Topology and membrane anchoring of the coronavirus replication complex: Not all hydrophobic domains of nsp3 and nsp6 are membrane spanning

Journal of Virology

Volumn 82, Issue 24, 2008, Pages 12392-12405

  Oostra, Monique ^a   Hagemeijer, Marne C ^a   Van Gent, Michiel ^a   Bekker, Cornelis P J ^a   Te Lintelo, Eddie G ^a   Rottier, Peter J M ^a   De Haan, Cornelis A M ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 4; NONSTRUCTURAL PROTEIN 5; PROTEIN NSP6; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CORONAVIRUS; GENE SEQUENCE; HEPATITIS VIRUS; LIPID BILAYER; MEMBRANE STRUCTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; VIRUS GENE; VIRUS REPLICATION; VIRUS STRAIN;

CELL LINE; CELL MEMBRANE; CORONAVIRUS; GENE DELETION; GLYCOPROTEINS; HYDROPHOBICITY; MUTATION; PROTEIN BINDING; VIRAL NONSTRUCTURAL PROTEINS; VIRUS INTERNALIZATION; VIRUS REPLICATION;

CORONAVIRUS; MURINE HEPATITIS VIRUS; SARS CORONAVIRUS;

EID: 57349156648     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01219-08     Document Type: Article

References (65)

