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. 2005;287:95–131. doi: 10.1007/3-540-26765-4_4

Viral and Cellular Proteins Involved in Coronavirus Replication

S T Shi 2, M M C Lai 2
Editor: Luis Enjuanes1
PMCID: PMC7121242  PMID: 15609510

Abstract

As the largest RNA virus, coronavirus replication employs complex mechanisms and involves various viral and cellular proteins. The first open reading frame of the coronavirus genome encodes a large polyprotein, which is processed into a number of viral proteins required for viral replication directly or indirectly. These proteins include the RNA-dependent RNA polymerase (RdRp), RNA helicase, proteases, metal-binding proteins, and a number of other proteins of unknown function. Genetic studies suggest that most of these proteins are involved in viral RNA replication. In addition to viral proteins, several cellular proteins, such as heterogeneous nuclear ribonucleoprotein (hnRNP) A1, polypyrimidine-tract-binding (PTB) protein, poly(A)-binding protein (PABP), and mitochondrial aconitase (m-aconitase), have been identified to interact with the critical cis-acting elements of coronavirus replication. Like many other RNA viruses, coronavirus may subvert these cellular proteins from cellular RNA processing or translation machineries to play a role in viral replication.

Keywords: Mouse Hepatitis Virus, Equine Arteritis Virus, Murine Coronavirus, Mouse Hepatitis Virus Strain, Coronavirus Replication

Contributor Information

Luis Enjuanes, Email: L.Enjuanes@cnb.uam.es.

M. M. C. Lai, Email: michlai@hsc.usc.edu

References

  1. Ahola T., den Boon J.A., Ahlquist P. Helicase and capping enzyme active site mutations in brome mosaic virus protein 1a cause defects in template recruitment, negative-strand RNA synthesis, and viral RNA capping. J Virol. 2000;74:8803–8811. doi: 10.1128/JVI.74.19.8803-8811.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baker S.C., Lai M.M. 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]
  3. Baker S.C., Shieh C.K., Soe L.H., Chang M.F., Vannier D.M., Lai M.M. Identification of a domain required for autoproteolytic cleavage of murine coronavirus gene A polyprotein. J Virol. 1989;63:3693–3699. doi: 10.1128/jvi.63.9.3693-3699.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baker S.C., Yokomori K., Dong S., Carlisle R., Gorbalenya A.E., Koonin E.V., Lai M.M. Identification of the catalytic sites of a papain-like cysteine proteinase of murine coronavirus. J Virol. 1993;67:6056–6063. doi: 10.1128/jvi.67.10.6056-6063.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baker T.A., Bell S.P. Polymerases and the replisome: machines within machines. Cell. 1998;92:295–305. doi: 10.1016/S0092-8674(00)80923-X. [DOI] [PubMed] [Google Scholar]
  6. Baric R.S., Fu K., Schaad M.C., Stohlman S.A. Establishing a genetic recombination map for murine coronavirus strain A59 complementation groups. Virology. 1990;177:646–656. doi: 10.1016/0042-6822(90)90530-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Baric R.S., Nelson G.W., Fleming J.O., Deans R.J., Keck J.G., Casteel N., Stohlman S.A. Interactions between coronavirus nucleocapsid protein and viral RNAs: implications for viral transcription. J Virol. 1988;62:4280–4287. doi: 10.1128/jvi.62.11.4280-4287.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Baric R.S., Schaad M.C., Wei T., Fu K.S., Lum K., Shieh C., Stohlman S.A. Murine coronavirus temperature sensitive mutants. Adv Exp Med Biol. 1990;276:349–356. doi: 10.1007/978-1-4684-5823-7_47. [DOI] [PubMed] [Google Scholar]
  9. Behrens S.E., Tomei L., De Francesco R. Identification and properties of the RNA-dependent RNA polymerase of hepatitis C virus. EMBO J. 1996;15:12–22. [PMC free article] [PubMed] [Google Scholar]
  10. Beinert H., Kennedy M.C. Aconitase, a two-faced protein: enzyme and iron regulatory factor. FASEB J. 1993;7:1442–1449. doi: 10.1096/fasebj.7.15.8262329. [DOI] [PubMed] [Google Scholar]
  11. Ben-David Y., Bani M.R., Chabot B., De Koven A., Bernstein A. Retroviral insertions downstream of the heterogeneous nuclear ribonucleoprotein A1 gene in erythroleukemia cells: evidence that A1 is not essential for cell growth. Mol Cell Biol. 1992;12:4449–4455. doi: 10.1128/mcb.12.10.4449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Bienz K., Egger D., Pfister T. Characteristics of the poliovirus replication complex. Arch Virol Suppl. 1994;9:147–157. doi: 10.1007/978-3-7091-9326-6_15. [DOI] [PubMed] [Google Scholar]
  13. Bilodeau P.S., Domsic J.K., Mayeda A., Krainer A.R., Stoltzfus C.M. RNA splicing at human immunodeficiency virus type 1 3′ splice site A2 is regulated by binding of hnRNP A/B proteins to an exonic splicing silencer element. J Virol. 2001;75:8487–8497. doi: 10.1128/JVI.75.18.8487-8497.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Black A.C., Luo J., Chun S., Bakker A., Fraser J.K., Rosenblatt J.D. Specific binding of polypyrimidine tract binding protein and hnRNP A1 to HIV-1 CRS elements. Virus Genes. 1996;12:275–285. doi: 10.1007/BF00284648. [DOI] [PubMed] [Google Scholar]
  15. Black A.C., Luo J., Watanabe C., Chun S., Bakker A., Fraser J.K., Morgan J.P., Rosenblatt J.D. Polypyrimidine tract-binding protein and heterogeneous nuclear ribonucleoprotein A1 bind to human T-cell leukemia virus type 2 RNA regulatory elements. J Virol. 1995;69:6852–6858. doi: 10.1128/jvi.69.11.6852-6858.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Blackwell J.L., Brinton M.A. Translation elongation factor-1 alpha interacts with the 3′ stem-loop region of West Nile virus genomic RNA. J Virol. 1997;71:6433–6444. doi: 10.1128/jvi.71.9.6433-6444.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Blumenthal T., Carmichael G.G. RNA replication: function and structure of Qbeta-replicase. Annu Rev Biochem. 1979;48:525–548. doi: 10.1146/annurev.bi.48.070179.002521. [DOI] [PubMed] [Google Scholar]
  18. Bonilla P.J., Gorbalenya A.E., Weiss S.R. Mouse hepatitis virus strain A59 RNA polymerase gene ORF 1a: heterogeneity among MHV strains. Virology. 1994;198:736–740. doi: 10.1006/viro.1994.1088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Bonilla P.J., Hughes S.A., Pinon J.D., Weiss S.R. Characterization of the leader papain-like proteinase of MHV-A59: identification of a new in vitro cleavage site. Virology. 1995;209:489–497. doi: 10.1006/viro.1995.1281. [DOI] [PubMed] [Google Scholar]
  20. Bonilla P.J., Hughes S.A., Weiss S.R. Characterization of a second cleavage site and demonstration of activity in trans by the papain-like proteinase of the murine coronavirus mouse hepatitis virus strain A59. J Virol. 1997;71:900–909. doi: 10.1128/jvi.71.2.900-909.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Bost A.G., Carnahan R.H., Lu X.T., Denison M.R. Four proteins processed from the replicase gene polyprotein of mouse hepatitis virus colocalize in the cell periphery and adjacent to sites of virion assembly. J Virol. 2000;74:3379–3387. doi: 10.1128/JVI.74.7.3379-3387.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Bost A.G., Prentice E., Denison M.R. Mouse hepatitis virus replicase protein complexes are translocated to sites of M protein accumulation in the ERGIC at late times of infection. Virology. 2001;285:21–29. doi: 10.1006/viro.2001.0932. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Bothwell A.L., Ballard D.W., Philbrick W.M., Lindwall G., Maher S.E., Bridgett M.M., Jamison S.F., Garcia-Blanco M.A. Murine polypyrimidine tract binding protein. Purification, cloning, and mapping of the RNA binding domain. J Biol Chem. 1991;266:24657–24663. [PubMed] [Google Scholar]
