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. 2002 May 25;8(2):101–111. doi: 10.1006/smvy.1997.0109

Recombination and Coronavirus Defective Interfering RNAs

David A Brian a, Willy JM Spaan b
PMCID: PMC7129747  PMID: 32288442

Abstract

Naturally occurring defective interfering RNAs have been found in 4 of 14 coronavirus species. They range in size from 2.2 kb to approximately 25 kb, or 80% of the 30-kb parent virus genome. The large DI RNAs do not in all cases appear to require helper virus for intracellular replication and it has been postulated that they may on their own function as agents of disease. Coronavirus DI RNAs appear to arise by internal deletions (through nonhomologous recombination events) on the virus genome or on DI RNAs of larger size by a polymerase strand-switching (copy-choice) mechanism. In addition to their use in the study of virus RNA replication and virus assembly, coronavirus DI RNAs are being used in a major way to study the mechanism of a high-frequency, site-specific RNA recombination event that leads to leader acquisition during virus replication (i.e., the leader fusion event that occurs during synthesis of subgenomic mRNAs, and the leader-switching event that can occur during DI RNA replication), a distinguishing feature of coronaviruses (and arteriviruses). Coronavirus DI RNAs are also being engineered as vehicles for the generation of targeted recombinants of the parent virus genome.

Keywords: RNA recombination, leader fusion, recombinant coronaviruses

Footnotes

S. G. Siddell, Ed.

References

REFERENCES

  • 1.Makino S., Fujioka N., Fujiwara K. Structure of the intracellular defective viral RNAs of defective interfering particles of mouse hepatitis virus. J. Virol. 1985;54:329–336. doi: 10.1128/jvi.54.2.329-336.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Makino S., Shieh C.-K., Soe L.H., Baker S.C., Lai M.M.C. Primary structure and translation of a defective interfering RNA of murine coronavirus. Virology. 1988;166:550–560. doi: 10.1016/0042-6822(88)90526-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.van der Most R.G., Bredenbeek P.J., Spaan W.J.M. A domain at the 3′ end of the polymerase gene is essential for encapsidation of coronavirus defective interfering RNAs. J. Virol. 1991;65:3219–3226. doi: 10.1128/jvi.65.6.3219-3226.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Chang R.Y., Hofmann M.A., Sethna P.B., Brian D.A. A cis-acting function for the coronavirus leader in defective-interfering RNA replication. J. Virol. 1994;68:8223–8231. doi: 10.1128/jvi.68.12.8223-8231.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Mendez A., Smerdou C., Izeta A., Gebauer F., Enjuanes L. Molecular characterization of transmissible gastroenteritis coronavirus defective interfering genomes: Packaging and heterogeneity. Virology. 1996;217:495–507. doi: 10.1006/viro.1996.0144. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Penzes Z., Tibbles K., Shaw K., Britton P., Brown T.D.K., Cavanagh D. Characterization of a replicating and packaged defective RNA of avian coronavirus infectious bronchitis virus. Virology. 1994;203:286–293. doi: 10.1006/viro.1994.1486. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Kim K.H., Makino S. Two murine coronavirus genes suffice for viral RNA synthesis. J. Virol. 1995;69:2313–2321. doi: 10.1128/jvi.69.4.2313-2321.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Makino S., Yokomori K., Lai M.M.C. Analysis of efficiently packaged defective interfering RNAs of murine coronavirus: Localization of a possible RNA-packaging signal. J. Virol. 1990;64:6045–6053. doi: 10.1128/jvi.64.12.6045-6053.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Masters P., Koetzner C.A., Kerr C.A., Heo Y. Optimization of targeted RNA recombination and mapping of a novel nucleocapsid gene mutation in coronavirus mouse hepatitis virus. J. Virol. 1994;68:328–337. doi: 10.1128/jvi.68.1.328-337.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Mounir S., Talbot P.J. Human coronavirus OC43 RNA 4 lacks two open reading frames located downstream of the S gene of bovine coronavirus. Virology. 1993;192:355–360. doi: 10.1006/viro.1993.1043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Taguchi F., Ikeda T., Makino S., Yoshikura H. A murine coronavirus MHV-S isolate from persistently infected cells has a leader and two consensus sequences between the M and N genes. Virology. 1994;198:355–359. doi: 10.1006/viro.1994.1041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Lai M.M.C. Coronavirus: Organization, replication, and expression of genome. Annu. Rev. Microbiol. 1990;44:303–333. doi: 10.1146/annurev.mi.44.100190.001511. [DOI] [PubMed] [Google Scholar]
