1887

Abstract

Many positive-stranded RNA viruses use subgenomic mRNAs to express part of their genetic information. To produce structural and accessory proteins, members of the order Nidovirales (corona-, toro-, arteri- and roniviruses) generate a 3′ co-terminal nested set of at least three and often seven to nine mRNAs. Coronavirus and arterivirus subgenomic transcripts are not only 3′ co-terminal but also contain a common 5′ leader sequence, which is derived from the genomic 5′ end. Their synthesis involves a process of discontinuous RNA synthesis that resembles similarity-assisted RNA recombination. Most models proposed over the past 25 years assume co-transcriptional fusion of subgenomic RNA leader and body sequences, but there has been controversy over the question of whether this occurs during plus- or minus-strand synthesis. In the latter model, which has now gained considerable support, subgenomic mRNA synthesis takes place from a complementary set of subgenome-size minus-strand RNAs, produced by discontinuous minus-strand synthesis. Sense–antisense base-pairing interactions between short conserved sequences play a key regulatory role in this process. In view of the presumed common ancestry of nidoviruses, the recent finding that ronivirus and torovirus mRNAs do not contain a common 5′ leader sequence is surprising. Apparently, major mechanistic differences must exist between nidoviruses, which raises questions about the functions of the common leader sequence and nidovirus transcriptase proteins and the evolution of nidovirus transcription. In this review, nidovirus transcription mechanisms are compared, the experimental systems used are critically assessed and, in particular, the impact of recently developed reverse genetic systems is discussed.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.81611-0
2006-06-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/87/6/1403.html?itemId=/content/journal/jgv/10.1099/vir.0.81611-0&mimeType=html&fmt=ahah

References

  1. Adkins S., Siegel R. W., Sun J. H., Kao C. C. 1997; Minimal templates directing accurate initiation of subgenomic RNA synthesis in vitro by the brome mosaic virus RNA-dependent RNA polymerase. RNA 3:634–647
    [Google Scholar]
  2. Almazan F., Gonzalez J. M., Penzes Z., Izeta A., Calvo E., Plana-Duran J., Enjuanes L. 2000; Engineering the largest RNA virus genome as an infectious bacterial artificial chromosome. Proc Natl Acad Sci U S A 97:5516–5521 [CrossRef]
    [Google Scholar]
  3. Almazan F., Galan C., Enjuanes L. 2004; The nucleoprotein is required for efficient coronavirus genome replication. J Virol 78:12683–12688 [CrossRef]
    [Google Scholar]
  4. Alonso S., Izeta A., Sola I., Enjuanes L. 2002; Transcription regulatory sequences and mRNA expression levels in the coronavirus transmissible gastroenteritis virus. J Virol 76:1293–1308 [CrossRef]
    [Google Scholar]
  5. An S., Makino S. 1998; Characterizations of coronavirus cis -acting RNA elements and the transcription step affecting its transcription efficiency. Virology 243:198–207 [CrossRef]
    [Google Scholar]
  6. Baker S. C., Lai M. M. C. 1990; An in vitro system for the leader-primed transcription of coronavirus mRNAs. EMBO J 9:4173–4179
    [Google Scholar]
  7. Baric R. S., Yount B. 2000; Subgenomic negative-strand RNA function during mouse hepatitis virus infection. J Virol 74:4039–4046 [CrossRef]
    [Google Scholar]
  8. Baric R. S., Stohlman S. A., Lai M. M. C. 1983; Characterization of replicative intermediate RNA of mouse hepatitis virus: presence of leader RNA sequences on nascent chains. J Virol 48:633–640
    [Google Scholar]
  9. Bhardwaj K., Guarino L., Kao C. C. 2004; The severe acute respiratory syndrome coronavirus Nsp15 protein is an endoribonuclease that prefers manganese as a cofactor. J Virol 78:12218–12224 [CrossRef]
    [Google Scholar]
  10. Brian D. A., Spaan W. J. M. 1997; Recombination and coronavirus defective interfering RNAs. Semin Virol 8:101–111 [CrossRef]
    [Google Scholar]
  11. Brockway S. M., Clay C. T., Lu X. T., Denison M. R. 2003; Characterization of the expression, intracellular localization, and replication complex association of the putative mouse hepatitis virus RNA-dependent RNA polymerase. J Virol 77:10515–10527 [CrossRef]
    [Google Scholar]
  12. Carpenter C. D., Oh J. W., Zhang C., Simon A. E. 1995; Involvement of a stem-loop structure in the location of junction sites in viral RNA recombination. J Mol Biol 245:608–622 [CrossRef]
    [Google Scholar]
  13. Casais R., Thiel V., Siddell S. G., Cavanagh D., Britton P. 2001; Reverse genetics system for the avian coronavirus infectious bronchitis virus. J Virol 75:12359–12369 [CrossRef]
    [Google Scholar]
  14. Cascone P. J., Carpenter C. D., Li X. H., Simon A. E. 1990; Recombination between satellite RNAs of turnip crinkle virus. EMBO J 9:1709–1715
    [Google Scholar]
  15. Cascone P. J., Haydar T. F., Simon A. E. 1993; Sequences and structures required for recombination between virus-associated RNAs. Science 260:801–805 [CrossRef]
