The transcriptome of the baculovirus Autographa californica multiple nucleopolyhedrovirus in Trichoplusia ni cells

Journal of Virology

Volumn 87, Issue 11, 2013, Pages 6391-6405

  Chen, Yun Ru ^a   Zhong, Silin ^a   Fei, Zhangjun ^a   Hashimoto, Yoshifumi ^a,c   Xiang, Jenny Z ^b   Zhang, Shiying ^a   Blissard, Gary W ^a  

^a Boyce Thompson Institute for Plant Research   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c Protein Sciences Corp   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY RNA; MESSENGER RNA;

ANIMAL CELL; ARTICLE; AUTOGRAPHA CALIFORNICA MULTIPLE NUCLEOPOLYHEDROVIRUS; BACULOVIRUS; CONSENSUS SEQUENCE; CONTROLLED STUDY; DEEP SEQUENCING; GENE CLUSTER; GENE EXPRESSION REGULATION; GENE LOCATION; GENE MAPPING; GENETIC PROCEDURES; INSECT CELL; NOCTUIDAE; NONHUMAN; OPEN READING FRAME; POLYADENYLATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN MOTIF; RNA SEQUENCE; RNA SPLICING; TATA BOX; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; TRICHOPLUSIA NI; VIRUS CELL INTERACTION;

ANIMALS; GENE EXPRESSION REGULATION, VIRAL; MOTHS; NUCLEOPOLYHEDROVIRUS; OPEN READING FRAMES; REGULATORY SEQUENCES, NUCLEIC ACID; TRANSCRIPTION, GENETIC; TRANSCRIPTOME; VIRAL PROTEINS;

EID: 84878207473     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00194-13     Document Type: Article

References (98)