  24. Brayton P.R., Lai M.M., Patton C.D., Stohlman S.A. Characterization of two RNA polymerase activities induced by mouse hepatitis virus. J Virol. 1982;42:847–853. doi: 10.1128/jvi.42.3.847-853.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Brayton P.R., Stohlman S.A., Lai M.M. Further characterization of mouse hepatitis virus RNA-dependent RNA polymerases. Virology. 1984;133:197–201. doi: 10.1016/0042-6822(84)90439-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Bredenbeek P.J., Pachuk C.J., Noten A.F., Charite J., Luytjes W., Weiss S.R., Spaan W.J. The primary structure and expression of the second open reading frame of the polymerase gene of the coronavirus MHV-A59; a highly conserved polymerase is expressed by an efficient ribosomal frameshifting mechanism. Nucleic Acids Res. 1990;18:1825–1832. doi: 10.1093/nar/18.7.1825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Brierley I., Boursnell M.E., Binns M.M., Bilimoria B., Blok V.C., Brown T.D., Inglis S.C. An efficient ribosomal frame-shifting signal in the polymerase-encoding region of the coronavirus IBV. EMBO J. 1987;6:3779–3785. doi: 10.1002/j.1460-2075.1987.tb02713.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Buck K.W. Comparison of the replication of positive-stranded RNA viruses of plants and animals. Adv Virus Res. 1996;47:159–251. doi: 10.1016/S0065-3527(08)60736-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Burd C.G., Dreyfuss G. Conserved structures and diversity of functions of RNA-binding proteins. Science. 1994;265:615–621. doi: 10.1126/science.8036511. [DOI] [PubMed] [Google Scholar]
  30. Caputi M., Mayeda A., Krainer A.R., Zahler A.M. hnRNP A/B proteins are required for inhibition of HIV-1 pre-mRNA splicing. EMBO J. 1999;18:4060–4067. doi: 10.1093/emboj/18.14.4060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Caputi M., Zahler A.M. SR proteins and hnRNP H regulate the splicing of the HIV-1 tev-specific exon 6D. EMBO J. 2002;21:845–855. doi: 10.1093/emboj/21.4.845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Chambers T.J., Hahn C.S., Galler R., Rice C.M. Flavivirus genome organization, expression, and replication. Annu Rev Microbiol. 1990;44:649–688. doi: 10.1146/annurev.mi.44.100190.003245. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. 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]
  35. Chung R.T., Kaplan L.M. Heterogeneous nuclear ribonucleoprotein I (hnRNP-I/PTB) selectively binds the conserved 3′ terminus of hepatitis C viral RNA. Biochem Biophys Res Commun. 1999;254:351–362. doi: 10.1006/bbrc.1998.9949. [DOI] [PubMed] [Google Scholar]
  36. Cologna R., Spagnolo J.F., Hogue B.G. Identification of nucleocapsid binding sites within coronavirus-defective genomes. Virology. 2000;277:235–249. doi: 10.1006/viro.2000.0611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Compton S.R., Rogers D.B., Holmes K.V., Fertsch D., Remenick J., McGowan J.J. In vitro replication of mouse hepatitis virus strain A59. J Virol. 1987;61:1814–1820. doi: 10.1128/jvi.61.6.1814-1820.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Craig A.W., Haghighat A., Yu A.T., Sonenberg N. Interaction of polyadenylate-binding protein with the eIF4G homologue PAIP enhances translation. Nature. 1998;392:520–523. doi: 10.1038/33198. [DOI] [PubMed] [Google Scholar]
  39. Das T., Mathur M., Gupta A.K., Janssen G.M., Banerjee A.K. RNA polymerase of vesicular stomatitis virus specifically associates with translation elongation factor-1αβγ for its activity. Proc Natl Acad Sci USA. 1998;95:1449–1454. doi: 10.1073/pnas.95.4.1449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. De P B., Lesoon A., Banerjee A.K. Human parainfluenza virus type 3 transcription in vitro: role of cellular actin in mRNA synthesis. J Virol. 1991;65:3268–3275. doi: 10.1128/jvi.65.6.3268-3275.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. de la Cruz J., Kressler D., Linder P. Unwinding RNA in Saccharomyces cerevisiae: DEAD-box proteins and related families. Trends Biochem Sci. 1999;24:192–198. doi: 10.1016/S0968-0004(99)01376-6. [DOI] [PubMed] [Google Scholar]
  42. Denison M., Perlman S. Identification of putative polymerase gene product in cells infected with murine coronavirus A59. Virology. 1987;157:565–568. doi: 10.1016/0042-6822(87)90303-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Denison M.R., Hughes S.A., Weiss S.R. Identification and characterization of a 65-kDa protein processed from the gene 1 polyprotein of the murine coronavirus MHV-A59. Virology. 1995;207:316–320. doi: 10.1006/viro.1995.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Denison M.R., Kim J.C., Ross T. Inhibition of coronavirus MHV-A59 replication by proteinase inhibitors. Adv Exp Med Biol. 1995;380:391–397. doi: 10.1007/978-1-4615-1899-0_64. [DOI] [PubMed] [Google Scholar]
  45. Denison M.R., Spaan W.J., van der Meer Y., Gibson C.A., Sims A.C., Prentice E., Lu X.T. The putative helicase of the coronavirus mouse hepatitis virus is processed from the replicase gene polyprotein and localizes in complexes that are active in viral RNA synthesis. J Virol. 1999;73:6862–6871. doi: 10.1128/jvi.73.8.6862-6871.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Denison M.R., Zoltick P.W., Hughes S.A., Giangreco B., Olson A.L., Perlman S., Leibowitz J.L., Weiss S.R. Intracellular processing of the N-terminal ORF 1a proteins of the coronavirus MHV-A59 requires multiple proteolytic events. Virology. 1992;189:274–284. doi: 10.1016/0042-6822(92)90703-R. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Dennis D.E., Brian D.A. RNA-dependent RNA polymerase activity in coronavirus-infected cells. J Virol. 1982;42:153–164. doi: 10.1128/jvi.42.1.153-164.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Diez J., Ishikawa M., Kaido M., Ahlquist P. Identification and characterization of a host protein required for efficient template selection in viral RNA replication. Proc Natl Acad Sci USA. 2000;97:3913–3918. doi: 10.1073/pnas.080072997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Dong S., Baker S.C. Determinants of the p28 cleavage site recognized by the first papain-like cysteine proteinase of murine coronavirus. Virology. 1994;204:541–549. doi: 10.1006/viro.1994.1567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Dreyfuss G., Matunis M.J., Pinol-Roma S., Burd C.G. hnRNP proteins and the biogenesis of mRNA. Annu Rev Biochem. 1993;62:289–321. doi: 10.1146/annurev.bi.62.070193.001445. [DOI] [PubMed] [Google Scholar]
