Experimental Pathways towards Developing a Rotavirus Reverse Genetics System: Synthetic Full Length Rotavirus ssRNAs Are Neither Infectious nor Translated in Permissive Cells

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Richards, James E ^a   Desselberger, Ulrich ^a   Lever, Andrew M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; ENHANCED GREEN FLUORESCENT PROTEIN; MESSENGER RNA; NONSTRUCTURAL PROTEIN 2; NONSTRUCTURAL PROTEIN 5; SINGLE STRANDED RNA;

ARTICLE; COMPUTER MODEL; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; CYTOTOXICITY; FOWLPOX VIRUS; GENETIC TRANSFECTION; IN VITRO STUDY; MOLECULAR CLONING; NONHUMAN; PROTEIN SYNTHESIS; RABBIT; RETICULOCYTE; REVERSE GENETICS; RNA TRANSCRIPTION; RNA TRANSLATION; ROTAVIRUS; VIRUS GENOME; VIRUS RECOMBINANT; VIRUS STRAIN;

ANIMALS; BLOTTING, WESTERN; CATTLE; ELECTROPHORESIS, AGAR GEL; GENES, VIRAL; POLYMERASE CHAIN REACTION; PROTEIN BIOSYNTHESIS; RNA, VIRAL; ROTAVIRUS; TRANSFECTION;

EID: 84883435685     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074328     Document Type: Article

References (93)

1. Estes MK, Kapikian AZ (2007) Rotaviruses. In: Knipe DM, Howley PM, editors. Fields Virology. 5th ed: Lippincott Williams & Wilkins/Wolters Kluwer, Philadelphia. 1917-1974.
2. Tate JE, Burton AH, Boschi-Pinto C, Steele AD, Duque J, et al. (2012) 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. The Lancet Infectious Diseases 12: 136-141.
3. Vesikari T, Matson DO, Dennehy P, Van Damme P, Santosham M, et al. (2006) Safety and Efficacy of a Pentavalent Human-Bovine (WC3) Reassortant Rotavirus Vaccine. New England Journal of Medicine 354: 23-33.
4. Ruiz-Palacios GM, Perez-Schael I, Velazquez FR, Abate H, Breuer T, et al. (2006) Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. New England Journal of Medicine 354: 11-22.
5. SAGE (2009) Meeting of the immunization strategic advisory group of experts, April 2009- conclusions and recommendations. Weekly Epidemiological Record 84: 220-235.
6. Cortes JE, Curns AT, Tate JE, Cortese MM, Patel MM, et al. (2011) Rotavirus vaccine and health care utilization for diarrhea in U.S. children. New England Journal of Medicine 365: 1108-1117.
7. Macartney KK, Porwal M, Dalton D, Cripps T, Maldigri T, et al. (2011) Decline in rotavirus hospitalisations following introduction of Australia's national rotavirus immunisation programme. Journal of Paediatrics and Child Health 47: 266-270.
8. Zeller M, Patton JT, Heylen E, De Coster S, Ciarlet M, et al. (2011) Genetic analyses reveal differences in the VP7 and VP4 antigenic epitopes between human rotaviruses circulating in Belgium and rotaviruses in Rotarix and RotaTeq. Journal of Clinical Microbiology.
9. Armah GE, Breiman RF, Tapia MD, Dallas MJ, Neuzil KM, et al. (2012) Immunogenicity of the pentavalent rotavirus vaccine in African infants. Vaccine 30Supplement 1: A86-A93.
10. Lewis KDC, Dallas MJ, Victor JC, Ciarlet M, Mast TC, et al. (2012) Comparison of two clinical severity scoring systems in two multi-center, developing country rotavirus vaccine trials in Africa and Asia. Vaccine 30Supplement 1: A159-A166.
11. Madhi SA, Cunliffe NA, Steele D, Witte De, Kirsten M, et al. (2010) Effect of human rotavirus vaccine on severe diarrhea in african infants. New England Journal of Medicine 362: 289-298.
12. Zaman K, Anh DD, Victor JC, Shin S, Yunus M, et al. (2010) Efficacy of pentavalent rotavirus vaccine against severe rotavirus gastroenteritis in infants in developing countries in Asia: a randomised, double-blind, placebo-controlled trial. The Lancet 376: 615-623.
