Characterization of a critical interaction between the coronavirus nucleocapsid protein and nonstructural protein 3 of the viral replicase-transcriptase complex

Journal of Virology

Volumn 87, Issue 16, 2013, Pages 9159-9172

  Hurst, Kelley R ^a   Koetzner, Cheri A ^a   Masters, Paul S ^a  

^a WADSWORTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC RNA; NONSTRUCTURAL PROTEIN 3; NUCLEOCAPSID PROTEIN; REPLICASE; TRANSCRIPTASE; UBIQUITIN; UBIQUITIN LIKE DOMAIN; UNCLASSIFIED DRUG; VIRUS ENZYME;

ARTICLE; BINDING AFFINITY; BINDING SITE; CHIMERA; COMPLEX FORMATION; CONTROLLED STUDY; CORONAVIRUS; ENZYME ASSAY; GENOME ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; VIRUS GENOME; VIRUS IDENTIFICATION; VIRUS INFECTIVITY;

ANIMALS; CELL LINE; CORONAVIRUS, BOVINE; MICE; MURINE HEPATITIS VIRUS; NUCLEOCAPSID PROTEINS; PROTEIN INTERACTION MAPPING; RECOMBINATION, GENETIC; TRANSGENES; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84881243429     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01275-13     Document Type: Article

References (72)

1. Masters PS. 2006. The molecular biology of coronaviruses. Adv. Virus Res. 66:193-292.
2. Perlman S, Netland J. 2009. Coronaviruses post-SARS: update on replication and pathogenesis. Nat. Rev. Microbiol. 7:439-450.
3. van Boheemen S, de Graaf M, Lauber C, Bestebroer TM, Raj VS, Zaki AM, Osterhaus AD, Haagmans BL, Gorbalenya AE, Snijder EJ, Fouchier RA. 2012. Genomic characterization of a newly discovered coronavirus associated with acute respiratory distress syndrome in humans. mBio 3(6):e00473-12. doi:10.1128/mBio.00473-12.
4. de Groot RJ, Baker SC, Baric RS, Brown CS, Drosten C, Enjuanes L, Fouchier RA, Galiano M, Gorbalenya AE, Memish Z, Perlman S, Poon LL, Snijder EJ, Stephens GM, Woo PC, Zaki AM, Zambon M, Ziebuhr J. 15 May 2013. Middle East respiratory syndrome coronavirus (MERSCoV); announcement of the Coronavirus Study Group. J. Virol. doi:10 .1128/JVI.01244-13.
5. Koetzner CA, Parker MM, Ricard CS, Sturman LS, Masters PS. 1992. Repair and mutagenesis of the genome of a deletion mutant of the coronavirus mouse hepatitis virus by targeted RNA recombination. J. Virol. 66:1841-1848.
6. Kuo L, Masters PS. 2002. Genetic evidence for a structural interaction between the carboxy termini of the membrane and nucleocapsid proteins of mouse hepatitis virus. J. Virol. 76:4987-4999.
7. Hurst KR, Kuo L, Koetzner CA, Ye R, Hsue B, Masters PS. 2005. A major determinant for membrane protein interaction localizes to the carboxy-terminal domain of the mouse coronavirus nucleocapsid protein. J. Virol. 79:13285-13297.
8. Hurst KR, Koetzner CA, Masters PS. 2009. Identification of in vivointeracting domains of the murine coronavirus nucleocapsid protein. J. Virol. 83:7221-7234.
9. Grossoehme NE, Li L, Keane SC, Liu P, Dann CE III, Leibowitz JL, Giedroc DP. 2009. Coronavirus N protein N-terminal domain (NTD) specifically binds the transcriptional regulatory sequence (TRS) and melts TRS-cTRS RNA duplexes. J. Mol. Biol. 394:544-557.
10. Ma Y, Tong X, Xu X, Li X, Lou Z, Rao Z. 2010. Structures of the Nand C-terminal domains of MHV-A59 nucleocapsid protein corroborate a conserved RNA-protein binding mechanism in coronavirus. Protein Cell 1:688-697.
