Paramecium bursaria chlorella virus 1 proteome reveals novel architectural and regulatory features of a giant virus

Journal of Virology

Volumn 86, Issue 16, 2012, Pages 8821-8834

  Dunigan, David D ^a   Cerny, Ronald L ^a   Bauman, Andrew T ^b   Roach, Jared C ^c   Lane, Leslie C ^a   Agarkova, Irina V ^a   Wulser, Kurt ^a   Yanai Balser, Giane M ^a   Gurnon, James R ^a   Vitek, Jason C ^a   Kronschnabel, Bernard J ^a   Jeanniard, Adrien ^d   Blanc, Guillaume ^d   Upton, Chris ^e   Duncan, Garry A ^f   McClung, O William ^f   Ma, Fangrui ^a   Van Etten, James L ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b Ocean Biologics   (United States)

^c INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^d CNRS Aix Marseille University   (France)

^e UNIVERSITY OF VICTORIA   (Canada)

^f NEBRASKA WESLEYAN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSFER RNA; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CHLORELLA; CHLORELLA VARIABILIS; CHLORELLA VIRUS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CODON; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE MAPPING; GENETIC CODE; GENETIC DATABASE; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PARAMECIUM BURSARIA CHLORELLA VIRUS 1; PREDICTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; SIGNAL TRANSDUCTION; STRUCTURAL PROTEOMICS; TRANSCRIPTION REGULATION; VIRION; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS MORPHOGENESIS;

GENOME, VIRAL; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PARAMECIUM; PHYCODNAVIRIDAE; PROTEOME; SEQUENCE ANALYSIS, DNA; VIRAL PROTEINS;

EID: 84865104083     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00907-12     Document Type: Article

References (67)