13. Matthijnssens J, Ciarlet M, McDonald S, Attoui H, Bányai K, et al. (2011) Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Archives of Virology 156: 1397-1413.
14. Matthijnssens J, Otto P, Ciarlet M, Desselberger U, Van Ranst M, et al. (2012) VP6-sequence-based cutoff values as a criterion for rotavirus species demarcation. Archives of Virology 157: 1177-1182.
15. Blackhall J, Fuentes A, Magnusson G, (1996) Genetic stability of a porcine rotavirus RNA segment during repeated plaque isolation. Virology 225: 181-190.
16. Matthijnssens J, Heylen E, Zeller M, Rahman M, Lemey P, et al. (2010) Phylodynamic Analyses of Rotavirus Genotypes G9 and G12 Underscore Their Potential for Swift Global Spread. Molecular Biology and Evolution 27: 2431-2436.
17. Desselberger U, Iturriza-Gómara M, Gray JJ, (2001) Rotavirus epidemiology and surveillance. Novartis Foundation Symposium 238: 125-147.
18. Kobayashi T, Antar AAR, Boehme KW, Danthi P, Eby EA, et al. (2007) A plasmid-based reverse genetics system for animal double-stranded RNA viruses. Cell Host and Microbe 1: 147-157.
19. Kobayashi T, Ooms LS, Ikizler M, Chappell JD, Dermody TS, (2010) An improved reverse genetics system for mammalian orthoreoviruses. Virology 398: 194-200.
20. Boyce M, Celma C, Roy P, (2008) Development of reverse genetics systems for Bluetongue virus: recovery of infectious virus from synthetic RNA transcripts. Journal of Virology 82: 8339-8348.
21. Matsuo E, Celma CCP, Roy P, (2010) A reverse genetics system of African horse sickness virus reveals existence of primary replication. FEBS Letters 584: 3386-3391.
22. Komoto S, Kugita M, Sasaki J, Taniguchi K, (2008) Generation of recombinant rotavirus with an antigenic mosaic of cross-reactive neutralization epitopes on VP4. Journal of Virology 82: 6753-6757.
23. Komoto S, Sasaki J, Taniguchi K, (2006) Reverse genetics system for introduction of site-specific mutations into the double-stranded RNA genome of infectious rotavirus. Proceedings of the National Academy of Sciences of the United States of America 103: 4646-4651.
24. Troupin C, Dehee A, Schnuriger A, Vende P, Poncet D, et al. (2010) Rearranged Genomic RNA Segments Offer a New Approach to the Reverse Genetics of Rotaviruses. Journal of Virology 84: 6711-6719.
25. Trask SD, Taraporewala ZF, Boehme KW, Dermody TS, Patton JT, (2010) Dual selection mechanisms drive efficient single-gene reverse genetics for rotavirus. Proceedings of the National Academy of Sciences of the United States of America 107: 18652-18657.
26. Navarro A, Trask SD, Patton JT (2013) Generation of Genetically Stable Recombinant Rotaviruses Containing Novel Genome Rearrangements and Heterologous Sequences by Reverse Genetics. Journal of Virology: In press.
27. Boyce M, Roy P, (2007) Recovery of infectious Bluetongue virus from RNA. Journal of Virology 81: 2179-2186.
28. Roner MR, Joklik WK, (2001) Reovirus reverse genetics: Incorporation of the CAT gene into the reovirus genome. Proceedings of the National Academy of Sciences of the United States of America 98: 8036-8041.
29. Yunus MA, Chung LMW, Chaudhry Y, Bailey D, Goodfellow I, (2010) Development of an optimized RNA-based murine norovirus reverse genetics system. Journal of Virological Methods 169: 112-118.
30. Maan S, Rao S, Maan NS, Anthony SJ, Attoui H, et al. (2007) Rapid cDNA synthesis and sequencing techniques for the genetic study of bluetongue and other dsRNA viruses. Journal of Virological Methods 143: 132-139.
31. Potgieter AC, Page NA, Liebenberg J, Wright IM, Landt O, et al. (2009) Improved strategies for sequence-independent amplification and sequencing of viral double-stranded RNA genomes. Journal of General Virology 90: 1423-1432.