11. Chang CK, Hsu YL, Chang YH, Chao FA, Wu MC, Huang YS, Hu CK, Huang TH. 2009. Multiple nucleic acid binding sites and intrinsic disorder of severe acute respiratory syndrome coronavirus nucleocapsid protein: implications for ribonucleocapsid protein packaging. J. Virol. 83: 2255-2264.
12. Verma S, Bednar V, Blount A, Hogue BG. 2006. Identification of functionally important negatively charged residues in the carboxy end of mouse hepatitis coronavirus A59 nucleocapsid protein. J. Virol. 80:4344-4355.
13. Verma S, Lopez LA, Bednar V, Hogue BG. 2007. Importance of the penultimate positive charge in mouse hepatitis coronavirus A59 membrane protein. J. Virol. 81:5339-5348.
14. Almazán F, Galán C, Enjuanes L. 2004. The nucleoprotein is required for efficient coronavirus genome replication. J. Virol. 78:12683-12688.
15. Zúñiga S, Cruz JL, Sola I, Mateos-Gómez PA, Palacio L, Enjuanes L. 2010. Coronavirus nucleocapsid protein facilitates template switching and is required for efficient transcription. J. Virol. 84:2169-2175.
16. Thiel V, Herold J, Schelle B, Siddell SG. 2001. Viral replicase gene products suffice for coronavirus discontinuous transcription. J. Virol. 75: 6676-6681.
17. Schelle B, Karl N, Ludewig B, Siddell SG, Thiel V. 2005. Selective replication of coronavirus genomes that express nucleocapsid protein. J. Virol. 79:6620-6630.
18. Denison MR, Spaan WJ, van der Meer Y, Gibson CA, Sims AC, Prentice E, Lu XT. 1999. 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. 73:6862-6871.
19. van der Meer Y, Snijder EJ, Dobbe JC, Schleich S, Denison MR, Spaan WJ, Locker JK. 1999. Localization of mouse hepatitis virus nonstructural proteins and RNA synthesis indicates a role for late endosomes in viral replication. J. Virol. 73:7641-7657.
20. Sims AC, Ostermann J, Denison MR. 2000. Mouse hepatitis virus replicase proteins associate with two distinct populations of intracellular membranes. J. Virol. 74:5647-5654.
21. Stertz S, Reichelt M, Spiegel M, Kuri T, Martínez-Sobrido L, GarcíaSastre A, Weber F, Kochs G. 2007. The intracellular sites of early replication and budding of SARS-coronavirus. Virology 361:304-315.
22. Verheije MH, Hagemeijer MC, Ulasli M, Reggiori F, Rottier PJ, Masters PS, de Haan CA. 2010. The coronavirus nucleocapsid protein is dynamically associated with the replication-transcription complexes. J. Virol. 84:11575-11579.
23. Hurst KR, Ye R, Goebel SJ, Jayaraman P, Masters PS. 2010. 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. 84:10276-10288.
24. Saikatendu KS, Joseph JS, Subramanian V, Clayton T, Griffith M, Moy K, Velasquez J, Neuman BW, Buchmeier MJ, Stevens RC, Kuhn P. 2005. Structural basis of severe acute respiratory syndrome coronavirus ADP-ribose-1"-phosphate dephosphorylation by a conserved domain of nsP3. Structure. 13:1665-1675.
25. Egloff MP, Malet H, Putics A, Heinonen M, Dutartre H, Frangeul A, Gruez A, Campanacci V, Cambillau C, Ziebuhr J, Ahola T, Canard B. 2006. Structural and functional basis for ADP-ribose and poly(ADPribose) binding by viral macro domains. J. Virol. 80:8493-8502.
26. Ratia K, Saikatendu KS, Santarsiero BD, Barretto N, Baker SC, Stevens RC, Mesecar AD. 2006. Severe acute respiratory syndrome coronavirus papain-like protease: structure of a viral deubiquitinating enzyme. Proc. Natl. Acad. Sci. U. S. A. 103:5717-5722.