1. Abrescia NG, et al. 2004. Insights into assembly from structural analysis of bacteriophage PRD1. Nature 432:68-74.
2. Agarkova I, et al. 2008. Chlorovirus-mediated membrane depolarization of Chlorella alters secondary active transport of solutes. J. Virol. 82:12181-12190.
3. Agarkova IV, Dunigan DD, Van Etten JL. 2006. Virion-associated restriction endonucleases of chloroviruses. J. Virol. 80:8114-8123.
4. Blanc G, et al. 2010. The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex. Plant Cell 22:2943-2955.
5. Cherrier MV, et al. 2009. An icosahedral algal virus has a complex unique vertex decorated by a spike. Proc. Natl. Acad. Sci. U. S. A. 106:11085-11089.
6. Chuchird N, et al. 2002. A variable region on the chlorovirus CVK2 genome contains five copies of the gene for Vp260, a viral-surface glycoprotein. Virology 295:289-298.
7. Chung C-S, et al. 2006. Vaccinia virus proteome: identification of proteins in vaccinia virus intracellular mature virion particles. J. Virol. 80: 2127-2140.
8. Cockburn J, et al. 2004. Membrane structure and interactions with protein and DNA in bacteriophage PRD1. Nature 432:122-125.
9. Craig R, Beavis RC. 2004. TANDEM: matching proteins with tandem mass spectra. Bioinformatics 20:1466-1467.
10. Dereeper A, et al. 2008. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36:W465-W469.
11. Dunigan DD, Fitzgerald LA, Van Etten JL. 2006. Phycodnaviruses: a peek at genetic diversity. Virus Res. 117:119-132.
12. Frohns F, et al. 2006. Potassium ion channels of chlorella viruses cause rapid depolarization of host cells during infection. J. Virol. 80:2437-2444.
13. Graves MV, Meints RH. 1992. Characterization of the major capsid protein and cloning of its gene from algal virus PBCV-1. Virology 188: 198-207.
14. Higdon R, Hogan J, Kolker N, van Belle G, Kolker E. 2007. Experimentspecific estimation of peptide identification probabilities using a randomized database. OMICS 11:351-356.
15. Higdon R, Hogan J, Van Belle G, Kolker E. 2005. Randomized sequence databases for tandem mass spectrometry peptide and protein identification. OMICS 9:364-379.
16. Higdon R, Kolker E. 2007. A predictive model for identifying proteins by a single peptide match. Bioinformatics 23:277-280.
17. Ishihama Y, et al. 2005. Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol. Cell. Proteomics 4:1265-1272.
18. Iyer L, Balaji S, Koonin E, Aravind L. 2006. Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res. 117:156-184.
19. Käll L, Krogh A, Sonnhammer EL. 2004. A combined transmembrane topology and signal peptide prediction method. J. Mol. Biol. 338:1027-1036.
20. Kang M, Dunigan DD, Van Etten JL. 2005. Chloroviruses: a genus of Phycodnaviridae that infects certain chlorella-like green algae. Mol. Plant Pathol. 6:213-224.
21. Kattenhorn L, et al. 2004. Identification of proteins associated with murine cytomegalovirus virions. J. Virol. 78:11187-11197.
22. Kuznetsov YG, Gurnon JR, Van Etten JL, McPherson A. 2005. Atomic force microscopy investigation of a chlorella virus, PBCV-1. J. Struct. Biol. 149:256-263.
23. Landstein D, Burbank DE, Nietfeldt JW, Van Etten JL. 1995. Large deletions in antigenic variants of the chlorella virus PBCV-1. Virology 214:413-420.
24. Lane L. 1978. A simple method for stabilizing protein-sulfhydryl groups during SDS-gel electrophoresis. Anal. Biochem. 86:655-664.
25. Li Y, et al. 1997. Analysis of 74 kb of DNA located at the right end of the 330-kb chlorella virus PBCV-1 genome. Virology 237:360-377.
26. + channel Kcv in the replication of chlorella virus PBCV-1. FEBS Lett. 552:7-11.
27. Meints RH, Burbank DE, Van Etten JL, Lamport DT. 1988. Properties of the chlorella receptor for the virus PBCV-1. Virology 164:15-21.
28. Meints RH, Lee K, Burbank DE, Van Etten JL. 1984. Infection of a chlorella-like alga with the virus, PBCV-1: ultrastructural studies. Virology 138:341-346.
29. Möller S, Croning MDR, Apweiler R. 2001. Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 17:646-653.
30. Nandhagopal N, et al. 2002. The structure and evolution of the major capsid protein of a large, lipid-containing DNA virus. Proc. Natl. Acad. Sci. U. S. A. 99:14758-14763.
31. + from host cells during early phase of infection. Virology 372:340-348.
32. O'Connor CM, Kedes DH. 2006. Mass spectrometric analyses of purified rhesus monkey rhadinovirus reveal 33 virion-associated proteins. J. Virol. 80:1574-1583.
33. Onimatsu H, Suganuma K, Uenoyama S, Yamada T. 2006. C-terminal repetitive motifs in Vp130 present at the unique vertex of the chlorovirus capsid are essential for binding to the host chlorella cell wall. Virology 353:432-442.