    [Google Scholar]
  16. Cavanagh D. 1997; Nidovirales: a new order comprising Coronaviridae and Arteriviridae . Arch Virol 142:629–633
    [Google Scholar]
  17. Chang R. Y., Hofmann M. A., Sethna P. B., Brian D. A. 1994; A cis-acting function for the coronavirus leader in defective interfering RNA replication. J Virol 68:8223–8231
    [Google Scholar]
  18. Chang R. Y., Krishnan R., Brian D. A. 1996; The UCUAAAC promoter motif is not required for high-frequency leader recombination in bovine coronavirus defective interfering RNA. J Virol 70:2720–2729
    [Google Scholar]
  19. Choi I. R., White K. A. 2002; An RNA activator of subgenomic mRNA1 transcription in tomato bushy stunt virus. J Biol Chem 277:3760–3766 [CrossRef]
    [Google Scholar]
  20. Choi I. R., Ostrovsky M., Zhang G., White K. A. 2001; Regulatory activity of distal and core RNA elements in tombusvirus subgenomic mRNA2 transcription. J Biol Chem 276:41761–41768 [CrossRef]
    [Google Scholar]
  21. Coley S. E., Lavi E., Sawicki S. G., Fu L., Schelle B., Karl N., Siddell S. G., Thiel V. 2005; Recombinant mouse hepatitis virus strain A59 from cloned, full-length cDNA replicates to high titers in vitro and is fully pathogenic in vivo. J Virol 79:3097–3106 [CrossRef]
    [Google Scholar]
  22. Cowley J. A., Dimmock C. M., Spann K. M., Walker P. J. 2000; Gill-associated virus of Penaeus monodon prawns: an invertebrate virus with ORF1a and ORF1b genes related to arteri- and coronaviruses. J Gen Virol 81:1473–1484
    [Google Scholar]
  23. Cowley J. A., Dimmock C. M., Walker P. J. 2002; Gill-associated nidovirus of Penaeus monodon prawns transcribes 3′-coterminal subgenomic mRNAs that do not possess 5′-leader sequences. J Gen Virol 83:927–935
    [Google Scholar]
  24. Curtis K. M., Yount B., Baric R. S. 2002; Heterologous gene expression from transmissible gastroenteritis virus replicon particles. J Virol 76:1422–1434 [CrossRef]
    [Google Scholar]
  25. Curtis K. M., Yount B., Sims A. C., Baric R. S. 2004; Reverse genetic analysis of the transcription regulatory sequence of the coronavirus transmissible gastroenteritis virus. J Virol 78:6061–6066 [CrossRef]
    [Google Scholar]
  26. den Boon J. A., Snijder E. J., Chirnside E. D., de Vries A. A. F., Horzinek M. C., Spaan W. J. M. 1991; Equine arteritis virus is not a togavirus but belongs to the coronaviruslike superfamily. J Virol 65:2910–2920
    [Google Scholar]
  27. den Boon J. A., Spaan W. J. M., Snijder E. J. 1995; Equine arteritis virus subgenomic RNA transcription: UV inactivation and translation inhibition studies. Virology 213:364–372 [CrossRef]
    [Google Scholar]
  28. den Boon J. A., Kleijnen M. F., Spaan W. J. M., Snijder E. J. 1996; Equine arteritis virus subgenomic mRNA synthesis: analysis of leader-body junctions and replicative-form RNAs. J Virol 70:4291–4298
    [Google Scholar]
  29. de Vries A. A. F., Chirnside E. D., Bredenbeek P. J., Gravestein L. A., Horzinek M. C., Spaan W. J. M. 1990; All subgenomic mRNAs of equine arteritis virus contain a common leader sequence. Nucleic Acids Res 18:3241–3247 [CrossRef]
    [Google Scholar]
  30. de Vries A. A. F., Horzinek M. C., Rottier P. J. M., de Groot R. J. 1997; The genome organization of the Nidovirales : similarities and differences between arteri-, toro-, and coronaviruses. Semin Virol 8:33–47 [CrossRef]
    [Google Scholar]
  31. de Vries A. A. F., Glaser A. L., Raamsman M. J., Rottier P. J. M. 2001; Recombinant equine arteritis virus as an expression vector. Virology 284:259–276 [CrossRef]
    [Google Scholar]
  32. Drosten C., Gunther S., Preiser W. & 23 other authors 2003; Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N Engl J Med 348:1967–1976 [CrossRef]
    [Google Scholar]
  33. Egloff M. P., Ferron F., Campanacci V. & 7 other authors 2004; The severe acute respiratory syndrome-coronavirus replicative protein nsp9 is a single-stranded RNA-binding subunit unique in the RNA virus world. Proc Natl Acad Sci U S A 101:3792–3796 [CrossRef]
    [Google Scholar]
  34. Fischer F., Stegen C. F., Koetzner C. A., Masters P. S. 1997; Analysis of a recombinant mouse hepatitis virus expressing a foreign gene reveals a novel aspect of coronavirus transcription. J Virol 71:5148–5160
    [Google Scholar]
  35. Fouchier R. A., Hartwig N. G., Bestebroer T. M., Niemeyer B., de Jong J. C., Simon J. H., Osterhaus A. D. 2004; A previously undescribed coronavirus associated with respiratory disease in humans. Proc Natl Acad Sci U S A 101:6212–6216 [CrossRef]
    [Google Scholar]
  36. Fu K., Baric R. S. 1992; Evidence for variable rates of recombination in the MHV genome. Virology 189:88–102 [CrossRef]
    [Google Scholar]
  37. Fu K., Baric R. S. 1994; Map locations of mouse hepatitis virus temperature-sensitive mutants: confirmation of variable rates of recombination. J Virol 68:7458–7466
    [Google Scholar]
