Ecology, Evolution and Organismal Biology Publications Ecology, Evolution and Organismal Biology

2014 Lymantria dispar iflavirus 1 (LdIV1), a new model to study iflaviral persistence in lepidopterans Lymantria dispar iflavirus 1 (LdIV1), a new model to study iflaviral persistence in lepidopterans The cell line IPLB-LD-652Y, derived from the gypsy moth (Lymantria dispar L.), is routinely used to study interactions between viruses and insect hosts. Here we report the full genome sequence and biological characteristics of a small RNA virus, designated Lymantria dispar iflavirus 1 (LdIV1), that was discovered to persistently infect IPLB-LD-652Y. LdIV1 belongs to the genus Iflavirus. LdIV1 formed icosahedral particles of approx. 30 nm in diameter and contained a 10 044 nt polyadenylated, positive-sense RNA genome encoding a predicted polyprotein of 2980 aa. LdIV1 was induced by a viral suppressor of RNA silencing, suggesting that acute infection is restricted by RNA interference (RNAi). We detected LdIV1 in all tested tissues of gypsy-moth larvae and adults, but the virus was absent from other L. dispar-derived cell lines. We confirmed LdIV1 infectivity in two of these cell lines (IPLB-LD-652 and IPLB-LdFB). Our results provide a novel system to explore persistent infections in lepidopterans and a new model for the study of iflaviruses, a rapidly expanding group of viruses, many of which covertly infect their hosts.

[1]  A. Briscoe,et al.  Genome Sequence of a Novel Iflavirus from mRNA Sequencing of the Butterfly Heliconius erato , 2014, Genome Announcements.

[2]  S. Emrich,et al.  Genetic Characterization of a Novel Iflavirus Associated with Vomiting Disease in the Chinese Oak Silkmoth Antheraea pernyi , 2014, PloS one.

[3]  N. Nakashima,et al.  Complete genome sequences of two iflaviruses from the brown planthopper, Nilaparvata lugens , 2014, Archives of Virology.

[4]  R. L. Harrison,et al.  Complete Genome Sequence of a Novel Iflavirus from the Transcriptome of Halyomorpha halys, the Brown Marmorated Stink Bug , 2013, Genome Announcements.

[5]  L. Sundström,et al.  A Metatranscriptomic Approach to the Identification of Microbiota Associated with the Ant Formica exsecta , 2013, PloS one.

[6]  Tetsuya Kobayashi,et al.  The genome sequence and transmission of an iflavirus from the brown planthopper, Nilaparvata lugens. , 2013, Virus research.

[7]  Yingying Li,et al.  Virome Profiling of Bats from Myanmar by Metagenomic Analysis of Tissue Samples Reveals More Novel Mammalian Viruses , 2013, PloS one.

[8]  N. Vodovar,et al.  RNA-mediated interference and reverse transcription control the persistence of RNA viruses in the insect model Drosophila , 2013, Nature Immunology.

[9]  Narmada Thanki,et al.  CDD: conserved domains and protein three-dimensional structure , 2012, Nucleic Acids Res..

[10]  Yves-Jacques Schneider,et al.  Insect cells as factories for biomanufacturing. , 2012, Biotechnology advances.

[11]  M. Saleh,et al.  Living with the enemy: viral persistent infections from a friendly viewpoint. , 2012, Current opinion in microbiology.

[12]  E. Domingo,et al.  Viral Quasispecies Evolution , 2012, Microbiology and Molecular Reviews.

[13]  J. Roh,et al.  Complete genome sequence of a novel picorna-like virus isolated from Spodoptera exigua , 2012 .

[14]  Xi Zhou,et al.  Identification and characterization of Iflavirus 3C-like protease processing activities , 2012, Virology.

[15]  Michael E. Sparks,et al.  The Lymantria dispar IPLB-Ld652Y Cell Line Transcriptome Comprises Diverse Virus-Associated Transcripts , 2011, Viruses.

