The structure and functions of coronavirus genomic 3' and 5' ends

Virus Research

Volumn 206, Issue , 2015, Pages 120-133

  Yang, Dong ^a   Leibowitz, Julian L ^b  

^a UNIVERSITY OF TENNESSEE COLLEGE OF MEDICINE   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Cis Acting sequences; Coronaviruses; RNA binding proteins; RNA secondary structure; Virus replication

Indexed keywords

VIRUS PROTEIN; VIRUS RNA; 3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; RNA BINDING PROTEIN;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ALPHACORONAVIRUS 1; BETACORONAVIRUS; CORONAVIRIDAE; GAMMACORONAVIRUS; GENE INTERACTION; GENOME ANALYSIS; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PHYLOGENY; POSITIVE-STRAND RNA VIRUS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; REVIEW; RNA REPLICATION; RNA SYNTHESIS; RNA TRANSLATION; SARS CORONAVIRUS; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS VIABILITY; VIRUS VIRULENCE; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; CONFORMATION; CONSERVED SEQUENCE; GENETIC TRANSCRIPTION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; PHYSIOLOGY; PROMOTER REGION; VIRUS GENOME;

ANIMALIA; CORONAVIRUS; SARS CORONAVIRUS;

3' UNTRANSLATED REGIONS; 5' UNTRANSLATED REGIONS; ANIMALS; CONSERVED SEQUENCE; CORONAVIRUS; GENOME, VIRAL; HOST-PATHOGEN INTERACTIONS; HUMANS; MODELS, BIOLOGICAL; NUCLEIC ACID CONFORMATION; PROMOTER REGIONS, GENETIC; RNA, VIRAL; RNA-BINDING PROTEINS; TRANSCRIPTION, GENETIC; VIRUS REPLICATION;

EID: 84931561305     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2015.02.025     Document Type: Review

References (152)

1. Arbour N., Cote G., Lachance C., Tardieu M., Cashman N.R., Talbot P.J. Acute and persistent infection of human neural cell lines by human coronavirus OC43. J. Virol. 1999, 73(4):3338-3350.
2. 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(11):4280-4287.
3. Baric R.S., Yount B. Subgenomic negative-strand RNA function during mouse hepatitis virus infection. J. Virol. 2000, 74(9):4039-4046.
4. Bhardwaj K., Guarino L., Kao C.C. The severe acute respiratory syndrome coronavirus Nsp15 protein is an endoribonuclease that prefers manganese as a cofactor. J. Virol. 2004, 78(22):12218-12224.
5. 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(7):1825-1832.
6. Brian D.A., Baric R.S. Coronavirus genome structure and replication. Curr. Top. Microbiol. Immunol. 2005, 287:1-30.
7. Brockway S.M., Clay C.T., Lu X.T., Denison M.R. Characterization of the expression, intracellular localization, and replication complex association of the putative mouse hepatitis virus RNA-dependent RNA polymerase. J. Virol. 2003, 77(19):10515-10527.
8. Brockway S.M., Denison M.R. Mutagenesis of the murine hepatitis virus nsp1-coding region identifies residues important for protein processing, viral RNA synthesis, and viral replication. Virology 2005, 340(2):209-223.
9. Brown C.G., Nixon K.S., Senanayake S.D., Brian D.A. An RNA stem-loop within the bovine coronavirus nsp1 coding region is a cis-acting element in defective interfering RNA replication. J. Virol. 2007, 81(14):7716-7724.
10. 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(3):834-840.
11. Casais R., Thiel V., Siddell S.G., Cavanagh D., Britton P. Reverse genetics system for the avian coronavirus infectious bronchitis virus. J. Virol. 2001, 75(24):12359-12369.
12. Chang C.K., Hsu Y.L., Chang Y.H., Chao F.A., Wu M.C., Huang Y.S., Hu C.K., Huang T.H. Multiple nucleic acid binding sites and intrinsic disorder of severe acute respiratory syndrome coronavirus nucleocapsid protein: implications for ribonucleocapsid protein packaging. J. Virol. 2009, 83(5):2255-2264.
13. 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(12):8223-8231.
14. Chen S.C., Olsthoorn R.C. Group-specific structural features of the 5'-proximal sequences of coronavirus genomic RNAs. Virology 2010, 401(1):29-41.