  38. Gonzalez J. M., Gomez-Puertas P., Cavanagh D., Gorbalenya A. E., Enjuanes L. 2003; A comparative sequence analysis to revise the current taxonomy of the family Coronaviridae . Arch Virol 148:2207–2235 [CrossRef]
    [Google Scholar]
  39. Gorbalenya A. E., Koonin E. V., Donchenko A. P., Blinov V. M. 1989; Coronavirus genome: prediction of putative functional domains in the non-structural polyprotein by comparative amino acid sequence analysis. Nucleic Acids Res 17:4847–4861 [CrossRef]
    [Google Scholar]
  40. Guarino L. A., Bhardwaj K., Dong W., Sun J., Holzenburg A., Kao C. C. 2005; Mutational analysis of the SARS virus nsp15 endoribonuclease: identification of residues affecting hexamer formation. J Mol Biol 353:1106–1117 [CrossRef]
    [Google Scholar]
  41. Guo J., Wu T., Anderson J., Kane B. F., Johnson D. G., Gorelick R. J., Henderson L. E., Levin J. G. 2000; Zinc finger structures in the human immunodeficiency virus type 1 nucleocapsid protein facilitate efficient minus- and plus-strand transfer. J Virol 74:8980–8988 [CrossRef]
    [Google Scholar]
  42. Haasnoot P. C., Brederode F. T., Olsthoorn R. C., Bol J. F. 2000; A conserved hairpin structure in Alfamovirus and Bromovirus subgenomic promoters is required for efficient RNA synthesis in vitro. RNA 6:708–716 [CrossRef]
    [Google Scholar]
  43. Hiscox J. A., Mawditt K. L., Cavanagh D., Britton P. 1995; Investigation of the control of coronavirus subgenomic mRNA transcription by using T7-generated negative-sense RNA transcripts. J Virol 69:6219–6227
    [Google Scholar]
  44. Hofmann M. A., Senanayake S. D., Brian D. A. 1993; A translation-attenuating intraleader open reading frame is selected on coronavirus mRNAs during persistent infection. Proc Natl Acad Sci U S A 90:11733–11737 [CrossRef]
    [Google Scholar]
  45. Hsue B., Masters P. S. 1999; Insertion of a new transcriptional unit into the genome of mouse hepatitis virus. J Virol 73:6128–6135
    [Google Scholar]
  46. Hussain S., Pan J., Chen Y. & 8 other authors 2005; Identification of novel subgenomic RNAs and noncanonical transcription initiation signals of severe acute respiratory syndrome coronavirus. J Virol 79:5288–5295 [CrossRef]
    [Google Scholar]
  47. Ivanov K. A., Hertzig T., Rozanov M., Bayer S., Thiel V., Gorbalenya A. E., Ziebuhr J. 2004; Major genetic marker of nidoviruses encodes a replicative endoribonuclease. Proc Natl Acad Sci U S A 101:12694–12699 [CrossRef]
    [Google Scholar]
  48. Jacobs L., Spaan W. J. M., Horzinek M. C., van der Zeijst B. A. 1981; Synthesis of subgenomic mRNA's of mouse hepatitis virus is initiated independently: evidence from UV transcription mapping. J Virol 39:401–406
    [Google Scholar]
  49. Jarvis T. C., Kirkegaard K. 1991; The polymerase in its labyrinth: mechanisms and implications of RNA recombination. Trends Genet 7:186–191 [CrossRef]
    [Google Scholar]
  50. Jeong Y. S., Makino S. 1994; Evidence for coronavirus discontinuous transcription. J Virol 68:2615–2623
    [Google Scholar]
  51. Jeong Y. S., Repass J. F., Kim Y. N., Hwang S. M., Makino S. 1996; Coronavirus transcription mediated by sequences flanking the transcription consensus sequence. Virology 217:311–322 [CrossRef]
    [Google Scholar]
  52. Joo M., Makino S. 1992; Mutagenic analysis of the coronavirus intergenic consensus sequence. J Virol 66:6330–6337
    [Google Scholar]
  53. Joo M., Makino S. 1995; The effect of two closely inserted transcription consensus sequences on coronavirus transcription. J Virol 69:272–280
    [Google Scholar]
  54. Keck J. G., Matsushima G. K., Makino S., Fleming J. O., Vannier D. M., Stohlman S. A., Lai M. M. C. 1988a; In vivo RNA-RNA recombination of coronavirus in mouse brain. J Virol 62:1810–1813
    [Google Scholar]
  55. Keck J. G., Soe L. H., Makino S., Stohlman S. A., Lai M. M. C. 1988b; RNA recombination of murine coronaviruses: recombination between fusion-positive mouse hepatitis virus A59 and fusion-negative mouse hepatitis virus 2. J Virol 62:1989–1998
    [Google Scholar]
  56. Kim K. H., Hemenway C. L. 1999; Long-distance RNA–RNA interactions and conserved sequence elements affect potato virus X plus-strand RNA accumulation. RNA 5:636–645 [CrossRef]
    [Google Scholar]
  57. Klovins J., Berzins V., van Duin J. 1998; A long-range interaction in Qbeta RNA that bridges the thousand nucleotides between the M-site and the 3′ end is required for replication. RNA 4:948–957 [CrossRef]
    [Google Scholar]
  58. Koev G., Mohan B. R., Miller W. A. 1999; Primary and secondary structural elements required for synthesis of barley yellow dwarf virus subgenomic RNA1. J Virol 73:2876–2885
    [Google Scholar]
  59. Komissarova N., Kashlev M. 1997a; RNA polymerase switches between inactivated and activated states by translocating back and forth along the DNA and the RNA. J Biol Chem 272:15329–15338 [CrossRef]
    [Google Scholar]
  60. Komissarova N., Kashlev M. 1997b; Transcriptional arrest: Escherichia coli RNA polymerase translocates backward, leaving the 3′ end of the RNA intact and extruded. Proc Natl Acad Sci U S A 94:1755–1760 [CrossRef]
