Inhibition of lassa virus glycoprotein cleavage and multicycle replication by site 1 protease-adapted α1- antitrypsin variants

PLoS Neglected Tropical Diseases

Volumn 3, Issue 6, 2009, Pages

  Maisa, Anna ^a   Ströher, Ute ^b,c   Klenk, Hans Dieter ^a   Garten, Wolfgang ^a   Strecker, Thomas ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^c UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 1 ANTITRYPSIN; PROTEIN C; SITE 1 PROTEASE ADAPTED ALPHA 1 ANTITRYPSIN; UNCLASSIFIED DRUG; ANTIVIRUS AGENT; GLYCOPROTEIN; MEMBRANE BOUND TRANSCRIPTION FACTOR PEPTIDASE, SITE 1; MEMBRANE-BOUND TRANSCRIPTION FACTOR PEPTIDASE, SITE 1; SERINE PROTEINASE; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FEMALE; LASSA VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN CLEAVAGE; PROTEIN MOTIF; PROTEIN PROCESSING; VIRUS INHIBITION; VIRUS REPLICATION; VIRUS TRANSMISSION; ANIMAL; BINDING SITE; CERCOPITHECUS; CHO CELL; CRICETULUS; DRUG ANTAGONISM; DRUG EFFECT; GENE VECTOR; GENETICS; HAMSTER; METABOLISM; PHYSIOLOGY; PROTEIN BINDING; VERO CELL; VESICULAR STOMATITIS VIRUS; VIRUS ASSEMBLY;

ALPHA 1-ANTITRYPSIN; AMINO ACID MOTIFS; ANIMALS; ANTIVIRAL AGENTS; BINDING SITES; CERCOPITHECUS AETHIOPS; CHO CELLS; CRICETINAE; CRICETULUS; GENETIC VECTORS; GLYCOPROTEINS; LASSA VIRUS; PROPROTEIN CONVERTASES; PROTEIN BINDING; SERINE ENDOPEPTIDASES; VERO CELLS; VESICULOVIRUS; VIRAL ENVELOPE PROTEINS; VIRUS ASSEMBLY; VIRUS REPLICATION;

EID: 68349099050     PISSN: None     EISSN: None     Source Type: Journal    
DOI: 10.1371/journal.pntd.0000446     Document Type: Article

References (90)

1. McCormick JB, Fisher-Hoch SP (2002) Lassa fever. Curr Top Microbiol Immunol 262: 75-109.
2. Salazar-Bravo J, Ruedas LA, Yates TL (2002) Mammalian reservoirs of arenaviruses. Curr Top Microbiol Immunol 262: 25-63.
3. Damonte EB, Coto CE (2002) Treatment of arenavirus infections: from basic studies to the challenge of antiviral therapy. Adv Virus Res 58: 125-155.
4. de la Torre JC (2008) Reverse genetics approaches to combat pathogenic arenaviruses. Antiviral Res 80: 239-250.
5. Kunz S, de la Torre JC (2005) Novel antiviral strategies to combat human Arenavirus infections. Curr Mol Med 5: 735-751.
6. Maiztegui JI, Fernandez NJ, de Damilano AJ (1979) Efficacy of immune plasma in treatment of Argentine haemorrhagic fever and association between treatment and a late neurological syndrome. Lancet 2: 1216-1217.
7. Enria DA, Maiztegui JI (1994) Antiviral treatment of Argentine hemorrhagic fever. Antiviral Res 23: 23-31.
8. Kilgore PE, Ksiazek TG, Rollin PE, Mills JN, Villagra MR, et al. (1997) Treatment of Bolivian hemorrhagic fever with intravenous ribavirin. Clin Infect Dis 24: 718-722.
9. McCormick JB, King IJ, Webb PA, Scribner CL, Craven RB, et al. (1986) Lassa fever. Effective therapy with ribavirin. N Engl J Med 314: 20-26.
10. Enria DA, Briggiler AM, Levis S, Vallejos D, Maiztegui JI, et al. (1987) Tolerance and antiviral effect of ribavirin in patients with Argentine hemorrhagic fever. Antiviral Res 7: 353-359.
11. Canonico PG, Kende M, Huggins JW (1984) The toxicology and pharmacology of ribavirin in experimental animals. Smith RA, Knight V, Smith JAD, eds. New York: Academic Press. pp 65-77.
12. Kochhar DM, Penner JD, Knudsen TB (1980) Embryotoxic, teratogenic, and metabolic effects of ribavirin in mice. Toxicol Appl Pharmacol 52: 99-112.
