription

Indexed keywords

AGNOPROTEIN; ALANINE; MUTANT PROTEIN; PHENYLALANINE; VIRUS DNA; VIRUS LARGE T ANTIGEN;

ALPHA HELIX; ANTIGEN BINDING; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; JC VIRUS; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PREDICTION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; T LYMPHOCYTE; VIRUS DNA CELL DNA INTERACTION; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANTIGENS, VIRAL, TUMOR; BASE SEQUENCE; BINDING SITES; CELL LINE; DNA REPLICATION; DNA, VIRAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HUMANS; JC VIRUS; MICROSCOPY, FLUORESCENCE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PROTEIN BINDING; RECOMBINANT FUSION PROTEINS; VIRAL REGULATORY AND ACCESSORY PROTEINS; VIRUS REPLICATION;

BK POLYOMAVIRUS; JC POLYOMAVIRUS;

EID: 84866179864     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.06.017     Document Type: Article

References (84)

1. Akan I., Sariyer I.K., Biffi R., Palermo V., Woolridge S., White M.K., Amini S., Khalili K., Safak M. Human polyomavirus JCV late leader peptide region contains important regulatory elements. Virology 2006, 349(1):66-78.
2. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25(17):3389-3402.
3. Alwine J.C. Evidence for simian virus 40 late transcriptional control: mixed infections of wild-type simian virus 40 and a late leader deletion mutant exhibit trans effects on late viral RNA synthesis. J. Virol. 1982, 42(3):798-803.
4. Berger J.R. The basis for modeling progressive multifocal leukoencephalopathy pathogenesis. Curr. Opin. Neurol. 2011, 24(3):262-267.
5. Bollag B., Frisque R.J. PAb 2000 specifically recognizes the large T and small t proteins of JC virus. Virus Res. 1992, 25(3):223-239.
6. Bollag B., Hofstetter C.A., Reviriego-Mendoza M.M., Frisque R.J. JC virus small T antigen binds phosphatase PP2A and Rb family proteins and is required for efficient viral DNA replication activity. PLoS One 2010, 5(5):e10606.
7. Bollag B., Mackeen P.C., Frisque R.J. Purified JC virus T antigen derived from insect cells preferentially interacts with binding site II of the viral core origin under replication conditions. Virology 1996, 218(1):81-93.
8. Bollag B., Prins C., Snyder E.L., Frisque R.J. Purified JC virus T and T' proteins differentially interact with the retinoblastoma family of tumor suppressor proteins. Virology 2000, 274(1):165-178.
9. Bolton D.L., Lenardo M.J. Vpr cytopathicity independent of G2/M cell cycle arrest in human immunodeficiency virus type 1-infected CD4+T cells. J. Virol. 2007, 81(17):8878-8890.
10. Borowiec J.A., Dean F.B., Bullock P.A., Hurwitz J. Binding and unwinding-how T antigen engages the SV40 origin of DNA replication. Cell 1990, 60(2):181-184.
11. Bourbigot S., Beltz H., Denis J., Morellet N., Roques B.P., Mely Y., Bouaziz S. The C-terminal domain of the HIV-1 regulatory protein Vpr adopts an antiparallel dimeric structure in solution via its leucine-zipper-like domain. Biochem. J. 2005, 387(Pt 2):333-341.
12. Bowden T.A., Aricescu A.R., Gilbert R.J., Grimes J.M., Jones E.Y., Stuart D.I. Structural basis of Nipah and Hendra virus attachment to their cell-surface receptor ephrin-B2. Nat. Struct. Mol. Biol. 2008, 15(6):567-572.
13. Brinda K.V., Kannan N., Vishveshwara S. Analysis of homodimeric protein interfaces by graph-spectral methods. Protein Eng. 2002, 15(4):265-277.
14. Cui J., Tungaturthi P.K., Ayyavoo V., Ghafouri M., Ariga H., Khalili K., Srinivasan A., Amini S., Sawaya B.E. The role of Vpr in the regulation of HIV-1 gene expression. Cell Cycle 2006, 5(22):2626-2638.