    [Google Scholar]
  61. Konings D. A., Bredenbeek P. J., Noten J. F., Hogeweg P., Spaan W. J. M. 1988; Differential premature termination of transcription as a proposed mechanism for the regulation of coronavirus gene expression. Nucleic Acids Res 16:10849–10860 [CrossRef]
    [Google Scholar]
  62. Krishnan R., Chang R. Y., Brian D. A. 1996; Tandem placement of a coronavirus promoter results in enhanced mRNA synthesis from the downstream-most initiation site. Virology 218:400–405 [CrossRef]
    [Google Scholar]
  63. Ksiazek T. G., Erdman D., Goldsmith C. S. & 23 other authors 2003; A novel coronavirus associated with severe acute respiratory syndrome. N Engl J Med 348:1953–1966 [CrossRef]
    [Google Scholar]
  64. Lai M. M. C. 1998; Cellular factors in the transcription and replication of viral RNA genomes: a parallel to DNA-dependent RNA transcription. Virology 244:1–12 [CrossRef]
    [Google Scholar]
  65. Lai M. M. C., Cavanagh D. 1997; The molecular biology of coronaviruses. Adv Virus Res 48:1–100 [CrossRef]
    [Google Scholar]
  66. Lai M. M. C., Holmes K. V. 2001; Coronaviridae . In Fields Virology pp  1163–1185 Edited by Knipe D. M., Howley P. M. Philadelphia, PA: Lippincott, Williams & Wilkins;
    [Google Scholar]
  67. Lai M. M. C., Patton C. D., Stohlman S. A. 1982a; Further characterization of mRNAs of mouse hepatitis virus: presence of common 5′-end nucleotides. J Virol 41:557–565
    [Google Scholar]
  68. Lai M. M. C., Patton C. D., Stohlman S. A. 1982b; Replication of mouse hepatitis virus: negative-stranded RNA and replicative form RNA are of genome length. J Virol 44:487–492
    [Google Scholar]
  69. Lai M. M. C., Patton C. D., Baric R. S., Stohlman S. A. 1983; Presence of leader sequences in the mRNA of mouse hepatitis virus. J Virol 46:1027–1033
    [Google Scholar]
  70. Lai M. M. C., Baric R. S., Brayton P. R., Stohlman S. A. 1984; Characterization of leader RNA sequences on the virion and mRNAs of mouse hepatitis virus, a cytoplasmic RNA virus. Proc Natl Acad Sci U S A 81:3626–3630 [CrossRef]
    [Google Scholar]
  71. Lai M. M. C., Baric R. S., Makino S., Keck J. G., Egbert J., Leibowitz J. L., Stohlman S. A. 1985; Recombination between nonsegmented RNA genomes of murine coronaviruses. J Virol 56:449–456
    [Google Scholar]
  72. Liao C. L., Lai M. M. C. 1992; RNA recombination in a coronavirus: recombination between viral genomic RNA and transfected RNA fragments. J Virol 66:6117–6124
    [Google Scholar]
  73. Lin H. X., White K. A. 2004; A complex network of RNA–RNA interactions controls subgenomic mRNA transcription in a tombusvirus. EMBO J 23:3365–3374 [CrossRef]
    [Google Scholar]
  74. Lin Y. J., Liao C. L., Lai M. M. C. 1994; Identification of the cis -acting signal for minus-strand RNA synthesis of a murine coronavirus: implications for the role of minus-strand RNA in RNA replication and transcription. J Virol 68:8131–8140
    [Google Scholar]
  75. Lin Y. J., Zhang X., Wu R. C., Lai M. M. C. 1996; The 3′ untranslated region of coronavirus RNA is required for subgenomic mRNA transcription from a defective interfering RNA. J Virol 70:7236–7240
    [Google Scholar]
  76. Lindenbach B. D., Sgro J. Y., Ahlquist P. 2002; Long-distance base pairing in flock house virus RNA1 regulates subgenomic RNA3 synthesis and RNA2 replication. J Virol 76:3905–3919 [CrossRef]
    [Google Scholar]
  77. Makino S., Stohlman S. A., Lai M. M. C. 1986; Leader sequences of murine coronavirus mRNAs can be freely reassorted: evidence for the role of free leader RNA in transcription. Proc Natl Acad Sci U S A 83:4204–4208 [CrossRef]
    [Google Scholar]
  78. Makino S., Soe L. H., Shieh C. K., Lai M. M. C. 1988; Discontinuous transcription generates heterogeneity at the leader fusion sites of coronavirus mRNAs. J Virol 62:3870–3873
    [Google Scholar]
  79. Makino S., Joo M., Makino J. K. 1991; A system for study of coronavirus mRNA synthesis: a regulated, expressed subgenomic defective interfering RNA results from intergenic site insertion. J Virol 65:6031–6041
    [Google Scholar]
  80. Masters P. S., Koetzner C. A., Kerr C. A., Heo Y. 1994; Optimization of targeted RNA recombination and mapping of a novel nucleocapsid gene mutation in the coronavirus mouse hepatitis virus. J Virol 68:328–337
    [Google Scholar]
  81. Meulenberg J. J. M., Bos-de Ruijter J. N. A., van de Graaf R., Wensvoort G., Moormann R. J. M. 1998; Infectious transcripts from cloned genome-length cDNA of porcine reproductive respiratory syndrome virus. J Virol 72:380–387
    [Google Scholar]
  82. Miller W. A., Koev G. 2000; Synthesis of subgenomic RNAs by positive-strand RNA viruses. Virology 273:1–8 [CrossRef]
    [Google Scholar]
  83. Miller W. A., Dreher T. W., Hall T. C. 1985; Synthesis of brome mosaic virus subgenomic RNA in vitro by internal initiation on (-)-sense genomic RNA. Nature 313:68–70 [CrossRef]
    [Google Scholar]
