Identification of giant Mimivirus protein functions using RNA interference

Frontiers in Microbiology

Volumn 6, Issue APR, 2015, Pages

  Sobhy, Haitham ^a   La Scola, Bernard ^a,b   Pagnier, Isabelle ^a   Raoult, Didier ^a,b   Colson, Philippe ^a,b  

^a AIX MARSEILLE UNIVERSITY   (France)

^b TIMONE HOSPITAL   (France)

Author keywords

Fiber; Giant virus; Megavirales; Mimivirus; Nucleocytoplasmic large DNA virus; RNA interference; Short interfering RNA

Indexed keywords

PROTEIN L725; PROTEIN L829; PROTEIN R135; PROTEIN R856; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ACANTHAMOEBA POLYPHAGA; AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE SILENCING; IMMUNOGOLD LABELING; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; METAGENOMICS; MIMIVIRUS; MOLECULAR GENETICS; NONHUMAN; OPEN READING FRAME; PHYLOGENETIC TREE; PROTEIN FUNCTION; PROTEOMICS; RNA INTERFERENCE; SEQUENCE HOMOLOGY; WESTERN BLOTTING;

DNA VIRUSES; MIMIVIRUS;

EID: 84930945766     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00345     Document Type: Article

References (42)

1. Abergel, C., Chenivesse, S., Byrne, D., Suhre, K., Arondel, V., and Claverie, J. M. (2005). Mimivirus TyrRS: preliminary structural and functional characterization of the first amino-acyl tRNA synthetase found in a virus. Acta. Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 61, 212-215. doi: 10.1107/S174430910500062X.
2. Abergel, C., Rudinger-Thirion, J., Giege, R., and Claverie, J. M. (2007). Virus-encoded aminoacyl-tRNA synthetases: structural and functional characterization of mimivirus TyrRS and MetRS. J. Virol. 81, 12406-12417. doi: 10.1128/JVI.01107-07.
3. Aherfi, S., Boughalmi, M., Pagnier, I., Fournous, G., La Scola, B., Raoult, D., et al. (2014). Complete genome sequence of tunisvirus, a new member of the proposed family Marseilleviridae. Arch. Virol. 159, 2349-2358. doi: 10.1007/s00705-014-2023-5.
4. Arslan, D., Legendre, M., Seltzer, V., Abergel, C., and Claverie, J. M. (2011). Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae. Proc. Natl. Acad. Sci. U.S.A. 108, 17486-17491. doi: 10.1073/pnas.1110889108.
5. Azza, S., Cambillau, C., Raoult, D., and Suzan-Monti, M. (2009). Revised Mimivirus major capsid protein sequence reveals intron-containing gene structure and extra domain. BMC Mol. Biol. 10:39. doi: 10.1186/1471-2199-10-39.
6. Blatch, G. L., and Lassle, M. (1999). The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays 21, 932-939. doi: 10.1002/(SICI)1521-1878(199911)21:11<932::AID-BIES5>3.0.CO;2-N.
7. Boughalmi, M., Pagnier, I., Aherfi, S., Colson, P., Raoult, D., and La Scola, B. (2013a). First isolation of a Marseillevirus in the Diptera Syrphidae Eristalis tenax. Intervirology 56, 386-394. doi: 10.1159/000354560.
8. Boughalmi, M., Saadi, H., Pagnier, I., Colson, P., Fournous, G., Raoult, D., et al. (2013b). High-throughput isolation of giant viruses of the Mimiviridae and Marseilleviridae families in the Tunisian environment. Environ. Microbiol. 15, 2000-2007. doi: 10.1111/1462-2920.12068.
9. Boyer, M., Azza, S., Barrassi, L., Klose, T., Campocasso, A., Pagnier, I., et al. (2011). Mimivirus shows dramatic genome reduction after intraamoebal culture. Proc. Natl. Acad. Sci. U.S.A. 108, 10296-10301. doi: 10.1073/pnas.1101118108.
10. Boyer, M., Gimenez, G., Suzan-Monti, M., and Raoult, D. (2010). Classification and determination of possible origins of ORFans through analysis of nucleocytoplasmic large DNA viruses. Intervirology 53, 310-320. doi: 10.1159/000312916.