  • 13.Spaan W., Cavanagh D., Horzinek M.C. Coronaviruses: Structure and genome expression. J. Gen. Virol. 1988;69:2939–2952. doi: 10.1099/0022-1317-69-12-2939. [DOI] [PubMed] [Google Scholar]
  • 14.van der Most R.G., Spaan W.J.M. The Coronaviridae. Plenum Press; London: 1995. Coronavirus replication, transcription, and RNA recombination. p. 11–31. [Google Scholar]
  • 15.Furuya T., Macnaughton T.B., La Monica N., Lai M.M.C. Natural evolution of coronavirus defective-interfering RNA involves RNA recombination. Virology. 1993;194:408–413. doi: 10.1006/viro.1993.1277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Lai M.M.C. RNA recombination in animal and plant viruses. Microbiol. Rev. 1992;56:61–79. doi: 10.1128/mr.56.1.61-79.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Holland J. Defective viral genomes. In: Fields B.N., Knipe D.M., editors. Fundamental Virology. Raven Press; New York: 1991. pp. 151–165. [Google Scholar]
  • 18.King A.M.Q. Genetic recombination in positive strand RNA viruses. In: Domingo E., Holland J.J., Ahlquist P., editors. RNA Genetics. CRC Press; Boca Raton: 1988. pp. 149–165. [Google Scholar]
  • 19.Schlesinger S. The generation and amplification of defective interfering RNAs. In: Domingo E., Holland J.J., Ahlquist P., editors. RNA genetics. CRC Press; Boca Raton: 1988. pp. 167–185. [Google Scholar]
  • 20.Chang R.Y., Brian D.A. Cis-requirement for N-specific protein sequence in bovine coronavirus defective interfering RNA replication. J. Virol. 1996;70:2201–2207. doi: 10.1128/jvi.70.4.2201-2207.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.de Groot R.J., van der Most R.G., Spaan W.J.M. The fitness of defective interfering murine coronavirus DI-a and its derivatives is decreased by nonsense and frameshift mutations. J. Virol. 1992;66:5898–5905. doi: 10.1128/jvi.66.10.5898-5905.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Kim Y.N., Lai M.M.C., Makino S. Generation and selection of coronavirus defective interfering RNA with large open reading frame by RNA recombination and possible editing. Virology. 1993;194:244–253. doi: 10.1006/viro.1993.1255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.van der Most R.G., Luytjes W., Rutjes S., Spaan W.J.M. Translation but not the encoded sequence is essential for the efficient propagation of the defective interfering RNAs of the coronavirus mouse hapatitis virus. J. Virol. 1995;69:3744–3751. doi: 10.1128/jvi.69.6.3744-3751.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Liao C.L., Lai M.M.C. A cis-acting viral protein is not required for the replication of a coronavirus defective-interfering RNA. Virology. 1995;209:428–436. doi: 10.1006/viro.1995.1275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Penzes Z., Wroe C., Brown T.D.K., Britton P., Cavanagh D. Replication and packaging of coronavirus infectious bronchitis virus defective RNAs lacking a long open reading frame. J. Virol. 1996;70:8660–8668. doi: 10.1128/jvi.70.12.8660-8668.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Fosmire J.A., Hwang K., Makino S. Identification and characterization of a coronavirus packaging signal. J. Virol. 1992;66:3522–3530. doi: 10.1128/jvi.66.6.3522-3530.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Adami C., Pooley J., Glomb J., Stecker E., Fazal F., Fleming J.O., Baker S.C. Evolution of mouse hepatitis virus (MHV) during chronic infection: Quasispecies nature of the persisting MHV RNA. Virology. 1995;209:337–346. doi: 10.1006/viro.1995.1265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Maeda A., Hayashi M., Ishida K., Mizutani T., Watanabe T., Namioka S. Characterization of DBT cell clones derived from cells persistently infected with the JHM strain of mouse hepatitis virus. J. Vet. Med. Sci. 1995;57:813–817. doi: 10.1292/jvms.57.813. [DOI] [PubMed] [Google Scholar]