1. Herniou EA, Arif BM, Becnel JJ, Blissard GW, Bonning B, Harrison R, Jehle JA, Theilmann DA, Vlak JM. 2011. Baculoviridae, p 163-173. In King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (ed), Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, New York, NY.
2. Blissard GW, Rohrmann GF. 1990. Baculovirus diversity and molecular biology. Annu. Rev. Entomol. 35:127-155.
3. Hu Y. 2006. Baculovirus vectors for gene therapy. Adv. Virus Res. 68:287-320.
4. Hu YC. 2005. Baculovirus as a highly efficient expression vector in insect and mammalian cells. Acta Pharmacol. Sin. 26:405-416.
5. Kenoutis C, Efrose RC, Swevers L, Lavdas AA, Gaitanou M, Matsas R, Iatrou K. 2006. Baculovirus-mediated gene delivery into mammalian cells does not alter their transcriptional and differentiating potential but is accompanied by early viral gene expression. J. Virol. 80:4135-4146.
6. Kost TA, Condreay JP, Ames RS. 2010. Baculovirus gene delivery: a flexible assay development tool. Curr. Gene Ther. 10:168-173.
7. Kost TA, Condreay JP, Jarvis DL. 2005. Baculovirus as versatile vectors for protein expression in insect and mammalian cells Nat. Biotechnol. 23:567-575.
8. Miller LK (ed). 1997. The baculoviruses. Plenum Press, New York, NY.
9. Rohrmann GF. 2011. Baculovirus molecular biology, 2nd ed. National Library of Medicine, Bethesda, MD. http://www.ncbi.nlm.nih.gov /bookshelf/br.fcgi?book-bacvir.
10. Summers MD, Smith GE. 1987. A manual of methods for baculovirus vectors and insect cell culture procedures. Texas Agricultural Experiment Station Bulletin No. 1555.
11. Ayres MD, Howard SC, Kuzio J, Lopez-Ferber M, Possee RD. 1994. The complete DNA sequence of Autographa californica nuclear polyhedrosis virus. Virology 202:586-605.
12. Friesen PD. 2007. Insect viruses, p 707-736. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed, vol 1. Lippincott Williams & Wilkins, Philadelphia, PA.
13. Grula MA, Buller PL, Weaver RF. 1981. Alpha amanitin-resistant viral RNA synthesis in nuclei isolated from nuclear polyhedrosis virus-infected Heliothis zea larvae and Spodoptera frugiperda cells. J. Virol. 38:916-921.
14. Kogan PH, Chen X, Blissard GW. 1995. Overlapping TATA-dependent and TATA-independent early promoter activities in the baculovirus gp64 envelope fusion protein gene. J. Virol. 69:1452-1461.
15. Lu A, Carstens EB. 1993. Immediate-early baculovirus genes transactivate the p143 gene promoter of Autographa californica nuclear polyhedrosis virus. Virology 195:710-718.
16. Ohresser M, Morin N, Cerutti M, Delsert C. 1994. Temporal regulation of a complex and unconventional promoter by viral products. J. Virol. 68:2589-2597.
17. Tomalski MD, Wu JG, Miller LK. 1988. The location, sequence, transcription, and regulation of a baculovirus DNA polymerase gene. Virology 167:591-600.
18. Passarelli AL, Guarino LA. 2007. Baculovirus late and very late gene regulation. Curr. Drug Targets 8:1103-1115.
19. Rapp JC, Wilson JA, Miller LK. 1998. Nineteen baculovirus open reading frames, including LEF-12, support late gene expression. J. Virol. 72: 10197-10206.
20. Rohrmann GF. 2011. Baculovirus molecular biology, 2nd ed. http://www .ncbi.nlm.nih.gov/books/NBK49500/. NCBI, Bethesda, MD.
21. Kool M, Ahrens CH, Goldbach RW, Rohrmann GF, Vlak JM. 1994. Identification of genes involved in DNA replication of the Autographa californica baculovirus. Proc. Natl. Acad. Sci. U. S. A. 91:11212-11216.
22. Lu A, Miller LK. 1995. The roles of eighteen baculovirus late expression factor genes in transcription and DNA replication. J. Virol. 69:975-982.
23. Guarino LA, Xu B, Jin J, Dong W. 1998. A virus-encoded RNA polymerase purified from baculovirus-infected cells. J. Virol. 72:7985-7991.
24. Li L, Harwood SH, Rohrmann GF. 1999. Identification of additional genes that influence baculovirus late gene expression. Virology 255:9-19.
25. Lu A, Miller LK. 1997. Regulation of baculovirus late and very late gene expression, p 193-216. In Miller LK (ed), The baculoviruses. Plenum Press, New York, NY.