15. Chen Y., Cai H., Pan J., Xiang N., Tien P., Ahola T., Guo D. Functional screen reveals SARS coronavirus nonstructural protein nsp14 as a novel cap N7 methyltransferase. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(9):3484-3489.
16. Cheng A., Zhang W., Xie Y., Jiang W., Arnold E., Sarafianos S.G., Ding J. Expression, purification, and characterization of SARS coronavirus RNA polymerase. Virology 2005, 335(2):165-176.
17. Choi K.S., Huang P., Lai M.M. Polypyrimidine-tract-binding protein affects transcription but not translation of mouse hepatitis virus RNA. Virology 2002, 303(1):58-68.
18. Choi K.S., Mizutani A., Lai M.M. SYNCRIP, a member of the heterogeneous nuclear ribonucleoprotein family, is involved in mouse hepatitis virus RNA synthesis. J. Virol. 2004, 78(23):13153-13162.
19. Coleman C.M., Frieman M.B. Coronaviruses: important emerging human pathogens. J. Virol. 2014, 88(10):5209-5212.
20. Cologna R., Hogue B.G. Identification of a bovine coronavirus packaging signal. J. Virol. 2000, 74(1):580-583.
21. Cologna R., Spagnolo J.F., Hogue B.G. Identification of nucleocapsid binding sites within coronavirus-defective genomes. Virology 2000, 277(2):235-249.
22. Dalton K., Casais R., Shaw K., Stirrups K., Evans S., Britton P., Brown T.D., Cavanagh D. cis-acting sequences required for coronavirus infectious bronchitis virus defective-RNA replication and packaging. J. Virol. 2001, 75(1):125-133.
23. de Groot R.J., Baker S.C., Baric R.S., Brown C.S., Drosten C., Enjuanes L., Fouchier R.A., Galiano M., Gorbalenya A.E., Memish Z.A., Perlman S., Poon L.L., Snijder E.J., Stephens G.M., Woo P.C., Zaki A.M., Zambon M., Ziebuhr J. Middle East respiratory syndrome coronavirus (MERS-CoV): announcement of the Coronavirus Study Group. J. Virol. 2013, 87(14):7790-7792.
24. de Haan C.A., Volders H., Koetzner C.A., Masters P.S., Rottier P.J. Coronaviruses maintain viability despite dramatic rearrangements of the strictly conserved genome organization. J. Virol. 2002, 76(24):12491-12502.
25. Decroly E., Imbert I., Coutard B., Bouvet M., Selisko B., Alvarez K., Gorbalenya A.E., Snijder E.J., Canard B. Coronavirus nonstructural protein 16 is a cap-0 binding enzyme possessing (nucleoside-2'O)-methyltransferase activity. J. Virol. 2008, 82(16):8071-8084.
26. DeDiego M.L., Alvarez E., Almazan F., Rejas M.T., Lamirande E., Roberts A., Shieh W.J., Zaki S.R., Subbarao K., Enjuanes L. A severe acute respiratory syndrome coronavirus that lacks the E gene is attenuated in vitro and in vivo. J. Virol. 2007, 81(4):1701-1713.
27. Delmas B., Gelfi J., L'Haridon R., Vogel L.K., Sjostrom H., Noren O., Laude H. Aminopeptidase N is a major receptor for the enteropathogenic coronavirus TGEV. Nature 1992, 357:417-420.
28. Drexler J.F., Corman V.M., Drosten C. Ecology, evolution and classification of bat coronaviruses in the aftermath of SARS. Antiviral Res. 2014, 101:45-56.
29. Dye C., Siddell S.G. Genomic RNA sequence of Feline coronavirus strain FIPV WSU-79/1146. J. Gen. Virol. 2005, 86(Pt 8):2249-2253.
30. Escors D., Izeta A., Capiscol C., Enjuanes L. Transmissible gastroenteritis coronavirus packaging signal is located at the 5' end of the virus genome. J. Virol. 2003, 77(14):7890-7902.
31. Fischer F., Stegen C.F., Masters P.S., Samsonoff W.A. Analysis of constructed E gene mutants of mouse hepatitis virus confirms a pivotal role for E protein in coronavirus assembly. J. Virol. 1998, 72(10):7885-7894.