  84. Molenkamp R., Greve S., Spaan W. J. M., Snijder E. J. 2000a; Efficient homologous RNA recombination and requirement for an open reading frame during replication of equine arteritis virus defective interfering RNAs. J Virol 74:9062–9070 [CrossRef]
    [Google Scholar]
  85. Molenkamp R., van Tol H., Rozier B. C., van der Meer Y., Spaan W. J. M., Snijder E. J. 2000b; The arterivirus replicase is the only viral protein required for genome replication and subgenomic mRNA transcription. J Gen Virol 81:2491–2496
    [Google Scholar]
  86. Nagy P. D., Bujarski J. J. 1993; Targeting the site of RNA–RNA recombination in brome mosaic virus with antisense sequences. Proc Natl Acad Sci U S A 90:6390–6394 [CrossRef]
    [Google Scholar]
  87. Nagy P. D., Bujarski J. J. 1995; Efficient system of homologous RNA recombination in brome mosaic virus: sequence and structure requirements and accuracy of crossovers. J Virol 69:131–140
    [Google Scholar]
  88. Nagy P. D., Bujarski J. J. 1996; Homologous RNA recombination in brome mosaic virus: AU-rich sequences decrease the accuracy of crossovers. J Virol 70:415–426
    [Google Scholar]
  89. Nagy P. D., Simon A. E. 1997; New insights into the mechanisms of RNA recombination. Virology 235:1–9 [CrossRef]
    [Google Scholar]
  90. Nagy P. D., Simon A. E. 1998a; In vitro characterization of late steps of RNA recombination in turnip crinkle virus. I. Role of motif1-hairpin structure. Virology 249:379–392 [CrossRef]
    [Google Scholar]
  91. Nagy P. D., Simon A. E. 1998b; In vitro characterization of late steps of RNA recombination in turnip crinkle virus. II. The role of the priming stem and flanking sequences. Virology 249:393–405 [CrossRef]
    [Google Scholar]
  92. Nagy P. D., Dzianott A., Ahlquist P., Bujarski J. J. 1995; Mutations in the helicase-like domain of protein 1a alter the sites of RNA-RNA recombination in brome mosaic virus. J Virol 69:2547–2556
    [Google Scholar]
  93. Nagy P. D., Zhang C., Simon A. E. 1998; Dissecting RNA recombination in vitro: role of RNA sequences and the viral replicase. EMBO J 17:2392–2403 [CrossRef]
    [Google Scholar]
  94. Nagy P. D., Pogany J., Simon A. E. 1999; RNA elements required for RNA recombination function as replication enhancers in vitro and in vivo in a plus-strand RNA virus. EMBO J 18:5653–5665 [CrossRef]
    [Google Scholar]
  95. Nelson G. W., Stohlman S. A., Tahara S. M. 2000; High affinity interaction between nucleocapsid protein and leader/intergenic sequence of mouse hepatitis virus RNA. J Gen Virol 81:181–188
    [Google Scholar]
  96. Nudler E., Avetissova E., Markovtsov V., Goldfarb A. 1996; Transcription processivity: protein-DNA interactions holding together the elongation complex. Science 273:211–217 [CrossRef]
    [Google Scholar]
  97. Nudler E., Mustaev A., Lukhtanov E., Goldfarb A. 1997; The RNA-DNA hybrid maintains the register of transcription by preventing backtracking of RNA polymerase. Cell 89:33–41 [CrossRef]
    [Google Scholar]
  98. Ozdarendeli A., Ku S., Rochat S., Williams G. D., Senanayake S. D., Brian D. A. 2001; Downstream sequences influence the choice between a naturally occurring noncanonical and closely positioned upstream canonical heptameric fusion motif during bovine coronavirus subgenomic mRNA synthesis. J Virol 75:7362–7374 [CrossRef]
    [Google Scholar]
  99. Pasternak A. O. 2003; Nidovirus transcription-regulating sequences . PhD thesis Leiden University;
  100. Pasternak A. O., Gultyaev A. P., Spaan W. J. M., Snijder E. J. 2000; Genetic manipulation of arterivirus alternative mRNA leader-body junction sites reveals tight regulation of structural protein expression. J Virol 74:11642–11653 [CrossRef]
    [Google Scholar]
  101. Pasternak A. O., van den Born E., Spaan W. J. M., Snijder E. J. 2001; Sequence requirements for RNA strand transfer during nidovirus discontinuous subgenomic RNA synthesis. EMBO J 20:7220–7228 [CrossRef]
    [Google Scholar]
  102. Pasternak A. O., van den Born E., Spaan W. J. M., Snijder E. J. 2003; The stability of the duplex between sense and antisense transcription-regulating sequences is a crucial factor in arterivirus subgenomic mRNA synthesis. J Virol 77:1175–1183 [CrossRef]
    [Google Scholar]
  103. Pasternak A. O., Spaan W. J. M., Snijder E. J. 2004; Regulation of relative abundance of arterivirus subgenomic mRNAs. J Virol 78:8102–8113 [CrossRef]
    [Google Scholar]
  104. Peiris J. S., Lai S. T., Poon L. L. 13 other authors 2003; Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361:1319–1325 [CrossRef]
    [Google Scholar]
  105. Peliska J. A., Benkovic S. J. 1992; Mechanism of DNA strand transfer reactions catalyzed by HIV-1 reverse transcriptase. Science 258:1112–1118 [CrossRef]
    [Google Scholar]
  106. Peliska J. A., Benkovic S. J. 1994; Fidelity of in vitro DNA strand transfer reactions catalyzed by HIV-1 reverse transcriptase. Biochemistry 33:3890–3895 [CrossRef]
    [Google Scholar]
