Arenavirus Z protein as an antiviral target: Virus inactivation and protein oligomerization by zinc finger-reactive compounds

Journal of General Virology

Volumn 87, Issue 5, 2006, Pages 1217-1228

  García, Cybele C ^a   Djavani, Mahmoud ^b   Topisirovic, Ivan ^c   Borden, Katherine L B ^c   Salvato, María S ^b   Damonte, Elsa B ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b UNIVERSITY OF MARYLAND   (United States)

^c INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

1 (2 GUANIDINE)PHENYLDISULFIDE; 1,2 DITHIANE 4,5 DIOL 1,1 DIOXIDE; 3 NITROPHENYLDISULFIDE; ALDRITHIOL 2; ANTIINFECTIVE AGENT; ANTIVIRUS AGENT; AROMATIC COMPOUND; AZOFORMAMIDE; BIS[2 [N' (2,4 DICHLOROBENZAL)]CARBOXAMIDE 1 BENZENE]DISULFIDE; CYSTEINE; DISULFIDE; FATTY ACID BINDING PROTEIN; METAL ION; NSC 203; NSC 20625; NSC 4493; NSC 624151; NSC 624152; PROMYELOCYTIC LEUKEMIA PROTEIN; RECOMBINANT PROTEIN; RIBAVIRIN; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; VIRUS GLYCOPROTEIN; VIRUS PROTEIN; VIRUS RNA; ZINC FINGER PROTEIN;

ANTIVIRAL ACTIVITY; ARENAVIRUS; ARTICLE; CONTROLLED STUDY; DISULFIDE BOND; DRUG EFFICACY; DRUG TARGETING; ELECTROPHORESIS; HUMAN; HUMAN CELL; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MOLECULAR WEIGHT; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FUNCTION; PROTEIN MOTIF; RNA REPLICATION; VIRION; VIRUS INACTIVATION; VIRUS INFECTION; VIRUS INHIBITION; VIRUS PARTICLE; VIRUS STRAIN;

ANIMALS; AZO COMPOUNDS; CARRIER PROTEINS; CELL LINE; DISULFIDES; HUMANS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; OLIGODEOXYRIBONUCLEOTIDES; RNA, VIRAL; VIRUS REPLICATION; ZINC FINGERS;

ARENAVIRUS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS;

EID: 33646131842     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.81667-0     Document Type: Article

References (71)