1. Almazán, F., J. M. Gonzalez, Z. Penzes, A. Izeta, E. Calvo, J. Plana-Duran, and L. Enjuanes. 2000. Engineering the largest RNA virus genome as an infectious bacterial artificial chromosome. Proc. Natl. Acad. Sci. USA 97:5516-5521.
2. Baker, S. C., K. Yokomori, S. Dong, R. Carlisle, A. E. Gorbalenya, E. V. Koonin, and M. M. Lai. 1993. Identification of the catalytic sites of a papain-like cysteine proteinase of murine coronavirus. J. Virol. 67:6056-6063.
3. Bhardwaj, K., L. Guarino, and C. C. Kao. 2004. The severe acute respiratory syndrome coronavirus Nsp15 protein is an endoribonuclease that prefers manganese as a cofactor. J. Virol. 78:12218-12224.
4. Bost, A. G., R. H. Carnahan, X. T. Lu, and M. R. Denison. 2000. 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. 74:3379-3387.
5. Bredenbeek, P. J., C. J. Pachuk, A. F. Noten, J. Charite, W. Luytjes, S. R. Weiss, and W. J. Spaan. 1990. The primary structure and expression of the second open reading frame of the polymerase gene of the coronavirus MHVA59; a highly conserved polymerase is expressed by an efficient ribosomal frameshifting mechanism. Nucleic Acids Res. 18:1825-1832.
6. Brockway, S. M., C. T. Clay, X. T. Lu, and M. R. Denison. 2003. Characterization of the expression, intracellular localization, and replication complex association of the putative mouse hepatitis virus RNA-dependent RNA polymerase. J. Virol. 77:10515-10527.
7. Cheng, A., W. Zhang, Y. Xie, W. Jiang, E. Arnold, S. G. Sarafianos, and J. Ding. 2005. Expression, purification, and characterization of SARS coronavirus RNA polymerase. Virology 335:165-176.
8. Clementz, M. A., A. Kanjanahaluethai, T. E. O'Brien, and S. C. Baker. 2008. Mutation in murine coronavirus replication protein nsp4 alters assembly of double membrane vesicles. Virology 375:118-129.
9. Decroly, E., I. Imbert, B. Coutard, M. Bouvet, B. Selisko, K. Alvarez, A. E. Gorbalenya, E. J. Snijder, and B. Canard. 2008. Coronavirus nonstructural protein 16 is a Cap-0 binding enzyme possessing (nucleoside-2′O)-methyltransferase activity. J. Virol. 82:8071-8084.
10. de Haan, C. A., P. Roestenberg, M. de Wit, A. A. de Vries, T. Nilsson, H. Vennema, and P. J. Rottier. 1998. Structural requirements for O glycosylation of the mouse hepatitis virus membrane protein. J. Biol. Chem. 273:29905-29914.
11. Denison, M. R., A. C. Sims, C. A. Gibson, and X. T. Lu. 1998. Processing of the MHV-A59 gene 1 polyprotein by the 3C-like proteinase. Adv. Exp. Med. Biol. 440:121-127.
12. Donaldson, E. F., R. L. Graham, A. C. Sims, M. R. Denison, and R. S. Baric. 2007. Analysis of murine hepatitis virus strain A59 temperature-sensitive mutant TS-LA6 suggests that nsp10 plays a critical role in polyprotein processing. J. Virol. 81:7086-7098.
13. Dos Ramos, F., M. Carrasco, T. Doyle, and I. Brierley. 2004. Programmed -1 ribosomal frameshifting in the SARS coronavirus. Biochem. Soc. Trans. 32:1081-1083.
14. Echeverri, A. C., and A. Dasgupta. 1995. Amino terminal regions of poliovirus 2C protein mediate membrane binding. Virology 208:540-553.
15. Elazar, M., P. Liu, C. M. Rice, and J. S. Glenn. 2004. An N-terminal amphipathic helix in hepatitis C virus (HCV) NS4B mediates membrane association, correct localization of replication complex proteins, and HCV RNA replication. J. Virol. 78:11393-11400.
16. Elroy-Stein, O., and B. Moss. 1990. Cytoplasmic expression system based on constitutive synthesis of bacteriophage T7 RNA polymerase in mammalian cells. Proc. Natl. Acad. Sci. USA 87:6743-6747.
17. Fan, K., L. Ma, X. Han, H. Liang, P. Wei, Y. Liu, and L. Lai. 2005. The substrate specificity of SARS coronavirus 3C-like proteinase. Biochem. Biophys. Res. Commun. 329:934-940.
18. Fuerst, T. R., E. G. Niles, F. W. Studier, and B. Moss. 1986. Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc. Natl. Acad. Sci. USA 83:8122-8126.
19. Gorbalenya, A. E., L. Enjuanes, J. Ziebuhr, and E. J. Snijder. 2006. Nidovirales: evolving the largest RNA virus genome. Virus Res. 117:17-37.
20. Gosert, R., A. Kanjanahaluethai, D. Egger, K. Bienz, and S. C. Baker. 2002. RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. J. Virol. 76:3697-3708.
21. Graham, R. L., A. C. Sims, S. M. Brockway, R. S. Baric, and M. R. Denison. 2005. The nsp2 replicase proteins of murine hepatitis virus and severe acute respiratory syndrome coronavirus are dispensable for viral replication. J. Virol. 79:13399-13411.
