Lymantria dispar iflavirus 1 (LdIV1), a new model to study iflaviral persistence in lepidopterans

Journal of General Virology

Volumn 95, Issue , 2014, Pages 2285-2296

  Carrillo Tripp, Jimena ^a   Krueger, Elizabeth N ^a   Harrison, Robert L ^b   Toth, Amy L ^a   Allen Miller, W ^a   Bonning, Bryony C ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLYPROTEIN; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; CELL LINE; CONTROLLED STUDY; GENE SEQUENCE; GENE SILENCING; INFECTION; LARVA; LYMANTRIA DISPAR; LYMANTRIA DISPAR IFLAVIRUS 1; NONHUMAN; NUCLEOTIDE SEQUENCE; PREDICTION; RNA INTERFERENCE; RNA VIRUS; VIRUS GENOME; VIRUS PARTICLE; ANIMAL; DNA SEQUENCE; GENETICS; ISOLATION AND PURIFICATION; LEPIDOPTERA; MOLECULAR GENETICS; ULTRASTRUCTURE; VIRION; VIROLOGY;

ANIMALS; CELL LINE; GENOME, VIRAL; LARVA; LEPIDOPTERA; MOLECULAR SEQUENCE DATA; POLYPROTEINS; RNA VIRUSES; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; VIRAL PROTEINS; VIRION;

EID: 85047695095     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.067710-0     Document Type: Article

References (76)

1. Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K. & Walter, P. (2002). Molecular Biology of the Cell, 4th edn. New York: Garland Science.
2. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389-3402.
3. Altschul, S. F., Wootton, J. C., Gertz, E. M., Agarwala, R., Morgulis, A., Schäffer, A. A. & Yu, Y. K. (2005). Protein database searches using compositionally adjusted substitution matrices. FEBS J 272, 5101- 5109.
4. Blom, N., Hansen, J., Brunak, S. & Blaas, D. (1996). Cleavage site analysis in picornaviral polyproteins: discovering cellular targets by neural networks. Protein Sci 5, 2203-2216.
5. Cavener, D. R. & Ray, S. C. (1991). Eukaryotic start and stop translation sites. Nucleic Acids Res 19, 3185-3192.
6. Chen, Y. P., Becnel, J. J. & Valles, S. M. (2012a). RNA Viruses Infecting Pest Insects. In Insect Pathology, 2nd edn, pp. 133-170. Edited by F. E. Vega & H. K. Kaya. San Diego: Academic Press.
7. Chen, Y. P., Nakashima, N., Christian, P. D., Bakonyi, T., Bonning, B. C., Valles, S. M. & Lightner, D. (2012b). Family Dicistroviridae. In Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses, pp. 840-845. Edited by A. M. Q. King, M. J. Adams, E. B. Carstens & E. J. Lefkowitz. London: Elsevier Academic.
8. Choi, J. Y., Kim, Y.-S., Wang, Y., Shin, S. W., Kim, I., Tao, X. Y., Liu, Q., Roh, J. Y., Kim, J. S. & Je, Y. H. (2012). Complete genome sequence of a novel picorna-like virus isolated from Spodoptera exigua. J Asia Pac Entomol 15, 259-263.
9. de Miranda, J. R. & Genersch, E. (2010). Deformed wing virus. J Invertebr Pathol 103 (Suppl 1), S48-S61.
10. de Miranda, J. R., Dainat, B., Locke, B., Cordoni, G., Berthoud, H., Gauthier, L., Neumann, P., Budge, G. E., Ball, B. V. & Stoltz, D. B. (2010). Genetic characterization of slow bee paralysis virus of the honeybee (Apis mellifera L.). J Gen Virol 91, 2524-2530.
11. Domingo, E., Sheldon, J. & Perales, C. (2012). Viral quasispecies evolution. Microbiol Mol Biol Rev 76, 159-216.
12. Drugmand, J.-C., Schneider, Y.-J. & Agathos, S. N. (2012). Insect cells as factories for biomanufacturing. Biotechnol Adv 30, 1140-1157.
13. Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783-791.
14. Garner, K. J. & Slavicek, J. M. (1999). Identification of a non-LTR retrotransposon from the gypsy moth. Insect Mol Biol 8, 231-242.
15. Geng, P., Li, W., Lin, L., de Miranda, J. R., Emrich, S., An, L. & Terenius, O. (2014). Genetic characterization of a novel Iflavirus associated with vomiting disease in the Chinese oak silkmoth Antheraea pernyi. PLoS ONE 9, e92107.
16. Ghosh, R. C., Ball, B. V., Willcocks, M. M. & Carter, M. J. (1999). The nucleotide sequence of sacbrood virus of the honey bee: an insect picorna-like virus. J Gen Virol 80, 1541-1549.
17. Goic, B. & Saleh, M. C. (2012). Living with the enemy: viral persistent infections from a friendly viewpoint. Curr Opin Microbiol 15, 531- 537.
18. Goic, B., Vodovar, N., Mondotte, J. A., Monot, C., Frangeul, L., Blanc, H., Gausson, V., Vera-Otarola, J., Cristofari, G. & Saleh, M. C. (2013). RNA-mediated interference and reverse transcription control the persistence of RNA viruses in the insect model Drosophila. Nat Immunol 14, 396-403.
19. Goodwin, R. H., Tompkins, G. J. & McCawley, P. (1978). Gypsy moth cell lines divergent in viral susceptibility. I. Culture and identification. In Vitro 14, 485-494.
20. Gorbalenya, A. E., Donchenko, A. P., Blinov, V. M. & Koonin, E. V. (1989). Cysteine proteases of positive strand RNA viruses and chymotrypsin-like serine proteases. A distinct protein superfamily with a common structural fold. FEBS Lett 243, 103-114.
21. Guzo, D., Dougherty, E. M., Lynn, D. E., Braun, S. K. & Weiner, R. M. (1991). Changes in macromolecular synthesis of gypsy moth cell line IPLB-Ld652Y induced by Autographa californica nuclear polyhedrosis virus infection. J Gen Virol 72, 1021-1029.
22. Harrison, R. L., Sparks, W. O. & Bonning, B. C. (2010). Autographa californica multiple nucleopolyhedrovirus ODV-E56 envelope protein is required for oral infectivity and can be substituted functionally by Rachiplusia ou multiple nucleopolyhedrovirus ODV-E56. J Gen Virol 91, 1173-1182.
23. He, B., Li, Z., Yang, F., Zheng, J., Feng, Y., Guo, H., Li, Y., Wang, Y., Su, N. & other authors (2013). Virome profiling of bats from Myanmar by metagenomic analysis of tissue samples reveals more novel mammalian viruses. PLoS ONE 8, e61950.
24. Hulo, C., de Castro, E., Masson, P., Bougueleret, L., Bairoch, A., Xenarios, I. & Le Mercier, P. (2011). ViralZone: a knowledge resource to understand virus diversity. Nucleic Acids Res 39 (Database issue), D576-D582.
25. Isawa, H., Asano, S., Sahara, K., Iizuka, T. & Bando, H. (1998). Analysis of genetic information of an insect picorna-like virus, infectious flacherie virus of silkworm: evidence for evolutionary relationships among insect, mammalian and plant picorna(-like) viruses. Arch Virol 143, 127-143.