  • 29.Makino S., Keck J.G., Stohlman S.A., Lai M.M.C. High frequency recombination of murine coronaviruses. J. Virol. 1986;57:729–737. doi: 10.1128/jvi.57.3.729-737.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.K. V. Holmes, M. M. C. Lai, 1996, Coronaviridae: The viruses and their replication, Virology, B. N. FieldsD. M. KnipeP. M. Howley, 1, Lippincott–Raven, Philadelphia, PA
  • 31.de Vries A.A.F., Chirnside E.D., Bredenbeek P.J., Gravestein L.A., Horzinek M.C., Spaan W.J.M. All subgenomic mRNAs of equine arteritis virus contain a common leader sequence. Nucleic Acids Res. 1990;18:3241–3247. doi: 10.1093/nar/18.11.3241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Jacobs L., Spaan W.J.M., Horzinek M.C., van der Zeijst B.A.M. Synthesis of subgenomic mRNAs of mouse hepatitis virus is initiated independently: Evidence from UV transcription mapping. J. Virol. 1981;39:401–406. doi: 10.1128/jvi.39.2.401-406.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Yokomori K., Banner L.R., Lai M.M.C. Coronavirus mRNA transcription: UV light transcriptional mapping studies suggest an early requirement for a genome-length template. J. Virol. 1992;66:4671–4678. doi: 10.1128/jvi.66.8.4671-4678.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Baric R.S., Stohlman S.A., Lai M.M.C. Characterization of replicative intermediate RNA of mouse hepatitis virus: Presence of leader RNA sequences on nascent chains. J. Virol. 1983;48:633–640. doi: 10.1128/jvi.48.3.633-640.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Spaan W., Delius H., Skinner M., Armstrong J., Rottier P., Smeekens S., van der Ziejst B.A., Siddell S.G. Coronavirus mRNA synthesis involves fusion of non-contiguous sequences. EMBO J. 1983;2:1839–1844. doi: 10.1002/j.1460-2075.1983.tb01667.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Chang R.Y., Krishnan R., Brian D.A. The UCUAAAC promoter motif is not required for high-frequency leader recombination in bovine coronavirus defective interfering RNA. J. Virol. 1996;70:2720–2729. doi: 10.1128/jvi.70.5.2720-2729.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Makino S., Lai M.M.C. High-frequency leader sequence switching during coronavirus defective interfering RNA replication. J. Virol. 1989;63:5285–5292. doi: 10.1128/jvi.63.12.5285-5292.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Banner L.R., Lai M.M.C. Random nature of coronavirus RNA recombination in the absence of selection pressure. Virology. 1991;185:441–445. doi: 10.1016/0042-6822(91)90795-D. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39.J. M. Coffin, 1996, Retroviridae: The viruses and their replication, Virology, B. N. FieldsD. M. KnipeP. M. Howley, 2, Lippincott–Raven, Philadelphia, PA
  • 40.Zhang X., Lai M.M.C. Unusual heterogeneity of leader–mRNA fusion in a murine coronavirus: Implications for the mechanism of RNA transcription and recombination. J. Virol. 1994;68:6626–6633. doi: 10.1128/jvi.68.10.6626-6633.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Jeong Y.S., Repass J.F., Kim Y.N., Hwang S.M., Makino S. Coronavirus transcription mediated by sequences flanking the transcription consensus sequence. Virology. 1996;217:311–322. doi: 10.1006/viro.1996.0118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Joo M., Makino S. Mutagenic analysis of the coronavirus intergenic consensus sequence. J. Virol. 1992;66:6330–6337. doi: 10.1128/jvi.66.11.6330-6337.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Krishnan R., Chang R.Y., Brian D.A. Tandem placement of a coronavirus promoter results in enhanced mRNA synthesis from the downstream-most initiation site. Virology. 1996;218:400–405. doi: 10.1006/viro.1996.0210. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44.Makino S., Joo M. Effect of intergenic consensus flanking sequences on coronavirus transcription. J. Virol. 1993;67:3304–3311. doi: 10.1128/jvi.67.6.3304-3311.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45.van Marle G., Luytjes W., van der Most R.G., van der Straaten T., Spaan W.J. Regulation of coronavirus mRNA transcription. J. Virol. 1995;69:7851–7856. doi: 10.1128/jvi.69.12.7851-7856.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.van der Most R.G., DeGroot R.J., Spaan W.J.M. Subgenomic RNA synthesis directed by a synthetic defective interfering RNA of mouse hepatitis virus: A study of coronavirus transcription initiation. J. Virol. 1994;68:3656–3666. doi: 10.1128/jvi.68.6.3656-3666.