  51. Froshauer S., Kartenbeck J., Helenius A. Alphavirus RNA replicase is located on the cytoplasmic surface of endosomes and lysosomes. J Cell Biol. 1988;107:2075–2086. doi: 10.1083/jcb.107.6.2075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Fu K., Baric R.S. Map locations of mouse hepatitis virus temperature-sensitive mutants: confirmation of variable rates of recombination. J Virol. 1994;68:7458–7466. doi: 10.1128/jvi.68.11.7458-7466.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Furuya T., Lai M.M.C. Three different cellular proteins bind to complementary sites on the 5′-end-positive and 3′ end-negative strands of mouse hepatitis virus RNA. J Virol. 1993;67:7215–7222. doi: 10.1128/jvi.67.12.7215-7222.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Gallie D.R. A tale of two termini: a functional interaction between the termini of an mRNA is a prerequisite for efficient translation initiation. Gene. 1998;216:1–11. doi: 10.1016/S0378-1119(98)00318-7. [DOI] [PubMed] [Google Scholar]
  55. Gamarnik A.V., Andino R. Two functional complexes formed by KH domain containing proteins with the 5′ noncoding region of poliovirus RNA. RNA. 1997;3:882–892. [PMC free article] [PubMed] [Google Scholar]
  56. Gamarnik A.V., Andino R. Switch from translation to RNA replication in a positive-stranded RNA virus. Genes Dev. 1998;12:2293–2304. doi: 10.1101/gad.12.15.2293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Gao H.Q., Schiller J.J., Baker S.C. Identification of the polymerase polyprotein products p72 and p65 of the murine coronavirus MHV-JHM. Virus Res. 1996;45:101–109. doi: 10.1016/S0168-1702(96)01368-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Gontarek R.R., Gutshall L.L., Herold K.M., Tsai J., Sathe G.M., Mao J., Prescott C., Del Vecchio A.M. hnRNP C and polypyrimidine tract-binding protein specifically interact with the pyrimidine-rich region within the 3′NTR of the HCV RNA genome. Nucleic Acids Res. 1999;27:1457–1463. doi: 10.1093/nar/27.6.1457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Gorbalenya A.E., Blinov V.M., Donchenko A.P., Koonin E.V. An NTP-binding motif is the most conserved sequence in a highly diverged monophyletic group of proteins involved in positive strand RNA viral replication. J Mol Evol. 1989;28:256–268. doi: 10.1007/BF02102483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Gorbalenya A.E., Koonin E.V. Viral proteins containing the purine NTP-binding sequence pattern. Nucleic Acids Res. 1989;17:8413–8440. doi: 10.1093/nar/17.21.8413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Gorbalenya A.E., Koonin E.V. Helicases: amino acid comparisons and structure-function relationships. Curr Opin Struct Biol. 1993;3:419–429. doi: 10.1016/S0959-440X(05)80116-2. [DOI] [Google Scholar]
  62. Gorbalenya A.E., Koonin E.V., Donchenko A.P., Blinov V.M. A novel superfamily of nucleoside triphosphate-binding motif containing proteins which are probably involved in duplex unwinding in DNA and RNA replication and recombination. FEBS Lett. 1988;235:16–24. doi: 10.1016/0014-5793(88)81226-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Gorbalenya A.E., Koonin E.V., Donchenko A.P., Blinov V.M. Coronavirus genome: prediction of putative functional domains in the non-structural polyprotein by comparative amino acid sequence analysis. Nucleic Acids Res. 1989;17:4847–4861. doi: 10.1093/nar/17.12.4847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Gorbalenya A.E., Koonin E.V., Lai M.M. Putative papain-related thiol proteases of positive-strand RNA viruses. Identification of rubi-and aphthovirus proteases and delineation of a novel conserved domain associated with proteases of rubi-, alpha-and coronaviruses. FEBS Lett. 1991;288:201–205. doi: 10.1016/0014-5793(91)81034-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Gorlach M., Burd C.G., Dreyfuss G. The mRNA poly(A)-binding protein: localization, abundance, and RNA-binding specificity. Exp Cell Res. 1994;211:400–407. doi: 10.1006/excr.1994.1104. [DOI] [PubMed] [Google Scholar]
  66. Grotzinger C., Heusipp G., Ziebuhr J., Harms U., Suss J., Siddell S.G. Characterization of a 105-kDa polypeptide encoded in gene 1 of the human coronavirus HCV 229E. Virology. 1996;222:227–235. doi: 10.1006/viro.1996.0413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Gutierrez-Escolano A.L., Brito Z.U., del Angel R.M., Jiang X. Interaction of cellular proteins with the 5′ end of Norwalk virus genomic RNA. J Virol. 2000;74:8558–8562. doi: 10.1128/JVI.74.18.8558-8562.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Hahm B., Kim Y.K., Kim J.H., Kim T.Y., Jang S.K. Heterogeneous nuclear ribonucleoprotein L interacts with the 3′ border of the internal ribosomal entry site of hepatitis C virus. J Virol. 1998;72:8782–8788. doi: 10.1128/jvi.72.11.8782-8788.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Hamilton B.J., Burns C.M., Nichols R.C., Rigby W.F.C. Modulation of AUUUA response element binding by heterogeneous nuclear ribonucleoprotein A1 in human T lymphocytes. The roles of cytoplasmic location, transcription, and phosphorylation. J Biol Chem. 1997;272:28732–28741. doi: 10.1074/jbc.272.45.28732. [DOI] [PubMed] [Google Scholar]
  70. Hamilton B.J., Nagy E., Malter J.S., Arrick B.A., Rigby W.F.C. Association of heterogeneous nuclear ribonucleoprotein A1 and C proteins with reiterated AUUUA sequences. J Biol Chem. 1993;268:8881–8887. [PubMed] [Google Scholar]
  71. Harris K.S., Xiang W., Alexander L., Lane W.S., Paul A.V., Wimmer E. Interaction of poliovirus polypeptide 3CDpro with the 5′ and 3′ termini of the poliovirus genome. Identification of viral and cellular cofactors needed for efficient binding. J Biol Chem. 1994;269:27004–27014. [PubMed] [Google Scholar]
  72. Hellen C.U., Pestova T.V., Litterst M., Wimmer E. The cellular polypeptide p57 (pyrimidine tract-binding protein) binds to multiple sites in the poliovirus 5′ nontranslated region. J Virol. 1994;68:941–950. doi: 10.1128/jvi.68.2.941-950.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Henics T., Sanfridson A., Hamilton B.J., Nagy E., Rigby W.F.C. Enhanced stability of interleukin-2 mRNA in MLA 144 cells. Possible role of cytoplasmic AU-rich sequence-binding proteins. J Biol Chem. 1994;269:5377–5383. [PubMed] [Google Scholar]
  74. Hentze M.W., Kuhn L.C. Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc Natl Acad Sci USA. 1996;93:8175–8182. doi: 10.1073/pnas.93.16.8175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Herold J., Gorbalenya A.E., Thiel V., Schelle B., Siddell S.G. Proteolytic processing at the amino terminus of human coronavirus 229E gene 1-encoded polyproteins: identification of a papain-like proteinase and its substrate. J Virol. 1998;72:910–918. doi: 10.1128/jvi.72.2.910-918.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Herold J., Siddell S.G. An ‘elaborated′ pseudoknot is required for high frequency frameshifting during translation of HCV 229E polymerase mRNA. Nucleic Acids Res. 1993;21:5838–5842. doi: 10.1093/nar/21.25.5838. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Herold J., Siddell S.G., Gorbalenya A.E. A human RNA viral cysteine proteinase that depends upon a unique Zn2+-binding finger connecting the two domains of a papain-like fold. J Biol Chem. 1999;274:14918–14925. doi: 10.1074/jbc.274.21.14918. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Hong Y., Hunt A.G. RNA polymerase activity catalyzed by a potyvirus-encoded RNA-dependent RNA polymerase. Virology. 1996;226:146–151. doi: 10.1006/viro.1996.0639. [DOI] [PubMed] [Google Scholar]