26. Jarvis, D. L., Weinkauf, C. & Guarino, L. A. (1996). Immediate-early baculovirus vectors for foreign gene expression in transformed or infected insect cells. Protein Expr Purif 8, 191-203.
27. Johansson, H., Dhaygude, K., Lindström, S., Helanterä, H., Sundström, L. & Trontti, K. (2013). A metatranscriptomic approach to the identification of microbiota associated with the ant Formica exsecta. PLoS ONE 8, e79777.
28. Jovel, J. & Schneemann, A. (2011). Molecular characterization of Drosophila cells persistently infected with Flock House virus. Virology 419, 43-53.
29. Kazuhiko, Y., Shinji, T. & Tosihiko, H. (1996). Replication of a small isometric virus in cultured Lymantria dispar (Lepidoptera: Lymantriidae) cells. Appl Entomol Zool (Jpn) 31, 637-641.
30. Killington, R. A., Stokes, A. & Hierholzer, J. C. (1996). PEG precipitation. In Virology Methods Manual, pp. 73-74. Edited by B. W. J. Mahy & H. O. Kangro. London: Academic Press.
31. Kim, M. K., Sisson, G. & Stoltz, D. (1996). Ichnovirus infection of an established gypsy moth cell line. J Gen Virol 77, 2321-2328.
32. Koonin, E. V., Dolja, V. V. & Morris, T. J. (1993). Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. Crit Rev Biochem Mol Biol 28, 375-430.
33. Kozak, M. (1999). Initiation of translation in prokaryotes and eukaryotes. Gene 234, 187-208.
34. Kuhn, J. H. & Jahrling, P. B. (2010). Clarification and guidance on the proper usage of virus and virus species names. Arch Virol 155, 445-453.
35. Lanzi, G., de Miranda, J. R., Boniotti, M. B., Cameron, C. E., Lavazza, A., Capucci, L., Camazine, S. M. & Rossi, C. (2006). Molecular and biological characterization of deformed wing virus of honeybees (Apis mellifera L.). J Virol 80, 4998-5009.
36. Léry, X., Fédière, G., Taha, A., Salah, M. & Giannotti, J. (1997). A new small RNA virus persistently infecting an established cell line of Galleria mellonella, induced by a heterologous infection. J Invertebr Pathol 69, 7-13.
37. Léry, X., Zeddam, J. L., Giannotti, J. & Abol-Ela, S. (1998). Evidence for two small viruses persistently infecting established cell lines of Phthorimaea operculella, deriving from embryos of the potato tuber moth. New Microbiol 21, 81-85.
38. Li, T. C., Scotti, P. D., Miyamura, T. & Takeda, N. (2007). Latent infection of a new alphanodavirus in an insect cell line. J Virol 81, 10890-10896.
39. Lu, J., Hu, Y., Hu, L., Zong, S., Cai, D., Wang, J., Yu, H. & Zhang, J. (2007). Ectropis obliqua picorna-like virus IRES-driven internal initiation of translation in cell systems derived from different origins. J Gen Virol 88, 2834-2838.
40. Lynn, D. E. (2001). Novel techniques to establish new insect cell lines. In Vitro Cell Dev Biol Anim 37, 319-321.
41. Lynn, D. E. (2006). Lepidopteran cell lines after long-term culture in alternative media: comparison of growth rates and baculovirus replication. In Vitro Cell Dev Biol Anim 42, 149-152.
42. Lynn, D. E., Dougherty, E. M., McClintock, J. T. & Loeb, M. (1988). Development of cell lines from various tissues of Lepidoptera. In Invertebrate and Fish Tissue Culture: Proceedings of the Seventh International Conference on Invertebrate and Fish Tissue Culture, pp. 239-242. Edited by Y. Kuroda, E. Kurstak & K. Maramorosch. Tokyo: Japan Scientific Societies Press.
43. Marchler-Bauer, A., Lu, S., Anderson, J. B., Chitsaz, F., Derbyshire, M. K., DeWeese-Scott, C., Fong, J. H., Geer, L. Y., Geer, R. C. & other authors (2011). CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39 (Database issue), D225-D229.
44. Marchler-Bauer, A., Zheng, C., Chitsaz, F., Derbyshire, M. K., Geer, L. Y., Geer, R. C., Gonzales, N. R., Gwadz, M., Hurwitz, D. I. & other authors (2013). CDD: conserved domains and protein threedimensional structure. Nucleic Acids Res 41 (Database issue), D348- D352.
45. McClintock, J. T., Dougherty, E. M. & Weiner, R. M. (1986). Semipermissive replication of a nuclear polyhedrosis virus of Autographa californica in a gypsy moth cell line. J Virol 57, 197-204.
46. McIntosh, A. H., Grasela, J. J. & Popham, H. J. R. (2005). AcMNPV in permissive, semipermissive, and nonpermissive cell lines from arthropoda. In Vitro Cell Dev Biol Anim 41, 298-304.
47. McKelvey, T. A., Lynn, D. E., Gundersen-Rindal, D., Guzo, D., Stoltz, D. A., Guthrie, K. P., Taylor, P. B. & Dougherty, E. M. (1996). Transformation of gypsy moth (Lymantria dispar) cell lines by infection with Glyptapanteles indiensis polydnavirus. Biochem Biophys Res Commun 225, 764-770.
48. Millán-Leiva, A., Jakubowska, A. K., Ferré, J. & Herrero, S. (2012). Genome sequence of SeIV-1, a novel virus from the Iflaviridae family infective to Spodoptera exigua. J Invertebr Pathol 109, 127-133.
49. Moore, B. A. (2009). Lymantria dispar. In Global Review of Forest Pest and Diseases: A Thematic Study Prepared in the Framework of the Global Forest Resources Assessment 2005, pp. 99-102. Edited by B. A. Moore & G. Allard. Rome: Food and Agriculture Organization of The United Nations.
