Coronavirus N Protein N-Terminal Domain (NTD) Specifically Binds the Transcriptional Regulatory Sequence (TRS) and Melts TRS-cTRS RNA Duplexes

Journal of Molecular Biology

Volumn 394, Issue 3, 2009, Pages 544-557

  Grossoehme, Nicholas E ^a   Li, Lichun ^b   Keane, Sarah C ^a   Liu, Pinghua ^c   Dann III, Charles E ^a   Leibowitz, Julian L ^c   Giedroc, David P ^a  

^a INDIANA UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c TEXAS A AND M UNIVERSITY SYSTEM   (United States)

Author keywords

coronavirus replication; nucleocapsid protein; protein RNA interactions; SARS coronavirus; transcriptional regulatory sequence

Indexed keywords

ALANINE; AROMATIC CARBOXYLIC ACID; DOUBLE STRANDED RNA; GENOMIC RNA; NUCLEIC ACID BASE; NUCLEOCAPSID PROTEIN; SINGLE STRANDED RNA; TYROSINE;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING KINETICS; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CORONAVIRUS; GENE MUTATION; MURINE HEPATITIS CORONAVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN RNA BINDING; REGULATORY RNA SEQUENCE; RNA SYNTHESIS; RNA TRANSCRIPTION; STOICHIOMETRY; STRUCTURE ANALYSIS; TRANSCRIPTION REGULATION; VIRUS GENOME; VIRUS REPLICATION;

CORONAVIRUS; HEPATITIS A VIRUS; MURINE HEPATITIS VIRUS; SARS CORONAVIRUS;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CRYSTALLOGRAPHY, X-RAY; KINETICS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MURINE HEPATITIS VIRUS; MUTAGENESIS, SITE-DIRECTED; NUCLEIC ACID CONFORMATION; NUCLEOCAPSID PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; REGULATORY ELEMENTS, TRANSCRIPTIONAL; RNA, VIRAL; SARS VIRUS; SEQUENCE HOMOLOGY, AMINO ACID; STATIC ELECTRICITY; THERMODYNAMICS;

EID: 70350728646     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.09.040     Document Type: Article

References (59)