11. Boyer, M., Yutin, N., Pagnier, I., Barrassi, L., Fournous, G., Espinosa, L., et al. (2009). Giant Marseillevirus highlights the role of amoebae as a melting pot in emergence of chimeric microorganisms. Proc. Natl. Acad. Sci. U.S.A. 106, 21848-21853. doi: 10.1073/pnas.0911354106.
12. Callahan, M. A., Handley, M. A., Lee, Y. H., Talbot, K. J., Harper, J. W., and Panganiban, A. T. (1998). Functional interaction of human immunodeficiency virus type 1 Vpu and Gag with a novel member of the tetratricopeptide repeat protein family. J. Virol. 72, 5189-5197.
13. Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540-552. doi: 10.1093/oxfordjournals.molbev.a026334.
14. Colson, P., De Lamballerie, X., Yutin, N., Asgari, S., Bigot, Y., Bideshi, D. K., et al. (2013). "Megavirales," a proposed new order for eukaryotic nucleocytoplasmic large DNA viruses. Arch. Virol. 158, 2517-2521. doi: 10.1007/s00705-013-1768-6.
15. Colson, P., Yutin, N., Shabalina, S. A., Robert, C., Fournous, G., La Scola, B., et al. (2011). Viruses with more than 1,000 genes: Mamavirus, a new Acanthamoeba polyphaga mimivirus strain, and reannotation of Mimivirus genes. Genome Biol. Evol. 3, 737-742. doi: 10.1093/gbe/evr048.
16. Cortajarena, A. L., and Regan, L. (2006). Ligand binding by TPR domains. Protein Sci. 15, 1193-1198. doi: 10.1110/ps.062092506.
17. D'Andrea, L. D., and Regan, L. (2003). TPR proteins: the versatile helix. Trends Biochem. Sci. 28, 655-662. doi: 10.1016/j.tibs.2003.10.007.
18. Das, A. K., Cohen, P. W., and Barford, D. (1998). The structure of the tetratricopeptide repeats of protein phosphatase 5: implications for TPR-mediated protein-protein interactions. EMBO J. 17, 1192-1199. doi: 10.1093/emboj/17.5.1192.
19. Fischer, M. G., Allen, M. J., Wilson, W. H., and Suttle, C. A. (2010). Giant virus with a remarkable complement of genes infects marine zooplankton. Proc. Natl. Acad. Sci. U.S.A. 107, 19508-19513. doi: 10.1073/pnas.1007615107.
20. Forterre, P. (2010). Giant viruses: conflicts in revisiting the virus concept. Intervirology 53, 362-378. doi: 10.1159/000312921.
21. Jensen, O. N., Houthaeve, T., Shevchenko, A., Cudmore, S., Ashford, T., Mann, M., et al. (1996). Identification of the major membrane and core proteins of vaccinia virus by two-dimensional electrophoresis. J. Virol. 70, 7485-7497.
22. Jeshtadi, A., Burgos, P., Stubbs, C. D., Parker, A. W., King, L. A., Skinner, M. A., et al. (2010). Interaction of poxvirus intracellular mature virion proteins with the TPR domain of kinesin light chain in live infected cells revealed by two-photon-induced fluorescence resonance energy transfer fluorescence lifetime imaging microscopy. J. Virol. 84, 12886-12894. doi: 10.1128/JVI.01395-10.
23. Klose, T., Kuznetsov, Y. G., Xiao, C., Sun, S., Mcpherson, A., and Rossmann, M. G. (2010). The three-dimensional structure of Mimivirus. Intervirology 53, 268-273. doi: 10.1159/000312911.
24. Kuznetsov, Y. G., Xiao, C., Sun, S., Raoult, D., Rossmann, M., and Mcpherson, A. (2010). Atomic force microscopy investigation of the giant mimivirus. Virology 404, 127-137. doi: 10.1016/j.virol.2010.05.007.
25. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., Mcgettigan, P. A., Mcwilliam, H., et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948. doi: 10.1093/bioinformatics/btm404.
26. La Scola, B., Audic, S., Robert, C., Jungang, L., De Lamballerie, X., Drancourt, M., et al. (2003). A giant virus in amoebae. Science 299, 2033. doi: 10.1126/science.1081867.