50. Murakami, R., Suetsugu, Y., Kobayashi, T. & Nakashima, N. (2013). The genome sequence and transmission of an iflavirus from the brown planthopper, Nilaparvata lugens. Virus Res 176, 179-187.
51. Murakami, R., Suetsugu, Y. & Nakashima, N. (2014). Complete genome sequences of two iflaviruses from the brown planthopper, Nilaparvata lugens. Arch Virol 159, 585-588.
52. Nayak, A., Berry, B., Tassetto, M., Kunitomi, M., Acevedo, A., Deng, C., Krutchinsky, A., Gross, J., Antoniewski, C. & Andino, R. (2010). Cricket paralysis virus antagonizes Argonaute 2 to modulate antiviral defense in Drosophila. Nat Struct Mol Biol 17, 547-554.
53. Oliveira, D. C., Hunter, W. B., Ng, J., Desjardins, C. A., Dang, P. M. & Werren, J. H. (2010). Data mining cDNAs reveals three new single stranded RNA viruses in Nasonia (Hymenoptera: Pteromalidae). Insect Mol Biol 19 (Suppl 1), 99-107.
54. Ongus, J. R., Peters, D., Bonmatin, J. M., Bengsch, E., Vlak, J. M. & van Oers, M. M. (2004). Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor. J Gen Virol 85, 3747-3755.
55. Ongus, J. R., Roode, E. C., Pleij, C. W., Vlak, J. M. & van Oers, M. M. (2006). The 59 non-translated region of Varroa destructor virus 1 (genus Iflavirus): structure prediction and IRES activity in Lymantria dispar cells. J Gen Virol 87, 3397-3407.
56. Perera, O. P., Snodgrass, G. L., Allen, K. C., Jackson, R. E., Becnel, J. J., O'Leary, P. F. & Luttrell, R. G. (2012). The complete genome sequence of a single-stranded RNA virus from the tarnished plant bug, Lygus lineolaris (Palisot de Beauvois). J Invertebr Pathol 109, 11-19.
57. Pfeifer, T. A., Ring, M. & Grigliatti, T. A. (2000). Identification and analysis of Lydia, a LTR retrotransposon from Lymantria dispar. Insect Mol Biol 9, 349-356.
58. Reineke, A. & Asgari, S. (2005). Presence of a novel small RNAcontaining virus in a laboratory culture of the endoparasitic wasp Venturia canescens (Hymenoptera: Ichneumonidae). J Insect Physiol 51, 127-135.
59. Rivers, T. M. (1937). Viruses and Koch's postulates. J Bacteriol 33, 1- 12.
60. Rueckert, R. R. & Wimmer, E. (1984). Systematic nomenclature of picornavirus proteins. J Virol 50, 957-959.
61. Ryabov, E. V. (2007). A novel virus isolated from the aphid Brevicoryne brassicae with similarity to Hymenoptera picorna-like viruses. J Gen Virol 88, 2590-2595.
62. Ryan, M. D. & Flint, M. (1997). Virus-encoded proteinases of the picornavirus super-group. J Gen Virol 78, 699-723.
63. Saitou, N. & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406-425.
64. Sharov, A. A., Leonard, D., Liebhold, A. M., Roberts, E. A. & Dickerson, W. (2002). "Slow The Spread'': A national program to contain the gypsy moth. J Forest 100, 30-35.
65. Smith, G., Macias-Munñoz, A. & Briscoe, A. D. (2014). Genome sequence of a novel iflavirus from mRNA sequencing of the butterfly Heliconius erato. Genome Announc 2, e00398-14.
66. Sparks, M. E. & Gundersen-Rindal, D. E. (2011). The Lymantria dispar IPLB-Ld652Y cell line transcriptome comprises diverse virusassociated transcripts. Viruses 3, 2339-2350.
67. Sparks, M. E., Gundersen-Rindal, D. E. & Harrison, R. L. (2013). Complete genome sequence of a novel iflavirus from the transcriptome of Halyomorpha halys, the brown marmorated stink bug. Genome Announc 1, e00910-13.
68. Summers, M. D. & Smith, G. E. (1987). A Manual of Methods for Baculovirus Vectors and Insect Cell Culture Procedures. College Station, TX: Department of Entomology Texas Agricultural Experiment Station and Texas A&M University College Station.
69. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28, 2731-2739.
70. Vaughn, J. L., Goodwin, R. H., Tompkins, G. J. & McCawley, P. (1977). The establishment of two cell lines from the insect Spodoptera frugiperda (Lepidoptera; Noctuidae). In Vitro 13, 213-217.
71. Wang, X., Zhang, J., Lu, J., Yi, F., Liu, C. & Hu, Y. (2004). Sequence analysis and genomic organization of a new insect picorna-like virus, Ectropis obliqua picorna-like virus, isolated from Ectropis obliqua. J Gen Virol 85, 1145-1151.
72. Winter, J., Hall, R. L. & Moyer, R. W. (1995). The effect of inhibitors on the growth of the entomopoxvirus from Amsacta moorei in Lymantria dispar (gypsy moth) cells. Virology 211, 462-473.
73. Wu, C. Y., Lo, C. F., Huang, C. J., Yu, H. T. & Wang, C. H. (2002). The complete genome sequence of Perina nuda picorna-like virus, an insect-infecting RNA virus with a genome organization similar to that of the mammalian picornaviruses. Virology 294, 312-323.
74. Ye, S., Xia, H. J., Dong, C., Cheng, Z. Y., Xia, X. L., Zhang, J. M., Zhou, X. & Hu, Y. Y. (2012). Identification and characterization of iflavirus 3C-like protease processing activities. Virology 428, 136-145.
75. Zuckerkandl, E. & Pauling, L. (1965). Evolutionary divergence and convergence in proteins. In Evolving Genes and Proteins, pp. 97-166. Edited by V. Bryson & H. J. Vogel. New York: Academic Press.
76. Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31, 3406-3415.