[16]  A. Schneemann,et al.  Molecular characterization of Drosophila cells persistently infected with Flock House virus. , 2011, Virology.

[17]  M. Nei,et al.  MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. , 2011, Molecular biology and evolution.

[18]  Narmada Thanki,et al.  CDD: a Conserved Domain Database for the functional annotation of proteins , 2010, Nucleic Acids Res..

[19]  Amos Bairoch,et al.  ViralZone: a knowledge resource to understand virus diversity , 2010, Nucleic Acids Res..

[20]  G. Budge,et al.  Genetic characterization of slow bee paralysis virus of the honeybee (Apis mellifera L.). , 2010, The Journal of general virology.

[21]  R. L. Harrison,et al.  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. , 2010, The Journal of general virology.

[22]  R. Andino,et al.  Cricket Paralysis Virus (CrPV) antagonizes Argonaute 2 to modulate antiviral defense in Drosophila , 2010, Nature Structural &Molecular Biology.

[23]  J. Kuhn,et al.  Clarification and guidance on the proper usage of virus and virus species names , 2010, Archives of Virology.

[24]  J. Werren,et al.  Data mining cDNAs reveals three new single stranded RNA viruses in Nasonia (Hymenoptera: Pteromalidae) , 2010, Insect molecular biology.

[25]  Liu Hu,et al.  Ectropis obliqua picorna-like virus IRES-driven internal initiation of translation in cell systems derived from different origins. , 2007, The Journal of general virology.

[26]  E. Ryabov A novel virus isolated from the aphid Brevicoryne brassicae with similarity to Hymenoptera picorna-like viruses. , 2007, The Journal of general virology.

[27]  P. Scotti,et al.  Latent Infection of a New Alphanodavirus in an Insect Cell Line , 2007, Journal of Virology.

[28]  C. Pleij,et al.  The 5' non-translated region of Varroa destructor virus 1 (genus Iflavirus): structure prediction and IRES activity in Lymantria dispar cells. , 2006, The Journal of general virology.

[29]  C. Cameron,et al.  Molecular and Biological Characterization of Deformed Wing Virus of Honeybees (Apis mellifera L.) , 2006, Journal of Virology.

[30]  D. E. Lynn Lepidopteran cell lines after long-term culture in alternative media: Comparison of growth rates and baculovirus replication , 2006, In Vitro Cellular & Developmental Biology - Animal.

[31]  R. Agarwala,et al.  Protein database searches using compositionally adjusted substitution matrices , 2005, The FEBS journal.

[32]  A. Mcintosh,et al.  AcMNPV in permissive, semipermissive, and nonpermissive cell lines from arthropoda , 2005, In Vitro Cellular & Developmental Biology - Animal.

[33]  S. Asgari,et al.  Presence of a novel small RNA-containing virus in a laboratory culture of the endoparasitic wasp Venturia canescens (Hymenoptera: Ichneumonidae). , 2005, Journal of insect physiology.

[34]  J. Vlak,et al.  Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor. , 2004, The Journal of general virology.

[35]  Jie Lu,et al.  Sequence analysis and genomic organization of a new insect picorna-like virus, Ectropis obliqua picorna-like virus, isolated from Ectropis obliqua. , 2004, The Journal of general virology.

[36]  Michael Zuker,et al.  Mfold web server for nucleic acid folding and hybridization prediction , 2003, Nucleic Acids Res..

[37]  Andrew M. Liebhold,et al.  “Slow The Spread”: A National Program to Contain the Gypsy Moth , 2002, Journal of Forestry.

[38]  C. Lo,et al.  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. , 2002, Virology.

[39]  D. E. Lynn Novel techniques to establish new insect cell lines , 2001, In Vitro Cellular & Developmental Biology - Animal.

[40]  T. Pfeifer,et al.  Identification and analysis of Lydia, a LTR retrotransposon from Lymantria dispar , 2000, Insect molecular biology.

[41]  M. Kozak Initiation of translation in prokaryotes and eukaryotes. , 1999, Gene.