32. Li W, Manktelow E, von Kirchbach JC, Gog JR, Desselberger U, et al. (2010) Genomic analysis of codon, sequence and structural conservation with selective biochemical-structure mapping reveals highly conserved and dynamic structures in rotavirus RNAs with potential cis-acting functions. Nucleic Acids Research 38: 7718-7735.
33. Kerby M, Sarma A, Patel M, Artenstein A, Opal S, et al. (2011) Early in vitro transcription termination in human H5 influenza viral RNA synthesis. Applied Biochemistry and Biotechnology 164: 497-513.
34. Cohen J, (1977) Ribonucleic acid polymerase activity associated with purified calf rotavirus. Journal of General Virology 36: 395-402.
35. Cohen J, Dobos P, (1979) Cell free transcription and translation of rotavirus RNA. Biochemical and Biophysical Research Communications 88: 791-796.
36. Cohen J, Laporte J, Charpilienne A, Scherrer R, (1979) Activation of rotavirus RNA polymerase by calcium chelation. Archives of Virology 60: 177-186.
37. Chizhikov V, Patton JT, (2000) A four-nucleotide translation enhancer in the 3′-terminal consensus sequence of the nonpolyadenylated mRNAs of rotavirus. RNA 6: 814-825.
38. Rubio RM, Mora SI, Romero P, Arias CF, Lopez S (2013) Rotavirus prevents the expression of host responses by blocking the nucleo-cytoplasmic transport of polyadenylated mRNAs. Journal of Virology: In press.
39. Smith ML, Lazdins I, Holmes IH, (1980) Coding assignments of double-stranded RNA segments of SA 11 rotavirus established by in vitro translation. Journal of Virology 33: 976-982.
40. Afrikanova I, Fabbretti E, Miozzo MC, Burrone OR, (1998) Rotavirus NSP5 phosphorylation is up-regulated by interaction with NSP2. Journal of General Virology 79: 2679-2686.
41. Piron M, Vende P, Cohen J, Poncet D, (1998) Rotavirus RNA-binding protein NSP3 interacts with eIF4GI and evicts the poly(A) binding protein from eIF4F. The EMBO Journal 17: 5811-5821.
42. Kantharidis P, Dyall-Smith ML, Holmes IH, (1983) Completion of the gene coding assignments of SA11 rotavirus: gene products of segments 7, 8, and 9. Journal of Virology 48: 330-334.
43. McCrae MA, McCorquodale JG, (1982) The molecular biology of rotaviruses II. Identification of the protein-coding assignments of calf rotavirus genome RNA species. Virology 117: 435-443.
44. Yang AD, Barro M, Gorziglia MI, Patton JT, (2004) Translation enhancer in the 3′-untranslated region of rotavirus gene 6 mRNA promotes expression of the major capsid protein VP6. Archives of Virology 149: 303-321.
45. Matsuo E, Roy P, (2009) Bluetongue virus VP6 acts early in the replication cycle and can form the basis of chimeric virus formation. Journal of Virology 83: 8842-8848.
46. Eichwald C, Rodriguez JF, Burrone OR, (2004) Characterization of rotavirus NSP2/NSP5 interactions and the dynamics of viroplasm formation. Journal of General Virology 85: 625-634.
47. Zhang X, Virtanen A, Kleiman FE, (2010) To polyadenylate or to deadenylate: That is the question. Cell Cycle 9: 4437-4449.
48. Chen D, Zeng CQ, Wentz MJ, Gorziglia M, Estes MK, et al. (1994) Template-dependent, in vitro replication of rotavirus RNA. Journal of Virology 68: 7030-7039.
49. Chen D, Patton JT, (1998) Rotavirus RNA replication requires a single-stranded 3′ end for efficient minus-strand synthesis. Journal of Virology 72: 7387-7396.
50. Chen D, Patton JT, (2000) De novo synthesis of minus strand RNA by the rotavirus RNA polymerase in a cell-free system involves a novel mechanism of initiation. RNA 6: 1455-1467.
51. Lu X, McDonald SM, Tortorici MA, Tao YJ, Vasquez-Del Carpio R, et al. (2008) Mechanism for coordinated RNA packaging and genome replication by rotavirus polymerase VP1. Structure 16: 1678-1688.
52. Emeny JM, Morgan MJ, (1979) Regulation of the interferon system: evidence that vero cells have a genetic defect in interferon production. Journal of General Virology 43: 247-252.