13. Page T, Connor JD (1990) The metabolism of ribavirin in erythrocytes and nucleated cells. Int J Biochem 22: 379-383.
14. Fisher-Hoch SP, Gborie S, Parker L, Huggins J (1992) Unexpected adverse reactions during a clinical trial in rural west Africa. Antiviral Res 19: 139-147.
15. Muller MP, Dresser L, Raboud J, McGeer A, Rea E, et al. (2007) Adverse events associated with high-dose ribavirin: evidence from the Toronto outbreak of severe acute respiratory syndrome. Pharmacotherapy 27: 494-503.
16. Delgado S, Erickson BR, Agudo R, Blair PJ, Vallejo E, et al. (2008) Chapare virus, a newly discovered arenavirus isolated from a fatal hemorrhagic fever case in Bolivia. PLoS Pathog 4: e1000047. doi:10.1371/ journal.ppat.1000047.
17. Zeller H, Leitmeyer K, Santos CV, Coulombier D (2008) Unknown disease in South Africa identified as arenavirus infection. Euro Surveill 13: 19008.
18. Djavani M, Lukashevich IS, Sanchez A, Nichol ST, Salvato MS (1997) Completion of the Lassa fever virus sequence and identification of a RING finger open reading frame at the L RNA 5′ end. Virology 235: 414-418.
19. Auperin DD, McCormick JB (1989) Nucleotide sequence of the Lassa virus (Josiah strain) S genome RNA and amino acid sequence comparison of the N and GPC proteins to other arenaviruses. Virology 168: 421-425.
20. Eichler R, Lenz O, Strecker T, Garten W (2003) Signal peptide of Lassa virus glycoprotein GP-C exhibits an unusual length. FEBS Lett 538: 203-206.
21. Sakai J, Rawson RB, Espenshade PJ, Cheng D, Seegmiller AC, et al. (1998) Molecular identification of the sterol-regulated luminal protease that cleaves SREBPs and controls lipid composition of animal cells. Mol Cell 2: 505-514.
22. Seidah NG, Mowla SJ, Hamelin J, Mamarbachi AM, Benjannet S, et al. (1999) Mammalian subtilisin/kexin isozyme SKI-1: A widely expressed proprotein convertase with a unique cleavage specificity and cellular localization. Proc Natl Acad Sci U S A 96: 1321-1326.
23. Lenz O, ter Meulen J, Klenk HD, Seidah NG, Garten W (2001) The Lassa virus glycoprotein precursor GP-C is proteolytically processed by subtilase SKI-1/S1P. Proc Natl Acad Sci U S A 98: 12701-12705.
24. Neuman BW, Adair BD, Burns JW, Milligan RA, Buchmeier MJ, et al. (2005) Complementarity in the supramolecular design of arenaviruses and retroviruses revealed by electron cryomicroscopy and image analysis. J Virol 79: 3822-3830.
25. York J, Romanowski V, Lu M, Nunberg JH (2004) The signal peptide of the Junin arenavirus envelope glycoprotein is myristoylated and forms an essential subunit of the mature G1-G2 complex. J Virol 78: 10783-10792.
26. Beyer WR, Pöpplau D, Garten W, von Laer D, Lenz O (2003) Endoproteolytic processing of the lymphocytic choriomeningitis virus glycoprotein by the subtilase SKI-1/S1P. J Virol 77: 2866-2872.
27. Brown MS, Goldstein JL (1999) A proteolytic pathway that controls the cholesterol content of membranes, cells, and blood. Proc Natl Acad Sci U S A 96: 11041-11048.
28. Patra D, Xing X, Davies S, Bryan J, Franz C, et al. (2007) Site-1 protease is essential for endochondral bone formation in mice. J Cell Biol 179: 687-700.
29. Ye J, Rawson RB, Komuro R, Chen X, Dave UP, et al. (2000) ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 6: 1355-1364.
30. Schlombs K, Wagner T, Scheel J (2003) Site-1 protease is required for cartilage development in zebrafish. Proc Natl Acad Sci U S A 100: 14024-14029.
31. De Windt A, Rai M, Bernier L, Thelen K, Soini J, et al. (2007) Gene set enrichment analysis reveals several globally affected pathways due to SKI-1/S1P inhibition in HepG2 cells. DNA Cell Biol 26: 765-772.
32. Lenz O, ter Meulen J, Feldmann H, Klenk HD, Garten W (2000) Identification of a novel consensus sequence at the cleavage site of the Lassa virus glycoprotein. J Virol 74: 11418-11421.