  79. Hsue B., Hartshorne T., Masters P.S. Characterization of an essential RNA secondary structure in the 3′ untranslated region of the murine coronavirus genome. J Virol. 2000;74:6911–6921. doi: 10.1128/JVI.74.15.6911-6921.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Hsue B., Masters P.S. A bulged stem-loop structure in the 3′ untranslated region of the genome of the coronavirus mouse hepatitis virus is essential for replication. J Virol. 1997;71:7567–7578. doi: 10.1128/jvi.71.10.7567-7578.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Huang P., Lai M.M. Heterogeneous nuclear ribonucleoprotein a1 binds to the 3′-untranslated region and mediates potential 5′-3′ end cross talks of mouse hepatitis virus RNA. J Virol. 2001;75:5009–5017. doi: 10.1128/JVI.75.11.5009-5017.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Huang P., Lai M.M.C. Polypyrimidine tract-binding protein binds to the complementary strand of the mouse hepatitis virus 3′ untranslated region, thereby altering RNA conformation. J Virol. 1999;73:9110–9116. doi: 10.1128/jvi.73.11.9110-9116.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Huang Y.T., Romito R.R., De B.P., Banerjee A.K. Characterization of the in vitro system for the synthesis of mRNA from human respiratory syncytial virus. Virology. 1993;193:862–867. doi: 10.1006/viro.1993.1195. [DOI] [PubMed] [Google Scholar]
  84. Hughes S.A., Bonilla P.J., Weiss S.R. Identification of the murine coronavirus p28 cleavage site. J Virol. 1995;69:809–813. doi: 10.1128/jvi.69.2.809-813.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Imataka H., Gradi A., Sonenberg N. A newly identified N-terminal amino acid sequence of human eIF4G binds poly(A)-binding protein and functions in poly(A)-dependent translation. EMBO J. 1998;17:7480–7489. doi: 10.1093/emboj/17.24.7480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Ito T., Lai M.M.C. Determination of the secondary structure of and cellular protein binding to the 3′-untranslated region of the hepatitis C virus RNA genome. J Virol. 1997;71:8698–8706. doi: 10.1128/jvi.71.11.8698-8706.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Jackson R.J., Kaminski A. Internal initiation of translation in eukaryotes: the picornavirus paradigm and beyond. RNA. 1995;1:985–1000. [PMC free article] [PubMed] [Google Scholar]
  88. Jankowsky E., Gross C.H., Shuman S., Pyle A.M. The DExH protein NPH-II is a processive and directional motor for unwinding RNA. Nature. 2000;403:447–451. doi: 10.1038/35000239. [DOI] [PubMed] [Google Scholar]
  89. Jendrach M., Thiel V., Siddell S. Characterization of an internal ribosome entry site within mRNA 5 of murine hepatitis virus. Arch Virol. 1999;144:921–933. doi: 10.1007/s007050050556. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Joshi R.L., Ravel J.M., Haenni A.L. Interaction of turnip yellow mosaic virus Val-RNA with eukaryotic elongation factor EF-1α. Search for a function. EMBO J. 1986;5:1143–1148. doi: 10.1002/j.1460-2075.1986.tb04339.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Kadare G., Haenni A.L. Virus-encoded RNA helicases. J Virol. 1997;71:2583–2590. doi: 10.1128/jvi.71.4.2583-2590.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Kaminski A., Hunt S.L., Patton J.G., Jackson R.J. Direct evidence that polypyrimidine tract binding protein (PTB) is essential for internal initiation of translation of encephalomyocarditis virus RNA. RNA. 1995;1:924–938. [PMC free article] [PubMed] [Google Scholar]
  93. Kanjanahaluethai A., Baker S.C. Identification of mouse hepatitis virus papainlike proteinase 2 activity. J Virol. 2000;74:7911–7921. doi: 10.1128/JVI.74.17.7911-7921.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Kennedy M.C., Mende-Mueller L., Blondin G.A., Beinert H. Purification and characterization of cytosolic aconitase from beef liver and its relationship to the iron-responsive element binding protein. Proc Natl Acad Sci USA. 1992;89:11730–11734. doi: 10.1073/pnas.89.24.11730. [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Kim H.Y., LaVaute T., Iwai K., Klausner R.D., Rouault T.A. Identification of a conserved and functional iron-responsive element in the 5′-untranslated region of mammalian mitochondrial aconitase. J Biol Chem. 1996;271:24226–24230. doi: 10.1074/jbc.271.39.24226. [DOI] [PubMed] [Google Scholar]
  96. Kim J.C., Spence R.A., Currier P.F., Lu X., Denison M.R. Coronavirus protein processing and RNA synthesis is inhibited by the cysteine proteinase inhibitor E64d. Virology. 1995;208:1–8. doi: 10.1006/viro.1995.1123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  97. 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]
  98. Kim Y.N., Jeong Y.S., Makino S. Analysis of cis-acting sequences essential for coronavirus defective interfering RNA replication. Virology. 1993;197:53–63. doi: 10.1006/viro.1993.1566. [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. Kim Y.N., Makino S. Characterization of a murine coronavirus defective interfering RNA internal cis-acting replication signal. J Virol. 1995;69:4963–4971. doi: 10.1128/jvi.69.8.4963-4971.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. Klausner R.D., Rouault T.A., Harford J.B. Regulating the fate of mRNA: the control of cellular iron metabolism. Cell. 1993;72:19–28. doi: 10.1016/0092-8674(93)90046-S. [DOI] [PubMed] [Google Scholar]
  101. Koolen M.J., Osterhaus A.D., Van Steenis G., Horzinek M.C., Van der Zeijst B.A. Temperature-sensitive mutants of mouse hepatitis virus strain A59: isolation, characterization and neuropathogenic properties. Virology. 1983;125:393–402. doi: 10.1016/0042-6822(83)90211-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  102. Koonin E.V., Dolja V.V. Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. Crit Rev Biochem Mol Biol. 1993;28:375–430. doi: 10.3109/10409239309078440. [DOI] [PubMed] [Google Scholar]
  103. Kuhn L.C., Hentze M.W. Coordination of cellular iron metabolism by post-transcriptional gene regulation. J Inorg Biochem. 1992;47:183–195. doi: 10.1016/0162-0134(92)84064-T. [DOI] [PubMed] [Google Scholar]
  104. Lai M.M.C. Cellular factors in the transcription and replication of viral RNA genomes: a parallel to DNA-dependent RNA transcription. Virology. 1998;244:1–12. doi: 10.1006/viro.1998.9098. [DOI] [PubMed] [Google Scholar]