  107. Posthuma C. C., Nedialkova D. D., Zevenhoven-Dobbe J. C., Blokhuis J. H., Gorbalenya A. E., Snijder E. J. 2006; Site-directed mutagenesis of the nidovirus replicative endoribonuclease NendoU exerts pleiotropic effects on the arterivirus life cycle. J Virol 80:1653–1661 [CrossRef]
    [Google Scholar]
  108. Reeder R. H., Lang W. H. 1997; Terminating transcription in eukaryotes: lessons learned from RNA polymerase I. Trends Biochem Sci 22:473–477 [CrossRef]
    [Google Scholar]
  109. Satyanarayana T., Gowda S., Ayllon M. A., Albiach-Marti M. R., Rabindran S., Dawson W. O. 2002; The p23 protein of Citrus tristeza virus controls asymmetrical RNA accumulation. J Virol 76:473–483 [CrossRef]
    [Google Scholar]
  110. Sawicki S. G., Sawicki D. L. 1990; Coronavirus transcription: subgenomic mouse hepatitis virus replicative intermediates function in RNA synthesis. J Virol 64:1050–1056
    [Google Scholar]
  111. Sawicki S. G., Sawicki D. L. 1995; Coronaviruses use discontinuous extension for synthesis of subgenome-length negative strands. Adv Exp Med Biol 380:499–506
    [Google Scholar]
  112. Sawicki S. G., Sawicki D. L. 2005; Coronavirus transcription: a perspective. Curr Top Microbiol Immunol 287:31–55
    [Google Scholar]
  113. Sawicki D. L., Wang T., Sawicki S. G. 2001; The RNA structures engaged in replication and transcription of the A59 strain of mouse hepatitis virus. J Gen Virol 82:385–396
    [Google Scholar]
  114. Sawicki S. G., Sawicki D. L., Younker D., Meyer Y., Thiel V., Stokes H., Siddell S. G. 2005; Functional and genetic analysis of coronavirus replicase-transcriptase proteins. PLoS Pathog 4:310–322
    [Google Scholar]
  115. Schaad M. C., Stohlman S. A., Egbert J., Lum K., Fu K., Wei T. Jr, Baric R. S. 1990; Genetics of mouse hepatitis virus transcription: identification of cistrons which may function in positive and negative strand RNA synthesis. Virology 177:634–645 [CrossRef]
    [Google Scholar]
  116. Schelle B., Karl N., Ludewig B., Siddell S. G., Thiel V. 2005; Selective replication of coronavirus genomes that express nucleocapsid protein. J Virol 79:6620–6630 [CrossRef]
    [Google Scholar]
  117. Sengupta D. J., Wickens M., Fields S. 1999; Identification of RNAs that bind to a specific protein using the yeast three-hybrid system. RNA 5:596–601 [CrossRef]
    [Google Scholar]
  118. Sethna P. B., Hung S. L., Brian D. A. 1989; Coronavirus subgenomic minus-strand RNAs and the potential for mRNA replicons. Proc Natl Acad Sci U S A 86:5626–5630 [CrossRef]
    [Google Scholar]
  119. Seybert A., van Dinten L. C., Snijder E. J., Ziebuhr J. 2000; Biochemical characterization of the equine arteritis virus helicase suggests a close functional relationship between arterivirus and coronavirus helicases. J Virol 74:9586–9593 [CrossRef]
    [Google Scholar]
  120. Seybert A., Posthuma C. C., van Dinten L. C., Snijder E. J., Gorbalenya A. E., Ziebuhr J. 2005; A complex zinc finger controls the enzymatic activities of nidovirus helicases. J Virol 79:696–704 [CrossRef]
    [Google Scholar]
  121. Siddell S. G., Ziebuhr J., Snijder E. J. 2005; In Topley and Wilson's Microbiology and Microbial Infections . Virology Volume, 10th edn. pp  823–856 Edited by Mahy B. W., ter Meulen V. London: Hodder Arnold;
    [Google Scholar]
  122. Siegel R. W., Adkins S., Kao C. C. 1997; Sequence-specific recognition of a subgenomic RNA promoter by a viral RNA polymerase. Proc Natl Acad Sci U S A 94:11238–11243 [CrossRef]
    [Google Scholar]
  123. Siegel R. W., Bellon L., Beigelman L., Kao C. C. 1998; Moieties in an RNA promoter specifically recognized by a viral RNA-dependent RNA polymerase. Proc Natl Acad Sci U S A 95:11613–11618 [CrossRef]
    [Google Scholar]
  124. Siegel R. W., Bellon L., Beigelman L., Kao C. C. 1999; Use of DNA, RNA, and chimeric templates by a viral RNA-dependent RNA polymerase: evolutionary implications for the transition from the RNA to the DNA world. J Virol 73:6424–6429
    [Google Scholar]
  125. Sit T. L., Vaewhongs A. A., Lommel S. A. 1998; RNA-mediated trans-activation of transcription from a viral RNA. Science 281:829–832 [CrossRef]
    [Google Scholar]
  126. Sivakumaran K., Kao C. C. 1999; Initiation of genomic plus-strand RNA synthesis from DNA and RNA templates by a viral RNA-dependent RNA polymerase. J Virol 73:6415–6423
    [Google Scholar]
  127. Smits S. L., van Vliet A. L., Segeren K., el Azzouzi H., van Essen M., de Groot R. J. 2005; Torovirus non-discontinuous transcription: mutational analysis of a subgenomic mRNA promoter. J Virol 79:8275–8281 [CrossRef]
    [Google Scholar]
  128. Snijder E. J., Horzinek M. C. 1993; Toroviruses: replication, evolution and comparison with other members of the coronavirus-like superfamily. J Gen Virol 74:2305–2316 [CrossRef]
    [Google Scholar]
  129. Snijder E. J., Meulenberg J. J. M. 1998; The molecular biology of arteriviruses. J Gen Virol 79:961–979
    [Google Scholar]
  130. Snijder E. J., den Boon J. A., Bredenbeek P. J., Horzinek M. C., Rijnbrand R., Spaan W. J. M. 1990a; The carboxyl-terminal part of the putative Berne virus polymerase is expressed by ribosomal frameshifting and contains sequence motifs which indicate that toro- and coronaviruses are evolutionarily related. Nucleic Acids Res 18:4535–4542 [CrossRef]