27. Serrano P, Johnson MA, Almeida MS, Horst R, Herrmann T, Joseph JS, Neuman BW, Subramanian V, Saikatendu KS, Buchmeier MJ, Stevens RC, Kuhn P, Wüthrich K. 2007. Nuclear magnetic resonance structure of the N-terminal domain of nonstructural protein 3 from the severe acute respiratory syndrome coronavirus. J. Virol. 81:12049-12060.
28. Chatterjee A, Johnson MA, Serrano P, Pedrini B, Joseph JS, Neuman BW, Saikatendu K, Buchmeier MJ, Kuhn P, Wüthrich K. 2009. Nuclear magnetic resonance structure shows that the severe acute respiratory syndrome coronavirus-unique domain contains a macrodomain fold. J. Virol. 83:1823-1836.
29. Piotrowski Y, Hansen G, Boomaars-van der Zanden AL, Snijder EJ, Gorbalenya AE, Hilgenfeld R. 2009. Crystal structures of the X-domains of a group-1 and a group-3 coronavirus reveal that ADP-ribose-binding may not be a conserved property. Protein Sci. 18:6-16.
30. Tan J, Vonrhein C, Smart OS, Bricogne G, Bollati M, Kusov Y, Hansen G, Mesters JR, Schmidt CL, Hilgenfeld R. 2009. The SARS-unique domain (SUD) of SARS coronavirus contains two macrodomains that bind G-quadruplexes. PLoS Pathog. 5:e1000428. doi:10.1371/journal .ppat.1000428.
31. Xu Y, Cong L, Chen C, Wei L, Zhao Q, Xu X, Ma Y, Bartlam M, Rao Z. 2009. Crystal structures of two coronavirus ADP-ribose-1"-monophosphatases and their complexes with ADP-ribose: a systematic structural analysis of the viral ADRP domain. J. Virol. 83:1083-1092.
32. Serrano P, Johnson MA, Chatterjee A, Neuman BW, Joseph JS, Buchmeier MJ, Kuhn P, Wüthrich K. 2009. NMR structure of the nucleic acid-binding domain of the SARS coronavirus nonstructural protein 3. J. Virol. 83:12998-13008.
33. Ziebuhr J, Schelle B, Karl N, Minskaia E, Bayer S, Siddell SG, Gorbalenya AE, Thiel V. 2007. Human coronavirus 229E papain-like proteases have overlapping specificities but distinct functions in viral replication. J. Virol. 81:3922-3932.
34. Gadlage MJ, Denison MR. 2010. Exchange of the coronavirus replicase polyprotein cleavage sites alters protease specificity and processing. J. Virol. 84:6894-6898.
35. Baker SC, Yokomori K, Dong S, Carlisle R, Gorbalenya AE, Koonin EV, Lai MM. 1993. Identification of the catalytic sites of a papain-like cysteine proteinase of murine coronavirus. J. Virol. 67:6056-6063.
36. Dong S, Baker SC. 1994. Determinants of the p28 cleavage site recognized by the first papain-like cysteine proteinase of murine coronavirus. Virology 204:541-549.
37. Hughes SA, Bonilla PJ, Weiss SR. 1995. Identification of the murine coronavirus p28 cleavage site. J. Virol. 69:809-813.
38. Bonilla PJ, Hughes SA, Weiss SR. 1997. 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. 71:900-909.
39. Graham RL, Denison MR. 2006. Replication of murine hepatitis virus is regulated by papain-like proteinase 1 processing of nonstructural proteins 1, 2, and 3. J. Virol. 80:11610-11620.
40. Ziebuhr J, Thiel V, Gorbalenya AE. 2001. The autocatalytic release of a putative RNA virus transcription factor from its polyprotein precursor involves two paralogous papain-like proteases that cleave the same peptide bond. J. Biol. Chem. 276:33220-33232.
41. Keane SC, Giedroc DP. 2013. Solution structure of mouse hepatitis virus (MHV) nsp3a and determinants of the interaction with MHV nucleocapsid (N) protein. J. Virol. 87:3502-3515.
42. Yount B, Denison MR, Weiss SR, Baric RS. 2002. Systematic assembly of a full-length infectious cDNA of mouse hepatitis virus strain A59. J. Virol. 76:11065-11078.