1. Albiol Matanic, V. C. & Castilla, V. (2004). Antiviral activity of antimicrobial cationic peptides against Junin virus and herpes simplex virus. Int J Antimicrob Agents 23, 382-389.
2. Andrei, G. & De Clercq, E. (1990). Inhibitory effect of selected antiviral compounds on arenavirus replication in vitro. Antiviral Res 14, 287-299.
3. Auperin, D. D., Romanowski, V., Galinski, M. & Bishop, D. H. L. (1984). Sequencing studies of Pichinde arenavirus S RNA indicate a novel coding strategy, an ambisense viral S RNA. J Virol 52, 897-904.
4. Bartolotta, S., García, C. C., Candurra, N. A. & Damonte, E. B. (2001). Effect of fatty acids on arenavirus replication: inhibition of virus production by lauric acid. Arch Virol 146, 777-790.
5. Borden, K. L. B., Boddy, M. N., Lally, J., O'Reilly, N. J., Martin, S., Howe, K., Solomon, E. & Freemont, P. S. (1995). The solution structure of the RING finger domain from the acute promyelocytic leukaemia proto-oncoprotein PML. EMBO J 14, 1532-1541.
6. Borden, K. L. B., Campbell Dwyer, E. J., Carlile, G. W., Djavani, M. & Salvato, M. S. (1998a). Two RING finger proteins, the oncoprotein PML and the arenavirus Z protein, colocalize with the nuclear fraction of the ribosomal P proteins. J Virol 72, 3819-3826.
7. Borden, K. L. B., Campbell Dwyer, E. J. & Salvato, M. S. (1998b). An arenavirus RING (zinc-binding) protein binds the oncoprotein promyelocyte leukemia protein (PML) and relocates PML nuclear bodies to the cytoplasm. J Virol 72, 758-766.
8. 2-terminal BRCA1 RING finger domain. J Biol Chem 273, 7795-7799.
9. Burns, N. J., III, Barnett, B. B., Huffman, J. H., Dawson, M. I., Sidwell, R. W., De Clercq, E. & Kende, M. (1988). A newly developed immunofluorescent assay for determining the Pichinde virus-inhibitory effects of selected nucleoside analogues. Antiviral Res 10, 89-98.
10. Campbell Dwyer, E. J., Lai, H., MacDonald, R. C., Salvato, M. S. & Borden, K. L. B. (2000). The lymphocytic choriomeningitis virus RING protein Z associates with eukaryotic initiation factor 4E and selectively represses translation in a RING-dependent manner. J Virol 74, 3293-3300.
11. Candurra, N. A., Maskin, L. & Damonte, E. B. (1996). Inhibition of arenavirus multiplication in vitro by phenotiazines. Antiviral Res 31, 149-158.
12. Capili, A. D., Schultz, D. C., Rauscher, F. J., III & Borden, K. L. B. (2001). Solution structure of the PHD domain from the KAP-1 corepressor: structural determinants for PHD, RING and LIM zinc-binding domains. EMBO J 20, 165-177.
13. Castilla, V., Barquero, A. A., Mersich, S. E. & Coto, C. E. (1998). In vitro anti-Junin virus activity of a peptide isolated from Melia azedarach L. leaves. Int J Antimicrob Agents 10, 67-75.
14. Charrel, R. N., Lemasson, J.-J., Garbutt, M., Khelifa, R., De Micco, P., Feldmann, H. & de Lamballerie, X. (2003). New insights into the evolutionary relationships between arenaviruses provided by comparative analysis of small and large segment sequences. Virology 317, 191-196.
15. Chen, X., Chu, M. & Giedroc, D. P. (2000). Spectroscopic characterization of Co(II)-, Ni(II)-, and Cd(II) -substituted wild-type and non-native retroviral-type zinc finger peptides. J Biol Inorg Chem 5, 93-101.
16. Clegg, J. C. S. (2002). Molecular phylogeny of the arenaviruses. Curr Top Microbiol Immunol 262, 1-24.
17. Cordo, S. M., Candurra, N. A. & Damonte, E. B. (1999). Myristic acid analogs are inhibitors of Junin virus replication. Microbes Infect 1, 609-614.
