Baculovirus VP1054 is an acquired cellular PURα, a nucleic acid-binding protein specific for GGN repeats

Journal of Virology

Volumn 87, Issue 15, 2013, Pages 8465-8480

  Marek, Martin ^a,b,c   Romier, Christophe ^c   Galibert, Lionel ^b   Merten, Otto Wilhelm ^b   van Oers, Monique M ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b GÉNÉTHON   (France)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; POLYHEDRIN; PUR ALPHA PROTEIN; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN; VP1054 PROTEIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE DELETION; GENE TRANSFER; GENETIC CONSERVATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; VIRUS ASSEMBLY; VIRUS GENE; VIRUS GENOME; VIRUS NUCLEOCAPSID; VIRUS REPLICATION; VIRUS TRANSMISSION; VP1054 GENE;

EID: 84880600955     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00068-13     Document Type: Article

References (63)

1. Slack J, Arif BM. 2006. The baculoviruses occlusion-derived virus: virion structure and function. Adv. Virus Res. 69:99-165.
2. van Oers MM, Vlak JM. 2007. Baculovirus genomics. Curr. Drug Targets 8:1051-1068.
3. Au S, Pante N. 2012. Nuclear transport of baculovirus: revealing the nuclear pore complex passage. J. Struct. Biol. 177:90-98.
4. Thiem SM, Miller LK. 1989. Identification, sequence, and transcriptional mapping of the major capsid protein gene of the baculovirus Autographa californica nuclear polyhedrosis virus. J. Virol. 63:2008-2018.
5. Blissard GW, Quant-Russell RL, Rohrmann GF, Beaudreau GS. 1989. Nucleotide sequence, transcriptional mapping, and temporal expression of the gene encoding p39, a major structural protein of the multicapsid nuclear polyhedrosis virus of Orgyia pseudotsugata. Virology 168:354-362.
6. Lanier LM, Volkman LE. 1998. Actin binding and nucleation by Autographa californica M nucleopolyhedrovirus. Virology 243:167-177.
7. Lu S, Ge G, Qi Y. 2004. Ha-VP39 binding to actin and the influence of F-actin on assembly of progeny virions. Arch. Virol. 149:2187-2198.
8. Fraser MJ. 1986. Ultrastructural observations of virion maturation in Autographa californica nuclear polyhedrosis virus infected Spodoptera frugiperda cell cultures. J. Ultrastruct. Mol. Struct. Res. 95:189-195.
9. Kool M, Ahrens CH, Vlak JM, Rohrmann GF. 1995. Replication of baculovirus DNA. J. Gen. Virol. 76:2103-2118.
10. Carstens EB. 2009. AcMNPV as a model for baculovirusDNAreplication. Virol. Sin. 24:243-267.
11. Fujisawa H, Hearing P. 1994. Structure, function and specificity of the DNA packaging signals in double-stranded DNA viruses. Semin. Virol. 5:5-13.
12. Hammarskjöld ML, Winberg G. 1980. Encapsidation of adenovirus 16 DNA is directed by a small DNA sequence at the left end of the genome. Cell 20:787-795.
13. Oppenheim A, Sandalon Z, Peleg A, Shaul O, Nicolis S, Ottolenghi S. 1992. A cis-acting DNA signal for encapsidation of simian virus 40. J. Virol. 66:5320-5328.
14. Hodge PD, Stow ND. 2001. Effects of mutations within the herpes simplex virus type 1 DNA encapsidation signal on packaging efficiency. J. Virol. 75:8977-8986.
15. Cohen DPA, Marek M, Davies BG, Vlak JM, van Oers MM. 2009. Encyclopedia of Autographa californica nucleopolyhedrovirus genes. Virol. Sin. 24:359-414.
16. Vanarsdall AL, Okano K, Rohrmann GF. 2006. Characterization of the role of very late expression factor 1 in baculovirus capsid structure and DNA processing. J. Virol. 80:1724-1733.
17. Marek M, Merten Galibert O-WL, Vlak JM, van Oers MM. 2011. Baculovirus VP80 protein and the F-actin cytoskeleton interact and connect the viral replication factory with the nuclear periphery. J. Virol. 85:5350-5362.
18. Marek M, Merten Francis-Devaraj O-WF, van Oers MM. 2012. Essential C-terminal region of the baculovirus minor capsid protein VP80 binds DNA. J. Virol. 86:1728-1738.
19. Wu W, Liang H, Kan J, Liu C, Yuan M, Liang C, Yang K, Pang Y. 2008. Autographa californica multiple nucleopolyhedrovirus 38K is a novel nucleocapsid protein that interacts with VP1054, VP39, VP80, and itself. J. Virol. 82:12356-12364.