15. Darbinyan A., Darbinian N., Safak M., Radhakrishnan S., Giordano A., Khalili K. Evidence for dysregulation of cell cycle by human polyomavirus, JCV, late auxiliary protein. Oncogene 2002, 21(36):5574-5581.
16. Daugherty M.D., Booth D.S., Jayaraman B., Cheng Y., Frankel A.D. HIV Rev response element (RRE) directs assembly of the Rev homooligomer into discrete asymmetric complexes. Proc. Nat. Acad. Sci. U.S.A. 2010, 107(28):12481-12486.
17. Daugherty M.D., Liu B., Frankel A.D. Structural basis for cooperative RNA binding and export complex assembly by HIV Rev. Nat. Struct. Mol. Biol. 2010, 17(11):1337-1342.
18. Del Valle L., Gordon J., Enam S., Delbue S., Croul S., Abraham S., Radhakrishnan S., Assimakopoulou M., Katsetos C.D., Khalili K. Expression of human neurotropic polyomavirus JCV late gene product agnoprotein in human medulloblastoma. J. Nat. Cancer. Inst. 2002, 94(4):267-273.
19. DePamphilis M.L.a.M.K.B. Replication of SV40 and polyomavirus chromosomas. The Polyomaviridae 1986, Vol. 1. Plenum Press, New York.
20. Dhe-Paganon S., Werner E.D., Nishi M., Hansen L., Chi Y.I., Shoelson S.E. A phenylalanine zipper mediates APS dimerization. Nat. Struct. Mol. Biol. 2004, 11(10):968-974.
21. DiMattia M.A., Watts N.R., Stahl S.J., Rader C., Wingfield P.T., Stuart D.I., Steven A.C., Grimes J.M. Implications of the HIV-1 Rev dimer structure at 3.2 a resolution for multimeric binding to the Rev response element. Proc. Nat. Acad. Sci. U.S.A. 2010, 107(13):5810-5814.
22. Dingwall C., Laskey R.A. Protein import into the cell nucleus. Annu. Rev. Cell. Biol. 1986, 2:367-390.
23. Dingwall C., Laskey R.A. Nuclear targeting sequences-a consensus?. Trends Biochem. Sci. 1991, 16(12):478-481.
24. Fanning E., Knippers R. Structure and function of simian virus 40 large tumor antigen. Annu. Rev. Biochem. 1992, 61:55-85.
25. Frisque R.J., Bream G.L., Cannella M.T. Human polyomavirus JC virus genome. J. Virol. 1984, 51(2):458-469.
26. Fritz J.V., Didier P., Clamme J.P., Schaub E., Muriaux D., Cabanne C., Morellet N., Bouaziz S., Darlix J.L., Mely Y., de Rocquigny H. Direct Vpr-Vpr interaction in cells monitored by two photon fluorescence correlation spectroscopy and fluorescence lifetime imaging. Retrovirology 2008, 5:87.
27. Fritz J.V., Dujardin D., Godet J., Didier P., De Mey J., Darlix J.L., Mely Y., de Rocquigny H. HIV-1 Vpr oligomerization but not that of Gag directs the interaction between Vpr and Gag. J. Virol. 2010, 84(3):1585-1596.
28. Gallivan J.P., Dougherty D.A. Cation-pi interactions in structural biology. Proc. Nat. Acad. Sci. U.S.A. 1999, 96(17):9459-9464.
29. Gilbert J., Nomura S., Anderson C.W., George K. Identification of the SV40 agnoproduct: a DNA binding protein. Nature 1981, 291:346-349.
30. Godet A.N., Guergnon J., Croset A., Cayla X., Falanga P.B., Colle J.H., Garcia A. PP2A1 binding, cell transducing and apoptotic properties of Vpr (77-92): a new functional domain of HIV-1 Vpr proteins. PLoS One 2010, 5(11):e13760.
31. Grueneberg D.A., Natesan S., Alexandre C., Gilman M.Z. Human and Drosophila homeodomain proteins that enhance the DNA-binding activity of serum response factor. Science 1992, 257(5073):1089-1095.
32. Haggerty S., Walker D.L., Frisque R.J. JC virus-simian virus 40 genomes containing heterologous regulatory signals and chimeric early regions: identification of regions restricting transformation by JC virus. J. Virol. 1989, 63(5):2180-2190.