1. Zhong N.S., Zheng B.J., Li Y.M., Poon L.L.M., Xie Z.H., Chan K.H., et al. Epidemiology and cause of severe acute respiratory syndrome (SARS) in Guangdong, People's Republic of China, in February, 2003. The Lancet 362 (2003) 1353-1358
2. Pyrc K., Jebbink M.F., Berkhout B., and van der Hoek L. Genome structure and transcriptional regulation of human coronavirus NL63. Virol. J. 1 (2004) 7
3. Woo P.C., Lau S.K., Chu C.M., Chan K.H., Tsoi H.W., Huang Y., et al. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J. Virol. 79 (2005) 884-895
4. De Albuquerque N., Baig E., Ma X., Zhang J., He W., Rowe A., et al. Murine hepatitis virus strain 1 produces a clinically relevant model of severe acute respiratory syndrome in A/J mice. J. Virol. 80 (2006) 10382-10394
5. Pasternak A.O., Spaan W.J.M., and Snijder E.J. Nidovirus transcription: how to make sense...?. J. Gen. Virol. 87 (2006) 1403-1421
6. Sawicki S.G., and Sawicki D.L. A new model for coronavirus transcription. Adv. Exp. Med. Biol. 440 (1998) 215-219
7. Zuniga S., Sola I., Alonso S., and Enjuanes L. Sequence motifs involved in the regulation of discontinuous coronavirus subgenomic RNA synthesis. J. Virol. 78 (2004) 980-994
8. Li L., Kang H., Liu P., Makkinje N., Williamson S.T., Leibowitz J.L., et al. Structural lability in stem-loop 1 drives a 5′ UTR-3′ UTR interaction in coronavirus replication. J. Mol. Biol. 377 (2008) 790-803
9. Calvo E., Escors D., Lopez J.A., Gonzalez J.M., Alvarez A., Arza E., et al. Phosphorylation and subcellular localization of transmissible gastroenteritis virus nucleocapsid protein in infected cells. J. Gen. Virol. 86 (2005) 2255-2267
10. White T.C., Yi Z., and Hogue B.G. Identification of mouse hepatitis coronavirus A59 nucleocapsid protein phosphorylation sites. Virus Res. 126 (2007) 139-148
11. Barcena M., Oostergetel G.T., Bartelink W., Faas F.G., Verkleij A., Rottier P.J., et al. Cryo-electron tomography of mouse hepatitis virus: Insights into the structure of the coronavirion. Proc. Natl Acad. Sci. USA 106 (2009) 582-587
12. Baric R.S., Nelson G.W., Fleming J.O., Deans R.J., Keck J.G., Casteel N., et al. Interactions between coronavirus nucleocapsid protein and viral RNAs: implications for viral transcription. J. Virol. 62 (1988) 4280-4287
13. Eleouet J.F., Slee E.A., Saurini F., Castagne N., Poncet D., Garrido C., et al. The viral nucleocapsid protein of transmissible gastroenteritis coronavirus (TGEV) is cleaved by caspase-6 and-7 during TGEV-induced apoptosis. J. Virol. 74 (2000) 3975-3983
14. Stohlman S.A., Baric R.S., Nelson G.N., Soe L.H., Welter L.M., and Deans R.J. Specific interaction between coronavirus leader RNA and nucleocapsid protein. J. Virol. 62 (1988) 4288-4295
15. Nelson G.W., Stohlman S.A., and Tahara S.M. High affinity interaction between nucleocapsid protein and leader/intergenic sequence of mouse hepatitis virus RNA. J. Gen. Virol. 81 (2000) 181-188
16. Compton S.R., Rogers D.B., Holmes K.V., Fertsch D., Remenick J., and McGowan J.J. In vitro replication of mouse hepatitis virus strain A59. J. Virol. 61 (1987) 1814-1820
17. Thiel V., Ivanov K.A., Putics A., Hertzig T., Schelle B., Bayer S., et al. Mechanisms and enzymes involved in SARS coronavirus genome expression. J. Gen. Virol. 84 (2003) 2305-2315
18. Zúñiga S., Sola I., Moreno J.L., Sabella P., Plana-Durán J., and Enjuanes L. Coronavirus nucleocapsid protein is an RNA chaperone. Virology 357 (2007) 215-227
19. Huang M., Maynard A., Turpin J.A., Graham L., Janini G.M., Covell D.G., et al. Anti-HIV agents that selectively target retroviral nucleocapsid protein zinc fingers without affecting cellular zinc finger proteins. J. Med. Chem. 41 (1998) 1371-1381
20. Chang C.-k., Sue S.-C., Yu T.-h., Hsieh C.-M., Tsai C.-K., Chiang Y.-C., et al. Modular organization of SARS coronavirus nucleocapsid protein. J. Biomed. Sci. 13 (2006) 59-72
21. Surjit M., Liu B., Kumar P., Chow V.T.K., and Lal S.K. The nucleocapsid protein of the SARS coronavirus is capable of self-association through a C-terminal 209 amino acid interaction domain. Biochem. Biophys. Res. Commun. 317 (2004) 1030-1036