  105. Lai M.M.C., Cavanagh D. The molecular biology of coronaviruses. Adv Virus Res. 1997;48:1–100. doi: 10.1016/S0168-1702(96)01421-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  106. Landers T.A., Blumenthal T., Weber K. Function and structure in ribonucleic acid phage Q beta ribonucleic acid replicase. The roles of the different subunits in transcription of synthetic templates. J Biol Chem. 1974;249:5801–5808. [PubMed] [Google Scholar]
  107. Le H, Tanguay R.L., Balasta M.L., Wei C.C., Browning K.S., Metz A.M., Goss D.J., Gallie D.R. Translation initiation factors eIF-iso4G and eIF-4B interact with the poly(A)-binding protein and increase its RNA binding activity. J Biol Chem. 1997;272:16247–16255. doi: 10.1074/jbc.272.26.16247. [DOI] [PubMed] [Google Scholar]
  108. Lee H.J., Shieh C.K., Gorbalenya A.E., Koonin E.V., La Monica N., Tuler J., Bagdzhadzhyan A., Lai M.M. The complete sequence (22 kilobases) of murine coronavirus gene 1 encoding the putative proteases and RNA polymerase. Virology. 1991;180:567–582. doi: 10.1016/0042-6822(91)90071-I. [DOI] [PMC free article] [PubMed] [Google Scholar]
  109. Leibowitz J.L., DeVries J.R. Synthesis of virus-specific RNA in permeabilized murine coronavirus-infected cells. Virology. 1988;166:66–75. doi: 10.1016/0042-6822(88)90147-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  110. Leibowitz J.L., DeVries J.R., Haspel M.V. Genetic analysis of murine hepatitis virus strain JHM. J Virol. 1982;42:1080–1087. doi: 10.1128/jvi.42.3.1080-1087.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  111. Li H.P., Huang P., Park S., Lai M.M.C. Polypyrimidine tract-binding protein binds to the leader RNA of mouse hepatitis virus and serves as a regulator of viral transcription. J Virol. 1999;73:772–777. doi: 10.1128/jvi.73.1.772-777.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  112. Li H.P., Zhang X., Duncan R., Comai L., Lai M.M.C. Heterogeneous nuclear ribonucleoprotein A1 binds to the transcription-regulatory region of mouse hepatitis virus RNA. Proc Natl Acad Sci USA. 1997;94:9544–9549. doi: 10.1073/pnas.94.18.9544. [DOI] [PMC free article] [PubMed] [Google Scholar]
  113. Liao C.L., Lai M.M.C. Requirement of the 5′ end genomic sequence as an upstream cis-acting element for coronavirus subgenomic mRNA transcription. J Virol. 1994;68:4727–4737. doi: 10.1128/jvi.68.8.4727-4737.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  114. Lim K.P., Liu D.X. Characterization of the two overlapping papain-like proteinase domains encoded in gene 1 of the coronavirus infectious bronchitis virus and determination of the C-terminal cleavage site of an 87-kDa protein. Virology. 1998;245:303–312. doi: 10.1006/viro.1998.9164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  115. Lim K.P., Ng L.F., Liu D.X. Identification of a novel cleavage activity of the first papain-like proteinase domain encoded by open reading frame 1a of the coronavirus avian infectious bronchitis virus and characterization of the cleavage products. J Virol. 2000;74:1674–1685. doi: 10.1128/JVI.74.4.1674-1685.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  116. Lin Y.J., Lai M.M. Deletion mapping of a mouse hepatitis virus defective interfering RNA reveals the requirement of an internal and discontiguous sequence for replication. J Virol. 1993;67:6110–6118. doi: 10.1128/jvi.67.10.6110-6118.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  117. Lin Y.J., Liao C.L., Lai M.M. 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. 1994;68:8131–8140. doi: 10.1128/jvi.68.12.8131-8140.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  118. Lin Y.J., Zhang X., Wu R.C., Lai M.M.C. The 3′ untranslated region of coronavirus RNA is required for subgenomic mRNA transcription from a defective interfering RNA. J Virol. 1996;70:7236–7240. doi: 10.1128/jvi.70.10.7236-7240.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  119. Linder P., Daugeron M.C. Are DEAD-box proteins becoming respectable helicases? Nat Struct Biol. 2000;7:97–99. doi: 10.1038/72464. [DOI] [PubMed] [Google Scholar]
  120. Liu D.X., Brierley I., Tibbles K.W., Brown T.D. A 100-kilodalton polypeptide encoded by open reading frame (ORF) 1b of the coronavirus infectious bronchitis virus is processed by ORF 1a products. J Virol. 1994;68:5772–5780. doi: 10.1128/jvi.68.9.5772-5780.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. Liu D.X., Brown T.D. Characterisation and mutational analysis of an ORF 1a-encoding proteinase domain responsible for proteolytic processing of the infectious bronchitis virus 1a/1b polyprotein. Virology. 1995;209:420–427. doi: 10.1006/viro.1995.1274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  122. Liu D.X., Shen S., Xu H.Y., Wang S.F. Proteolytic mapping of the coronavirus infectious bronchitis virus 1b polyprotein: evidence for the presence of four cleavage sites of the 3C-like proteinase and identification of two novel cleavage products. Virology. 1998;246:288–297. doi: 10.1006/viro.1998.9199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  123. Liu Q., Johnson R.F., Leibowitz J.L. Secondary structural elements within the 3′ untranslated region of mouse hepatitis virus strain JHM genomic RNA. J Virol. 2001;75:12105–12113. doi: 10.1128/JVI.75.24.12105-12113.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  124. Liu Q., Yu W., Leibowitz J.L. A specific host cellular protein binding element near the 3′ end of mouse hepatitis virus genomic RNA. Virology. 1997;232:74–85. doi: 10.1006/viro.1997.8553. [DOI] [PubMed] [Google Scholar]
  125. Lohman T.M., Bjornson K.P. Mechanisms of helicase-catalyzed DNA unwinding. Annu Rev Biochem. 1996;65:169–214. doi: 10.1146/annurev.bi.65.070196.001125. [DOI] [PubMed] [Google Scholar]
  126. Lohmann V., Korner F., Herian U., Bartenschlager R. Biochemical properties of hepatitis C virus NS5B RNA-dependent RNA polymerase and identification of amino acid sequence motifs essential for enzymatic activity. J Virol. 1997;71:8416–8428. doi: 10.1128/jvi.71.11.8416-8428.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  127. Lu X., Lu Y., Denison M.R. Intracellular and in vitro-translated 27-kDa proteins contain the 3C-like proteinase activity of the coronavirus MHV-A59. Virology. 1996;222:375–382. doi: 10.1006/viro.1996.0434. [DOI] [PMC free article] [PubMed] [Google Scholar]
  128. Lu X.T., Sims A.C., Denison M.R. Mouse hepatitis virus 3C-like protease cleaves a 22-kilodalton protein from the open reading frame 1a polyprotein in virus-infected cells and in vitro. J Virol. 1998;72:2265–2271. doi: 10.1128/jvi.72.3.2265-2271.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  129. Lu Y., Denison M.R. Determinants of mouse hepatitis virus 3C-like proteinase activity. Virology. 1997;230:335–342. doi: 10.1006/viro.1997.8479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  130. Lu Y., Lu X., Denison M.R. Identification and characterization of a serine-like proteinase of the murine coronavirus MHV-A59. J Virol. 1995;69:3554–3559. doi: 10.1128/jvi.69.6.3554-3559.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  131. Luytjes W., Bredenbeek P.J., Noten A.F., Horzinek M.C., Spaan W.J. Sequence of mouse hepatitis virus A59 mRNA 2: indications for RNA recombination between coronaviruses and influenza C virus. Virology. 1988;166:415–422. doi: 10.1016/0042-6822(88)90512-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  132. Ma A.S., Moran-Jones K., Shan J., Munro T.P., Snee M.J., Hoek K.S., Smith R. hnRNP A3, a novel RNA trafficking response element binding protein. J Biol Chem. 2002;8:8. doi: 10.1074/jbc.M200050200. [DOI] [PubMed] [Google Scholar]