18. Cornu, T. I. & de la Torre, J. C. (2001). RING finger Z protein of lymphocytic choriomeningitis virus (LCMV) inhibits transcription and RNA replication of an LCMV S-segment minigenome. J Virol 75, 9415-9426.
19. Cornu, T. I. & de la Torre, J. C. (2002). Characterization of the arenavirus RING finger Z protein regions required for Z-mediated inhibition of viral RNA synthesis. J Virol 76, 6678-6688.
20. Damonte, E. B. & Coto, C. E. (2002). Treatment of arenavirus infections: from basic studies to the challenge of antiviral therapy. Adv Virus Res 58, 125-155.
21. Damonte, E. B., Mersich, S. E. & Candurra, N. A. (1994). Intracellular processing and transport of Junin virus glycoproteins influences virion infectivity. Virus Res 34, 317-326.
22. Djavani, M., Topisirovic, I., Zapata, J. C. & 8 other authors (2005). The proline-rich homeodomain (PRH/HEX) protein is down-regulated in liver during infection with lymphocytic choriomeningitis virus. J Virol 79, 2461-2473.
23. Eichler, R., Lenz, O., Strecker, T., Eickmann, M., Klenk, H.-D. & Garten, W. (2003a). Identification of Lassa virus glycoprotein signal peptide as a trans-acting maturation factor. EMBO Rep 4, 1084-1088.
24. Eichler, R., Lenz, O., Strecker, T. & Garten, W. (2003b). Signal peptide of Lassa virus glycoprotein GP-C exhibits an unusual length. FEBS Lett 538, 203-206.
25. Eichler, R., Strecker, T., Kolesnikova, L., ter Meulen, J., Weissenhorn, W., Becker, S., Klenk, H. D., Garten, W. & Lenz, O. (2004). Characterization of the Lassa virus matrix protein Z: electron microscopic study of virus-like particles and interaction with the nucleoprotein (NP). Virus Res 100, 249-255.
26. Enría, D. A. & Maiztegui, J. I. (1994). Antiviral treatment of Argentine hemorrhagic fever. Antiviral Res 23, 23-31.
27. Fasman, G. D. (editor) (1996). Circular Dichroism and the Conformational Analysis of Biomolecules. New York: Plenum.
28. Franze-Fernández, M. T., Iapalucci, S., López, N. & Rossi, C. (1993). Subgenomic RNAs of Tacaribe virus. In The Arenaviridae, pp. 113-132. Edited by M. S. Salvato. New York: Plenum.
29. Freed, E. O. (2002). Viral late domains. J Virol 76, 4679-4687.
30. García, C. C., Candurra, N. A. & Damonte, E. B. (2000). Antiviral and virucidal activities against arenaviruses of zinc-finger active compounds. Antivir Chem Chemother 11, 231-238.
31. García, C. C., Candurra, N. A. & Damonte, E. B. (2002a). Mode of inactivation of arenaviruses by disulfide-based compounds. Antiviral Res 55, 437-446.
32. García, C. C., Rosso, M. L., Bertoni, M. D., Maier, M. S. & Damonte, E. B. (2002b). Evaluation of the antiviral activity against Junin virus of macrocyclic trichothecenes produced by the hypocrealean epibiont of Baccharis coridifolia. Planta Med 68, 209-212.
33. García, C. C., Brousse, B. N., Carlucci, M. J., Moglioni, A. G., Martins Alho, M., Moltrasio, G. Y., D'Accorso, N. B. & Damonte, E. B. (2003a). Inhibitory effect of thiosemicarbazone derivatives on Junin virus replication in vitro. Antivir Chem Chemother 14, 99-105.
34. García, C. C., Candurra, N. A. & Damonte, E. B. (2003b). Differential inhibitory action of two azoic compounds against arenaviruses. Int J Antimicrob Agents 21, 319-324.
35. Garcin, D., Rochat, S. & Kolakofsky, D. (1993). The Tacaribe arenavirus small zinc finger protein is required for both mRNA synthesis and genome replication. J Virol 67, 807-812.
36. Grande-Pérez, A., Lázaro, E., Lowenstein, P., Domingo, E. & Manrubia, S. C. (2005). Suppression of viral infectivity through lethal defection. Proc Natl Acad Sci U S A 102, 4448-4452.