22. Yu I.-M., Oldham M.L., Zhang J., and Chen J. Crystal Structure of the Severe Acute Respiratory Syndrome (SARS) Coronavirus nucleocapsid protein dimerization domain reveals evolutionary linkage between Corona-and Arteriviridae. J. Biol. Chem. 281 (2006) 17134-17139
23. Chang C.-K., Hsu Y.-L., Chang Y.-H., Chao F.-A., Wu M.-C., Huang Y.-S., et al. multiple nucleic acid binding sites and intrinsic disorder of severe acute respiratory syndrome coronavirus nucleocapsid protein: Implications for ribonucleocapsid protein packaging. J. Virol. 83 (2009) 2255-2264
24. Jayaram H., Fan H., Bowman B.R., Ooi A., Jayaram J., Collisson E.W., et al. X-ray structures of the N-and C-terminal domains of a coronavirus nucleocapsid protein: implications for nucleocapsid formation. J. Virol. 80 (2006) 6612-6620
25. Takeda M., Chang C.-k., Ikeya T., Güntert P., Chang Y.-h., Hsu Y.-l., et al. Solution structure of the C-terminal dimerization domain of SARS Coronavirus nucleocapsid proteins solved by the SAIL-NMR method. J. Mol. Biol. 380 (2008) 608-622
26. Chen C.-Y., Chang C.-k., Chang Y.-W., Sue S.-C., Bai H.-I., Riang L., et al. Structure of the SARS coronavirus nucleocapsid protein RNA-binding dimerization domain suggests a mechanism for helical packaging of viral RNA. J. Mol. Biol. 368 (2007) 1075-1086
27. Huang Q., Yu L., Petros A.M., Gunasekera A., Liu Z., Xu N., et al. Structure of the N-terminal RNA-binding domain of the SARS CoV nucleocapsid protein. Biochemistry 43 (2004) 6059-6063
28. Fan H., Ooi A., Tan Y.W., Wang S., Fang S., Liu D.X., et al. The nucleocapsid protein of coronavirus infectious bronchitis virus: Crystal structure of its N-terminal domain and multimerization properties. Structure 13 (2005) 1859-1868
29. Luo H., Ye F., Chen K., Shen X., and Jiang H. SR-Rich motif plays a pivotal role in recombinant SARS Coronavirus nucleocapsid protein multimerization. Biochemistry 44 (2005) 15351-15358
30. Hurst K.R., Koetzner C.A., and Masters P.S. Identification of in vivo-interacting domains of the murine coronavirus nucleocapsid protein. J. Virol. 83 (2009) 7221-7234
31. Almazan F., Gonzalez J.M., Penzes Z., Izeta A., Calvo E., Plana-Duran J., et al. Engineering the largest RNA virus genome as an infectious bacterial artificial chromosome. Proc. Natl Acad. Sci. USA 97 (2000) 5516-5521
32. Stalcup R.P., Baric R.S., and Leibowitz J.L. Genetic complementation among three panels of mouse hepatitis virus gene 1 mutants. Virology 241 (1998) 112-121
33. Mascotti D.P., and Lohman T.M. Thermodynamic extent of counterion release upon binding oligolysines to single-stranded nucleic acids. Proc. Natl Acad. Sci. USA 87 (1990) 3142-3146
34. Chen X., Agarwal A., and Giedroc D.P. Structural and functional heterogeneity among the zinc fingers of human MRE-binding transcription factor-1. Biochemistry 37 (1998) 11152-11161
35. Record M.T., Ha J.-H., Fisher M.A., and Robert T.S. Analysis of equilibrium and kinetic measurements to determine thermodynamic origins of stability and specificity and mechanism of formation of site-specific complexes between proteins and helical DNA. Methods Enzymol. 208 (1991) 291-343
36. Saikatendu K.S., Joseph J.S., Subramanian V., Neuman B.W., Buchmeier M.J., Stevens R.C., et al. Ribonucleocapsid formation of severe acute respiratory syndrome coronavirus through molecular action of the N-terminal domain of N protein. J. Virol. 81 (2007) 3913-3921
37. Rota P.A., Oberste M.S., Monroe S.S., Nix W.A., Campagnoli R., Icenogle J.P., et al. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300 (2003) 1394-1399
38. Marra M.A., Jones S.J.M., Astell C.R., Holt R.A., Brooks-Wilson A., Butterfield Y.S.N., et al. The genome sequence of the SARS-associated coronavirus. Science 300 (2003) 1399-1404
39. Yount B., Roberts R.S., Lindesmith L., and Baric R.S. Rewiring the severe acute respiratory syndrome coronavirus (SARS-CoV) transcription circuit: Engineering a recombination-resistant genome. Proc. Natl Acad. Sci. USA 103 (2006) 12546-12551