  133. Mahy B.W., Siddell S., Wege H., ter Meulen V. RNA-dependent RNA polymerase activity in murine coronavirus-infected cells. J Gen Virol. 1983;64:103–111. doi: 10.1099/0022-1317-64-1-103. [DOI] [PubMed] [Google Scholar]
  134. 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]
  135. Martin J.P., Koehren F., Rannou J.J., Kirn A. Temperature-sensitive mutants of mouse hepatitis virus type 3 (MHV-3): isolation, biochemical and genetic characterization. Arch Virol. 1988;100:147–160. doi: 10.1007/BF01487679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  136. Mayeda A., Munroe S.H., Caceres J.F., Krainer A.R. Function of conserved domains of hnRNP A1 and other hnRNP A/B proteins. EMBO J. 1994;13:5483–5495. doi: 10.1002/j.1460-2075.1994.tb06883.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  137. Meerovitch K., Svitkin Y.V., Lee H.S., Lejbkowicz F., Kenan D.J., Chan E.K., Agol V.I., Keene J.D., Sonenberg N. La autoantigen enhances and corrects aberrant translation of poliovirus RNA in reticulocyte lysate. J Virol. 1993;67:3798–3807. doi: 10.1128/jvi.67.7.3798-3807.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  138. Michael W.M., Siomi H., Choi M., Pinol-Roma S., Nakielny S., Liu Q., Dreyfuss G. Signal sequences that target nuclear import and nuclear export of pre-mRNAbinding proteins. Cold Spring Harb Symp Quant Biol. 1995;60:663–668. doi: 10.1101/sqb.1995.060.01.071. [DOI] [PubMed] [Google Scholar]
  139. Miller D.J., Schwartz M.D., Ahlquist P. Flock house virus RNA replicates on outer mitochondrial membranes in Drosophila cells. J Virol. 2001;75:11664–11676. doi: 10.1128/JVI.75.23.11664-11676.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  140. Molenkamp R., van Tol H., Rozier B.C., van der Meer Y., Spaan W.J., Snijder E.J. The arterivirus replicase is the only viral protein required for genome replication and subgenomic mRNA transcription. J Gen Virol. 2000;81:2491–2496. doi: 10.1099/0022-1317-81-10-2491. [DOI] [PubMed] [Google Scholar]
  141. Moyer S.A., Baker S.C., Horikami S.M. Host cell proteins required for measles virus reproduction. J Gen Virol. 1990;71:775–783. doi: 10.1099/0022-1317-71-4-775. [DOI] [PubMed] [Google Scholar]
  142. Moyer S.A., Baker S.C., Lessard J.L. Tubulin: a factor necessary for the synthesis of both Sendai virus and vesicular stomatitis virus RNAs. Proc Natl Acad Sci USA. 1986;83:5405–5409. doi: 10.1073/pnas.83.15.5405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  143. Nanda S.K., Leibowitz J.L. Mitochondrial aconitase binds to the 3′ untranslated region of the mouse hepatitis virus genome. J Virol. 2001;75:3352–3362. doi: 10.1128/JVI.75.7.3352-3362.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  144. Nelson G.W., Stohlman S.A., Tahara S.M. High affinity interaction between nucleocapsid protein and leader/intergenic sequence of mouse hepatitis virus RNA. J Gen Virol. 2000;81:181–188. doi: 10.1099/0022-1317-81-1-181. [DOI] [PubMed] [Google Scholar]
  145. Neufeld K.L., Richards O.C., Ehrenfeld E. Purification, characterization, and comparison of poliovirus RNA polymerase from native and recombinant sources. J Biol Chem. 1991;266:24212–24219. [PubMed] [Google Scholar]
  146. Niepmann M. Porcine polypyrimidine tract-binding protein stimulates translation initiation at the internal ribosome entry site of foot-and-mouth-disease virus. FEBS Lett. 1996;388:39–42. doi: 10.1016/0014-5793(96)00509-1. [DOI] [PubMed] [Google Scholar]
  147. Niepmann M., Petersen A., Meyer K., Beck E. Functional involvement of polypyrimidine tract-binding protein in translation initiation complexes with the internal ribosome entry site of foot-and-mouth disease virus. J Virol. 1997;71:8330–8339. doi: 10.1128/jvi.71.11.8330-8339.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  148. Oglesbee M.J., Liu Z., Kenney H., Brooks C.L. The highly inducible member of the 70 kDa family of heat shock proteins increases canine distemper virus polymerase activity. J Gen Virol. 1996;77:2125–2135. doi: 10.1099/0022-1317-77-9-2125. [DOI] [PubMed] [Google Scholar]
  149. Osman T.A., Buck K.W. The tobacco mosaic virus RNA polymerase complex contains a plant protein related to the RNA-binding subunit of yeast eIF-3. J Virol. 1997;71:6075–6082. doi: 10.1128/jvi.71.8.6075-6082.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  150. Pardigon N., Strauss J.H. Mosquito homolog of the La autoantigen binds to Sindbis virus RNA. J Virol. 1996;70:1173–1181. doi: 10.1128/jvi.70.2.1173-1181.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  151. Parsley T.B., Towner J.S., Blyn L.B., Ehrenfeld E., Semler B.L. Poly (rC) binding protein 2 forms a ternary complex with the 5′-terminal sequences of poliovirus RNA and the viral 3CD proteinase. RNA. 1997;3:1124–1134. [PMC free article] [PubMed] [Google Scholar]
  152. Perlman S., Ries D., Bolger E., Chang L.J., Stoltzfus C.M. MHV nucleocapsid synthesis in the presence of cycloheximide and accumulation of negative strand MHV RNA. Virus Res. 1986;6:261–272. doi: 10.1016/0168-1702(86)90074-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  153. Pinol-Roma S., Dreyfuss G. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature. 1992;355:730–732. doi: 10.1038/355730a0. [DOI] [PubMed] [Google Scholar]
  154. Pinon J.D., Mayreddy R.R., Turner J.D., Khan F.S., Bonilla P.J., Weiss S.R. Efficient autoproteolytic processing of the MHV-A59 3C-like proteinase from the flanking hydrophobic domains requires membranes. Virology. 1997;230:309–322. doi: 10.1006/viro.1997.8503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  155. Pinon J.D., Teng H., Weiss S.R. Further requirements for cleavage by the murine coronavirus 3C-like proteinase: identification of a cleavage site within ORF1b. Virology. 1999;263:471–484. doi: 10.1006/viro.1999.9954. [DOI] [PMC free article] [PubMed] [Google Scholar]
  156. Pogue G.P., Huntley C.C., Hall T.C. Common replication strategies emerging from the study of diverse groups of positive-strand RNA viruses. Arch Virol Suppl. 1994;9:181–194. doi: 10.1007/978-3-7091-9326-6_18. [DOI] [PubMed] [Google Scholar]
  157. Quadt R., Kao C.C., Browning K.S., Hershberger R.P., Ahlquist P. Characterization of a host protein associated with brome mosaic virus RNA-dependent RNA polymerase. Proc Natl Acad Sci USA. 1993;90:1498–1502. doi: 10.1073/pnas.90.4.1498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  158. Robb J.A., Bond C.W. Pathogenic murine coronaviruses. I. Characterization of biological behavior in vitro and virus-specific intracellular RNA of strongly neurotropic JHMVand weakly neurotropic A59V viruses. Virology. 1979;94:352–370. doi: 10.1016/0042-6822(79)90467-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  159. Rothstein M.A., Richards O.C., Amin C., Ehrenfeld E. Enzymatic activity of poliovirus RNA polymerase synthesized in Escherichia coli from viral cDNA. Virology. 1988;164:301–308. doi: 10.1016/0042-6822(88)90542-9. [DOI] [PubMed] [Google Scholar]