26. Passarelli AL, Miller LK. 1993. Identification and characterization of lef-1, a baculovirus gene involved in late and very late gene expression. J. Virol.,67,3481-3488.
27. Todd JW, Passarelli AL, Miller LK. 1995. Eighteen baculovirus genes, including lef-11, p35, 39K, and p47, support late gene expression. J. Virol. 69:968-974.
28. Garrity DB, Chang M-J, Blissard GW. 1997. Late promoter selection in the baculovirus gp64 envelope fusion protein gene. Virology 231:167-181.
29. Morris TD, Miller LK. 1994. Mutational analysis of a baculovirus major late promoter. Gene 140:147-153.
30. Rohrmann GF. 1986. Polyhedrin structure. J. Gen. Virol. 67:1499-1513.
31. Jiang SS, Chang IS, Huang LW, Chen PC, Wen CC, Liu SC, Chien LC, Lin CY, Hsiung CA, Juang JL. 2006. Temporal transcription program of recombinant Autographa californica multiple nucleopolyhedrosis virus. J. Virol. 80:8989-8999.
32. Smith I, Juang JL. 2007. Misleading messengers? Interpreting baculovirus transcriptional array profiles. J. Virol. 81:7819-7821.
33. Yamagishi J, Burnett ED, Harwood SH, Blissard GW. 2007. The AcMNPV pp31 gene is not essential for productive AcMNPV replication or late gene transcription but appears to increase levels of most viral transcripts. Virology 365:34-47.
34. Xue J, Qiao N, Zhang W, Cheng RL, Zhang XQ, Bao YY, Xu YP, Gu LZ, Han JD, Zhang CX. 2012. Dynamic interactions between Bombyx mori nucleopolyhedrovirus and its host cells revealed by transcriptome analysis. J. Virol. 86:7345-7359.
35. Hink WF. 1970. Established insect cell line from the cabbage looper, Trichoplusia ni. Nature 226:466-467.
36. Zhong S, Joung JG, Zheng Y, Chen YR, Liu B, Shao Y, Xiang JZ, Fei Z, Giovannoni JJ. 2011. High-throughput Illumina strand-specific RNA sequencing library preparation. Cold Spring Harb. Protoc. 2011:940-949.
37. Langmead B. 2010. Aligning short sequencing reads with Bowtie. Curr. Protoc. Bioinformatics 32:11.7.1-11.7.14. doi:10.1002/0471250953.bi1107s32.
38. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25. doi:10.1186/gb-2009-10-3-r25.
39. Ni T, Corcoran DL, Rach EA, Song S, Spana EP, Gao Y, Ohler U, Zhu J. 2010. A paired-end sequencing strategy to map the complex landscape of transcription initiation. Nat. Methods 7:521-527.
40. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. 2009. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37:W202-W208.
41. Bailey TL. 2002. Discovering novel sequence motifs with MEME. Curr. Protoc. Bioinformatics 2002:2.4.1-2.4.35. doi:10.1002/0471250953.bi0204s00
42. Bailey TL, Elkan C. 1994. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2:28-36.
43. Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105-1111.
44. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5:621-628.
45. de Hoon MJ, Imoto S, Nolan J, Miyano S. 2004. Open source clustering software. Bioinformatics 20:1453-1454.
46. Wu X, Stewart S, Theilmann DA. 1993. Alternative transcriptional initiation as a novel mechanism for regulating expression of a baculovirus trans activator. J. Virol. 67:5833-5842.
47. Juven-Gershon T, Hsu JY, Theisen JW, Kadonaga JT. 2008. The RNA polymerase II core promoter-the gateway to transcription. Curr. Opin. Cell Biol. 20:253-259.
48. Smale ST, Kadonaga JT. 2003. The RNA polymerase II core promoter. Annu. Rev. Biochem. 72:449-479.
49. Blissard GW, Kogan PH, Wei R, Rohrmann GF. 1992. A synthetic early promoter from a baculovirus: Roles of the TATA box and conserved start site CAGT sequence in basal levels of transcription. Virology 190:783-793.
50. Blissard GW, Rohrmann GF. 1991. Baculovirus gp64 gene expression: analysis of sequences modulating early transcription and transactivation by IE1. J. Virol. 65:5820-5827.
51. Pullen SS, Friesen PD. 1995. The CAGT motif functions as an initiator element during early transcription of the baculovirus transregulator ie-1. J. Virol. 69:3575-3583.
52. Blissard GW, Rohrmann GF. 1989. Location, sequence, transcriptional mapping, and temporal expression of the gp64 envelope glycoprotein gene of the Orgyia pseudotsugata multicapsid nuclear polyhedrosis virus. Virology 170:537-555.