33. Hay N., Skolnik-David H., Aloni Y. Attenuation in the control of SV40 gene expression. Cell 1982, 29(1):183-193.
34. Hirt B. Selective extraction of polyoma DNA from infected mouse cell cultures. J. Mol. Biol. 1967, 26(2):365-369.
35. Hou-Jong M.H., Larsen S.H., Roman A. Role of the agnoprotein in regulation of simian virus 40 replication and maturation pathways. J. Virol. 1987, 61(3):937-939.
36. Iordanskiy S., Zhao Y., DiMarzio P., Agostini I., Dubrovsky L., Bukrinsky M. Heat-shock protein 70 exerts opposing effects on Vpr-dependent and Vpr-independent HIV-1 replication in macrophages. Blood 2004, 104(6):1867-1872.
37. Jackson M.R., Beahm R., Duvvuru S., Narasimhan C., Wu J., Wang H.N., Philip V.M., Hinde R.J., Howell E.E. A preference for edgewise interactions between aromatic rings and carboxylate anions: the biological relevance of anion-quadrupole interactions. J. Phys. Chem. B 2007, 111(28):8242-8249.
38. Johannessen M., Myhre M.R., Dragset M., Tummler C., Moens U. Phosphorylation of human polyomavirus BK agnoprotein at Ser-11 is mediated by PKC and has an important regulative function. Virology 2008, 379(1):97-109.
39. Khalili K., Feigenbaum L., Khoury G. Evidence for a shift in 5'-termini of early viral RNA during the lytic cycle of JC virus. Virology 1987, 158(2):469-472.
40. Khalili K., White M.K., Sawa H., Nagashima K., Safak M. The agnoprotein of polyomaviruses: a multifunctional auxiliary protein. J. Cell Physiol. 2005, 204(1):1-7.
41. Kim J., Woolridge S., Biffi R., Borghi E., Lassak A., Ferrante P., Amini S., Khalili K., Safak M. Members of the AP-1 family, c-Jun and c-Fos, functionally interact with JC virus early regulatory protein large T antigen. J. Virol. 2003, 77(9):5241-5252.
42. King G., Oates J., Patel D., van den Berg H.A., Dixon A.M. Towards a structural understanding of the smallest known oncoprotein: investigation of the bovine papillomavirus E5 protein using solution-state NMR. Biochim. Biophys. Acta 2011, 1808(6):1493-1501.
43. Kleinschmidt-DeMasters B.K., Tyler K.L. Progressive multifocal leukoencephalopathy complicating treatment with natalizumab and interferon beta-1a for multiple sclerosis. N. Engl. J. Med. 2005, 353(4):369-374.
44. Langer-Gould A., Atlas S.W., Green A.J., Bollen A.W., Pelletier D. Progressive multifocal leukoencephalopathy in a patient treated with natalizumab. N. Engl. J. Med. 2005, 353(4):375-381.
45. Lashgari M.S., Tada H., Amini S., Khalili K. Regulation of JCVL promoter function: transactivation of JCVL promoter by JCV and SV40 early proteins. Virology 1989, 170(1):292-295.
46. Leger H., Sock E., Renner K., Grummt F., Wegner M. Functional interaction between the POU domain protein Tst-1/Oct-6 and the high-mobility-group protein HMG-I/Y. Mol. Cell Biol. 1995, 15(7):3738-3747.
47. Lynch K.J., Frisque R.J. Identification of critical elements within the JC virus DNA replication origin. J. Virol. 1990, 64(12):5812-5822.
48. Lynch K.J., Frisque R.J. Factors contributing to the restricted DNA replicating activity of JC virus. Virology 1991, 180(1):306-317.
49. Lynch K.J., Haggerty S., Frisque R.J. DNA replication of chimeric JC virus-simian virus 40 genomes. Virology 1994, 204(2):819-822.
50. Major E.O., Amemiya K., Tornatore C.S., Houff S.A., Berger J.R. Pathogenesis and molecular biology of progressive multifocal leukoencephalopathy, the JC virus-induced demyelinating disease of the human brain. Clin. Microbiol. Rev. 1992, 5(1):49-73.
