Junín virus infection activates the type I interferon pathway in a RIG-I-dependent manner

PLoS Neglected Tropical Diseases

Volumn 6, Issue 5, 2012, Pages

  Huang, Cheng ^a   Kolokoltsova, Olga A ^a   Yun, Nadezdha E ^a   Seregin, Alexey V ^a   Poussard, Allison L ^a   Walker, Aida G ^a   Brasier, Allan R ^a   Zhao, Yingxin ^a   Tian, Bing ^a   de la Torre, Juan Carlos ^b   Paessler, Slobodan ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; INTERFERON; INTERFERON REGULATORY FACTOR 3; MESSENGER RNA; RETINOIC ACID INDUCIBLE PROTEIN I; SMALL INTERFERING RNA; STAT1 PROTEIN; DDX58 PROTEIN, HUMAN; DEAD BOX PROTEIN; STAT1 PROTEIN, HUMAN;

ANIMAL CELL; ARGENTINE HEMORRHAGIC FEVER; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; EPITHELIUM CELL; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; JUNIN VIRUS; MACROPHAGE; MICROBIAL SENSITIVITY TEST; MONOCYTE; NONHUMAN; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VENEZUELAN EQUINE ENCEPHALOMYELITIS ALPHAVIRUS; VIRUS VIABILITY; WESTERN BLOTTING; AMERICAN HEMORRHAGIC FEVER; ARENAVIRUS INFECTION; CELL LINE; GENE EXPRESSION PROFILING; IMMUNOLOGY; METABOLISM; PATHOGENICITY; PHOSPHORYLATION; VIROLOGY;

ARENAVIRIDAE INFECTIONS; CELL LINE; DEAD-BOX RNA HELICASES; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; HEMORRHAGIC FEVER, AMERICAN; HUMANS; INTERFERON TYPE I; JUNIN VIRUS; PHOSPHORYLATION; STAT1 TRANSCRIPTION FACTOR;

EID: 84863698000     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0001659     Document Type: Article

References (54)