  160. Sachs A.B., Sarnow P., Hentze M.W. Starting at the beginning, middle, and end: translation initiation in eukaryotes. Cell. 1997;89:831–838. doi: 10.1016/S0092-8674(00)80268-8. [DOI] [PubMed] [Google Scholar]
  161. Sawicki S.G., Sawicki D.L. Coronavirus minus-strand RNA synthesis and effect of cycloheximide on coronavirus RNA synthesis. J Virol. 1986;57:328–334. doi: 10.1128/jvi.57.1.328-334.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  162. Schaad M.C., Stohlman S.A., Egbert J., Lum K., Fu K., Wei T., Jr., Baric R.S. Genetics of mouse hepatitis virus transcription: identification of cistrons which may function in positive and negative strand RNA synthesis. Virology. 1990;177:634–645. doi: 10.1016/0042-6822(90)90529-Z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  163. Schalinske K.L., Chen O.S., Eisenstein R.S. Iron differentially stimulates translation of mitochondrial aconitase and ferritin mRNAs in mammalian cells. Implications for iron regulatory proteins as regulators of mitochondrial citrate utilization. J Biol Chem. 1998;273:3740–3746. doi: 10.1074/jbc.273.6.3740. [DOI] [PubMed] [Google Scholar]
  164. Schiller J.J., Kanjanahaluethai A., Baker S.C. Processing of the coronavirus MHV-JHM polymerase polyprotein: identification of precursors and proteolytic products spanning 400 kilodaltons of ORF1a. Virology. 1998;242:288–302. doi: 10.1006/viro.1997.9010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  165. Schmid S.R., Linder P. D-E-A-D protein family of putative RNA helicases. Mol Microbiol. 1992;6:283–291. doi: 10.1111/j.1365-2958.1992.tb01470.x. [DOI] [PubMed] [Google Scholar]
  166. Schwartz M., Chen J., Janda M., Sullivan M., den Boon J., Ahlquist P. A positive-strand RNA virus replication complex parallels form and function of retrovirus capsids. Mol Cell. 2002;9:505–514. doi: 10.1016/S1097-2765(02)00474-4. [DOI] [PubMed] [Google Scholar]
  167. Schwarz B., Routledge E., Siddell S.G. Murine coronavirus nonstructural protein ns2 is not essential for virus replication in transformed cells. J Virol. 1990;64:4784–4791. doi: 10.1128/jvi.64.10.4784-4791.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  168. Seybert A., Hegyi A., Siddell S.G., Ziebuhr J. The human coronavirus 229E superfamily 1 helicase has RNA and DNA duplex-unwinding activities with 5′-to-3′ polarity. RNA. 2000;6:1056–1068. doi: 10.1017/S1355838200000728. [DOI] [PMC free article] [PubMed] [Google Scholar]
  169. Shen X., Masters P.S. Evaluation of the role of heterogeneous nuclear ribonucleoprotein A1 as a host factor in murine coronavirus discontinuous transcription and genome replication. Proc Natl Acad Sci USA. 2001;98:2717–2722. doi: 10.1073/pnas.031424298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  170. Shi S.T., Huang P., Li H.P., Lai M.M.C. Heterogeneous nuclear ribonucleoprotein A1 regulates RNA synthesis of a cytoplasmic virus. EMBO J. 2000;19:4701–4711. doi: 10.1093/emboj/19.17.4701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  171. Shi S.T., Schiller J.J., Kanjanahaluethai A., Baker S.C., Oh J.W., Lai M.M. Colocalization and membrane association of murine hepatitis virus gene 1 products and de novo-synthesized viral RNA in infected cells. J Virol. 1999;73:5957–5969. doi: 10.1128/jvi.73.7.5957-5969.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  172. Shi S.T., Yu G.Y., Lai M.M.C. Multiple type A/B heterogeneous nuclear ribonucleoproteins (hnRNPs) can replace hnRNP A1 in mouse hepatitis virus RNA synthesis. J Virol. 2003;11:10584–10593. doi: 10.1128/JVI.77.19.10584-10593.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  173. Sims A.C., Ostermann J., Denison M.R. Mouse hepatitis virus replicase proteins associate with two distinct populations of intracellular membranes. J Virol. 2000;74:5647–5654. doi: 10.1128/JVI.74.12.5647-5654.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  174. Siomi H., Dreyfuss G. A nuclear localization domain in the hnRNP A1 protein. J Cell Biol. 1995;129:551–560. doi: 10.1083/jcb.129.3.551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  175. Snijder E.J., van Tol H., Roos N., Pedersen K.W. Non-structural proteins 2 and 3 interact to modify host cell membranes during the formation of the arterivirus replication complex. J Gen Virol. 2001;82:985–994. doi: 10.1099/0022-1317-82-5-985. [DOI] [PubMed] [Google Scholar]
  176. Sokolowski M., Schwartz S. Heterogeneous nuclear ribonucleoprotein C binds exclusively to the functionally important UUUUU-motifs in the human papillomavirus type-1 AU-rich inhibitory element. Virus Res. 2001;73:163–175. doi: 10.1016/S0168-1702(00)00238-0. [DOI] [PubMed] [Google Scholar]
  177. Spagnolo J.F., Hogue B.G. Host protein interactions with the 3′ end of bovine coronavirus RNA and the requirement of the poly(A) tail for coronavirus defective genome replication. J Virol. 2000;74:5053–5065. doi: 10.1128/JVI.74.11.5053-5065.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  178. Spangberg K., Wiklund L., Schwartz S. HuR, a protein implicated in oncogene and growth factor mRNA decay, binds to the 3′ ends of hepatitis C virus RNA of both polarities. Virology. 2000;274:378–390. doi: 10.1006/viro.2000.0461. [DOI] [PubMed] [Google Scholar]
  179. Stalcup R.P., Baric R.S., Leibowitz J.L. Genetic complementation among three panels of mouse hepatitis virus gene 1 mutants. Virology. 1998;241:112–121. doi: 10.1006/viro.1997.8957. [DOI] [PubMed] [Google Scholar]
  180. Stohlman S.A., Baric R.S., Nelson G.N., Soe L.H., Welter L.M., Deans R.J. Specific interaction between coronavirus leader RNA and nucleocapsid protein. J Virol. 1988;62:4288–4295. doi: 10.1128/jvi.62.11.4288-4295.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  181. Svitkin Y.V., Ovchinnikov L.P., Dreyfuss G., Sonenberg N. General RNA binding proteins render translation cap dependent. EMBO J. 1996;15:7147–7155. [PMC free article] [PubMed] [Google Scholar]
  182. Tahara S., Bergmann C., Nelson G., Anthony R., Dietlin T., Kyuwa S., Stohlman S. Effects of mouse hepatitis virus infection on host cell metabolism. Adv Exp Med Biol. 1993;342:111–116. doi: 10.1007/978-1-4615-2996-5_18. [DOI] [PubMed] [Google Scholar]
  183. 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]
  184. Tahara S.M., Dietlin T.A., Nelson G.W., Stohlman S.A., Manno D.J. Mouse hepatitis virus nucleocapsid protein as a translational effector of viral mRNAs. Adv Exp Med Biol. 1998;440:313–318. doi: 10.1007/978-1-4615-5331-1_41. [DOI] [PubMed] [Google Scholar]