32. Fosmire J.A., Hwang K., Makino S. Identification and characterization of a coronavirus packaging signal. J. Virol. 1992, 66(6):3522-3530.
33. Galan C., Sola I., Nogales A., Thomas B., Akoulitchev A., Enjuanes L., Almazan F. Host cell proteins interacting with the 3' end of TGEV coronavirus genome influence virus replication. Virology 2009, 391(2):304-314.
34. Gerna G., Passarani N., Battaglia M., Rondanelli E.G. Human enteric coronaviruses: antigenic relatedness to human coronavirus OC43 and possible etiologic role in viral gastroenteritis. J. Infect. Dis. 1985, 151(5):796-803.
35. Goebel S.J., Hsue B., Dombrowski T.F., Masters P.S. Characterization of the RNA components of a putative molecular switch in the 3' untranslated region of the murine coronavirus genome. J. Virol. 2004, 78(2):669-682.
36. Goebel S.J., Miller T.B., Bennett C.J., Bernard K.A., Masters P.S. A hypervariable region within the 3' cis-acting element of the murine coronavirus genome is nonessential for RNA synthesis but affects pathogenesis. J. Virol. 2007, 81(3):1274-1287.
37. Goebel S.J., Taylor J., Masters P.S. The 3' cis-acting genomic replication element of the severe acute respiratory syndrome coronavirus can function in the murine coronavirus genome. J. Virol. 2004, 78(14):7846-7851.
38. Gorbalenya A.E., Enjuanes L., Ziebuhr J., Snijder E.J. Nidovirales: evolving the largest RNA virus genome. Virus Res. 2006, 117(1):17-37.
39. Gosert R., Kanjanahaluethai A., Egger D., Bienz K., Baker S.C. RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. J. Virol. 2002, 76(8):3697-3708.
40. Grossoehme N.E., Li L., Keane S.C., Liu P., Dann C.E., Leibowitz J.L., Giedroc D.P. Coronavirus N protein N-terminal domain (NTD) specifically binds the transcriptional regulatory sequence (TRS) and melts TRS-cTRS RNA duplexes. J. Mol. Biol. 2009, 394(3):544-557.
41. Guan B.J., Su Y.P., Wu H.Y., Brian D.A. Genetic evidence of a long-range RNA-RNA interaction between the genomic 5' untranslated region and the nonstructural protein 1 coding region in murine and bovine coronaviruses. J. Virol. 2012, 86(8):4631-4643.
42. Guan B.J., Wu H.Y., Brian D.A. An optimal cis-replication stem-loop IV in the 5' untranslated region of the mouse coronavirus genome extends 16 nucleotides into open reading frame 1. J. Virol. 2011, 85(11):5593-5605.
43. Gustin K.M., Guan B.J., Dziduszko A., Brian D.A. Bovine coronavirus nonstructural protein 1 (p28) is an RNA binding protein that binds terminal genomic cis-replication elements. J. Virol. 2009, 83(12):6087-6097.
44. Hiscox J.A., Mawditt K.L., Cavanagh D., Britton P. Investigation of the control of coronavirus subgenomic mRNA transcription by using T7-generated negative-sense RNA transcripts. J. Virol. 1995, 69:6219-6227.
45. Hofmann H., Pyrc K., van der Hoek L., Geier M., Berkhout B., Pöhlmann S. Human coronavirus NL63 employs the severe acute respiratory syndrome coronavirus receptor for cellular entry. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(22):7988-7993.
46. Holmes K.V., Lai M.C. Coronaviridae: the viruses and their replication. Virology 1996, vol. 1:1075-1093. Lippincott-Raven, Philadelphia.
47. 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(15):6911-6921.
48. 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(10):7567-7578.
49. Huang P., Lai M.M. 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(11):9110-9116.
50. 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(11):5009-5017.
51. Hurst K.R., Koetzner C.A., Masters P.S. Identification of in vivo-interacting domains of the murine coronavirus nucleocapsid protein. J. Virol. 2009, 83(14):7221-7234.
52. Hurst K.R., Kuo L., Koetzner C.A., Ye R., Hsue B., Masters P.S. A major determinant for membrane protein interaction localizes to the carboxy-terminal domain of the mouse coronavirus nucleocapsid protein. J. Virol. 2005, 79(21):13285-13297.