51. Major E.O., Miller A.E., Mourrain P., Traub R.G., de Widt E., Sever J. Establishment of a line of human fetal glial cells that supports JC virus multiplication. Proc. Nat. Acad. Sci. U.S.A. 1985, 82(4):1257-1261.
52. Margolskee R.F., Nathans D. Suppression of a VP1 mutant of simian virus 40 by missense mutations in serine codons of the viral agnogene. J. Virol. 1983, 48(2):405-409.
53. Milardi D., Sciacca M.F., Pappalardo M., Grasso D.M., La Rosa C. The role of aromatic side-chains in amyloid growth and membrane interaction of the islet amyloid polypeptide fragment LANFLVH. Eur. Biophys. J. 2011, 40(1):1-12.
54. Moens U., Ludvigsen M., Van Ghelue M. Human polyomaviruses in skin diseases. Patholog. Res. Int. 2011, 2011:123491.
55. Morellet N., Bouaziz S., Petitjean P., Roques B.P. NMR structure of the HIV-1 regulatory protein VPR. J. Mol. Biol. 2003, 327(1):215-227.
56. Myhre M.R., Olsen G.H., Gosert R., Hirsch H.H., Rinaldo C.H. Clinical polyomavirus BK variants with agnogene deletion are non-functional but rescued by trans-complementation. Virology 2010, 398(1):12-20.
57. Ng S.C., Mertz J.E., Sanden-Will S., Bina M. Simian virus 40 maturation in cells harboring mutants deleted in the agnogene. J. Biol. Chem. 1985, 260(2):1127-1132.
58. Okada Y., Suzuki T., Sunden Y., Orba Y., Kose S., Imamoto N., Takahashi H., Tanaka S., Hall W.W., Nagashima K., Sawa H. Dissociation of heterochromatin protein 1 from lamin B receptor induced by human polyomavirus agnoprotein: role in nuclear egress of viral particles. EMBO Rep. 2005, 6(5):452-457.
59. Philip V., Harris J., Adams R., Nguyen D., Spiers J., Baudry J., Howell E.E., Hinde R.J. A survey of aspartate-phenylalanine and glutamate-phenylalanine interactions in the protein data bank: searching for anion-pi pairs. Biochemistry 2011, 50(14):2939-2950.
60. Pless S.A., Millen K.S., Hanek A.P., Lynch J.W., Lester H.A., Lummis S.C., Dougherty D.A. A cation-pi interaction in the binding site of the glycine receptor is mediated by a phenylalanine residue. J. Neurosci. 2008, 28(43):10937-10942.
61. Pletneva E.V., Laederach A.T., Fulton D.B., Kostic N.M. The role of cation-pi interactions in biomolecular association. Design of peptides favoring interactions between cationic and aromatic amino acid side chains. J. Am. Chem. Soc. 2001, 123(26):6232-6245.
62. Poon B., Chang M.A., Chen I.S. Vpr is required for efficient Nef expression from unintegrated human immunodeficiency virus type 1 DNA. J. Virol. 2007, 81(19):10515-10523.
63. Raj G.V., Gordon J., Logan T.J., Hall D.J., Deluca A., Giordano A., Khalili K. Characterization of glioma cells derived from polyomavirus-induced brain tumors in hamsters. Int. J. Oncol. 1995, 7:801-808.
64. Roy A., Kucukural A., Zhang Y. I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 2010, 5(4):725-738.
65. Sadowska B., Barrucco R., Khalili K., Safak M. Regulation of human polyomavirus JC virus gene transcription by AP-1 in glial cells. J. Virol. 2003, 77(1):665-672.
66. Safak M., Barrucco R., Darbinyan A., Okada Y., Nagashima K., Khalili K. Interaction of JC virus agno protein with T antigen modulates transcription and replication of the viral genome in glial cells. J. Virol. 2001, 75(3):1476-1486.
67. Safak M., Gallia G.L., Ansari S.A., Khalili K. Physical and functional interaction between the Y-box binding protein YB-1 and human polyomavirus JC virus large T antigen. J. Virol. 1999, 73(12):10146-10157.