    [Google Scholar]
  131. Snijder E. J., Horzinek M. C., Spaan W. J. M. 1990b; A 3′-coterminal nested set of independently transcribed mRNAs is generated during Berne virus replication. J Virol 64:331–338
    [Google Scholar]
  132. Snijder E. J., Bredenbeek P. J., Dobbe J. C. & 7 other authors 2003; Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage. J Mol Biol 331:991–1004 [CrossRef]
    [Google Scholar]
  133. Snijder E. J., Siddell S. G., Gorbalenya A. E. 2005; The order Nidovirales. In Topley and Wilson's Microbiology and Microbial Infections Virology Volume pp  390–404 Edited by Mahy B. W, ter Meulen V. London: Hodder Arnold;
    [Google Scholar]
  134. Sola I., Alonso S., Zuniga S., Balasch M., Plana-Duran J., Enjuanes L. 2003; Engineering the transmissible gastroenteritis virus genome as an expression vector inducing lactogenic immunity. J Virol 77:4357–4369 [CrossRef]
    [Google Scholar]
  135. Sola I., Moreno J. L., Zuniga S., Alonso S., Enjuanes L. 2005; Role of nucleotides immediately flanking the transcription-regulating sequence core in coronavirus subgenomic mRNA synthesis. J Virol 79:2506–2516 [CrossRef]
    [Google Scholar]
  136. Spaan W. J. M., Rottier P. J. M., Horzinek M. C., van der Zeijst B. A. M. 1982; Sequence relationships between the genome and the intracellular RNA species 1, 3, 6, and 7 of mouse hepatitis virus strain A59. J Virol 42:432–439
    [Google Scholar]
  137. Spaan W. J. M., Delius H., Skinner M., Armstrong J., Rottier P. J. M., Smeekens S., van der Zeijst B. A. M., Siddell S. G. 1983; Coronavirus mRNA synthesis involves fusion of non-contiguous sequences. EMBO J 2:1839–1844
    [Google Scholar]
  138. Stawicki S. S., Kao C. C. 1999; Spatial perturbations within an RNA promoter specifically recognized by a viral RNA-dependent RNA polymerase (RdRp) reveal that RdRp can adjust its promoter binding sites. J Virol 73:198–204
    [Google Scholar]
  139. Stern D. F., Sefton B. M. 1982; Synthesis of coronavirus mRNAs: kinetics of inactivation of infectious bronchitis virus RNA synthesis by UV light. J Virol 42:755–759
    [Google Scholar]
  140. Stirrups K., Shaw K., Evans S., Dalton K., Cavanagh D., Britton P. 2000; Leader switching occurs during the rescue of defective RNAs by heterologous strains of the coronavirus infectious bronchitis virus. J Gen Virol 81:791–801
    [Google Scholar]
  141. Sturman L. S., Eastwood C., Frana M. F., Duchala C., Baker F., Ricard C. S., Sawicki S. G., Holmes K. V. 1987; Temperature-sensitive mutants of MHV-A59. Adv Exp Med Biol 218:159–168
    [Google Scholar]
  142. Sutton G., Fry E., Carter L. & 14 other authors 2004; The nsp9 replicase protein of SARS-coronavirus, structure and functional insights. Structure 12:341–353 [CrossRef]
    [Google Scholar]
  143. Tahara S. M., Dietlin T. A., Bergmann C. C., Nelson G. W., Kyuwa S., Anthony R. P., Stohlman S. A. 1994; Coronavirus translational regulation: leader affects mRNA efficiency. Virology 202:621–630 [CrossRef]
    [Google Scholar]
  144. Thiel V., Herold J., Schelle B., Siddell S. G. 2001; Infectious RNA transcribed in vitro from a cDNA copy of the human coronavirus genome cloned in vaccinia virus. J Gen Virol 82:1273–1281
    [Google Scholar]
  145. Tijms M. A. 2004; Nsp1, a multifunctional regulator of the arterivirus life cycle . PhD thesis Leiden University;
  146. Tijms M. A., van Dinten L. C., Gorbalenya A. E., Snijder E. J. 2001; A zinc finger-containing papain-like protease couples subgenomic mRNA synthesis to genome translation in a positive-stranded RNA virus. Proc Natl Acad Sci U S A 98:1889–1894 [CrossRef]
    [Google Scholar]
  147. van den Born E., Gultyaev A. P., Snijder E. J. 2004; Secondary structure and function of the 5′-proximal region of the equine arteritis virus RNA genome. RNA 10:424–437 [CrossRef]
    [Google Scholar]
  148. van den Born E., Posthuma C. C., Gultyaev A. P., Snijder E. J. 2005; Discontinuous subgenomic RNA synthesis in arteriviruses is guided by an RNA hairpin structure located in the genomic leader region. J Virol 79:6312–6324 [CrossRef]
    [Google Scholar]
  149. van der Hoek L., Pyrc K., Jebbink M. F. & 7 other authors 2004; Identification of a new human coronavirus. Nat Med 10:368–373 [CrossRef]
    [Google Scholar]
  150. van der Most R. G., Spaan W. J. M. 1995; Coronavirus replication, transcription and RNA recombination. In The Coronaviridae pp  11–31 Edited by Siddell S. G. Plenum;
    [Google Scholar]
  151. van der Most R. G., de Groot R. J., Spaan W. J. M. 1994; Subgenomic RNA synthesis directed by a synthetic defective interfering RNA of mouse hepatitis virus: a study of coronavirus transcription initiation. J Virol 68:3656–3666
    [Google Scholar]
  152. van Dinten L. C., den Boon J. A., Wassenaar A. L., Spaan W. J. M., Snijder E. J. 1997; An infectious arterivirus cDNA clone: identification of a replicase point mutation that abolishes discontinuous mRNA transcription. Proc Natl Acad Sci U S A 94:991–996 [CrossRef]