53. Mosca JD, Pitha PM, (1986) Transcriptional and posttranscriptional regulation of exogenous human beta interferon gene in simian cells defective in interferon synthesis. Molecular and Cellular Biology 6: 2279-2283.
54. Mattion NM, Cohen J, Estes M (1994) The rotavirus proteins. Viral infections of the Gastrointestinal Tract. New York: Marcel Dekker. 169-249.
55. Tortorici MA, Shapiro BA, Patton JT, (2006) A base-specific recognition signal in the 5′ consensus sequence of rotavirus plus-strand RNAs promotes replication of the double-stranded RNA genome segments. RNA 12: 133-146.
56. Graf S, Strothmann D, Kurtz S, Steger G, (2006) A computational approach to search for non-coding RNAs in large genomic data. Small RNAs: Analysis and Regulatory functions of Nucleic Acids and Molecular Biology Series 17: 57-74.
57. Britton P, Green P, Kottier S, Mawditt KL, Penzes Z, et al. (1996) Expression of bacteriophage T7 RNA polymerase in avian and mammalian cells by a recombinant fowlpox virus. Journal of General Virology 77: 963-967.
58. Somogyi P, Frazier J, Skinner MA, (1993) Fowlpox virus host range restriction: gene expression, DNA replication, and morphogenesis in nonpermissive mammalian cells. Virology 197: 439-444.
59. Das SC, Baron MD, Skinner MA, Barrett T, (2000) Improved technique for transient expression and negative strand virus rescue using fowlpox T7 recombinant virus in mammalian cells. Journal of Virological Methods 89: 119-127.
60. Bass DM, Baylor MR, Chen C, Mackow EM, Bremont M, et al. (1992) Liposome-mediated transfection of intact viral particles reveals that plasma membrane penetration determines permissivity of tissue culture cells to rotavirus. The Journal of Clinical Investigation 90: 2313-2320.
61. Cohen J, Lefevre F, Estes MK, Bremont M, (1984) Cloning of bovine rotavirus (RF strain): Nucleotide sequence of the gene coding for the major capsid protein. Virology 138: 178-182.
62. Bremont M, Charpilienne A, Chabanne D, Cohen J, (1987) Nucleotide sequence and expression in Escherichia coli of the gene encoding the nonstructural protein NCVP2 of bovine rotavirus. Virology 161: 138-144.
63. Cohen J, Charpilienne A, Chilmonczyk S, Estes MK, (1989) Nucleotide sequence of bovine rotavirus gene 1 and expression of the gene product in baculovirus. Virology 171: 131-140.
64. Kumar A, Charpilienne A, Cohen J, (1989) Nucleotide sequence of the gene encoding for the RNA binding protein (VP2) of RF bovine rotavirus. Nucleic Acids Research 17: 2126.
65. Aponte C, Mattion NM, Estes MK, Charpilienne A, Cohen J, (1993) Expression of two bovine rotavirus non-structural proteins (NSP2, NSP3) in the baculovirus system and production of monoclonal antibodies directed against the expressed proteins. Archives of Virology 133: 85-95.
66. Poncet D, Lindenbaum P, L'Haridon R, Cohen J, (1997) In vivo and in vitro phosphorylation of rotavirus NSP5 correlates with its localization in viroplasms. Journal of Virology 71: 34-41.
67. Matsuo E, Celma CCP, Boyce M, Viarouge C, Sailleau C, et al. (2011) Generation of replication-defective virus-based vaccines that confer full protection in sheep against virulent BTV challenge. Journal of Virology 85: 10213-10221.
68. Ratinier M, Caporale M, Golder M, Franzoni G, Allan K, et al. (2011) Identification and Characterization of a Novel Non-Structural Protein of Bluetongue Virus. PLoS Pathog 7: e1002477.
69. Celma CCP, Roy P, (2009) A Viral Nonstructural Protein Regulates Bluetongue Virus Trafficking and Release. J Virol 83: 6806-6816.
70. Silvestri LS, Taraporewala ZF, Patton JT, (2004) Rotavirus replication: plus-sense templates for double-stranded RNA synthesis are made in viroplasms. Journal of Virology 78: 7763-7774.