[42]  B. Ball,et al.  The nucleotide sequence of sacbrood virus of the honey bee: an insect picorna-like virus. , 1999, The Journal of general virology.

[43]  A. James,et al.  Identification of a non‐LTR retrotransposon from the gypsy moth , 1999, Insect molecular biology.

[44]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[45]  M. Ryan,et al.  Virus-encoded proteinases of the picornavirus super-group. , 1997, The Journal of general virology.

[46]  S. Tsunekawa,et al.  Replication of a Small Isometric Virus in Cultured Lymantria dispar (Lepidoptera: Lymantriidae) Cells. , 1996 .

[47]  N. Blom,et al.  Cleavage site analysis in picornaviral polyproteins: Discovering cellular targets by neural networks , 1996, Protein science : a publication of the Protein Society.

[48]  D. Jarvis,et al.  Immediate-early baculovirus vectors for foreign gene expression in transformed or infected insect cells. , 1996, Protein expression and purification.

[49]  M. K. Kim,et al.  Ichnovirus infection of an established gypsy moth cell line. , 1996, The Journal of general virology.

[50]  D. Stoltz,et al.  Transformation of gypsy moth (Lymantria dispar) cell lines by infection with Glyptapanteles indiensis polydnavirus. , 1996, Biochemical and biophysical research communications.

[51]  R. Moyer,et al.  The effect of inhibitors on the growth of the entomopoxvirus from Amsacta moorei in Lymantria dispar (gypsy moth) cells. , 1995, Virology.

[52]  D. Cavener,et al.  Eukaryotic start and stop translation sites. , 1991, Nucleic acids research.

[53]  R. Weiner,et al.  Changes in macromolecular synthesis of gypsy moth cell line IPLB-Ld652Y induced by Autographa californica nuclear polyhedrosis virus infection. , 1991, The Journal of general virology.

[54]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[55]  R. Weiner,et al.  Semipermissive Replication of a Nuclear Polyhedrosis Virus of Autographa californica in a Gypsy Moth Cell Line , 1986, Journal of virology.

[56]  J. Felsenstein CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[57]  E. Wimmer,et al.  Systematic nomenclature of picornavirus proteins , 1984, Journal of virology.

[58]  G. J. Tompkins,et al.  Gypsy moth cell lines divergent in viral susceptibility , 1978, In Vitro.

[59]  G. J. Tompkins,et al.  The establishment of two cell lines from the insectspodoptera frugiperda (lepidoptera; noctuidae) , 1977, In Vitro.

[60]  T. Rivers Viruses and Koch's Postulates , 1937, Journal of bacteriology.

[61]  S. Herrero,et al.  Genome sequence of SeIV-1, a novel virus from the Iflaviridae family infective to Spodoptera exigua. , 2012, Journal of invertebrate pathology.

[62]  E. Genersch,et al.  Deformed wing virus. , 2010, Journal of invertebrate pathology.

[63]  P. Walter,et al.  Multifaceted physiological response allows yeast to adapt to the loss of the signal recognition particle-dependent protein-targeting pathway. , 2001, Molecular biology of the cell.

[64]  S. Abol-Ela,et al.  Evidence for two small viruses persistently infecting established cell lines of Phthorimaea operculella, deriving from embryos of the potato tuber moth. , 1998, The New Microbiologica.

[65]  H. Isawa,et al.  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 , 1998, Archives of Virology.

[66]  G. Fédière,et al.  A new small RNA virus persistently infecting an established cell line of Galleria mellonella, induced by a heterologous infection. , 1997, Journal of invertebrate pathology.

[67]  E. Koonin,et al.  Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. , 1993, Critical reviews in biochemistry and molecular biology.

[68]  M. Loeb,et al.  Development of Cell Lines from Various Tissues of Lepidoptera , 1988 .

[69]  M. Summers,et al.  A Manual of Methods for Baculovirus Vectors and Insect Cell Culture Procedures. , 1987 .

[70]  L. Pauling,et al.  Evolutionary Divergence and Convergence in Proteins , 1965 .