Inactivation of hantaviruses by N-ethylmaleimide preserves virion integrity

Journal of General Virology

Volumn 92, Issue 5, 2011, Pages 1189-1198

  Strandin, Tomas ^a   Hepojoki, Jussi ^a   Wang, Hao ^a   Vaheri, Antti ^a   Lankinen, Hilkka ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

5,5' DITHIOBIS(2 NITROBENZOIC ACID); FUNCTIONAL GROUP; GLYCOPROTEIN; MALEIMIDE; N ETHYLMALEIMIDE; STRUCTURAL PROTEIN; THIOL GROUP;

ALKYLATION; ANTIGENICITY; ARTICLE; BUNYAVIRUS; CELL ADHESION; HANTAVIRUS; MEMBRANE PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; PUUMALA VIRUS; VIRION; VIRUS INACTIVATION; VIRUS INFECTIVITY; WILD TYPE;

ANIMALS; ANTIGENS, VIRAL; CELL LINE; DISINFECTANTS; DITHIONITROBENZOIC ACID; ETHYLMALEIMIDE; HANTAVIRUS; PRESERVATIVES, PHARMACEUTICAL; VIRION; VIRUS ATTACHMENT; VIRUS INACTIVATION;

BUNYAVIRIDAE; HANTAVIRUS; PHLEBOVIRUS; PUUMALA;

EID: 79955630367     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.027896-0     Document Type: Article

References (53)