27. La Scola, B., Desnues, C., Pagnier, I., Robert, C., Barrassi, L., Fournous, G., et al. (2008). The virophage as a unique parasite of the giant Mimivirus. Nature 455, 100-104. doi: 10.1038/nature07218.
28. Legendre, M., Bartoli, J., Shmakova, L., Jeudy, S., Labadie, K., Adrait, A., et al. (2014). Thirty-thousand-year-old distant relative of giant icosahedral DNA viruses with a pandoravirus morphology. Proc. Natl. Acad. Sci. U.S.A. 111, 4274-4279. doi: 10.1073/pnas.1320670111.
29. Lin, J. Y., Mendu, V., Pogany, J., Qin, J., and Nagy, P. D. (2012). The TPR domain in the host Cyp40-like cyclophilin binds to the viral replication protein and inhibits the assembly of the tombusviral replicase. PLoS Pathog 8:e1002491. doi: 10.1371/journal.ppat.1002491.
30. Moreira, D., and Brochier-Armanet, C. (2008). Giant viruses, giant chimeras: the multiple evolutionary histories of Mimivirus genes. BMC Evol. Biol. 8:12. doi: 10.1186/1471-2148-8-12.
31. Philippe, N., Legendre, M., Doutre, G., Coute, Y., Poirot, O., Lescot, M., et al. (2013). Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science 341, 281-286. doi: 10.1126/science.1239181.
32. Piacente, F., Marin, M., Molinaro, A., De Castro, C., Seltzer, V., Salis, A., et al. (2012). Giant DNA virus mimivirus encodes pathway for biosynthesis of unusual sugar 4-amino-4,6-dideoxy-D-glucose (Viosamine). J. Biol. Chem. 287, 3009-3018. doi: 10.1074/jbc.M111.314559.
33. Price, M. N., Dehal, P. S., and Arkin, A. P. (2010). FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490. doi: 10.1371/journal.pone.0009490.
34. Raoult, D., Audic, S., Robert, C., Abergel, C., Renesto, P., Ogata, H., et al. (2004). The 1.2-megabase genome sequence of Mimivirus. Science 306, 1344-1350. doi: 10.1126/science.1101485.
35. Raoult, D., and Forterre, P. (2008). Redefining viruses: lessons from Mimivirus. Nat. Rev. Microbiol. 6, 315-319. doi: 10.1038/nrmicro1858.
36. Renesto, P., Abergel, C., Decloquement, P., Moinier, D., Azza, S., Ogata, H., et al. (2006). Mimivirus giant particles incorporate a large fraction of anonymous and unique gene products. J. Virol. 80, 11678-11685. doi: 10.1128/JVI.00940-06.
37. Saadi, H., Pagnier, I., Colson, P., Cherif, J. K., Beji, M., Boughalmi, M., et al. (2013a). First isolation of Mimivirus in a patient with pneumonia. Clin. Infect. Dis 57, e127-e134. doi: 10.1093/cid/cit354.
38. Saadi, H., Reteno, D. G., Colson, P., Aherfi, S., Minodier, P., Pagnier, I., et al. (2013b). Shan virus: a new mimivirus isolated from the stool of a Tunisian patient with pneumonia. Intervirology 56, 424-429. doi: 10.1159/000354564.
39. Sobhy, H., and Colson, P. (2012). Gemi: PCR primers prediction from multiple alignments. Comp. Funct. Genomics 2012, 783138. doi: 10.1155/2012/783138.
40. Tani, J., Shimamoto, S., Mori, K., Kato, N., Moriishi, K., Matsuura, Y., et al. (2013). Ca(2+)/S100 proteins regulate HCV virus NS5A-FKBP8/FKBP38 interaction and HCV virus RNA replication. Liver Int. 33, 1008-1018. doi: 10.1111/liv.12151.
41. Xiao, C., Kuznetsov, Y. G., Sun, S., Hafenstein, S. L., Kostyuchenko, V. A., Chipman, P. R., et al. (2009). Structural studies of the giant mimivirus. PLoS Biol. 7:e92. doi: 10.1371/journal.pbio.1000092.
42. Yoosuf, N., Yutin, N., Colson, P., Shabalina, S. A., Pagnier, I., Robert, C., et al. (2012). Related giant viruses in distant locations and different habitats: Acanthamoeba polyphaga moumouvirus represents a third lineage of the Mimiviridae that is close to the megavirus lineage. Genome Biol. Evol. 4, 1324-1330. doi: 10.1093/gbe/evs109.