68. Safak M., Sadowska B., Barrucco R., Khalili K. Functional interaction between JC virus late regulatory agnoprotein and cellular Y-box binding transcription factor, YB-1. J. Virol. 2002, 76(8):3828-3838.
69. Saribas A.S., Arachea B.T., White M.K., Viola R.E., Safak M. Human polyomavirus JC small regulatory agnoprotein forms highly stable dimers and oligomers: implications for their roles in agnoprotein function. Virology 2011, 420(1):51-65.
70. Saribas A.S., Ozdemir A., Lam C., Safak M. JC virus-induced progressive multifocal leukoencephalopathy. Future Virol. 2010, 5(3):313-323.
71. Sariyer I.K., Akan I., Palermo V., Gordon J., Khalili K., Safak M. Phosphorylation mutants of JC virus agnoprotein are unable to sustain the viral infection cycle. J. Virol. 2006, 80(8):3893-3903.
72. Sariyer I.K., Khalili K., Safak M. Dephosphorylation of JC virus agnoprotein by protein phosphatase 2A: inhibition by small t antigen. Virology 2008, 375(2):464-479.
73. Sariyer I.K., Saribas A.S., White M.K., Safak M. Infection by agnoprotein-negative mutants of polyomavirus JC and SV40 results in the release of virions that are mostly deficient in DNA content. Virol. J. 2011, 8:255.
74. Shi Z., Olson C.A., Bell A.J., Kallenbach N.R. Non-classical helix-stabilizing interactions: C-H...O H-bonding between Phe and Glu side chains in alpha-helical peptides. Biophys. Chem. 2002, 101-102:267-279.
75. Shi Z., Olson C.A., Kallenbach N.R. Cation-pi interaction in model alpha-helical peptides. J. Am. Chem. Soc. 2002, 124(13):3284-3291.
76. Sigrist C.J., Cerutti L., de Castro E., Langendijk-Genevaux P.S., Bulliard V., Bairoch A., Hulo N. PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Res. 2010, 38(Database issue):D161-D166.
77. Stillman B. Smart machines at the DNA replication fork. Cell 1994, 78(5):725-728.
78. Suzuki S., Tanaka T., Poyurovsky M.V., Nagano H., Mayama T., Ohkubo S., Lokshin M., Hosokawa H., Nakayama T., Suzuki Y., Sugano S., Sato E., Nagao T., Yokote K., Tatsuno I., Prives C. Phosphate-activated glutaminase (GLS2), a p53-inducible regulator of glutamine metabolism and reactive oxygen species. Proc. Nat. Acad. Sci. U.S.A. 2010, 107(16):7461-7466.
79. Suzuki T., Okada Y., Semba S., Orba Y., Yamanouchi S., Endo S., Tanaka S., Fujita T., Kuroda S., Nagashima K., Sawa H. Identification of FEZ1 as a protein that interacts with JC virus agnoprotein and microtubules: role of agnoprotein-induced dissociation of FEZ1 from microtubules in viral propagation. J. Biol. Chem. 2005, 280(26):24948-24956.
80. Suzuki T., Orba Y., Okada Y., Sunden Y., Kimura T., Tanaka S., Nagashima K., Hall W.W., Sawa H. The human polyoma JC virus agnoprotein acts as a viroporin. PLoS Pathog. 2010, 6(3):e1000801.
81. Tavis J.E., Frisque R.J. Altered DNA binding and replication activities of JC virus T-antigen mutants. Virology 1991, 183(1):239-250.
82. Unterstab G., Gosert R., Leuenberger D., Lorentz P., Rinaldo C.H., Hirsch H.H. The polyomavirus BK agnoprotein co-localizes with lipid droplets. Virology 2010, 399(2):322-331.
83. Van Assche G., Van Ranst M., Sciot R., Dubois B., Vermeire S., Noman M., Verbeeck J., Geboes K., Robberecht W., Rutgeerts P. Progressive multifocal leukoencephalopathy after natalizumab therapy for Crohn's disease. N. Engl. J. Med. 2005, 353(4):362-368.
84. Ziegler K., Bui T., Frisque R.J., Grandinetti A., Nerurkar V.R. A rapid in vitro polyomavirus DNA replication assay. J. Virol. Methods 2004, 122(1):123-127.