53. Hurst K.R., Ye R., Goebel S.J., Jayaraman P., Masters P.S. An interaction between the nucleocapsid protein and a component of the replicase-transcriptase complex is crucial for the infectivity of coronavirus genomic RNA. J. Virol. 2010, 84(19):10276-10288.
54. Imbert I., Guillemot J.C., Bourhis J.M., Bussetta C., Coutard B., Egloff M.P., Ferron F., Gorbalenya A.E., Canard B. A second, non-canonical RNA-dependent RNA polymerase in SARS coronavirus. EMBO J. 2006, 25(20):4933-4942.
55. Ivanov K.A., Ziebuhr J. Human coronavirus 229E nonstructural protein 13: characterization of duplex-unwinding, nucleoside triphosphatase, and RNA 5'-triphosphatase activities. J. Virol. 2004, 78(14):7833-7838.
56. Johnson R.F., Feng M., Liu P., Millership J.J., Yount B., Baric R.S., Leibowitz J.L. Effect of mutations in the mouse hepatitis virus 3'(+)42 protein binding element on RNA replication. J. Virol. 2005, 79(23):14570-14585.
57. Kang H., Feng M., Schroeder M.E., Giedroc D.P., Leibowitz J.L. Putative cis-acting stem-loops in the 5' untranslated region of the severe acute respiratory syndrome coronavirus can substitute for their mouse hepatitis virus counterparts. J. Virol. 2006, 80(21):10600-10614.
58. Kang H., Feng M., Schroeder M.E., Giedroc D.P., Leibowitz J.L. Stem-loop 1 in the 5' UTR of the SARS coronavirus can substitute for its counterpart in mouse hepatitis virus. Adv. Exp. Med. Biol. 2006, 581:105-108.
59. Keane S.C., Liu P., Leibowitz J.L., Giedroc D.P. Functional transcriptional regulatory sequence (TRS) RNA binding and helix destabilizing determinants of murine hepatitis virus (MHV) nucleocapsid (N) protein. J. Biol. Chem. 2012, 287(10):7063-7073.
60. Kim Y.N., Jeong Y.S., Makino S. Analysis of cis-acting sequences essential for coronavirus defective interfering RNA replication. Virology 1993, 197(1):53-63.
61. Kim Y.N., Makino S. Characterization of a murine coronavirus defective interfering RNA internal cis-acting replication signal. J. Virol. 1995, 69(8):4963-4971.
62. Knoops K., Kikkert M., Worm S.H., Zevenhoven-Dobbe J.C., van der Meer Y., Koster A.J., Mommaas A.M., Snijder E.J. SARS-coronavirus replication is supported by a reticulovesicular network of modified endoplasmic reticulum. PLoS Biol. 2008, 6(9):e226.
63. Kuo L., Masters P.S. The small envelope protein E is not essential for murine coronavirus replication. J. Virol. 2003, 77(8):4597-4608.
64. Kuo L., Masters P.S. Functional analysis of the murine coronavirus genomic RNA packaging signal. J. Virol. 2013, 87(9):5182-5192.
65. Lai M.M. RNA-protein interactions in the regulation of coronavirus RNA replication and transcription. Biol. Chem. 1997, 378(6):477-481.
66. Lai M.M. Cellular factors in the transcription and replication of viral RNA genomes: a parallel to DNA-dependent RNA transcription. Virology 1998, 244(1):1-12.
67. Lai M.M., Baric R.S., Brayton P.R., Stohlman S.A. 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. 1984, 81(12):3626-3630.
68. Lai M.M., Patton C.D., Baric R.S., Stohlman S.A. Presence of leader sequences in the mRNA of mouse hepatitis virus. J. Virol. 1983, 46(3):1027-1033.
69. Laing C., Schlick T. Analysis of four-way junctions in RNA structures. J. Mol. Biol. 2009, 390(3):547-559.
70. Lee C.W., Li L., Giedroc D.P. The solution structure of coronaviral stem-loop 2 (SL2) reveals a canonical CUYG tetraloop fold. FEBS Lett. 2011, 585:1049-1053.
71. 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(2):567-582.
72. Leibowitz J.L., Wilhelmsen K.C., Bond C.W. The virus-specific intracellular RNA species of two murine coronaviruses: MHV-a59 and MHV-JHM. Virology 1981, 114(1):39-51.