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47.Makino S., Stohlman S., Lai M.M.C. Leader sequence of murine coronavirus mRNAs can be freely reassorted: Evidence for the role of free leader RNA in transcription. Proc. Natl. Acad. Sci. USA. 1986;83:4202–4208. doi: 10.1073/pnas.83.12.4204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48.Makino S., Lai M.M.C. Evolution of the 5′-end of genomic RNA of murine coronaviruses during passages in vitro. Virology. 1989;169:227–232. doi: 10.1016/0042-6822(89)90060-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49.Sawicki S.G., Sawicki D.L. Coronavirus transcription: Subgenomic mouse hepatitis virus replicative intermediates function in mRNA synthesis. J. Virol. 1990;64:1050–1056. doi: 10.1128/jvi.64.3.1050-1056.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Shieh C.K., Soe L.H., Makino S., Chang M.F., Stohlman S.A., Lai M.M.C. The 5′-end sequence of the murine coronavirus genome: Implications for multiple fusion sites in leader-primed transcription. Virology. 1987;156:321–330. doi: 10.1016/0042-6822(87)90412-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.Baker S.C., Lai M.M.C. An in vitro system for the leader-primed transcription of coronavirus mRNAs. EMBO J. 1990;9:4173–4179. doi: 10.1002/j.1460-2075.1990.tb07641.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52.Zhang X., Lai M.M.C. A 5′-proximal sequence of murine coronavirus as a potential initiation site for genomic-length mRNA transcription. J. Virol. 1996;70:705–711. doi: 10.1128/jvi.70.2.705-711.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53.S. G. Sawicki, D. L. Sawicki, 1995, Coronaviruses use discontinuous extension for synthesis of subgenome-length negative strands, Corona- and Related Viruses, P. J. TalbotG. A. Levy, 499, 506, Plenum, New York [DOI] [PubMed]
  • 54.Hofmann M.A., Sethna P.B., Brian D.A. Bovine coronavirus mRNA replication continues throughout persistent infection in cell culture. J. Virol. 1990;64:4108–4114. doi: 10.1128/jvi.64.9.4108-4114.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 55.Schaad M.C., Baric R.S. Genetics of mouse hepatitis virus transcription: Evidence that subgenomic negative strands are functional templates. J. Virol. 1994;68:8169–8179. doi: 10.1128/jvi.68.12.8169-8179.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 56.Sethna P.B., Hofmann M.A., Brian D.A. Minus-strand copies of replicating coronavirus mRNAs contain antileaders. J. Virol. 1991;65:320–325. doi: 10.1128/jvi.65.1.320-325.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 57.Sethna P.B., Hung S.-L., Brian D.A. Coronavirus subgenomic minus-strand RNA and the potential for mRNA replicons. Proc. Natl. Acad. Sci. USA. 1989;86:5626–5630. doi: 10.1073/pnas.86.14.5626. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 58.Budzilowicz C.J., Wilczynski S.P., Weiss S.R. Three intergenic regions of coronavirus mouse hepatitis virus strain A59 genome RNA contain a common nucleotide sequence that is homologous to the 3′ end of the viral mRNA leader sequence. J. Virol. 1985;53:834–840. doi: 10.1128/jvi.53.3.834-840.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 59.Zhang X., Lai M.M.C. Interactions between the cytoplasmic proteins and the intergenic (promoter) sequence of mouse hepatitis virus RNA: Correlation with the amounts of subgenomic mRNA transcribed. J. Virol. 1995;69:1637–1644. doi: 10.1128/jvi.69.3.1637-1644.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 60.Hofmann M.A., Chang R.Y., Ku S., Brian D.A. Leader–mRNA junction sequences are unique for each subgenomic mRNA species in the bovine coronavirus and remain so throughout persistent infection. Virology. 1993;196:163–171. doi: 10.1006/viro.1993.1464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 61.Jarvis T.C., Kirkegaard K. The polymerase in its labyrinth: Mechanisms and implications of RNA recombination. Trends Genet. 1991;7:186–191. doi: 10.1016/0168-9525(91)90434-R. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 62.Joo M., Makino S. The effect of two closely inserted transcription consensus sequences on coronavirus transcription. J. Virol. 1995;69:272–280. doi: 10.1128/jvi.69.1.272-280.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 63.Makino S., Joo M., Makino J.K. A system for study of coronavirus mRNA synthesis: A regulated, expressed subgenomic defective interfering RNA results from intergenic site insertion. J. Virol. 1991;65:6031–6041. doi: 10.1128/jvi.65.11.6031-6041.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64.Carpenter C.D., Oh J.W., Zhang C., Simon A.E. Involvement of a stem-loop structure in the location of junction sites in viral RNA recombination. J. Mol. Biol. 1995;245:608–622. doi: 10.1006/jmbi.1994.0050. [DOI] [PubMed] [Google Scholar]