20. Luckow VA, Lee SC, Barry GF, Olins PO. 1993. Efficient generation of infectious recombinant baculoviruses by site-specific transposonmediated insertion of foreign genes into a baculovirus genome propagated in Escherichia coli. J. Virol. 67:4566-4579.
21. Marek M, van Oers MM, Devaraj FF, Vlak JM, Merten O-W. 2011. Engineering of baculovirus vectors for the manufacture of virion-free biopharmaceuticals. Biotech. Bioeng. 108:1056-1067.
22. Lung O, Westenberg M, Vlak JM, Zuidema D, Blissard GW. 2002. Pseudotyping Autographa californica multicapsid nucleopolyhedrovirus (AcMNPV): F proteins from group II NPVs are functionally analogous to AcMNPV GP64. J. Virol. 76:5729-5736.
23. Suzuki N, Nonaka H, Tsuge Y, Inui M, Yukawa H. 2005. New multipledeletion method for the Corynebacterium glutamicum genome, using a mutant lox sequence. Appl. Environ. Microbiol. 71:8472-8480.
24. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
25. van Lent JWM, Groenen JTM, Klinge-Roode EC, Rohrmann GF, Zuidema D, Vlak JM. 1990. Localization of the 34 kDa polyhedron envelope protein in Spodoptera frugiperda cells infected with Autographa californica nuclear polyhedrosis virus. Arch. Virol. 111:103-114.
26. Braunagel SC, Summers MD. 1994. Autographa californica nuclear polyhedrosis virus, PDV, and ECV viral envelopes and nucleocapsids: structural proteins, antigens, lipid and fatty acid profiles. Virology 202:315-328.
27. Wang M, Yin F, Shen S, Tan Y, Deng F, Vlak JM, Hu Z, Wang H. 2010. Partial functional rescue of Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus infectivity by replacement of F protein with GP64 from Autographa californica multicapsid nucleopolyhedrovirus. J. Virol. 84:11504-11514.
28. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. 2011. GenBank. Nucleic Acids Res. 39:D32-D37.
29. Altschul S, Madden T, Schaffer A, Zhang J, Zhang Z, Miller W, Lipman D. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
30. Letunic I, Doerks T, Bork P. 2009. SMART 6: recent updates and new developments. Nucleic Acids Res. 37:D229-D232.
31. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
32. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ. 2009. Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189-1191.
33. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599. doi:10.1093/molbev/msm092.
34. Bjellqvist B, Basse B, Olsen E, Celis JE. 1994. Reference points for comparisons of two-dimensional maps of proteins from different human cell types defined in a pH scale where isoelectric points correlate with polypeptide compositions. Electrophoresis 15:529-539.
35. Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A.2003. ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 31:3784-3788.
36. Graebsch A, Roche S, Niessing D. 2009. X-ray structure of Pur-α reveals a Whirly-like fold and an unusual nucleic-acid binding surface. Proc. Natl. Acad. Sci. U. S. A. 106:18521-18526.
37. Fiser A, Sali A. 2003. MODELLER: generation and refinement of homology-based protein structure models. Methods Enzymol. 374:461-491.
38. Laskowski RA, Macarthur MW, Moss DS, Thornton JM. 1993. PROCHECK-a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26:283-291.
39. Melo F, Feytmans E. 1998. Assessing protein structures with a non-local atomic interaction energy. J. Mol. Biol. 277:1141-1152.
40. Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N. 2010. ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res. 38:W529-W533.
41. Holm L, Kääriäinen S, Wilton C, Plewczynski D. 2006. Using Dali for structural comparison of proteins. Curr. Protoc. Bioinformatics 14:5.5.1-5.5.24. doi:10.1002/0471250953.bi0505s14.
42. Herniou EA, Jehle JA. 2007. Baculovirus phylogeny and evolution. Curr. Drug Targets 8:1043-1050.
43. Wang R, Deng F, Hou D, Zhao Y, Guo L, Wang H, Hu Z. 2010. Proteomics of the Autographa californica nucleopolyhedrovirus budded virions. J. Virol. 84:7233-7242.