73. Li H.P., Huang P., Park S., Lai M.M. 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(1):772-777.
74. Li H.P., Zhang X., Duncan R., Comai L., Lai M.M. Heterogeneous nuclear ribonucleoprotein A1 binds to the transcription-regulatory region of mouse hepatitis virus RNA. Proc. Natl. Acad. Sci. U. S. A. 1997, 94(18):9544-9549.
75. Li L., Kang H., Liu P., Makkinje N., Williamson S.T., Leibowitz J.L., Giedroc D.P. Structural lability in stem-loop 1 drives a 5' UTR-3' UTR interaction in coronavirus replication. J. Mol. Biol. 2008, 377(3):790-803.
76. Li W., Moore M.J., Vasilieva N., Sui J., Wong S.K., Berne M.A., Somasundaran M., Sullivan J.L., Luzuriaga K., Greenough T.C., Choe H., Farzan M. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 2003, 426(6965):450-454.
77. 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(10):6110-6118.
78. 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(12):8131-8140.
79. Liu P., Leibowitz J.L. RNA higher-order structures within the Coronavirus 5' and 3' untranslated regions and their roles in viral replication. Molecular biology of the SARS-Coronavirus 2010, 47-61. Springer, Heidelberg/Dordrecht/London/New York. S.K. Lal (Ed.).
80. Liu P., Li L., Keane S.C., Yang D., Leibowitz J.L., Giedroc D.P. Mouse hepatitis virus stem-loop 2 adopts a uYNMG(U)a-like tetraloop structure that is highly functionally tolerant of base substitutions. J. Virol. 2009, 83(23):12084-12093.
81. Liu P., Li L., Millership J.J., Kang H., Leibowitz J.L., Giedroc D.P. A U-turn motif-containing stem-loop in the coronavirus 5' untranslated region plays a functional role in replication. RNA 2007, 13(5):763-780.
82. Liu P., Yang D., Carter K., Masud F., Leibowitz J.L. Functional analysis of the stem loop S3 and S4 structures in the coronavirus 3'UTR. Virology 2013, 443(1):40-47.
83. 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(24):12105-12113.
84. 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(1):74-85.
85. Liu Y., Wimmer E., Paul A.V. Cis-acting RNA elements in human and animal plus-strand RNA viruses. Biochim. Biophys. Acta 2009, 1789(9-10):495-517.
86. Luytjes W., Gerritsma H., Spaan W.J. Replication of synthetic defective interfering RNAs derived from coronavirus mouse hepatitis virus-A59. Virology 1996, 216(1):174-183.
87. Maeda J., Repass J.F., Maeda A., Makino S. Membrane topology of coronavirus E protein. Virology 2001, 281(2):163-169.
88. 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(2):329-336.
89. 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(11):6031-6041.
90. Makino S., Shieh C.K., Soe L.H., Baker S.C., Lai M.M. Primary structure and translation of a defective interfering RNA of murine coronavirus. Virology 1988, 166(2):550-560.
91. Makino S., Yokomori K., Lai M.M. Analysis of efficiently packaged defective interfering RNAs of murine coronavirus: localization of a possible RNA-packaging signal. J. Virol. 1990, 64(12):6045-6053.
92. Marra M.A., Jones S.J., Astell C.R., Holt R.A., Brooks-Wilson A., Butterfield Y.S., Khattra J., Asano J.K., Barber S.A., Chan S.Y., Cloutier A., Coughlin S.M., Freeman D., Girn N., Griffith O.L., Leach S.R., Mayo M., McDonald H., Montgomery S.B., Pandoh P.K., Petrescu A.S., Robertson A.G., Schein J.E., Siddiqui A., Smailus D.E., Stott J.M., Yang G.S., Plummer F., Andonov A., Artsob H., Bastien N., Bernard K., Booth T.F., Bowness D., Czub M., Drebot M., Fernando L., Flick R., Garbutt M., Gray M., Grolla A., Jones S., Feldmann H., Meyers A., Kabani A., Li Y., Normand S., Stroher U., Tipples G.A., Tyler S., Vogrig R., Ward D., Watson B., Brunham R.C., Krajden M., Petric M., Skowronski D.M., Upton C., Roper R.L. The genome sequence of the SARS-associated coronavirus. Science 2003, 300(5624):1399-1404.