71. Rau M, Ohlmann T, Morley SJ, Pain VM, (1996) A Reevaluation of the Cap-binding Protein, eIF4E, as a Rate-limiting Factor for Initiation of Translation in Reticulocyte Lysate. Journal of Biological Chemistry 271: 8983-8990.
72. Koromilas A, Lazaris-Karatzas A, Sonenberg N, (1992) mRNAs containing extensive secondary structure in their 5′ non-coding region translate efficiently in cells overexpressing initiation factor eIF-4E. The EMBO Journal 11: 4153-4158.
73. Fabbretti E, Afrikanova I, Vascotto F, Burrone OR, (1999) Two non-structural rotavirus proteins, NSP2 and NSP5, form viroplasm-like structures in vivo. Journal of General Virology 80: 333-339.
74. Vende P, Piron M, Castagne N, Poncet D, (2000) Efficient translation of rotavirus mRNA requires simultaneous interaction of NSP3 with the eukaryotic translation initiation factor eIF4G and the mRNA 3′ end. Journal of Virology 74: 7064-7071.
75. Poncet D (2003) Translation of rotavirus mRNAs in the infected cell In: Desselberger U, Gray J, editors. Viral Gastroenteritis. Amsterdam, The Netherlands: Elsevier Science. 185-205.
76. Groft CM, Burley SK, (2002) Recognition of eIF4G by rotavirus NSP3 reveals a basis for mRNA circularization. Molecular Cell 9: 1273-1283.
77. Montero H, Arias CF, Lopez S, (2006) Rotavirus nonstructural protein NSP3 is not required for viral protein synthesis. Journal of Virology 80: 9031-9038.
78. Keryer-Bibens C, Legagneux V, Namanda-Vanderbeken A, Cosson B, Paillard L, et al. (2009) The rotaviral NSP3 protein stimulates translation of polyadenylated target mRNAs independently of its RNA-binding domain. Biochemical and Biophysical Research Communications 390: 302-306.
79. Padilla-Noriega L, Paniagua O, Guzmán-León S, (2002) Rotavirus Protein NSP3 Shuts Off Host Cell Protein Synthesis. Virology 298: 1-7.
80. Rojas M, Arias CF, Lopez S (2010) PKR is the kinase responsible for the phosphorylation of eIF2α in rotavirus infection. Journal of Virology: 10457-10466.
81. Young DF, Andrejeva L, Livingstone A, Goodbourn S, Lamb RA, et al. (2003) Virus replication in engineered human cells that do not respond to interferons. Journal of Virology 77: 2174-2181.
82. Lourenco S, Roy P, (2011) In vitro reconstitution of Bluetongue virus infectious cores. Proceedings of the National Academy of Sciences of the United States of America 108: 13746-13751.
83. McIntyre M, Rosenbaum V, Rappold W, Desselberger M, Wood D, et al. (1987) Biophysical characterization of rotavirus particles containing rearranged genomes. Journal of General Virology 68: 2961-2966.
84. Hundley F, Biryahwaho B, Gow M, Desselberger U, (1985) Genome rearrangements of bovine rotavirus after serial passage at high multiplicity of infection. Virology 143: 88-103.
85. Arnoldi F, Campagna M, Eichwald C, Desselberger U, Burrone OR, (2007) Interaction of rotavirus polymerase VP1 with nonstructural protein NSP5 is stronger than that with NSP2. Journal of Virology 81: 2128-2137.
86. Charpilienne A, Lepault J, Rey F, Cohen J, (2002) Identification of rotavirus VP6 residues located at the interface with VP2 that are essential for capsid assembly and transcriptase activity. Journal of Virology 76: 7822-7831.
87. Tortorici MA, Broering TJ, Nibert ML, Patton JT, (2003) Template recognition and formation of initiation complexes by the replicase of a segmented double-stranded RNA virus. Journal of Biological Chemistry 278: 32673-32682.
88. Flores J, Myslinski J, Kalica AR, Greenberg HB, Wyatt RG, et al. (1982) In vitro transcription of two human rotaviruses. Journal of Virology 43: 1032-1037.
89. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
90. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
91. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389-3402.
92. Waterhouse AM, Procter JB, Martin DMA, Clamp Ml, Barton GJ, (2009) Jalview Version 2 a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191.
93. Hofacker I, (2003) Vienna RNA secondary structure server. Nucleic Acids Res 31: 3429-3431.