22. Harcourt, B. H., D. Jukneliene, A. Kanjanahaluethai, J. Bechill, K. M. Severson, C. M. Smith, P. A. Rota, and S. C. Baker. 2004. Identification of severe acute respiratory syndrome coronavirus replicase products and characterization of papain-like protease activity. J. Virol. 78:13600-13612.
23. Hirokawa, T., S. Boon-Chieng, and S. Mitaku. 1998. SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14:378-379.
24. Imbert, I., J. C. Guillemot, J. M. Bourhis, C. Bussetta, B. Coutard, M. P. Egloff, F. Ferron, A. E. Gorbalenya, and B. Canard. 2006. A second, noncanonical RNA-dependent RNA polymerase in SARS coronavirus. EMBO J. 25:4933-4942.
25. Ivanov, K. A., T. Hertzig, M. Rozanov, S. Bayer, V. Thiel, A. E. Gorbalenya, and J. Ziebuhr. 2004. Major genetic marker of nidoviruses encodes a replicative endoribonuclease. Proc. Natl. Acad. Sci. USA 101:12694-12699.
26. Ivanov, K. A., V. Thiel, J. C. Dobbe, Y. van der Meer, E. J. Snijder, and J. Ziebuhr. 2004. Multiple enzymatic activities associated with severe acute respiratory syndrome coronavirus helicase. J. Virol. 78:5619-5632.
27. Ivanov, K. A., and J. Ziebuhr. 2004. Human coronavirus 229E nonstructural protein 13: characterization of duplex-unwinding, nucleoside triphosphatase, and RNA 5-triphosphatase activities. J. Virol. 78:7833-7838.
28. Kanjanahaluethai, A., Z. Chen, D. Jukneliene, and S. C. Baker. 2007. Membrane topology of murine coronavirus replicase nonstructural protein 3. Virology 361:391-401.
29. Kuiken, T., R. A. Fouchier, M. Schutten, G. F. Rimmelzwaan, G. van Amerongen, D. van Riel, J. D. Laman, T. de Jong, G. van Doornum, W. Lim, A. E. Ling, P. K. Chan, J. S. Tam, M. C. Zambon, R. Gopal, C. Drosten, S. van der Werf, N. Escriou, J. C. Manuguerra, K. Stohr, J. S. Peiris, and A. D. Osterhaus. 2003. Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet 362:263-270.
30. Locker, J. K., J. K. Rose, M. C. Horzinek, and P. J. Rottier. 1992. Membrane assembly of the triple-spanning coronavirusMprotein. Individual transmembrane domains show preferred orientation. J. Biol. Chem. 267:21911-21918.
31. Matthes, N., J. R. Mesters, B. Coutard, B. Canard, E. J. Snijder, R. Moll, and R. Hilgenfeld. 2006. The non-structural protein Nsp10 of mouse hepatitis virus binds zinc ions and nucleic acids. FEBS Lett. 580:4143-4149.
32. McMahon, H. T., and J. L. Gallop. 2005. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438:590-596.
33. Miller, S., S. Kastner, J. Krijnse-Locker, S. Buhler, and R. Bartenschlager. 2007. The non-structural protein 4A of dengue virus is an integral membrane protein inducing membrane alterations in a 2K-regulated manner. J. Biol. Chem. 282:8873-8882.
34. Miller, S., S. Sparacio, and R. Bartenschlager. 2006. Subcellular localization and membrane topology of the Dengue virus type 2 non-structural protein 4B. J. Biol. Chem. 281:8854-8863.
35. Oostra, M., C. A. de Haan, R. J. de Groot, and P. J. Rottier. 2006. Glycosylation of the severe acute respiratory syndrome coronavirus triple-spanning membrane proteins 3a and M. J. Virol. 80:2326-2336.
36. Oostra, M., C. A. de Haan, and P. J. Rottier. 2007. The 29-nucleotide deletion present in human but not in animal severe acute respiratory syndrome coronaviruses disrupts the functional expression of open reading frame 8. J. Virol. 81:13876-13888.
37. Oostra, M., E. G. te Lintelo, M. Deijs, M. H. Verheije, P. J. Rottier, and C. A. de Haan. 2007. Localization and membrane topology of coronavirus nonstructural protein 4: involvement of the early secretory pathway in replication. J. Virol. 81:12323-12336.
38. Paul, A. V., A. Molla, and E. Wimmer. 1994. Studies of a putative amphipathic helix in the N-terminus of poliovirus protein 2C. Virology 199:188-199.
39. Posthuma, C. C., K. W. Pedersen, Z. Lu, R. G. Joosten, N. Roos, J. C. Zevenhoven-Dobbe, and E. J. Snijder. 2008. Formation of the arterivirus replication/transcription complex: a key role for nonstructural protein 3 in the remodeling of intracellular membranes. J. Virol. 82:4480-4491.
40. Prentice, E., W. G. Jerome, T. Yoshimori, N. Mizushima, and M. R. Denison. 2004. Coronavirus replication complex formation utilizes components of cellular autophagy. J. Biol. Chem. 279:10136-10141.
41. Prentice, E., J. McAuliffe, X. Lu, K. Subbarao, and M. R. Denison. 2004. Identification and characterization of severe acute respiratory syndrome coronavirus replicase proteins. J. Virol. 78:9977-9986.
42. Putics, A., W. Filipowicz, J. Hall, A. E. Gorbalenya, and J. Ziebuhr. 2005. ADP-ribose-1″-monophosphatase: a conserved coronavirus enzyme that is dispensable for viral replication in tissue culture. J. Virol. 79:12721-12731.