  • 65.White A.K., Morris T.J. RNA determinants of junction site selection in RNA virus recombinants and defective interfering RNAs. RNA. 1995;1:1029–1040. [PMC free article] [PubMed] [Google Scholar]
  • 66.Nagy P.D., Bujarski J.J. Homologous RNA recombination in brome mosaic virus: AU-rich sequences decrease the accuracy of crossovers. J. Virol. 1996;70:415–426. doi: 10.1128/jvi.70.1.415-426.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 67.Simon A.E., Bujarski J.J. RNA–RNA recombination and evolution in virus-infected plants. Annu. Rev. Phytopathol. 1994;32:337–362. [Google Scholar]
  • 68.Zhang X., Liao C.L., Lai M.M.C. Coronavirus leader RNA regulates and initiates subgenomic mRNA transcription bothin transin cis. J. Virol. 1994;68:4736–4738. doi: 10.1128/jvi.68.8.4738-4746.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 69.Liao C.L., Lai M.M.C. RNA recombination in a coronavirus: Recombination between viral genomic RNA and transfected RNA fragments. J. Virol. 1992;66:6117–6124. doi: 10.1128/jvi.66.10.6117-6124.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 70.Joo M., Banerjee S., Makino S. Replication of murine coronavirus defective interfering RNA from negative-strand transcripts. J. Virol. 1996;70:5769–5776. doi: 10.1128/jvi.70.9.5769-5776.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 71.Koetzner C.A., Parker M.M., Ricard C.S., Sturman L.S., Masters P.S. Repair and mutagenesis of the genome of a deletion mutant of the coronavirus mouse hepatitis virus by targeted RNA recombination. J. Virol. 1992;66:1841–1848. doi: 10.1128/jvi.66.4.1841-1848.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 72.Peng D., Koetzner C.A., Masters P.S. Analysis of second-site revertants of a murine coronavirus and nucleocapsid protein deletion mutant and construction of nucleocapsid protein mutants by targeted RNA recombination. J. Virol. 1995;69:3449–3457. doi: 10.1128/jvi.69.6.3449-3457.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 73.van der Most R.G., Heijnen L., Spaan W.J.M., de Groot R.J. Homologous RNA recombination allows efficient introduction of site-specific mutations into the genome of coronavirus MHV-A59 via synthetic co-replicating RNAs. Nucleic Acids Res. 1991;20:3375–3381. doi: 10.1093/nar/20.13.3375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 74.Peng D., Koetzner C.A., McMahon T., Zhu Y., Masters P.S. Construction of murine coronavirus mutants containing interspecies chimeric nucleocapsid proteins. J. Virol. 1995;69:5475–5484. doi: 10.1128/jvi.69.9.5475-5484.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 75.Zhang L., Homberger F., Spaan W., Luytjes W. Recombinant genomic RNA of coronavirus MHV-A59 after co-replication with a DI RNA containing the MHV-RI spike gene. Virology. 1997;230:93–102. doi: 10.1006/viro.1997.8460. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 76.Tahara S.M., Dietlin T.A., Bergmann C.C., Nelson G.W., Kyuwa S., Anthony R.P., Stohlman S.A. Coronavirus translational regulation: Leader affects mRNA efficiency. Virology. 1994;202:621–630. doi: 10.1006/viro.1994.1383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 77.Snijder E.J., den Boon J.A., Horzinek M.C., Spaan W.J.M. Characterization of defective interfering RNAs of Berne virus. J. Gen. Virol. 1991;72:1635–1643. doi: 10.1099/0022-1317-72-7-1635. [DOI] [PubMed] [Google Scholar]
  • 78.van Dinten L.C., den Boon J.A., Wassenaar A.L.M., Spaan W.J.M., Snijder E.J. An infectious arterivirus cDNA clone: Identification of a replicase point mutation that abolishes discontinuous mRNA transcription. Proc. Natl. Acad. Sci. USA. 1997;94:991–996. doi: 10.1073/pnas.94.3.991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 79.Bos E.C., Luytjes W., van der Meulen H.V., Koerten H.K., Spaan W.J.M. The production of recombinant infectious DI particles of a murine coronavirus in the absence of helper virus. Virology. 1996;218:52–60. doi: 10.1006/viro.1996.0165. [DOI] [PMC free article] [PubMed] [Google Scholar]

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