44. Braunagel SC, Russell WK, Rosas-Acosta G, Russell DH, Summers MD. 2003. Determination of the protein composition of the occlusion-derived virus of Autographa californica nucleopolyhedrovirus. Proc. Natl. Acad. Sci. U. S. A. 100:9797-9802.
45. Luckow VA. 1993. Baculovirus systems for the expression of human gene products. Curr. Opin. Biotechnol. 4:564-572.
46. Heger A, Holm L. 2000. Rapid automatic detection and alignment of repeats in protein sequences. Proteins 41:224-237.
47. White MK, Johnson EM, Khalili K. 2009. Multiple roles for Purα in cellular and viral regulation. Cell Cycle 8:414-420.
48. Gallia GL, Johnson EM, Khalili K. 2000. Purα: a multifunctional singlestranded DNA-and RNA-binding protein. Nucleic Acids Res. 28:3197-3205.
49. Olszewski J, Miller LK. 1997. Identification and characterization of a baculovirus structural protein, VP1054, required for nucleocapsid formation. J. Virol. 71:5040-5050.
50. Liu C, Li Z, Wu W, Li L, Yuan M, Pan L, Yang K, Pang Y. 2008. Autographa californica multiple nucleopolyhedrovirus ac53 plays a role in nucleocapsid assembly. Virology 382:59-68.
51. Wortman MJ, Krachmarov CP, Kim JH, Gordon RG, Chepenik LG,Brady JN, Gallia GL, Khalili K, Johnson EM. 2000. Interaction of HIV-1 Tat with Purα in nuclei of human glial cells: characterization of RNAmediated protein-protein binding. J. Cell. Biochem. 77:65-74.
52. Gallia GL, Darbinian N, Tretiakova A, Ansari SA, Rappaport J, Brady J, Wortman MJ, Johnson EM, Khalili K. 1999. Association of HIV-1 Tat with the cellular protein, Purα, is mediated by RNA. Proc. Natl. Acad. Sci. U. S. A. 96:11572-11577.
53. Wang H, White MK, Kaminski R, Darbinian N, Amini S, Johnson EM, Khalili K, Rappaport J. 2008. Role of Purα in the modulation of homologous recombination-directed DNA repair by HIV-1 Tat. Anticancer Res. 28:1441-1447.
54. Chang CF, Gallia GL, Muralidharan V, Chen NN, Zoltick P, Johnson E, Khalili K. 1996. Evidence that replication of human neurotropic JC virus DNA in glial cells is regulated by the sequence-specific single-stranded DNA-binding protein Pur alpha. J. Virol. 70:4150-4156.
55. Chen NN, Chang CF, Gallia GL, Kerr DA, Johnson EM, Krachmarov CP, Barr SM, Frisque RJ, Bollag B, Khalili K. 1995. Cooperative action of cellular proteins YB-1 and Pur alpha with the tumor antigen of the human JC polyomavirus determines their interaction with the viral lytic control element. Proc. Natl. Acad. Sci. U. S. A. 92:1087-1091.
56. Ohkawa T, Volkman LE, Welch MD. 2010. Actin-based motility drives baculovirus transit to the nucleus and cell surface. J. Cell Biol. 190:187-195.
57. Machesky LM, Insall RH, Volkman LE. 2001. WASP homology sequences in baculoviruses. Trends Cell Biol. 11:286-287.
58. Castellano F, Clainche CL, Patin D, Carlier MF, Chavrier P. 2001. A WASp-VASP complex regulates actin polymerization at the plasma membrane. EMBO J. 20:5603-5614.
59. Wortman MJ, Johnson EM, Bergemann AD. 2005. Mechanism of DNA binding and localized strand separation by Pur-alpha and com-parison with Pur family member, Pur-beta. Biochim. Biophys. Acta 1743:64-78.
60. Darbinian N, Gallia GL, Khalili K. 2001. Helix-destabilizing properties of the human single-stranded DNA-and RNA-binding protein Purα. J. Cell. Biochem. 80:589-595.
61. Kool M, Voncken JW, van Lier FL, Tramper J, Vlak JM. 1991. Detection and analysis of Autographa californica nuclear polyhedrosis virus mutants with defective interfering properties. Virology 183:739-746.
62. Pijlman GP, Dortmans JC, Vermeesch AM, Yang K, Martens DE, Goldbach RW, Vlak JM. 2002. Pivotal role of the non-hr origin of DNA replication in the genesis of defective interfering baculoviruses. J. Virol. 76:5605-5611.
63. Giri L, Feiss MG, Bonning BC, Murhammer DW. 2012. Production of baculovirus defective interfering particles during serial passage is delayed by removing transposon target sites in fp25k. J. Gen. Virol. 93:389-399.