  185. Tan B.H., Fu J., Sugrue R.J., Yap E.H., Chan Y.C., Tan Y.H. Recombinant dengue type 1 virus NS5 protein expressed in Escherichia coli exhibits RNA-dependent RNA polymerase activity. Virology. 1996;216:317–325. doi: 10.1006/viro.1996.0067. [DOI] [PubMed] [Google Scholar]
  186. Tarun S.Z., Jr., Sachs A.B. Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBO J. 1996;15:7168–7177. [PMC free article] [PubMed] [Google Scholar]
  187. Tarun S.Z., Jr., Wells S.E., Deardorff J.A., Sachs A.B. Translation initiation factor eIF4G mediates in vitro poly(A) tail-dependent translation. Proc Natl Acad Sci USA. 1997;94:9046–9051. doi: 10.1073/pnas.94.17.9046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  188. Thiel V., Herold J., Schelle B., Siddell S.G. Viral replicase gene products suffice for coronavirus discontinuous transcription. J Virol. 2001;75:6676–6681. doi: 10.1128/JVI.75.14.6676-6681.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  189. Thiel V., Siddell S.G. Internal ribosome entry in the coding region of murine hepatitis virus mRNA 5. J Gen Virol. 1994;75:3041–3046. doi: 10.1099/0022-1317-75-11-3041. [DOI] [PubMed] [Google Scholar]
  190. Tijms M.A., van Dinten L.C., Gorbalenya A.E., Snijder E.J. A zinc finger-containing papain-like protease couples subgenomic mRNA synthesis to genome translation in a positive-stranded RNA virus. Proc Natl Acad Sci USA. 2001;98:1889–1894. doi: 10.1073/pnas.041390398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  191. Valcarcel J., Gebauer F. Post-transcriptional regulation: the dawn of PTB. Curr Biol. 1997;7:R705–708. doi: 10.1016/S0960-9822(06)00361-7. [DOI] [PubMed] [Google Scholar]
  192. van der Meer Y., Snijder E.J., Dobbe J.C., Schleich S., Denison M.R., Spaan W.J., Locker J.K. Localization of mouse hepatitis virus nonstructural proteins and RNA synthesis indicates a role for late endosomes in viral replication. J Virol. 1999;73:7641–7657. doi: 10.1128/jvi.73.9.7641-7657.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  193. van Dinten L.C., den Boon J.A., Wassenaar A.L., Spaan W.J., 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]
  194. van Dinten L.C., Rensen S., Gorbalenya A.E., Snijder E.J. Proteolytic processing of the open reading frame 1b-encoded part of arterivirus replicase is mediated by nsp4 serine protease and Is essential for virus replication. J Virol. 1999;73:2027–2037. doi: 10.1128/jvi.73.3.2027-2037.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  195. van Dinten L.C., Wassenaar A.L., Gorbalenya A.E., Spaan W.J., Snijder E.J. Processing of the equine arteritis virus replicase ORF1b protein: identification of cleavage products containing the putative viral polymerase and helicase domains. J Virol. 1996;70:6625–6633. doi: 10.1128/jvi.70.10.6625-6633.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  196. Van Dyke T.A., Flanegan J.B. Identification of poliovirus polypeptide P63 as a soluble RNA-dependent RNA polymerase. J Virol. 1980;35:732–740. doi: 10.1128/jvi.35.3.732-740.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  197. Wang Y., Zhang X. The nucleocapsid protein of coronavirus mouse hepatitis virus interacts with the cellular heterogeneous nuclear ribonucleoprotein A1 in vitro and in vivo. Virology. 1999;265:96–109. doi: 10.1006/viro.1999.0025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  198. Wang Y.F., Chen S.C., Wu F.Y., Wu C.W. The interaction between human cytomegalovirus immediate-early gene 2 (IE2) protein and heterogeneous ribonucleoprotein A1. Biochem Biophys Res Commun. 1997;232:590–594. doi: 10.1006/bbrc.1997.6334. [DOI] [PubMed] [Google Scholar]
  199. Weighardt F., Biamonti G., Riva S. Nucleo-cytoplasmic distribution of human hnRNP proteins: a search for the targeting domains in hnRNP A1. J Cell Sci. 1995;108:545–555. doi: 10.1242/jcs.108.2.545. [DOI] [PubMed] [Google Scholar]
  200. Williams G.D., Chang R.Y., Brian D.A. Evidence for a pseudoknot in the 3′ untranslated region of the bovine coronavirus genome. Adv Exp Med Biol. 1995;380:511–514. doi: 10.1007/978-1-4615-1899-0_81. [DOI] [PubMed] [Google Scholar]
  201. Wu-Baer F., Lane W.S., Gaynor R.B. Identification of a group of cellular cofactors that stimulate the binding of RNA polymerase II and TRP-185 to human immunodeficiency virus 1 TAR RNA. J Biol Chem. 1996;271:4201–4208. doi: 10.1074/jbc.271.8.4201. [DOI] [PubMed] [Google Scholar]
  202. Yokomori K., Banner L.R., Lai M.M. Heterogeneity of gene expression of the hemagglutinin-esterase (HE) protein of murine coronaviruses. Virology. 1991;183:647–657. doi: 10.1016/0042-6822(91)90994-M. [DOI] [PMC free article] [PubMed] [Google Scholar]
  203. Yokomori K., Lai M.M. Mouse hepatitis virus S RNA sequence reveals that nonstructural proteins ns4 and ns5a are not essential for murine coronavirus replication. J Virol. 1991;65:5605–5608. doi: 10.1128/jvi.65.10.5605-5608.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  204. Yu W., Leibowitz J.L. A conserved motif at the 3′ end of mouse hepatitis virus genomic RNA required for host protein binding and viral RNA replication. Virology. 1995;214:128–138. doi: 10.1006/viro.1995.9947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  205. Yu W., Leibowitz J.L. Specific binding of host cellular proteins to multiple sites within the 3′ end of mouse hepatitis virus genomic RNA. J Virol. 1995;69:2016–2023. doi: 10.1128/jvi.69.4.2016-2023.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  206. Yuan Z.H., Kumar U., Thomas H.C., Wen Y.M., Monjardino J. Expression, purification, and partial characterization of HCV RNA polymerase. Biochem Biophys Res Commun. 1997;232:231–235. doi: 10.1006/bbrc.1997.6249. [DOI] [PubMed] [Google Scholar]
  207. 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]
  208. Zhang X., Li H.P., Xue W., Lai M.M.C. Formation of a ribonucleoprotein complex of mouse hepatitis virus involving heterogeneous nuclear ribonucleoprotein A1 and transcription-regulatory elements of viral RNA. Virology. 1999;264:115–124. doi: 10.1006/viro.1999.9970. [DOI] [PubMed] [Google Scholar]
  209. Zhang X., Liao C.L., Lai M.M.C. Coronavirus leader RNA regulates and initiates subgenomic mRNA transcription both in trans and in cis. J Virol. 1994;68:4738–4746. doi: 10.1128/jvi.68.8.4738-4746.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  210. Zhang X.M., Lai M.M.C. Regulation of coronavirus RNA transcription is likely mediated by protein-RNA interactions. Adv Exp Med Biol. 1995;380:515–521. doi: 10.1007/978-1-4615-1899-0_82. [DOI] [PubMed] [Google Scholar]
  211. Ziebuhr J., Siddell S.G. Processing of the human coronavirus 229E replicase polyproteins by the virus-encoded 3C-like proteinase: identification of proteolytic products and cleavage sites common to pp1a and pp1ab. J Virol. 1999;73:177–185. doi: 10.1128/jvi.73.1.177-185.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  212. Ziebuhr J., Snijder E.J., Gorbalenya A.E. Virus-encoded proteinases and proteolytic processing in the Nidovirales. J Gen Virol. 2000;81:853–879. doi: 10.1099/0022-1317-81-4-853. [DOI] [PubMed] [Google Scholar]

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