Cytoplasmic tails of hantavirus glycoproteins interact with the nucleocapsid protein

Journal of General Virology

Volumn 91, Issue 9, 2010, Pages 2341-2350

  Hepojoki, J ^a   Strandin, T ^a   Wang, H ^a   Vapalahti, O ^a,b   Vaheri, A ^a   Lankinen, H ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GC; GLYCOPROTEIN GN; NUCLEOCAPSID PROTEIN; PEPTIDE; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN;

ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; CYTOPLASM; GENUS; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PUUMALA VIRUS; VIRION;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; BINDING SITES; CERCOPITHECUS AETHIOPS; HANTAVIRUS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEOCAPSID PROTEINS; PEPTIDE MAPPING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; PUUMALA VIRUS; RIBONUCLEOPROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; VERO CELLS; VIRAL ENVELOPE PROTEINS; VIRAL PROTEINS;

BUNYAVIRIDAE; HANTAVIRUS; PUUMALA VIRUS; TULA VIRUS;

EID: 77954217973     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.021006-0     Document Type: Article

References (55)

1. Alminaite, A., Backstrom, V., Vaheri, A. & Plyusnin, A. (2008). Oligomerization of hantaviral nucleocapsid protein: charged residues in the N-terminal coiled-coil domain contribute to intermolecular interactions. J Gen Virol 89, 2167-2174.
2. Barth, B. U. & Garoff, H. (1997). The nucleocapsid-binding spike subunit E2 of Semliki Forest virus requires complex formation with the E1 subunit for activity. J Virol 71, 7857-7865.
3. Eifan, S. A. & Elliott, R. M. (2009). Mutational analysis of the Bunyamwera orthobunyavirus nucleocapsid protein gene. J Virol 83, 11307-11317.
4. Elliott, R. M. (1997). Emerging viruses: the Bunyaviridae. Mol Med 3, 572-577.
5. Elliott, R. M., Bouloy, M., Calisher, C. H., Goldbach, R., Moyer, J. T., Nichol, S. T., Pettersson, R., Plyusnin, A. & Schmaljohn, C. (2000). Family Bunyaviridae. In Virus Taxonomy: Seventh Report of the International Committee on Taxonomy of Viruses, pp. 599-621. Edited by M. H. V. van Regenmortel, C. M. Fauquet, D. H. L. Bishop, E. B. Carstens, M. K. Estes, S. M. Lemon, J. Maniloff, M. A. Mayo, D. J. McGeoch, C. R. Pringle & R. B. Wickner. San Diego, CA: Academic Press.
6. Estrada, D. F., Boudreaux, D. M., Zhong, D., St Jeor, S. C. & De Guzman, R. N. (2009). The hantavirus glycoprotein G1 tail contains dual CCHC-type classical zinc fingers. J Biol Chem 284, 8654-8660.
7. Flint, S. J., Enquist, L. W., Krug, R. M., Racaniello, V. R. & Skalka, A. M. (2000). Principles of Virology: Molecular Biology, Pathogenesis, and Control. Washington, DC: American Society for Microbiology.
8. Frank, R. (2002). The SPOT-synthesis technique. Synthetic peptide arrays on membrane supports - principles and applications. J Immunol Methods 267, 13-26.
9. Gott, P., Stohwasser, R., Schnitzler, P., Darai, G. & Bautz, E. K. (1993). RNA binding of recombinant nucleocapsid proteins of hantaviruses. Virology 194, 332-337. (Pubitemid 23211766)
10. He, R., Leeson, A., Ballantine, M., Andonov, A., Baker, L., Dobie, F., Li, Y., Bastien, N., Feldmann, H. & other authors (2004). Characterization of protein-protein interactions between the nucleo-capsid protein and membrane protein of the SARS coronavirus. Virus Res 105, 121-125. (Pubitemid 39213935)
11. Hepojoki, J., Strandin, T., Vaheri, A. & Lankinen, H. (2010). Interactions and oligomerization of hantavirus glycoproteins. J Virol 84, 227-242.
12. Heyman, P., Vaheri, A., Lundkvist, A. & Avsic-Zupanc, T. (2009). Hantavirus infections in Europe: from virus carriers to a major public-health problem. Expert Rev Anti Infect Ther 7, 205-217.
13. Huiskonen, J. T., Hepojoki, J., Laurinmaki, P., Vaheri, A., Lankinen, H., Butcher, S. J. & Grunewald, K. (2010). Electron cryo-tomography of Tula hantavirus suggests a unique assembly paradigm for enveloped viruses. J Virol 84, 4889-4897.