    [Google Scholar]
  153. van Dinten L. C., van Tol H., Gorbalenya A. E., Snijder E. J. 2000; The predicted metal-binding region of the arterivirus helicase protein is involved in subgenomic mRNA synthesis, genome replication, and virion biogenesis. J Virol 74:5213–5223 [CrossRef]
    [Google Scholar]
  154. van Marle G., Luytjes W., van der Most R. G., van der Straaten T., Spaan W. J. M. 1995; Regulation of coronavirus mRNA transcription. J Virol 69:7851–7856
    [Google Scholar]
  155. van Marle G., Dobbe J. C., Gultyaev A. P., Luytjes W., Spaan W. J. M., Snijder E. J. 1999a; Arterivirus discontinuous mRNA transcription is guided by base pairing between sense and antisense transcription-regulating sequences. Proc Natl Acad Sci U S A 96:12056–12061 [CrossRef]
    [Google Scholar]
  156. van Marle G., van Dinten L. C., Spaan W. J. M., Luytjes W., Snijder E. J. 1999b; Characterization of an equine arteritis virus replicase mutant defective in subgenomic mRNA synthesis. J Virol 73:5274–5281
    [Google Scholar]
  157. van Vliet A. L., Smits S. L., Rottier P. J. M., de Groot R. J. 2002; Discontinuous and non-discontinuous subgenomic RNA transcription in a nidovirus. EMBO J 21:6571–6580 [CrossRef]
    [Google Scholar]
  158. von Grotthuss M., Wyrwicz L. S., Rychlewski L. 2003; mRNA cap-1 methyltransferase in the SARS genome. Cell 113:701–702 [CrossRef]
    [Google Scholar]
  159. Wang J., Carpenter C. D., Simon A. E. 1999; Minimal sequence and structural requirements of a subgenomic RNA promoter for turnip crinkle virus. Virology 253:327–336 [CrossRef]
    [Google Scholar]
  160. White K. A. 2002; The premature termination model: a possible third mechanism for subgenomic mRNA transcription in (+)-strand RNA viruses. Virology 304:147–154 [CrossRef]
    [Google Scholar]
  161. White K. A., Morris T. J. 1995; RNA determinants of junction site selection in RNA virus recombinants and defective interfering RNAs. RNA 1:1029–1040
    [Google Scholar]
  162. Wilson K. S., von Hippel P. H. 1995; Transcription termination at intrinsic terminators: the role of the RNA hairpin. Proc Natl Acad Sci U S A 92:8793–8797 [CrossRef]
    [Google Scholar]
  163. Woo P. C., Lau S. K., Chu C. M. & 12 other authors 2005; Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J Virol 79:884–895 [CrossRef]
    [Google Scholar]
  164. Wu W., Blumberg B. M., Fay P. J., Bambara R. A. 1995; Strand transfer mediated by human immunodeficiency virus reverse transcriptase in vitro is promoted by pausing and results in misincorporation. J Biol Chem 270:325–332 [CrossRef]
    [Google Scholar]
  165. Yan L., Velikanov M., Flook P., Zheng W., Szalma S., Kahn S. 2003; Assessment of putative protein targets derived from the SARS genome. FEBS Lett 554:257–263 [CrossRef]
    [Google Scholar]
  166. Yokomori K., Banner L. R., Lai M. M. 1992; Coronavirus mRNA transcription: UV light transcriptional mapping studies suggest an early requirement for a genomic-length template. J Virol 66:4671–4678
    [Google Scholar]
  167. Yount B., Denison M. R., Weiss S. R., Baric R. S. 2002; Systematic assembly of a full-length infectious cDNA of mouse hepatitis virus strain A59. J Virol 76:11065–11078 [CrossRef]
    [Google Scholar]
  168. Yount B., Curtis K. M., Fritz E. A., Hensley L. E., Jahrling P. B., Prentice E., Denison M. R., Geisbert T. W., Baric R. S. 2003; Reverse genetics with a full-length infectious cDNA of severe acute respiratory syndrome coronavirus. Proc Natl Acad Sci U S A 100:12995–13000 [CrossRef]
    [Google Scholar]
  169. Zhai Y., Sun F., Li X., Pang H., Xu X., Bartlam M., Rao Z. 2005; Insights into SARS-CoV transcription and replication from the structure of the nsp7-nsp8 hexadecamer. Nat Struct Mol Biol 12:980–986 [CrossRef]
    [Google Scholar]
  170. Zhang X., Lai M. M. C. 1994; Unusual heterogeneity of leader-mRNA fusion in a murine coronavirus: implications for the mechanism of RNA transcription and recombination. J Virol 68:6626–6633
    [Google Scholar]
  171. Zhang X., Liao C. L., Lai M. M. C. 1994; Coronavirus leader RNA regulates and initiates subgenomic mRNA transcription both in trans and in cis . J Virol 68:4738–4746
    [Google Scholar]
  172. Zhang G., Slowinski V., White K. A. 1999; Subgenomic mRNA regulation by a distal RNA element in a (+)-strand RNA virus. RNA 5:550–561 [CrossRef]
    [Google Scholar]
  173. Ziebuhr J., Snijder E. J., Gorbalenya A. E. 2000; Virus-encoded proteinases and proteolytic processing in the Nidovirales. J Gen Virol 81:853–879
    [Google Scholar]
  174. Zuniga S., Sola I., Alonso S., Enjuanes L. 2004; Sequence motifs involved in the regulation of discontinuous coronavirus subgenomic RNA synthesis. J Virol 78:980–994 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.81611-0
Loading
/content/journal/jgv/10.1099/vir.0.81611-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error