33. Rojek JM, Lee AM, Nguyen N, Spiropoulou CF, Kunz S (2008) Site 1 protease is required for proteolytic processing of the glycoproteins of the South American hemorrhagic fever viruses Junin, Machupo, and Guanarito. J Virol 82: 6045-6051.
34. Kunz S, Edelmann KH, de la Torre JC, Gorney R, Oldstone MB (2003) Mechanisms for lymphocytic choriomeningitis virus glycoprotein cleavage, transport, and incorporation into virions. Virology 314: 168-178.
35. Vincent MJ, Sanchez AJ, Erickson BR, Basak A, Chretien M, et al. (2003) Crimean-Congo hemorrhagic fever virus glycoprotein proteolytic processing by subtilase SKI-1. J Virol 77: 8640-8649.
36. Bergeron E, Vincent MJ, Nichol ST (2007) Crimean-Congo hemorrhagic fever virus glycoprotein processing by the endoprotease SKI-1/S1P is critical for virus infectivity. J Virol 81: 13271-13276.
37. Owen MC, Brennan SO, Lewis JH, Carrell RW (1983) Mutation of antitrypsin to antithrombin. alpha 1-antitrypsin Pittsburgh (358 Met leads to Arg), a fatal bleeding disorder. N Engl J Med 309: 694-698.
38. Anderson ED, Thomas L, Hayflick JS, Thomas G (1993) Inhibition of HIV-1 gp160-dependent membrane fusion by a furin-directed alpha 1-antitrypsin variant. J Biol Chem 268: 24887-24891.
39. Jean F, Thomas L, Molloy SS, Liu G, Jarvis MA, et al. (2000) A protein-based therapeutic for human cytomegalovirus infection. Proc Natl Acad Sci U S A 97: 2864-2869.
40. Watanabe M, Hirano A, Stenglein S, Nelson J, Thomas G, et al. (1995) Engineered serine protease inhibitor prevents furin-catalyzed activation of the fusion glycoprotein and production of infectious measles virus. J Virol 69: 3206-3210.
41. Bahbouhi B, Bendjennat M, Guetard D, Seidah NG, Bahraoui E (2000) Effect of alpha-1 antitrypsin Portland variant (alpha 1-PDX) on HIV-1 replication. Biochem J 352(Pt 1): 91-98.
42. Pullikotil P, Vincent M, Nichol ST, Seidah NG (2004) Development of protein-based inhibitors of the proprotein of convertase SKI-1/S1P: processing of SREBP-2, ATF6, and a viral glycoprotein. J Biol Chem 279: 17338-17347.
43. Higuchi R, Krummel B, Saiki RK (1988) A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res 16: 7351-7367.
44. Rawson RB, Cheng D, Brown MS, Goldstein JL (1998) Isolation of cholesterol-requiring mutant Chinese hamster ovary cells with defects in cleavage of sterol regulatory element-binding proteins at site 1. J Biol Chem 273: 28261-28269.
45. Lawson ND, Stillman EA, Whitt MA, Rose JK (1995) Recombinant vesicular stomatitis viruses from DNA. Proc Natl Acad Sci U S A 92: 4477-4481.
46. Rose NF, Roberts A, Buonocore L, Rose JK (2000) Glycoprotein exchange vectors based on vesicular stomatitis virus allow effective boosting and generation of neutralizing antibodies to a primary isolate of human immunodeficiency virus type 1. J Virol 74: 10903-10910.
47. Kretzschmar E, Buonocore L, Schnell MJ, Rose JK (1997) High-efficiency incorporation of functional influenza virus glycoproteins into recombinant vesicular stomatitis viruses. J Virol 71: 5982-5989.
48. Garbutt M, Liebscher R, Wahl-Jensen V, Jones S, Möller P, et al. (2004) Properties of replication-competent vesicular stomatitis virus vectors expressing glycoproteins of filoviruses and arenaviruses. J Virol 78: 5458-5465.
49. Klenk HD, Garten W, Rott R (1984) Inhibition of proteolytic cleavage of the hemagglutinin of influenza virus by the calcium-specific ionophore A23187. EMBO J 3: 2911-2915.
50. Matrosovich M, Matrosovich T, Garten W, Klenk HD (2006) New low-viscosity overlay medium for viral plaque assays. Virol J 3: 63.
51. Hierholzer JC, Killington RA (1996) Virus isolation and quantitation. In: Virology Methods Manual. Mathy BWJ, Kangro HO, eds. London: Academic Press. pp 25-46.
52. Strecker T, Eichler R, Meulen J, Weissenhorn W, Klenk H-D, et al. (2003) Lassa virus Z protein is a matrix protein and sufficient for the release of virus-like particles. J Virol 77: 10700-10705.