53. Xing K, Deng R, Wang J, Feng J, Huang M, Wang X. 2005. Analysis and prediction of baculovirus promoter sequences. Virus Res. 113:64-71.
54. Fitzgerald PC, Sturgill D, Shyakhtenko A, Oliver B, Vinson C. 2006. Comparative genomics of Drosophila and human core promoters. Genome Biol. 7:R53. doi:10.1186/gb-2006-7-7-r53.
55. Ohler U, Liao GC, Niemann H, Rubin GM. 2002. Computational analysis of core promoters in the Drosophila genome. Genome Biol. 3:RESEARCH0087. doi:10.1186/gb-2002-3-12-research0087.
56. Rach EA, Yuan HY, Majoros WH, Tomancak P, Ohler U. 2009. Motif composition, conservation and condition-specificity of single and alternative transcription start sites in the Drosophila genome. Genome Biol. 10:R73. doi:10.1186/gb-2009-10-7-r73.
57. Rankin C, Ooi BG, Miller LK. 1988. Eight base pairs encompassing the transcriptional start point are the major determinant for baculovirus polyhedrin gene expression. Gene 70:39-49.
58. Mignone F, Gissi C, Liuni S, Pesole G. 2002. Untranslated regions of mRNAs. Genome Biol. 3:REVIEWS0004. doi:10.1186/gb-2002-3-3-reviews0004.
59. Pesole G, Fiormarino G, Saccone C. 1994. Sequence analysis and compositional properties of untranslated regions of human mRNAs. Gene 140:219-225.
60. Yang Z, Bruno DP, Martens CA, Porcella SF, Moss B. 2011. Genomewide analysis of the 5= and 3= ends of vaccinia virus early mRNAs delineates regulatory sequences of annotated and anomalous transcripts. J. Virol. 85:5897-5909.
61. Gombart AF, Blissard GW, Rohrmann GF. 1989. Characterization of the genetic organization of the Hind-III M region of the multicapsid nuclear polyhedrosis virus of Orgyia pseudotsugata reveals major differences among baculoviruses. J. Gen. Virol. 70:1815-1828.
62. Oellig C, Happ B, Mueller T, Doerfler W. 1987. Overlapping sets of viral RNA species reflect the array of polypeptides in the Eco-RI J. and N fragments, map positions 81.2 to 85.0 of the Autographa californica nuclear polyhedrosis virus genome. J. Virol. 61:3048-3057.
63. Becker D, Knebel MD. 1993. Sequence and temporal appearance of the early transcribed baculovirus gene he65. J. Virol. 67:5867-5872.
64. Braunagel SC, He H, Ramamurthy P, Summers MD. 1996. Transcription, translation, and cellular localization of three Autographa californica nuclear polyhedrosis virus structural proteins: ODV-E18, ODV-E35, and ODV-EC27. Virology 222:100-114.
65. Durantel D, Croizier L, Ayres MD, Croizier G, Possee RD, Lopez-Ferber M. 1998. The pnk/pnl gene (ORF 86) of Autographa californica nucleopolyhedrovirus is a non-essential, immediate early gene. J. Gen. Virol. 79:629-637.
66. Lu A, Carstens EB. 1992. Transcription analysis of the EcoRI D region of the baculovirus Autographa californica nuclear polyhedrosis virus identifies an early 4-kilobase RNA encoding the essential p143 gene. J. Virol. 66:655-663.
67. Possee RD, Sun TP, Howard SC, Ayres MD, Hill-Perkins M, Gearing KL. 1991. Nucleotide sequence of the Autographa californica nuclear polyhedrosis 9.4 Kbp EcoRI-I and R polyhedrin gene region. Virology 185: 229-241.
68. Tomalski MD, Eldridge R, Miller LK. 1991. A baculovirus homolog of a Cu/Zn superoxide dismutase gene. Virology 184:149-161.
69. Jin J, Guarino LA. 2000. 3'-end formation of baculovirus late RNAs. J. Virol. 74:8930-8937.
70. Danckwardt S, Hentze MW, Kulozik AE. 2008. 3 prime end mRNA processing: molecular mechanisms and implications for health and disease. EMBO J. 27:482-498.
71. Luebbert H, Doerfler W. 1984. Transcription of overlapping sets of RNAs from the genome of Autographa californica nuclear polyhedrosis virus: a novel method for mapping RNAs. J. Virol. 52:255-265.
72. Broussard DR, Guarino LA, Jarvis DL. 1996. Mapping functional domains in AcMNPV pp31. Virology 222:318-331.
73. Evans JT, Leisy DJ, Rohrmann GF. 1997. Characterization of the interaction between the baculovirus replication factor LEF-1 and LEF-2. J. Virol. 71:3114-3119.
74. Hang X, Dong W, Guarino LA. 1995. The lef-3 gene of Autographa californica Nuclear Polyhedrosis Virus encodes a single-stranded DNAbinding protein. J. Virol. 69:3924-3928.