93. Masters P.S. The molecular biology of coronaviruses. Adv. Virus Res. 2006, 66:193-292.
94. Mateos-Gomez P.A., Morales L., Zuniga S., Enjuanes L., Sola I. Long-distance RNA-RNA interactions in the coronavirus genome form high-order structures promoting discontinuous RNA synthesis during transcription. J. Virol. 2013, 87(1):177-186.
95. Mathews D.H., Disney M.D., Childs J.L., Schroeder S.J., Zuker M., Turner D.H. Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proc. Natl. Acad. Sci. U. S. A. 2004, 101(19):7287-7292.
96. McRoy W.C., Baric R.S. Amino acid substitutions in the S2 subunit of mouse hepatitis virus variant V51 encode determinants of host range expansion. J. Virol. 2008, 82(3):1414-1424.
97. 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(2):495-507.
98. Minskaia E., Hertzig T., Gorbalenya A.E., Campanacci V., Cambillau C., Canard B., Ziebuhr J. Discovery of an RNA virus 3'→5' exoribonuclease that is critically involved in coronavirus RNA synthesis. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(13):5108-5113.
99. Morales L., Mateos-Gomez P.A., Capiscol C., del Palacio L., Enjuanes L., Sola I. Transmissible gastroenteritis coronavirus genome packaging signal is located at the 5' end of the genome and promotes viral RNA incorporation into virions in a replication-independent process. J. Virol. 2013, 87(21):11579-11590.
100. Murray R.S., Brown B., Brian D., Cabirac G.F. Detection of coronavirus RNA and antigen in multiple sclerosis brain. Ann. Neurol. 1992, 31(5):525-533.
101. Nanda S.K., Johnson R.F., Liu Q., Leibowitz J.L. Mitochondrial HSP70, HSP40, and HSP60 bind to the 3' untranslated region of the Murine hepatitis virus genome. Arch. Virol 2004, 149(1):93-111.
102. Nanda S.K., Leibowitz J.L. Mitochondrial aconitase binds to the 3' untranslated region of the mouse hepatitis virus genome. J. Virol. 2001, 75(7):3352-3362.
103. Narayanan K., Chen C.J., Maeda J., Makino S. Nucleocapsid-independent specific viral RNA packaging via viral envelope protein and viral RNA signal. J. Virol. 2003, 77(5):2922-2927.
104. Nash T.C., Buchmeier M.J. Entry of mouse hepatitis virus into cells by endosomal and nonendosomal pathways. Virology 1997, 233(1):1-8.
105. 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(Pt 1):181-188.
106. Pasternak A.O., van den Born E., Spaan W.J., Snijder E.J. The stability of the duplex between sense and antisense transcription-regulating sequences is a crucial factor in arterivirus subgenomic mRNA synthesis. J. Virol. 2003, 77(2):1175-1183.
107. 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(2):471-484.
108. Putics A., Filipowicz W., Hall J., Gorbalenya A.E., Ziebuhr J. ADP-ribose-1-monophosphatase: a conserved coronavirus enzyme that is dispensable for viral replication in tissue culture. J. Virol. 2005, 79(20):12721-12731.
109. Raj V.S., Mou H., Smits S.L., Dekkers D.H., Muller M.A., Dijkman R., Muth D., Demmers J.A., Zaki A., Fouchier R.A., Thiel V., Drosten C., Rottier P.J., Osterhaus A.D., Bosch B.J., Haagmans B.L. Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 2013, 495(7440):251-254.
110. Raman S., Bouma P., Williams G.D., Brian D.A. Stem-loop III in the 5' untranslated region is a cis-acting element in bovine coronavirus defective interfering RNA replication. J. Virol. 2003, 77(12):6720-6730.
111. Raman S., Brian D.A. Stem-loop IV in the 5' untranslated region is a cis-acting element in bovine coronavirus defective interfering RNA replication. J. Virol. 2005, 79(19):12434-12446.
112. Resta S., Luby J.P., Rosenfeld C.R., Siegel J.D. Isolation and propagation of a human enteric coronavirus. Science 1985, 229(4717):978-981.