53. Schnell MJ, Buonocore L, Kretzschmar E, Johnson E, Rose JK (1996) Foreign glycoproteins expressed from recombinant vesicular stomatitis viruses are incorporated efficiently into virus particles. Proc Natl Acad Sci U S A 93: 11359-11365.
54. Tani H, Komoda Y, Matsuo E, Suzuki K, Hamamoto I, et al. (2007) Replication-competent recombinant vesicular stomatitis virus encoding hepatitis C virus envelope proteins. J Virol 81: 8601-8612.
55. Gossen M, Freundlieb S, Bender G, Müller G, Hillen W, et al. (1995) Transcriptional activation by tetracyclines in mammalian cells. Science 268: 1766-1769.
56. Singh J, Itahana Y, Knight-Krajewski S, Kanagawa M, Campbell KP, et al. (2004) Proteolytic enzymes and altered glycosylation modulate dystroglycan function in carcinoma cells. Cancer Res 64: 6152-6159.
57. Stieneke-Gröber A, Vey M, Angliker H, Shaw E, Thomas G, et al. (1992) Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisin-like endoprotease. EMBO J 11: 2407-2414.
58. Bolken TC, Laquerre S, Zhang Y, Bailey TR, Pevear DC, et al. (2006) Identification and characterization of potent small molecule inhibitor of hemorrhagic fever New World arenaviruses. Antiviral Res 69: 86-97.
59. Larson RA, Dai D, Hosack VT, Tan Y, Bolken TC, et al. (2008) Identification of a broad-spectrum arenavirus entry inhibitor. J Virol 82: 10768-10775.
60. Lee AM, Rojek JM, Gundersen A, Ströher U, Juteau JM, et al. (2008) Inhibition of cellular entry of lymphocytic choriomeningitis virus by amphipathic DNA polymers. Virology 372: 107-117.
61. Lee AM, Rojek JM, Spiropoulou CF, Gundersen AT, Jin W, et al. (2008) Unique small molecule entry inhibitors of hemorrhagic fever arenaviruses. J Biol Chem 283: 18734-18742.
62. Müller S, Günther S (2007) Broad-spectrum antiviral activity of small interfering RNA targeting the conserved RNA termini of Lassa virus. Antimicrob Agents Chemother 51: 2215-2218.
63. Acosta EG, Bruttomesso AC, Bisceglia JA, Wachsman MB, Galagovsky LR, et al. (2008) Dehydroepiandrosterone, epiandrosterone and synthetic derivatives inhibit Junin virus replication in vitro. Virus Res 135: 203-212.
64. Sepulveda CS, Fascio ML, Mazzucco MB, Palacios ML, Pellon RF, et al. (2008) Synthesis and evaluation of N-substituted acridones as antiviral agents against haemorrhagic fever viruses. Antivir Chem Chemother 19: 41-47.
65. Capul AA, de la Torre JC (2008) A cell-based luciferase assay amenable to high-throughput screening of inhibitors of arenavirus budding. Virology 382: 107-114.
66. Garcia CC, Djavani M, Topisirovic I, Borden KL, Salvato MS, et al. (2006) Arenavirus Z protein as an antiviral target: virus inactivation and protein oligomerization by zinc finger-reactive compounds. J Gen Virol 87: 1217-1228.
67. Gowen BB, Smee DF, Wong MH, Hall JO, Jung KH, et al. (2008) Treatment of late stage disease in a model of arenaviral hemorrhagic fever: T-705 efficacy and reduced toxicity suggests an alternative to ribavirin. PLoS ONE 3: e3725. doi:10.1371/journal.pone.0003725.
68. Cordelier P, Strayer DS (2003) Conditional expression of alpha1-antitrypsin delivered by recombinant SV40 vectors protects lymphocytes against HIV. Gene Ther 10: 2153-2156.
69. Cordelier P, Zern MA, Strayer DS (2003) HIV-1 proprotein processing as a target for gene therapy. Gene Ther 10: 467-477.
70. Johnson KM, McCormick JB, Webb PA, Smith ES, Elliott LH, et al. (1987) Clinical virology of Lassa fever in hospitalized patients. J Infect Dis 155: 456-464.
71. Ströher U, Willihnganz L, Jean F, Feldmann H (2007) Blockage of filoviral glycoprotein processing by use of a protein-based inhibitor. J Infect Dis 196(Suppl 2): S271-S275.