1. Abell, B. A. & Brown, D. T. (1993). Sindbis virus membrane fusion is mediated by reduction of glycoprotein disulfide bridges at the cell surface. J Virol 67, 5496-5501.
2. Abou-Jaoudé, G. & Sureau, C. (2007). Entry of hepatitis delta virus requires the conserved cysteine residues of the hepatitis B virus envelope protein antigenic loop and is blocked by inhibitors of thiol-disulfide exchange. J Virol 81, 13057-13066.
3. Appenzeller-Herzog, C. & Ellgaard, L. (2008). The human PDI family: versatility packed into a single fold. Biochim Biophys Acta 1783, 535-548.
4. Arthur, LO., Bess, JW., Chertova, EN., Rossio, JL., Esser, MT., Benveniste, RE., Henderson, LE. & Lifson, JD. (1998). Chemical inactivation of retroviral infectivity by targeting nucleocapsid protein zinc fingers: a candidate SIV vaccine. AIDS Res Hum Retroviruses 14 (Suppl. 3), S311-S319.
5. Boukhvalova, M. S., Prince, G. A. & Blanco, J. C. (2010). Inactivation of respiratory syncytial virus by zinc finger reactive compounds. Virol J 7, 20.
6. Chertova, E., Crise, B. J., Morcock, D. R., Bess, J. W., Jr, Henderson, L. E. & Lifson, J. D. (2003). Sites, mechanism of action and lack of reversibility of primate lentivirus inactivation by preferential covalent modification of virion internal proteins. Curr Mol Med 3, 265-272.
7. De Clercq, E. (2002). New anti-HIV agents and targets. Med Res Rev 22, 531-565.
8. 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.
9. Freedman, R. B., Hirst, T. R. & Tuite, M. F. (1994). Protein disulphide isomerase: building bridges in protein folding. Trends Biochem Sci 19, 331-336.
10. Gallagher, T. M. (1996). Murine coronavirus membrane fusion is blocked by modification of thiols buried within the spike protein. J Virol 70, 4683-4690.
11. Garćia, C. C., Candurra, N. A. & Damonte, E. B. (2000). Antiviral and virucidal activities against arenaviruses of zinc-finger active compounds. Antivir Chem Chemother 11, 231-237.
12. Garćia, C. C., Djavani, M., Topisirovic, I., Borden, K. L., Salvato, M. S. & Damonte, E. B. (2006). Arenavirus Z protein as an antiviral target: virus inactivation and protein oligomerization by zinc finger-reactive compounds. J Gen Virol 87, 1217-1228.
13. Garry, C. E. & Garry, R. F. (2004). Proteomics computational analyses suggest that the carboxyl terminal glycoproteins of Bunyaviruses are class II viral fusion protein (beta-penetrenes). Theor Biol Med Model 1, 10.
14. Gavrilovskaya, I. N., Shepley, M., Shaw, R., Ginsberg, M. H. & Mackow, E. R. (1998). β3 Integrins mediate the cellular entry of hantaviruses that cause respiratory failure. Proc Natl Acad Sci USA 95, 7074-7079.
15. Guo, J., Wu, T., Anderson, J., Kane, B. F., Johnson, D. G., Gorelick, R. J., Henderson, L. E. & Levin, J. G. (2000). Zinc finger structures in the human immunodeficiency virus type 1 nucleocapsid protein facilitate efficient minus- and plus-strand transfer. J Virol 74, 8980-8988.
16. Hepojoki, J., Strandin, T., Vaheri, A. & Lankinen, H. (2010a). Interactions and oligomerization of hantavirus glycoproteins. J Virol 84, 227-242.
17. Hepojoki, J. M., Strandin, T., Wang, H., Vapalahti, O., Vaheri, A. & Lankinen, H. (2010b). Cytoplasmic tails of hantavirus glycoproteins interact with the nucleocapsid protein. J Gen Virol 91, 2341-2350.
18. Huiskonen, J. T., Hepojoki, J., Laurinmäki, P., Vaheri, A., Lankinen, H., Butcher, S. J. & Grünewald, K. (2010). Electron cryotomography of Tula hantavirus suggests a unique assembly paradigm for enveloped viruses. J Virol 84, 4889-4897.
19. Jain, S., McGinnes, L. W. & Morrison, T. G. (2007). Thiol/disulfide exchange is required for membrane fusion directed by the Newcastle disease virus fusion protein. J Virol 81, 2328-2339.
20. Johnson, P. E., Turner, R. B., Wu, Z. R., Hairston, L., Guo, J., Levin, J. G. & Summers, M. F. (2000). A mechanism for plus-strand transfer enhancement by the HIV-1 nucleocapsid protein during reverse transcription. Biochemistry 39, 9084-9091.
21. Kallio, E. R., Klingström, J., Gustafsson, E., Manni, T., Vaheri, A., Henttonen, H., Vapalahti, O. & Lundkvist, A. (2006). Prolonged survival of Puumala hantavirus outside the host: evidence for indirect transmission via the environment. J Gen Virol 87, 2127-2134.
22. Klempa, B., Meisel, H., Räth, S., Bartel, J., Ulrich, R. & Krüger, D. H. (2003). Occurrence of renal and pulmonary syndrome in a region of northeast Germany where Tula hantavirus circulates. J Clin Microbiol 41, 4894-4897.
23. Kuismanen, E., Hedman, K., Saraste, J. & Pettersson, R. F. (1982). Uukuniemi virus maturation: accumulation of virus particles and viral antigens in the Golgi complex. Mol Cell Biol 2, 1444-1458.
24. Lifson, J. D., Rossio, J. L., Piatak, M., Bess, J., Chertova, E., Schneider, D. K., Coalter, V. J., Poore, B., Kiser, R. F. & other authors (2004). Evaluation of the safety, immunogenicity, and protective efficacy of whole inactivated simian immunodeficiency virus (SIV) vaccines with conformationally and functionally intact envelope glycoproteins. AIDS Res Hum Retroviruses 20, 772-787.
25. Lu, W., Arraes, L. C., Ferreira, W. T. & Andrieu, J. M. (2004). Therapeutic dendritic-cell vaccine for chronic HIV-1 infection. Nat Med 10, 1359-1365.
26. 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.
27. Lundkvist, A., Hörling, J., Athlin, L., Rosén, 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.