37. Guillerm, G., Guillerm, D., Vandenplas-Vitkowski, C., Glapski, C. & De Clercq, E. (2003). Inactivation of S-adenosyl-L-homocysteine hydrolase with novel 5′-thioadenosine derivatives. Antiviral effects. Bioorg Med Chem Lett 13, 1649-1652.
38. Hass, M., Gölnitz, U., Müller, S., Becker-Ziaja, B. & Günther, S. (2004). Replicon system for Lassa virus. J Virol 78, 13793-13803.
39. Howard, C. R. (1993). Antigenic diversity among the arenaviruses. In The Arenaviridae, pp. 37-49. Edited by M. S. Salvato. New York: Plenum.
40. Huang, M., Maynard, A., Turpin, J. A., Graham, L., Janini, G. M., Covell, D. G. & Rice, W. G. (1998). Anti-HIV agents that selectively target retroviral nucleocapsid protein zinc fingers without affecting cellular zinc finger proteins. J Med Chem 41, 1371-1381.
41. Huggins, J. W., Robins, R. K. & Canonico, P. G. (1984). Synergistic antiviral effects of ribavirin and the C-nucleoside analogs tiazofurin and selenazofurin against togaviruses, bunyaviruses, and arenaviruses. Antimicrob Agents Chemother 26, 476-480.
42. Kentsis, A., Gordon, R. E. & Borden, K. L. B. (2002). Self-assembly properties of a model RING domain. Proc Natl Acad Sci U S A 99, 667-672.
43. López, N., Jácamo, R. & Franze-Fernández, M. T. (2001). Transcription and RNA replication of Tacaribe virus genome and antigenome analogs require N and L proteins: Z protein is an inhibitor of these processes. J Virol 75, 12241-12251.
44. McCormick, J. B. & Fisher-Hoch, S. P. (2002). Lassa fever. Curr Top Microbiol Immunol 262, 75-109.
45. McCormick, J. B., King, I. J., Webb, P. A., Scribner, C. L., Craven, R. B., Johnson, K. M., Elliot, L. H. & Belmont-Williams, R. (1986). Lassa fever. Effective therapy with ribavirin. N Engl J Med 314, 20-26.
46. McKee, K. T., Jr, Huggins, J. W., Trahan, C. J. & Mahlandi, B. G. (1988). Ribavirin prophylaxis and therapy for experimental Argentine hemorrhagic fever. Antimicrob Agents Chemother 32, 1304-1309.
47. Miller Jenkins, L. M., Byrd, J. C., Hare, T. & 7 other authors (2005). Studies on the mechanism of inactivation of the HIV-1 nucleocapsid protein NCp7 with 2-mercaptobenzamide thioesters. J Med Chem 48, 2847-2858.
48. Neuman, B. W., Adair, B. D., Burns, J. W., Milligan, R. A., Buchmeier, M. J. & Yeager, M. (2005). Complementarity in the supramolecular design of arenaviruses and retroviruses revealed by electron cryomicroscopy and image analysis. J Virol 79, 3822-3830.
49. Perez, M., Craven, R. C. & de la Torre, J. C. (2003). The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies. Proc Natl Acad Sci U S A 100, 12978-12983.
50. Perez, M., Greenwald, D. L. & de la Torre, J. C. (2004). Myristoylation of the RING finger Z protein is essential for arenavirus budding. J Virol 78, 11443-11448.
51. Peters, C. J. (2002). Human infection with arenaviruses in the Americas. Curr Top Microbiol Immunol 262, 65-74.
52. Rein, A., Ott, D. E., Mirro, J., Arthur, L. O., Rice, W. & Henderson, L. E. (1996). Inactivation of murine leukemia virus by compounds that react with the zinc finger in the viral nucleocapsid protein. J Virol 70, 4966-4972.
53. Rice, W. G., Turpin, J. A., Schaeffer, C. A. & 7 other authors (1996). Evaluation of selected chemotypes in coupled cellular and molecular target-based screens identifies novel HIV-1 zinc finger inhibitors. J Med Chem 39, 3606-3616.
54. Roehm, P. C. & Berg, J. M. (1997). Sequential metal binding by the RING finger domain of BRCA1. Biochemistry 36, 10240-10245.
55. Rotz, L. D., Khan, A. S., Lillibridge, S. R., Ostroff, S. M. & Hughes, J. M. (2002). Public health assessment of potential biological terrorism agents. Emerg Infect Dis 8, 225-230.