40. Liu P., Li L., Millership J.J., Kang H., Leibowitz J.L., and Giedroc D.P. A U-turn motif-containing stem-loop in the coronavirus 5′ untranslated region plays a functional role in replication. RNA 13 (2007) 763-780
41. Myong S., Cui S., Cornish P.V., Kirchhofer A., Gack M.U., Jung J.U., et al. Cytosolic Viral Sensor RIG-I is a 5′-triphosphate-dependent translocase on double-stranded RNA. Science 323 (2009) 1070-1074
42. Auweter S.D., Oberstrass F.C., and Allain F.H.-T. Sequence-specific binding of single-stranded RNA: is there a code for recognition?. Nucleic Acids Res. 34 (2006) 4943-4959
43. Spriggs S., Garyu L., Connor R., and Summers M.F. Potential intra-and intermolecular interactions involving the unique-5′ region of the HIV-1 5′-UTR. Biochemistry 47 (2008) 13064-13073
44. Tan Y.W., Fang S., Fan H., Lescar J., and Liu D.X. Amino acid residues critical for RNA-binding in the N-terminal domain of the nucleocapsid protein are essential determinants for the infectivity of coronavirus in cultured cells. Nucleic Acids Res. 34 (2006) 4816-4825
45. Narayanan K., Kim K.H., and Makino S. Characterization of N protein self-association in coronavirus ribonucleoprotein complexes. Virus Res. 98 (2003) 131-140
46. Hsieh P.-K., Chang S.C., Huang C.-C., Lee T.-T., Hsiao C.-W., Kou Y.-H., et al. Assembly of Severe acute respiratory syndrome coronavirus RNA packaging signal into virus-like particles is nucleocapsid dependent. J. Virol. 79 (2005) 13848-13855
47. Butcher S.J., Grimes J.M., Makeyev E.V., Bamford D.H., and Stuart D.I. A mechanism for initiating RNA-dependent RNA polymerization. Nature 410 (2001) 235-240
48. Lesburg C.A., Cable M.B., Ferrari E., Hong Z., Mannarino A.F., and Weber P.C. Crystal structure of the RNA-dependent RNA polymerase from hepatitis C virus reveals a fully encircled active site. Nat. Struct. Mol. Biol. 6 (1999) 937-943
49. Chinnaswamy S., Yarbrough I., Palaninathan S., Kumar C.T.R., Vijayaraghavan V., Demeler B., et al. A locking mechanism regulates RNA synthesis and host protein interaction by the hepatitis C virus polymerase. J. Biol. Chem. 283 (2008) 20535-20546
50. Schelle B., Karl N., Ludewig B., Siddell S.G., and Thiel V. Selective replication of coronavirus genomes that express nucleocapsid protein. J. Virol. 79 (2005) 6620-6630
51. van Hemert M.J., van den Worm S.H.E., Knoops K.v., Mommaas A.M., Gorbalenya A.E., and Snijder E.J. SARS-coronavirus replication/transcription complexes are membrane-protected and need a host factor for activity in vitro. PLoS Pathog. e1000054 (2008) 4
52. Nixon P.L., Rangan A., Kim Y.G., Rich A., Hoffman D.W., Hennig M., et al. Solution structure of a luteoviral P1-P2 frameshifting mRNA pseudoknot. J. Mol. Biol. 322 (2002) 621-633
53. Sheffield P., Garrard S., and Derewenda Z. Overcoming expression and purification problems of RhoGDI using a family of "parallel" expression vectors. Prot. Express Purif. 15 (1999) 34-39
54. VanZile M.L., Cosper N.J., Scott R.A., and Giedroc D.P. The zinc metalloregulatory protein Synechococcus PCC7942 SmtB binds a single zinc ion per monomer with high affinity in a tetrahedral coordination geometry. Biochemistry 39 (2000) 11818-11829
55. Painter J., and Merritt E.A. TLSMD web server for the generation of multi-group TLS models. J. Appl. Crystallogr. 39 (2006) 109-111
56. Kuzmic P. Program DYNAFIT for the analysis of enzyme kinetic data: application to HIV proteinase. Anal. Biochem. 237 (1996) 260-273
57. MicroCal. MicroCalorimeter User's Manual (2002), Northampton, MA
58. Yount B., Denison M.R., Weiss S.R., and Baric R.S. Systematic assembly of a full-length infectious cDNA of mouse hepatitis virus strain A59. J. Virol. 76 (2002) 11065-11078
59. Johnson R.F., Feng M., Liu P., Millership J.J., Yount B., Baric R.S., et al. The effect of mutations in the mouse hepatitis virus 3′(+)42 protein binding element on RNA replication. J. Virol. 79 (2005) 14570-14585