14. Kaukinen, P., Vaheri, A. & Plyusnin, A. (2005). Hantavirus nucleocapsid protein: a multifunctional molecule with both house-keeping and ambassadorial duties. Arch Virol 150, 1693-1713. (Pubitemid 41176630)
15. Klempa, B. (2009). Hantaviruses and climate change. Clin Microbiol Infect 15, 518-523.
16. Kuismanen, E. (1984). Posttranslational processing of Uukuniemi virus glycoproteins G1 and G2. J Virol 51, 806-812.
17. Li, X. D., Makela, T. P., Guo, D., Soliymani, R., Koistinen, V., Vapalahti, O., Vaheri, A. & Lankinen, H. (2002). Hantavirus nucleocapsid protein interacts with the Fas-mediated apoptosis enhancer Daxx. J Gen Virol 83, 759-766. (Pubitemid 34284859)
18. Liu, L., Celma, C. C. & Roy, P. (2008). Rift Valley fever virus structural proteins: expression, characterization and assembly of recombinant proteins. Virol J 5, 82.
19. Lo, S. Y., Selby, M. J. & Ou, J. H. (1996). Interaction between hepatitis C virus core protein and E1 envelope protein. J Virol 70, 5177-5182. (Pubitemid 26240689)
20. Lundkvist, A. & Niklasson, B. (1992). Bank vole monoclonal antibodies against Puumala virus envelope glycoproteins: identification of epitopes involved in neutralization. Arch Virol 126, 93-105.
21. Lundkvist, A., Fatouros, A. & Niklasson, B. (1991). Antigenic variation of European haemorrhagic fever with renal syndrome virus strains characterized using bank vole monoclonal antibodies. J Gen Virol 72, 2097-2103.
22. Lundkvist, A., Horling, J., Athlin, L., Rosen, A. & Niklasson, B. (1993). Neutralizing human monoclonal antibodies against Puumala virus, causative agent of nephropathia epidemica: a novel method using antigen-coated magnetic beads for specific B cell isolation. J Gen Virol 74, 1303-1310. (Pubitemid 23230246)
23. Martin, M. L., Lindsey-Regnery, H., Sasso, D. R., McCormick, J. B. & Palmer, E. (1985). Distinction between Bunyaviridae genera by surface structure and comparison with Hantaan virus using negative stain electron microscopy. Arch Virol 86, 17-28. (Pubitemid 16249820)
24. Mertz, G. J., Hjelle, B., Crowley, M., Iwamoto, G., Tomicic, V. & Vial, P. A. (2006). Diagnosis and treatment of new world hantavirus infections. Curr Opin Infect Dis 19, 437-442. (Pubitemid 44338102)
25. Metsikko, K. & Garoff, H. (1990). Oligomers of the cytoplasmic domain of the p62/E2 membrane protein of Semliki Forest virus bind to the nucleocapsid in vitro. J Virol 64, 4678-4683.
26. Nakai, K., Okamoto, T., Kimura-Someya, T., Ishii, K., Lim, C. K., Tani, H., Matsuo, E., Abe, T., Mori, Y. & other authors (2006). Oligomerization of hepatitis C virus core protein is crucial for interaction with the cytoplasmic domain of E1 envelope protein. J Virol 80, 11265-11273.
27. Narayanan, K., Maeda, A., Maeda, J. & Makino, S. (2000). Characterization of the coronavirus M protein and nucleocapsid interaction in infected cells. J Virol 74, 8127-8134.
28. Nichol, S. T., Beaty, B. J., Elliott, R. M., Goldbach, R., Plyusnin, A., Schmaljohn, C. S. & Tesh, R. B. (2005). Family Bunyaviridae. In Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses, pp. 695-716. Edited by C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger & L. A. Ball. San Diego, CA: Elsevier Academic Press.
29. Overby, A. K., Pettersson, R. F. & Neve, E. P. (2007a). The glycoprotein cytoplasmic tail of Uukuniemi virus (Bunyaviridae) interacts with ribonucleoproteins and is critical for genome packaging. J Virol 81, 3198-3205.
30. C glycoproteins are important for intracellular targeting and the budding of virus-like particles. J Virol 81, 11381-11391.
31. Pensiero, M. N. & Hay, J. (1992). The Hantaan virus M-segment glycoproteins G1 and G2 can be expressed independently. J Virol 66, 1907-1914.
32. Persson, R. & Pettersson, R. F. (1991). Formation and intracellular transport of a heterodimeric viral spike protein complex. J Cell Biol 112, 257-266.
33. Pini, N. (2004). Hantavirus pulmonary syndrome in Latin America. Curr Opin Infect Dis 17, 427-431.
34. Plyusnin, A. & Morzunov, S. P. (2001). Virus evolution and genetic diversity of hantaviruses and their rodent hosts. Curr Top Microbiol Immunol 256, 47-75.