43. Ye R, Montalto-Morrison C, Masters PS. 2004. Genetic analysis of determinants for spike glycoprotein assembly into murine coronavirus virions: distinct roles for charge-rich and cysteine-rich regions of the endodomain. J. Virol. 78:9904-9917.
44. Masters PS, Koetzner CA, Kerr CA, Heo Y. 1994. Optimization of targeted RNA recombination and mapping of a novel nucleocapsid gene mutation in the coronavirus mouse hepatitis virus. J. Virol. 68:328-337.
45. Neuman BW, Joseph JS, Saikatendu KS, Serrano P, Chatterjee A, Johnson MA, Liao L, Klaus JP, Yates JR III, Wüthrich K, Stevens RC, Buchmeier MJ, Kuhn P. 2008. Proteomics analysis unravels the functional repertoire of coronavirus nonstructural protein 3. J. Virol. 82: 5279-5294.
46. Barretto N, Jukneliene D, Ratia K, Chen Z, Mesecar AD, Baker SC. 2005. The papain-like protease of severe acute respiratory syndrome coronavirus has deubiquitinating activity. J. Virol. 79:15189-15198.
47. Woo PC, Lau SK, Chu CM, Chan KH, Tsoi HW, Huang Y, Wong BH, Poon RW, Cai JJ, Luk WK, Poon LL, Wong SS, Guan Y, Peiris JS, Yuen KY. 2005. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J. Virol. 79:884-895.
48. Woo PC, Lau SK, Yip CC, Huang Y, Tsoi HW, Chan KH, Yuen KY. 2006. Comparative analysis of 22 coronavirus HKU1 genomes reveals a novel genotype and evidence of natural recombination in coronavirus HKU1. J. Virol. 80:7136-7145.
49. Das Sarma J, Fu L, Hingley ST, Lavi E. 2001. Mouse hepatitis virus type-2 infection in mice: an experimental model system of acute meningitis and hepatitis. Exp. Mol. Pathol. 71:1-12.
50. Yount B, Curtis KM, Baric RS. 2000. Strategy for systematic assembly of large RNA and DNA genomes: transmissible gastroenteritis virus model. J. Virol. 74:10600-10611.
51. Casais R, Thiel V, Siddell SG, Cavanagh D, Britton P. 2001. Reverse genetics system for the avian coronavirus infectious bronchitis virus. J. Virol. 75:12359-12369.
52. Yount B, Curtis KM, Fritz EA, Hensley LE, Jahrling PB, Prentice E, Denison MR, Geisbert TW, Baric RS. 2003. Reverse genetics with a full-length infectious cDNA of severe acute respiratory syndrome coronavirus. Proc. Natl. Acad. Sci. U. S. A. 100:12995-13000.
53. Coley SE, Lavi E, Sawicki SG, Fu L, Schelle B, Karl N, Siddell SG, Thiel V. 2005. Recombinant mouse hepatitis virus strain A59 from cloned, full-length cDNA replicates to high titers in vitro and is fully pathogenic in vivo. J. Virol. 79:3097-3106.
54. Kuo L, Masters PS. 2003. The small envelope protein E is not essential for murine coronavirus replication. J. Virol. 77:4597-4608.
55. Keane SC, Liu P, Leibowitz JL, Giedroc DP. 2012. Functional transcriptional regulatory sequence (TRS) RNA binding and helix destabilizing determinants of murine hepatitis virus (MHV) nucleocapsid (N) protein. J. Biol. Chem. 287:7063-7073.
56. Kuo L, Godeke GJ, Raamsman MJ, Masters PS, Rottier PJ. 2000. Retargeting of coronavirus by substitution of the spike glycoprotein ectodomain: crossing the host cell species barrier. J. Virol. 74:1393-1406.
57. Imbert I, Snijder EJ, Dimitrova M, Guillemot JC, Lécine P, Canard B. 2008. The SARS-coronavirus PLnc domain of nsp3 as a replication/ transcription scaffolding protein. Virus Res. 133:136-148.