56. Salvato, M. S. (1993). Molecular biology of the prototype arenavirus, lymphocytic choriomeningitis virus. In The Arenaviridae, pp. 133-156. Edited by M. S. Salvato. New York: Plenum.
57. Salvato, M. S. & Shimomaye, E. M. (1989). The completed sequence of lymphocytic choriomeningitis virus reveals a unique RNA structure and a gene for a zinc finger protein. Virology 173, 1-10.
58. Salvato, M. S., Schweighofer, K. J., Burns, J. & Shimomaye, E. M. (1992). Biochemical and immunological evidence that the 11 kDa zinc-binding protein of lymphocytic choriomeningitis virus is a structural component of the virus. Virus Res 22, 185-198.
59. Salvato, M. S., Clegg, J. C. S., Buchmeier, M. J., Charrel, R. N., Gonzalez, J.-P., Lukashevich, I. S., Peters, C. J., Rico-Hesse, R. & Romanowski, V. (2005). Arenaviridae. In Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses, pp. 725-733. Edited by C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger & L. A. Ball. London: Elsevier/Academic Press.
60. Sánchez, A. B., Perez, M., Cornu, T. & de la Torre, J. C. (2005). RNA interference-mediated virus clearance from cells both acutely and chronically infected with the prototypic arenavirus lymphocytic choriomeningitis virus. J Virol 79, 11071-11081.
61. Smee, D. F., Morris, J. L., Barnard, D. L. & Van Aerschot, A. (1992). Selective inhibition of arthropod-borne and arenaviruses in vitro by 3′-fluoro-3′-deoxyadenosine. Antiviral Res 18, 151-162.
62. Smee, D. F., Gilbert, J., Leonhardt, J. A., Barnett, B. B., Huggins, J. H. & Sidwell, R. W. (1993). Treatment of lethal Pichinde virus infections in weanling LVG/Lak hamsters with ribavirin, ribamidine, selenazofurin, and ampligen. Antiviral Res 20, 57-70.
63. Strecker, T., Eichler, R., ter Meulen, J., Weissenhorn, W., Klenk, H. D., Garten, W. & Lenz, O. (2003). Lassa virus Z protein is a matrix protein sufficient for the release of virus-like particles. J Virol 77, 10700-10705.
64. Topisirovic, I., Capili, A. D. & Borden, K. L. B. (2002). Gamma interferon and cadmium treatments modulate eukaryotic initiation factor 4E-dependent mRNA transport of cyclin D1 in a PML-dependent manner. Mol Cell Biol 22, 6183-6198.
65. Tortorici, M. A., Ghiringhelli, P. D., Lozano, M. E., Albariño, C. G. & Romanowski, V. (2001). Zinc-binding properties of Junín virus nucleocapsid protein. J Gen Virol 82, 121-128.
66. 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.
67. Turpin, J. A., Song, Y., Inman, J. K., Huang, M., Wallqvist, A., Maynard, A., Covell, D. G., Rice, W. G. & Appella, E. (1999). Synthesis and biological properties of novel pyridinioalkanoyl thiolesters (PATE) as anti-HIV-1 agents that target the viral nucleocapsid protein zinc fingers. J Med Chem 42, 67-86.
68. Uckun, F. M., Petkevich, A. S., Vassilev, A. O., Tibbles, H. E. & Titov, L. (2004). Stampidine prevents mortality in an experimental mouse model of viral hemorrhagic fever caused by Lassa virus. BMC Infect Dis 4, 1.
69. Wachsman, M. B., López, E. M. F., Ramírez, J. A., Galagovsky, L. R. & Coto, C. E. (2000). Antiviral effect of brassinosteroids against herpes virus and arenaviruses. Antivir Chem Chemother 11, 71-77.
70. Witvrouw, M., Desmyter, J. & De Clercq, E. (1994). Antiviral portrait series. 4. Polysulfates as inhibitors of HIV and other enveloped viruses. Antivir Chem Chemother 5, 345-359.
71. Wulff, H., Lange, J. V. & Webb, P. A. (1978). Interrelationships among arenaviruses measured by indirect immunofluorescence. Intervirology 9, 344-350.