35. Plyusnin, A., Vapalahti, O. & Vaheri, A. (1996). Hantaviruses: genome structure, expression and evolution. J Gen Virol 77, 2677-2687.
36. Plyusnin, A., Kukkonen, S. K., Plyusnina, A., Vapalahti, O. & Vaheri, A. (2002). Transfection-mediated generation of functionally competent Tula hantavirus with recombinant S RNA segment. EMBO J 21, 1497-1503.
37. Razzauti, M., Plyusnina, A., Sironen, T., Henttonen, H. & Plyusnin, A. (2009). Analysis of Puumala hantavirus in a bank vole population in northern Finland: evidence for co-circulation of two genetic lineages and frequent reassortment between strains. J Gen Virol 90, 1923-1931.
38. Ribeiro, D., Borst, J. W., Goldbach, R. & Kormelink, R. (2009). Tomato spotted wilt virus nucleocapsid protein interacts with both viral glycoproteins Gn and Gc in planta. Virology 383, 121-130.
39. Rodriguez, L. L., Owens, J. H., Peters, C. J. & Nichol, S. T. (1998). Genetic reassortment among viruses causing hantavirus pulmonary syndrome. Virology 242, 99-106.
40. Schmaljohn, C. & Hjelle, B. (1997). Hantaviruses: a global disease problem. Emerg Infect Dis 3, 95-104.
41. Schonrich, G., Rang, A., Lutteke, N., Raftery, M. J., Charbonnel, N. & Ulrich, R. G. (2008). Hantavirus-induced immunity in rodent reservoirs and humans. Immunol Rev 225, 163-189.
42. Shi, X. & Elliott, R. M. (2002). Golgi localization of Hantaan virus glycoproteins requires coexpression of G1 and G2. Virology 300, 31-38.
43. Snippe, M., Willem Borst, J., Goldbach, R. & Kormelink, R. (2007). Tomato spotted wilt virus Gc and N proteins interact in vivo. Virology 357, 115-123.
44. Spiropoulou, C. F. (2001). Hantavirus maturation. Curr Top Microbiol Immunol 256, 33-46.
45. Sturman, L. S., Holmes, K. V. & Behnke, J. (1980). Isolation of coronavirus envelope glycoproteins and interaction with the viral nucleocapsid. J Virol 33, 449-462.
46. Vaheri, A., Vapalahti, O. & Plyusnin, A. (2008). How to diagnose hantavirus infections and detect them in rodents and insectivores. Rev Med Virol 18, 277-288.
47. Vapalahti, O., Kallio-Kokko, H., Narvanen, A., Julkunen, I., Lundkvist, A., Plyusnin, A., Lehvaslaiho, H., Brummer-Korvenkontio, M., Vaheri, A. & Lankinen, H. (1995). Human B-cell epitopes of Puumala virus nucleocapsid protein, the major antigen in early serological response. J Med Virol 46, 293-303.
48. Vapalahti, O., Lundkvist, A., Kallio-Kokko, H., Paukku, K., Julkunen, I., Lankinen, H. & Vaheri, A. (1996). Antigenic properties and diagnostic potential of Puumala virus nucleocapsid protein expressed in insect cells. J Clin Microbiol 34, 119-125.
49. Vapalahti, O., Mustonen, J., Lundkvist, A., Henttonen, H., Plyusnin, A. & Vaheri, A. (2003). Hantavirus infections in Europe. Lancet Infect Dis 3, 653-661.
50. Vaux, D. J., Helenius, A. & Mellman, I. (1988). Spike-nucleocapsid interaction in Semliki Forest virus reconstructed using network antibodies. Nature 336, 36-42.
51. Venien-Bryan, C. & Fuller, S. D. (1994). The organization of the spike complex of Semliki Forest virus. J Mol Biol 236, 572-583.
52. Vogel, R. H., Provencher, S. W., von Bonsdorff, C. H., Adrian, M. & Dubochet, J. (1986). Envelope structure of Semliki Forest virus reconstructed from cryo-electron micrographs. Nature 320, 533-535.
53. Wang, Y., Boudreaux, D. M., Estrada, D. F., Egan, C. W., St Jeor, S. C. & De Guzman, R. N. (2008). NMR structure of the N-terminal coiled coil domain of the Andes hantavirus nucleocapsid protein. J Biol Chem 283, 28297-28304.
54. Wang, H., Alminaite, A., Vaheri, A. & Plyusnin, A. (2010). Interaction between hantaviral nucleocapsid protein and the cytoplasmic tail of surface glycoprotein Gn. Virus Res 151, 205-212.
55. Weaver, S. C., Frey, T. K., Huang, H. V., Kinney, R. M., Rice, C. M., Roehrig, J. T., Shope, R. E. & Strauss, E. G. (2005). Family Togaviridae. In Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses, pp. 999-1008. Edited by C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger & L. A. Ball. San Diego, CA: Elsevier Academic Press.