113. Rota P.A., Oberste M.S., Monroe S.S., Nix W.A., Campagnoli R., Icenogle J.P., Penaranda S., Bankamp B., Maher K., Chen M.H., Tong S., Tamin A., Lowe L., Frace M., DeRisi J.L., Chen Q., Wang D., Erdman D.D., Peret T.C., Burns C., Ksiazek T.G., Rollin P.E., Sanchez A., Liffick S., Holloway B., Limor J., McCaustland K., Olsen-Rasmussen M., Fouchier R., Gunther S., Osterhaus A.D., Drosten C., Pallansch M.A., Anderson L.J., Bellini W.J. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 2003, 300(5624):1394-1399.
114. Rousset S., Moscovici O., Lebon P., Barbet J.P., Helardot P., Mace B., Bargy F., Le Tan V., Chany C. Intestinal lesions containing coronavirus-like particles in neonatal necrotizing enterocolitis: an ultrastructural analysis. Pediatrics 1984, 73(2):218-224.
115. Sawicki S.G., Sawicki D.L. Coronavirus transcription: subgenomic mouse hepatitis virus replicative intermediates function in RNA synthesis. J. Virol. 1990, 64(3):1050-1056.
116. Sawicki S.G., Sawicki D.L. A new model for coronavirus transcription. Adv. Exp. Med. Biol. 1998, 440:215-219.
117. 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(2):288-302.
118. Sethna P.B., Hung S.L., Brian D.A. Coronavirus subgenomic minus-strand RNAs and the potential for mRNA replicons. Proc. Natl. Acad. Sci. U. S. A. 1989, 86(14):5626-5630.
119. 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. U. S. A. 2001, 98(5):2717-2722.
120. Shi S.T., Yu G.Y., Lai M.M. Multiple type A/B heterogeneous nuclear ribonucleoproteins (hnRNPs) can replace hnRNP A1 in mouse hepatitis virus RNA synthesis. J. Virol. 2003, 77(19):10584-10593.
121. Snijder E.J., Bredenbeek P.J., Dobbe J.C., Thiel V., Ziebuhr J., Poon L.L., Guan Y., Rozanov M., Spaan W.J., Gorbalenya A.E. Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage. J. Mol. Biol. 2003, 331(5):991-1004.
122. Sola I., Moreno J.L., Zuniga S., Alonso S., Enjuanes L. Role of nucleotides immediately flanking the transcription-regulating sequence core in coronavirus subgenomic mRNA synthesis. J. Virol. 2005, 79(4):2506-2516.
123. Sonenberg N. mRNA 5' cap binding protein eIF4E and control of cell growth. Translational Control 1996, 245-270. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. J.W.B. Hershey, M.B. M, N. Sonenberg (Eds.).
124. Sonenberg N., Morgan M.A., Merrick W.C., Shatkin A.J. A polypeptide in eukaryotic initiation factors that crosslinks specifically to the 5'-terminal cap in mRNA. Proc. Natl. Acad. Sci. U. S. A. 1978, 75(10):4843-4847.
125. Spaan W.J., Rottier P.J., Horzinek M.C., van der Zeijst B.A. Sequence relationships between the genome and the intracellular RNA species 1, 3, 6, and 7 of mouse hepatitis virus strain A59. J. Virol. 1982, 42(2):432-439.
126. 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(11):5053-5065.
127. Stadler K., Masignani V., Eickmann M., Becker S., Abrignani S., Klenk H.D., Rappuoli R. SARS - beginning to understand a new virus. Nat. Rev. Microbiol. 2003, 1(3):209-218.
128. Stammler S.N., Cao S., Chen S.J., Giedroc D.P. A conserved RNA pseudoknot in a putative molecular switch domain of the 3'-untranslated region of coronaviruses is only marginally stable. RNA 2011, 17(9):1747-1759.
129. 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(11):4288-4295.
130. 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.
131. van der Most R.G., Bredenbeek P.J., Spaan W.J. A domain at the 3' end of the polymerase gene is essential for encapsidation of coronavirus defective interfering RNAs. J. Virol. 1991, 65(6):3219-3226.
132. van der Most R.G., de Groot 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.
133. van Marle G., Dobbe J.C., Gultyaev A.P., Luytjes W., Spaan W.J., Snijder E.J. Arterivirus discontinuous mRNA transcription is guided by base pairing between sense and antisense transcription-regulating sequences. Proc. Natl. Acad. Sci. U. S. A. 1999, 96(21):12056-12061.