72. Jean F, Stella K, Thomas L, Liu G, Xiang Y, et al. (1998) alpha1-Antitrypsin Portland, a bioengineered serpin highly selective for furin: application as an antipathogenic agent. Proc Natl Acad Sci U S A 95: 7293-7298.
73. Pullikotil P, Benjannet S, Mayne J, Seidah NG (2007) The proprotein convertase SKI-1/S1P: alternate translation and subcellular localization. J Biol Chem 282: 27402-27413.
74. Schäfer W, Stroh A, Berghöfer S, Seiler J, Vey M, et al. (1995) Two independent targeting signals in the cytoplasmic domain determine trans-Golgi network localization and endosomal trafficking of the proprotein convertase furin. EMBO J 14: 2424-2435.
75. Teuchert M, Berghöfer S, Klenk HD, Garten W (1999) Recycling of furin from the plasma membrane. Functional importance of the cytoplasmic tail sorting signals and interaction with the AP-2 adaptor medium chain subunit. J Biol Chem 274: 36781-36789.
76. Garten W, Hallenberger S, Ortmann D, Schaäfer W, Vey M, et al. (1994) Processing of viral glycoproteins by the subtilisin-like endoprotease furin and its inhibition by specific peptidylchloroalkylketones. Biochimie 76: 217-225.
77. Hallenberger S, Bosch V, Angliker H, Shaw E, Klenk HD, et al. (1992) Inhibition of furin-mediated cleavage activation of HIV-1 glycoprotein gp160. Nature 360: 358-361.
78. Strecker T, Lenz O, ter Meulen J, Klenk H-D, Garten W (2002) Potential Inhibitors for SKI-1/S1P which cleaves the Lassa virus glycoprotein precursor GP-C. XIIth International Congress of Virology, IUMS, Paris, France.
79. Pasquato A, Pullikotil P, Asselin MC, Vacatello M, Paolillo L, et al. (2006) The proprotein convertase SKI-1/S1P. In vitro analysis of Lassa virus glycoprotein-derived substrates and ex vivo validation of irreversible peptide inhibitors. J Biol Chem 281: 23471-23481.
80. Strecker T, Maisa A, Eichler R, ter Meulen J, Klenk H-D, et al. (2004) Identification of inhibitors for the Lassa virus GP-C activating enzyme SKI-1/S1P. Gordon Research Conference on Proprotein Processing, Trafficking & Secretion, New London, USA.
81. Hawkins JL, Robbins MD, Warren LC, Xia D, Petras SF, et al. (2008) Pharmacologic inhibition of site 1 protease activity inhibits sterol regulatory element-binding protein processing and reduces lipogenic enzyme gene expression and lipid synthesis in cultured cells and experimental animals. J Pharmacol Exp Ther 326: 801-808.
82. Basak S, Mohottalage D, Basak A (2006) Multibranch and pseudopeptide approach for design of novel inhibitors of subtilisin kexin isozyme-1. Protein Pept Lett 13: 863-876.
83. Bodvard K, Mohlin J, Knecht W (2007) Recombinant expression, purification, and kinetic and inhibitor characterisation of human site-1-protease. Protein Expr Purif 51: 308-319.
84. He Y, Duan W, Tan SL (2007) Emerging host cell targets for hepatitis C therapy. Drug Discov Today 12: 209-217.
85. Provencher VM, Coccaro E, Lacasse JJ, Schang LM (2004) Antiviral drugs that target cellular proteins may play major roles in combating HIV resistance. Curr Pharm Des 10: 4081-4101.
86. Schang LM, St Vincent MR, Lacasse JJ (2006) Five years of progress on cyclin-dependent kinases and other cellular proteins as potential targets for antiviral drugs. Antivir Chem Chemother 17: 293-320.
87. Neumann G, Feldmann H, Watanabe S, Lukashevich I, Kawaoka Y (2002) Reverse genetics demonstrates that proteolytic processing of the Ebola virus glycoprotein is not essential for replication in cell culture. J Virol 76: 406-410.
88. Neumann G, Geisbert TW, Ebihara H, Geisbert JB, Daddario-DiCaprio KM, et al. (2007) Proteolytic processing of the Ebola virus glycoprotein is not critical for Ebola virus replication in nonhuman primates. J Virol 81: 2995-2998.
89. Volchkov VE, Feldmann H, Volchkova VA, Klenk HD (1998) Processing of the Ebola virus glycoprotein by the proprotein convertase furin. Proc Natl Acad Sci U S A 95: 5762-5767.
90. Klenk HD, Garten W (1994) Host cell proteases controlling virus pathogenicity. Trends Microbiol 2: 39-43.