34. Onimatsu H, Sugimoto I, Fujie M, Usami S, Yamada T. 2004. Vp130, a chloroviral surface protein that interacts with the host Chlorella cell wall. Virology 319:71-80.
35. Que Q, et al. 1994. Protein glycosylation and myristylation in chlorella virus PBCV-1 and its antigenic variants. Virology 203:320-327.
36. Renesto P, et al. 2006. Mimivirus giant particles incorporate a large fraction of anonymous and unique gene products. J. Virol. 80:11678-11685.
37. Resch W, Hixson KK, Moore RJ, Lipton MS, Moss B. 2007. Protein composition of the vaccinia virus mature virion. Virology 358:233-247.
38. Santoni V, Molloy M, Rabilloud T. 2000. Membrane proteins and proteomics: un amour impossible? Electrophoresis 21:1054-1070.
39. Shevchenko A, Wilm M, Vorm O, Mann M. 1996. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68:850-858.
40. Short CM, Rusanova O, Short SM. 2011. Quantification of virus genes provides evidence for seed-bank populations of phycodnaviruses in Lake Ontario, Canada. ISME J. 5:810-821.
41. Skrdla MP, Burbank DE, Xia Y, Meints RH, Van Etten JL. 1984. Structural proteins and lipids in a virus, PBCV-1, which replicates in a chlorella-like alga. Virology 135:308-315.
42. Song WJ, et al. 2004. Functional genomics analysis of Singapore grouper iridovirus: complete sequence determination and proteomic analysis. J. Virol. 78:12576-12590.
43. Stothard P, Wishart DS. 2005. Circular genome visualization and exploration using CGView. Bioinformatics 21:537-539.
44. Stros M, Launholt D, Grasser KD. 2007. The HMG-box: a versatile protein domain occurring in a wide variety of DNA-binding proteins. Cell. Mol. Life Sci. 64:2590-2606.
45. Sugimoto I, Onimatsu H, Fujie M, Usami S, Yamada T. 2004. vAL-1, a novel polysaccharide lyase encoded by chlorovirus CVK2. FEBS Lett. 559: 51-56.
46. Sun L, Adams B, Gurnon J, Ye Y, Van Etten JL. 1999. Characterization of two chitinase genes and one chitosanase gene encoded by chlorella virus PBCV-1. Virology 263:376-387.
47. Thiel G, Moroni A, Dunigan D, Van Etten JL. 2010. Initial events associated with virus PBCV-1 infection of Chlorella NC64A. Prog. Bot. 71:169-183.
48. Thomas JO. 2001. HMG1 and 2: architectural DNA-binding proteins. Biochem. Soc. Trans. 29:395-401.
49. Tusnády GE, Simon I. 2001. The HMMTOP transmembrane topology prediction server. Bioinformatics 17:849-850.
50. +channel Kcv. Ph.D. dissertation. Universita Degli Studi di Milano, Milan, Italy.
51. Van Etten JL, Burbank DE, Kuczmarski D, Meints RH. 1983. Virus infection of culturable chlorella-like algae and development of a plaque assay. Science 219:994-996.
52. Van Etten JL, Burbank DE, Xia Y, Meints RH. 1983. Growth cycle of a virus, PBCV-1, that infects chlorella-like algae. Virology 126:117-125.
53. Van Etten JL, Dunigan DD. 2012. Chloroviruses: not your every day plant virus. Trends Plant Sci. 17:1-8.
54. Van Etten JL, Graves MV, Muller DG, Boland W, Delaroque N. 2002. Phycodnaviridae-large DNA algal viruses. Arch. Virol. 147:1479-1516.
55. Van Etten JL, Lane LC, Meints RH. 1991. Viruses and viruslike particles of eukaryotic algae. Microbiol. Rev. 55:586-620.
56. Van Etten JL, Meints RH. 1999. Giant viruses infecting algae. Annu. Rev. Microbiol. 53:447-494.
57. Van Etten JL, Van Etten CH, Johnson JK, Burbank DE. 1985. A survey for viruses from fresh water that infect a eucaryotic chlorella-like green alga. Appl. Environ. Microbiol. 49:1326-1328.
58. Wulfmeyer T, et al. 2012. Structural organization of DNA in chlorella viruses. PLoS One 7:e30133. doi:10.1371/journal.pone.0030133.
59. Yamada T, Furukawa S, Hamazaki T, Songsri P. 1996. Characterization of DNA-binding proteins and protein kinase activities in chlorella virus CVK2. Virology 219:395-406.
60. Yamada T, Higashiyama T, Fukuda T. 1991. Screening of natural waters for viruses which infect chlorella cells. Appl. Environ. Microbiol. 57:3433-3437.
61. Yamada T, Onimatsu H, Van Etten JL. 2006. Chlorella viruses. Adv. Virus Res. 66:293-366.
62. Yan X, et al. 2005. The structure of a T=169d algal virus, PBCV-1, at 15 Å resolution. Microsc. Microanal. 11:1056-1057.
63. Yan X, et al. 2000. Structure and assembly of large lipid-containing dsDNA viruses. Nat. Struct. Biol. 7:101-103.
64. Yanai-Balser GM, et al. 2010. Microarray analysis of chlorella virus PBCV-1 transcription. J. Virol. 84:532-542.
65. Zhang X, et al. 2011. Three-dimensional structure and function of the Paramecium bursaria chlorella virus capsid. Proc. Natl. Acad. Sci. U. S. A. 108:14837-14842.
66. Zhang Y, et al. 2003. Characterization of a chlorella virus PBCV-1 encoded ribonuclease III. Virology 317:73-83.
67. Zhang Y, Strasser P, Grabherr R, Van Etten JL. 1994. Hairpin loop structure at the termini of the chlorella virus PBCV-1 genome. Virology 202:1079-1082.