134. Wang H., Yang P., Liu K., Guo F., Zhang Y., Zhang G., Jiang C. SARS coronavirus entry into host cells through a novel clathrin- and caveolae-independent endocytic pathway. Cell Res. 2008, 18(2):290-301.
135. Weiss S.R., Hughes S.A., Bonilla P.J., Turner J.D., Leibowitz J.L., Denison M.R. Coronavirus polyprotein processing. Arch. Virol. Suppl. 1994, 9:349-358.
136. Weiss S.R., Leibowitz J.L. Pathogenesis of murine coronavirus infections. Nidoviruses 2007, 259-278. ASM Press, Washington, DC. S. Perlman, T. Gallagher, E.J. Snijder (Eds.).
137. Williams G.D., Chang R.Y., Brian D.A. A phylogenetically conserved hairpin-type 3' untranslated region pseudoknot functions in coronavirus RNA replication. J. Virol. 1999, 73(10):8349-8355.
138. Williams R.K., Jiang G.S., Holmes K.V. Receptor for mouse hepatitis virus is a member of the carcinoembryonic antigen family of glycoproteins. Proc. Natl. Acad. Sci. U. S. A. 1991, 88(13):5533-5536.
139. Wu H.Y., Guan B.J., Su Y.P., Fan Y.H., Brian D.A. Reselection of a genomic upstream open reading frame in mouse hepatitis coronavirus 5'-untranslated-region mutants. J. Virol. 2014, 88(2):846-858.
140. Wu H.Y., Guy J.S., Yoo D., Vlasak R., Urbach E., Brian D.A. Common RNA replication signals exist among group 2 coronaviruses: evidence for in vivo recombination between animal and human coronavirus molecules. Virology 2003, 315(1):174-183.
141. Yang D., Liu P., Giedroc D.P., Leibowitz J. Mouse hepatitis virus stem-loop 4 functions as a spacer element required to drive subgenomic RNA synthesis. J. Virol. 2011, 85(17):9199-9209.
142. Yang D., Liu P., Wudeck E.V., Giedroc D.P., Leibowitz J.L. SHAPE analysis of the RNA secondary structure of the Mouse Hepatitis Virus 5' untranslated region and N-terminal nsp1 coding sequences. Virology 2015, 475:15-27.
143. Yeager C.L., Ashmun R.A., Williams R.K., Cardellichio C.B., Shapiro L.H., Look A.T., Holmes K.V. Human aminopeptidase N is a receptor for human coronavirus. Nature 1992, 357:420-422.
144. Yount B., Curtis K.M., Baric R.S. Strategy for systematic assembly of large RNA and DNA genomes: transmissible gastroenteritis virus model. J. Virol. 2000, 74(22):10600-10611.
145. 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(1):128-138.
146. 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(4):2016-2023.
147. Zaki A.M., van Boheemen S., Bestebroer T.M., Osterhaus A.D., Fouchier R.A. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N. Engl. J. Med. 2012, 367(19):1814-1820.
148. Ziebuhr J., Snijder E.J., Gorbalenya A.E. Virus-encoded proteinases and proteolytic processing in the Nidovirales. J. Gen. Virol. 2000, 81(Pt 4):853-879.
149. Zuniga S., Cruz J.L., Sola I., Mateos-Gomez P.A., Palacio L., Enjuanes L. Coronavirus nucleocapsid protein facilitates template switching and is required for efficient transcription. J. Virol. 2010, 84(4):2169-2175.
150. Zuniga S., Sola I., Alonso S., Enjuanes L. Sequence motifs involved in the regulation of discontinuous coronavirus subgenomic RNA synthesis. J. Virol. 2004, 78(2):980-994.
151. Zuniga S., Sola I., Moreno J.L., Sabella P., Plana-Duran J., Enjuanes L. Coronavirus nucleocapsid protein is an RNA chaperone. Virology 2007, 357(2):215-227.
152. Zust R., Miller T.B., Goebel S.J., Thiel V., Masters P.S. Genetic interactions between an essential 3' cis-acting RNA pseudoknot, replicase gene products, and the extreme 3' end of the mouse coronavirus genome. J. Virol. 2008, 82(3):1214-1228.