75. Mikhailov VS, Mikhailova AL, Iwanaga M, Gomi S, Maeda S. 1998. Bombyx mori nucleopolyhedrovirus encodes a DNA-binding protein capable of destabilizing duplex DNA. J. Virol. 72:3107-3116.
76. Mikhailov VS, Rohrmann GF. 2002. Baculovirus replication factor LEF-1 is a DNA primase. J. Virol. 76:2287-2297.
77. Hill-Perkins MS, Possee RD. 1990. A baculovirus expression vector derived from the basic protein promoter of Autographa californica nuclear polyhedrosis virus. J. Gen. Virol. 71:971-976.
78. Cooper SJ, Trinklein ND, Anton ED, Nguyen L, Myers RM. 2006. Comprehensive analysis of transcriptional promoter structure and function in 1% of the human genome. Genome Res. 16:1-10.
79. Ooi BG, Miller LK. 1990. Transcription of the baculovirus polyhedrin gene reduces the levels of an antisense transcript initiated downstream. J. Virol. 64:3126-3129.
80. Chisholm GE, Henner DJ. 1988. Multiple early transcripts and splicing of the Autographa californica nuclear polyhedrosis virus IE-1 gene. J. Virol. 62:3193-3200.
81. Kovacs GR, Guarino LA, Graham BL, Summers MD. 1991. Identification of spliced baculovirus RNAs expressed late in infection. Virology 185:633-643.
82. Pearson MN, Rohrmann GF. 1997. Splicing is required for transactivation by the immediate early gene 1 of the Lymantria dispar multinucleocapsid nuclear polyhedrosis virus. Virology 235:153-165.
83. Theilmann DA, Stewart S. 1991. Identification and characterization of the IE-1 gene of Orgyia pseudotsugata multicapsid nuclear polyhedrosis virus. Virology 180:492-508.
84. Theilmann DA, Willis LG, Bosch BJ, Forsythe IJ, Li Q. 2001. The baculovirus transcriptional transactivator ie0 produces multiple products by internal initiation of translation. Virology 290:211-223.
85. Pearson MN, Russell RL, Rohrmann GF. 2002. Transcriptional mapping of two genes encoding baculovirus envelope-associated proteins. J. Gen. Virol. 83:937-943.
86. Burset M, Seledtsov IA, Solovyev VV. 2000. Analysis of canonical and non-canonical splice sites in mammalian genomes. Nucleic Acids Res. 28:4364-4375.
87. Hall SL, Padgett RA. 1994. Conserved sequences in a class of rare eukaryotic nuclear introns with non-consensus splice sites. J. Mol. Biol. 239:357-365.
88. Nie Y, Theilmann DA. 2010. Deletion of AcMNPV AC16 and AC17 results in delayed viral gene expression in budded virus infected cells but not transfected cells. Virology 404:168-179.
89. 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.
90. 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.
91. van Mierlo JT, van Cleef KW, van Rij RP. 2011. Defense and counterdefense in the RNAi-based antiviral immune system in insects. Methods Mol. Biol. 721:3-22.
92. Bronkhorst AW, van Cleef KWR, Vodovar N, Ince I A, Blanc H, Vlak JM, Saleh M-C, van Rij RP. 2012. The DNA virus Invertebrate iridescent virus 6 is a target of the Drosophila RNAi machinery. Proc. Natl. Acad. Sci. U. S. A. 109:E3604-E3613.
93. Jayachandran B, Hussain M, Asgari S. 2012. RNA interference as a cellular defense mechanism against the DNA virus baculovirus. J. Virol. 86:13729-13734.
94. Kemp C, Mueller S, Goto A, Barbier V, Paro S, Bonnay F, Dostert C, Troxler L, Hetru C, Meignin C, Pfeffer S, Hoffmann JA, Imler J-L. 2013. Broad RNA interference-mediated antiviral immunity and virus-specific inducible responses in Drosophila. J. Immunol. 190:650-658.
95. Betenbaugh MJ, Ailor E, Whiteley E, Hinderliter P, Hsu TA. 1996. Chaperone and foldase coexpression in the baculovirus-insect cell expression system. Cytotechnology 20:149-159.
96. Lawrence SM, Huddleston KA, Tomiya N, Nguyen N, Lee YC, Vann WF, Coleman TA, Betenbaugh MJ. 2001. Cloning and expression of human sialic acid pathway genes to generate CMP-sialic acids in insect cells. Glycoconj. J. 18:205-213.
97. McGill R, Tukey JW, Larsen WA. 1978. Variations of box plots. Am. Stat. 32:12-16.
98. Landais I, Pommet J, Mita K, Nohata J, Gimenez S, Fournier P, Devauchelle G, Duonor-Cerutti M, Ogliastro M. 2001. Characterization of the cDNA encoding the 90 kDa heat-shock protein in the Lepidoptera Bombyx mori and Spodoptera frugiperda. Gene 271:223-231.