58. Pan J, Peng X, Gao Y, Li Z, Lu X, Chen Y, Ishaq M, Liu D, Dediego ML, Enjuanes L, Guo D. 2008. Genome-wide analysis of protein-protein interactions and involvement of viral proteins in SARS-CoV replication. PLoS One 3:e3299. doi:10.1371/journal.pone.0003299.
59. von Brunn A, Teepe C, Simpson JC, Pepperkok R, Friedel CC, Zimmer R, Roberts R, Baric R, Haas J. 2007. Analysis of intraviral protein-protein interactions of the SARS coronavirus ORFeome. PLoS One 2:e459. doi:10 .1371/journal.pone.0000459.
60. Repass JF, Makino S. 1998. Importance of the positive-strand RNA secondary structure of a murine coronavirus defective interfering RNA internal replication signal in positive-strand RNA synthesis. J. Virol. 72:7926-7933.
61. Johnson RF, Feng M, Liu P, Millership JJ, Yount B, Baric RS, Leibowitz JL. 2005. Effect of mutations in the mouse hepatitis virus 3'(+)42 protein binding element on RNA replication. J. Virol. 79:14570-14585.
62. Eriksson KK, Cervantes-Barragán L, Ludewig B, Thiel V. 2008. Mouse hepatitis virus liver pathology is dependent on ADP-ribose-1"-phosphatase, a viral function conserved in the alpha-like supergroup. J. Virol. 82:12325-12334.
63. Frieman M, Ratia K, Johnston RE, Mesecar AD, Baric RS. 2009. Severe acute respiratory syndrome coronavirus papain-like protease ubiquitinlike domain and catalytic domain regulate antagonism of IRF3 and NFkappaB signaling. J. Virol. 83:6689-6705.
64. Clementz MA, Chen Z, Banach BS, Wang Y, Sun L, Ratia K, Baez-Santos YM, Wang J, Takayama J, Ghosh AK, Li K, Mesecar AD, Baker SC. 2010. Deubiquitinating and interferon antagonism activities of coronavirus papain-like proteases. J. Virol. 84:4619-4629.
65. Putics A, Filipowicz W, Hall J, Gorbalenya AE, Ziebuhr J. 2005. ADPribose-1"monophosphatase: a conserved coronavirus enzyme that is dispensable for viral replication in tissue culture. J. Virol. 79:12721-12731.
66. Stokes HL, Baliji S, Hui CG, Sawicki SG, Baker SC, Siddell SG. 2010. A new cistron in the murine hepatitis virus replicase gene. J. Virol. 84: 10148-10158.
67. Oostra M, Hagemeijer MC, van Gent M, Bekker CP, te Lintelo EG, Rottier PJ, de Haan CA. 2008. Topology and membrane anchoring of the coronavirus replication complex: not all hydrophobic domains of nsp3 and nsp6 are membrane spanning. J. Virol. 82:12392-12405.
68. Kanjanahaluethai A, Chen Z, Jukneliene D, Baker SC. 2007. Membrane topology of murine coronavirus replicase nonstructural protein 3. Virology 361:391-401.
69. Knoops K, Kikkert M, Worm SH, Zevenhoven-Dobbe JC, van der Meer Y, Koster AJ, Mommaas AM, Snijder EJ. 2008. SARS-coronavirus replication is supported by a reticulovesicular network of modified endoplasmic reticulum. PLoS Biol. 6:e226. doi:10.1371/journal.pbio.0060226.
70. Züst R, Miller TB, Goebel SJ, Thiel V, Masters PS. 2008. 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. 82:1214-1228.
71. Snijder EJ, Bredenbeek PJ, Dobbe JC, Thiel V, Ziebuhr J, Poon LL, Guan Y, Rozanov M, Spaan WJ, Gorbalenya AE. 2003. Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage. J. Mol. Biol. 331:991-1004.
72. Johnson MA, Chatterjee A, Neuman BW, Wüthrich K. 2010. SARS coronavirus unique domain: three-domain molecular architecture in solution and RNA binding. J. Mol. Biol. 400:724-742.