28. Lundkvist, A., Vapalahti, O., Plyusnin, A., Sjölander, K. B., Niklasson, B. & Vaheri, A. (1996a). Characterization of Tula virus antigenic determinants defined by monoclonal antibodies raised against baculo-virus-expressed nucleocapsid protein. Virus Res 45, 29-44.
29. Lundkvist, A., Kallio-Kokko, H., Sjö lander, K. B., Lankinen, H., Niklasson, B., Vaheri, A. & Vapalahti, O. (1996b). Characterization of Puumala virus nucleocapsid protein: identification of B-cell epitopes and domains involved in protective immunity. Virology 216, 397-406.
30. Marsh, M. & Helenius, A. (2006). Virus entry: open sesame. Cell 124, 729-740.
31. McDonnell, N. B., De Guzman, R. N., Rice, W. G., Turpin, J. A. & Summers, M. F. (1997). Zinc ejection as a new rationale for the use of cystamine and related disulfide-containing antiviral agents in the treatment of AIDS. J Med Chem 40, 1969-1976.
32. Mirazimi, A., Mousavi-Jazi, M., Sundqvist, V. A. & Svensson, L. (1999). Free thiol groups are essential for infectivity of human cytomegalovirus. J Gen Virol 80, 2861-2865.
33. Morcock, D. R., Thomas, J. A., Gagliardi, T. D., Gorelick, R. J., Roser, J. D., Chertova, E. N., Bess, J. W., Ott, D. E., Sattentau, Q. J. & other authors (2005). Elimination of retroviral infectivity by N-ethylma-leimide with preservation of functional envelope glycoproteins. J Virol 79, 1533-1542.
34. Pettersson, R. F. (1974). Uukuniemi virus, a non-cubical tick-borne Arbovirus. PhD thesis, University of Helsinki, Helsinki, Finland.
35. Plyusnin, A., Vapalahti, O., Lankinen, H., Lehväslaiho, H., Apekina, N., Myasnikov, Y., Kallio-Kokko, H., Henttonen, H., Lundkvist, A. & other authors (1994). Tula virus: a newly detected hantavirus carried by European common voles. J Virol 68, 7833-7839.
36. Plyusnin, A., Vapalahti, O. & Vaheri, A. (1996). Hantaviruses: genome structure, expression and evolution. J Gen Virol 77, 2677-2687.
37. Potter, S. J., Chew, C. B., Steain, M., Dwyer, D. E. & Saksena, N. K. (2004). Obstacles to successful antiretroviral treatment of HIV-1 infection: problems and perspectives. Indian J Med Res 119, 217-237.
38. Rein, A., Henderson, L. E. & Levin, J. G. (1998). Nucleic-acid-chaperone activity of retroviral nucleocapsid proteins: significance for viral replication. Trends Biochem Sci 23, 297-301.
39. Rice, W. G., Schaeffer, C. A., Harten, B., Villinger, F., South, T. L., Summers, M. F., Henderson, L. E., Bess, J. W., Arthur, L. O. & other authors (1993). Inhibition of HIV-1 infectivity by zinc-ejecting aromatic C-nitroso compounds. Nature 361, 473-475.
40. Rice, W. G., Supko, J. G., Malspeis, L., Buckheit, R. W., Clanton, D., Bu, M., Graham, L., Schaeffer, C. A., Turpin, J. A. & other authors (1995). Inhibitors of HIV nucleocapsid protein zinc fingers as candidates for the treatment of AIDS. Science 270, 1194-1197.
41. Rossio, J. L., Esser, M. T., Suryanarayana, K., Schneider, D. K., Bess, J. W., Vasquez, G. M., Wiltrout, T. A., Chertova, E., Grimes, M. K. & other authors (1998). Inactivation of human immunodeficiency virus type 1 infectivity with preservation of conformational and functional integrity of virion surface proteins. J Virol 72, 7992-8001.
42. Ryser, H. J., Levy, E. M., Mandel, R. & DiSciullo, G. J. (1994). Inhibition of human immunodeficiency virus infection by agents that interfere with thiol-disulfide interchange upon virus-receptor interaction. Proc Natl Acad Sci USA 91, 4559-4563.
43. Sanders, D. A. (2000). Sulfhydryl involvement in fusion mechanisms. Subcell Biochem 34, 483-514.
44. Schmaljohn, C. & Hjelle, B. (1997). Hantaviruses: a global disease problem. Emerg Infect Dis 3, 95-104.
45. Schmaljohn, C. S., Hasty, S. E., Dalrymple, J. M., LeDuc, J. W., Lee, H. W., von Bonsdorff, C. H., Brummer-Korvenkontio, M., Vaheri, A., Tsai, T. F. & other authors (1985). Antigenic and genetic properties of viruses linked to hemorrhagic fever with renal syndrome. Science 227, 1041-1044.
46. Strandin, T., Hepojoki, J., Wang, H., Vaheri, A. & Lankinen, H. (2008). Hantaviruses and TNF-a act synergistically to induce ERK1/2 inactivation in Vero E6 cells. Virol J 5, 110.
47. Tischler, N. D., Gonzalez, A., Perez-Acle, T., Rosemblatt, M. & Valenzuela, P. D. (2005). Hantavirus Gc glycoprotein: evidence for a class II fusion protein. J Gen Virol 86, 2937-2947.
48. Tummino, P. J., Harvey, P. J., McQuade, T., Domagala, J., Gogliotti, R., Sanchez, J., Song, Y. & Hupe, D. (1997). The human immunodeficiency virus type 1 (HIV-1) nucleocapsid protein zinc ejection activity of disulfide benzamides and benzisothiazolones: correlation with anti-HIV and virucidal activities. Antimicrob Agents Chemother 41, 394-400.
49. Vapalahti, O., Kallio-Kokko, H., Närvänen, A., Julkunen, I., Lundkvist, A., Plyusnin, A., Lehväslaiho, 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.
50. Vapalahti, O., Lundkvist, A., Kukkonen, S. K., Cheng, Y., Gilljam, M., Kanerva, M., Manni, T., Pejcoch, M., Niemimaa, J. & other authors (1996). Isolation and characterization of Tula virus, a distinct serotype in the genus Hantavirus, family Bunyaviridae. J Gen Virol 77, 3063-3067.
51. Vapalahti, O., Mustonen, J., Lundkvist, A., Henttonen, H., Plyusnin, A. & Vaheri, A. (2003). Hantavirus infections in Europe. Lancet Infect Dis 3, 653-661.
52. 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.
53. Weissenhorn, W., Hinz, A. & Gaudin, Y. (2007). Virus membrane fusion. FEBS Lett 581, 2150-2155.