43. Ricagno, S., M. P. Egloff, R. Ulferts, B. Coutard, D. Nurizzo, V. Campanacci, C. Cambillau, J. Ziebuhr, and B. Canard. 2006. Crystal structure and mechanistic determinants of SARS coronavirus nonstructural protein 15 define an endoribonuclease family. Proc. Natl. Acad. Sci. USA 103:11892-11897.
44. Salonen, A., T. Ahola, and L. Kaariainen. 2005. Viral RNA replication in association with cellular membranes. Curr. Top. Microbiol. Immunol. 285:139-173.
45. Sawicki, S. G., D. L. Sawicki, and S. G. Siddell. 2007. A contemporary view of coronavirus transcription. J. Virol. 81:20-29.
46. Shi, S. T., and M. M. Lai. 2005. Viral and cellular proteins involved in coronavirus replication. Curr. Top. Microbiol. Immunol. 287:95-131.
47. Shi, S. T., J. J. Schiller, A. Kanjanahaluethai, S. C. Baker, J. W. Oh, and M. M. Lai. 1999. Colocalization and membrane association of murine hepatitis virus gene 1 products and de novo-synthesized viral RNA in infected cells. J. Virol. 73:5957-5969.
48. Snijder, E. J., Y. van der Meer, J. Zevenhoven-Dobbe, J. J. Onderwater, J. van der Meulen, H. K. Koerten, and A. M. Mommaas. 2006. Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex. J. Virol. 80:5927-5940.
49. Snijder, E. J., H. van Tol, N. Roos, and K. W. Pedersen. 2001. Non-structural proteins 2 and 3 interact to modify host cell membranes during the formation of the arterivirus replication complex. J. Gen. Virol. 82:985-994.
50. Sparks, J. S., X. Lu, and M. R. Denison. 2007. Genetic analysis of Murine hepatitis virus nsp4 in virus replication. J. Virol. 81:12554-12563.
51. Sutormin, R. A., and A. A. Mironov. 2006. Membrane probability profile construction based on amino acids sequences multiple alignment. Mol. Biol. [Engl. Transl. Mol. Biol. (Moscow)] 40:541-545.
52. Sutton, G., E. Fry, L. Carter, S. Sainsbury, T. Walter, J. Nettleship, N. Berrow, R. Owens, R. Gilbert, A. Davidson, S. Siddell, L. L. Poon, J. Diprose, D. Alderton, M. Walsh, J. M. Grimes, and D. I. Stuart. 2004. The nsp9 replicase protein of SARS-coronavirus, structure and functional insights. Structure 12:341-353.
53. Taguchi, F., and J. O. Fleming. 1989. Comparison of six different murine coronavirus JHM variants by monoclonal antibodies against the E2 glycoprotein. Virology 169:233-235.
54. Teterina, N. L., A. E. Gorbalenya, D. Egger, K. Bienz, and E. Ehrenfeld. 1997. Poliovirus 2C protein determinants of membrane binding and rearrangements in mammalian cells. J. Virol. 71:8962-8972.
55. Thiel, V., K. A. Ivanov, A. Putics, T. Hertzig, B. Schelle, S. Bayer, B. Weissbrich, E. J. Snijder, H. Rabenau, H. W. Doerr, A. E. Gorbalenya, and J. Ziebuhr. 2003. Mechanisms and enzymes involved in SARS coronavirus genome expression. J. Gen. Virol. 84:2305-2315.
56. Uchil, P. D., and V. Satchidanandam. 2003. Architecture of the flaviviral replication complex. Protease, nuclease, and detergents reveal encasement within double-layered membrane compartments. J. Biol. Chem. 278:24388-24398.
57. van der Meer, Y., E. J. Snijder, J. C. Dobbe, S. Schleich, M. R. Denison, W. J. Spaan, and J. K. Locker. 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.
58. van der Meer, Y., H. van Tol, J. K. Locker, and E. J. Snijder. 1998. ORF1a-encoded replicase subunits are involved in the membrane association of the arterivirus replication complex. J. Virol. 72:6689-6698.
59. Vennema, H., R. Rijnbrand, L. Heijnen, M. C. Horzinek, and W. J. Spaan. 1991. Enhancement of the vaccinia virus/phage T7 RNA polymerase expression system using encephalomyocarditis virus 5′-untranslated region sequences. Gene 108:201-209.
60. Yount, B., K. M. Curtis, and R. S. Baric. 2000. Strategy for systematic assembly of large RNA and DNA genomes: transmissible gastroenteritis virus model. J. Virol. 74:10600-10611.
61. Yount, B., M. R. Denison, S. R. Weiss, and R. S. Baric. 2002. Systematic assembly of a full-length infectious cDNA of mouse hepatitis virus strain A59. J. Virol. 76:11065-11078.
62. Zhai, Y., F. Sun, X. Li, H. Pang, X. Xu, M. Bartlam, and Z. Rao. 2005. Insights into SARS-CoV transcription and replication from the structure of the nsp7-nsp8 hexadecamer. Nat. Struct. Mol. Biol. 12:980-986.
63. Ziebuhr, J. 2005. The coronavirus replicase. Curr. Top. Microbiol. Immunol. 287:57-94.
64. Ziebuhr, J., E. J. Snijder, and A. E. Gorbalenya. 2000. Virus-encoded proteinases and proteolytic processing in the Nidovirales. J. Gen. Virol. 81:853-879.
65. Zimmerberg, J., and M. M. Kozlov. 2006. How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 7:9-19.