1. Buchmeier MJ, de la Torre J-C, Peters CJ, (2007) 51. Arenaviridae: The Viruses and Their Replication. In: Knipe DM, editors. Fields' Virology Philadelphia Lippincott, Williams and Wilkins pp. 1635-1668.
2. Tortorici MA, Albarino CG, Posik DM, Ghiringhelli PD, Lozano ME, et al. (2001) Arenavirus nucleocapsid protein displays a transcriptional antitermination activity in vivo. Virus Res 73: 41-55.
3. Meyer BJ, Southern PJ, (1994) Sequence heterogeneity in the termini of lymphocytic choriomeningitis virus genomic and antigenomic RNAs. J Virol 68: 7659-7664.
4. Beyer WR, Popplau 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.
5. 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.
6. Pinschewer DD, Perez M, Sanchez AB, de la Torre JC, (2003) Recombinant lymphocytic choriomeningitis virus expressing vesicular stomatitis virus glycoprotein. Proc Natl Acad Sci U S A 100: 7895-7900.
7. Poch O, Sauvaget I, Delarue M, Tordo N, (1989) Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO J 8: 3867-3874.
8. Perez M, Craven RC, de la Torre JC, (2003) The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies. Proc Natl Acad Sci U S A 100: 12978-12983.
9. Strecker T, Eichler R, Meulen J, Weissenhorn W, Dieter Klenk H, et al. (2003) Lassa virus Z protein is a matrix protein and sufficient for the release of virus-like particles [corrected]. J Virol 77: 10700-10705.
10. Urata S, Noda T, Kawaoka Y, Yokosawa H, Yasuda J, (2006) Cellular factors required for Lassa virus budding. J Virol 80: 4191-4195.
11. Peters CJ, (2002) Human infection with arenaviruses in the Americas. Curr Top Microbiol Immunol 262: 65-74.
12. McCormick JB, Fisher-Hoch SP, (2002) Lassa fever. Curr Top Microbiol Immunol 262: 75-109.
13. Geisbert TW, Jahrling PB, (2004) Exotic emerging viral diseases: progress and challenges. Nat Med 10: S110-121.
14. Levis SC, Saavedra MC, Ceccoli C, Feuillade MR, Enria DA, et al. (1985) Correlation between endogenous interferon and the clinical evolution of patients with Argentine hemorrhagic fever. J Interferon Res 5: 383-389.
15. Maiztegui JI, (1975) Clinical and epidemiological patterns of Argentine haemorrhagic fever. Bull World Health Organ 52: 567-575.
16. Enria DA, Briggiler AM, Sanchez Z, (2008) Treatment of Argentine hemorrhagic fever. Antiviral Res 78: 132-139.
17. Versteeg GA, Garcia-Sastre A, (2010) Viral tricks to grid-lock the type I interferon system. Curr Opin Microbiol 13: 508-516.
18. Borden EC, Sen GC, Uze G, Silverman RH, Ransohoff RM, et al. (2007) Interferons at age 50: past, current and future impact on biomedicine. Nat Rev Drug Discov 6: 975-990.
19. Bowie AG, Unterholzner L, (2008) Viral evasion and subversion of pattern-recognition receptor signalling. Nat Rev Immunol 8: 911-922.
20. Kawai T, Akira S, (2008) Toll-like receptor and RIG-I-like receptor signaling. Ann N Y Acad Sci 1143: 1-20.
21. Barbalat R, Lau L, Locksley RM, Barton GM, (2009) Toll-like receptor 2 on inflammatory monocytes induces type I interferon in response to viral but not bacterial ligands. Nat Immunol 10: 1200-1207.
22. Barral PM, Sarkar D, Su ZZ, Barber GN, DeSalle R, et al. (2009) Functions of the cytoplasmic RNA sensors RIG-I and MDA-5: key regulators of innate immunity. Pharmacol Ther 124: 219-234.
23. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, et al. (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441: 101-105.
24. Baum A, Sachidanandam R, Garcia-Sastre A, (2010) Preference of RIG-I for short viral RNA molecules in infected cells revealed by next-generation sequencing. Proc Natl Acad Sci U S A 107: 16303-16308.
25. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, et al. (2011) A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472: 481-485.
26. Ferbus D, Saavedra MC, Levis S, Maiztegui J, Falcoff R, (1988) Relation of endogenous interferon and high levels of 2′-5′ oligoadenylate synthetase in leukocytes from patients with Argentine hemorrhagic fever. J Infect Dis 157: 1061-1064.
27. Levis SC, Saavedra MC, Ceccoli C, Falcoff E, Feuillade MR, et al. (1984) Endogenous interferon in Argentine hemorrhagic fever. J Infect Dis 149: 428-433.
28. Heller MV, Saavedra MC, Falcoff R, Maiztegui JI, Molinas FC, (1992) Increased tumor necrosis factor-alpha levels in Argentine hemorrhagic fever. J Infect Dis 166: 1203-1204.
29. Marta RF, Montero VS, Hack CE, Sturk A, Maiztegui JI, et al. (1999) Proinflammatory cytokines and elastase-alpha-1-antitrypsin in Argentine hemorrhagic fever. Am J Trop Med Hyg 60: 85-89.
30. Marta RF, Montero VS, Molinas FC, (1998) Systemic disorders in Argentine haemorrhagic fever. Bulletin De L Institut Pasteur 96: 115-124.
31. Groseth A, Hoenen T, Weber M, Wolff S, Herwig A, et al. (2011) Tacaribe virus but not junin virus infection induces cytokine release from primary human monocytes and macrophages. PLoS Negl Trop Dis 5: e1137.
32. Cuevas CD, Lavanya M, Wang E, Ross SR, (2011) Junin virus infects mouse cells and induces innate immune responses. J Virol 85: 11058-11068.
33. Martinez-Sobrido L, Emonet S, Giannakas P, Cubitt B, Garcia-Sastre A, et al. (2009) Identification of amino acid residues critical for the anti-interferon activity of the nucleoprotein of the prototypic arenavirus lymphocytic choriomeningitis virus. J Virol 83: 11330-11340.
34. Martinez-Sobrido L, Giannakas P, Cubitt B, Garcia-Sastre A, de la Torre JC, (2007) Differential inhibition of type I interferon induction by arenavirus nucleoproteins. J Virol 81: 12696-12703.
35. Martinez-Sobrido L, Zuniga EI, Rosario D, Garcia-Sastre A, de la Torre JC, (2006) Inhibition of the type I interferon response by the nucleoprotein of the prototypic arenavirus lymphocytic choriomeningitis virus. J Virol 80: 9192-9199.
36. Kolokoltsova OA, Yun NE, Poussard AL, Smith JK, Smith JN, et al. (2010) Mice Lacking Alpha/Beta and Gamma Interferon Receptors Are Susceptible to Junin Virus Infection. J Virol 84: 13063-13067.
37. Yun NE, Linde NS, Dziuba N, Zacks MA, Smith JN, et al. (2008) Pathogenesis of XJ and Romero strains of Junin virus in two strains of guinea pigs. Am J Trop Med Hyg 79: 275-282.
38. Forbus J, Spratt H, Wiktorowicz J, Wu Z, Boldogh I, et al. (2006) Functional analysis of the nuclear proteome of human A549 alveolar epithelial cells by HPLC-high resolution 2-D gel electrophoresis. Proteomics 6: 2656-2672.
39. Fusaro VA, Mani DR, Mesirov JP, Carr SA, (2009) Prediction of high-responding peptides for targeted protein assays by mass spectrometry. Nat Biotechnol 27: 190-198.
40. Lange V, Picotti P, Domon B, Aebersold R, (2008) Selected reaction monitoring for quantitative proteomics: a tutorial. Mol Syst Biol 4: 222.
41. Spotts DR, Reich RM, Kalkhan MA, Kinney RM, Roehrig JT, (1998) Resistance to alpha/beta interferons correlates with the epizootic and virulence potential of Venezuelan equine encephalitis viruses and is determined by the 5′ noncoding region and glycoproteins. J Virol 72: 10286-10291.
42. Paessler S, Ni H, Petrakova O, Fayzulin RZ, Yun N, et al. (2006) Replication and clearance of Venezuelan equine encephalitis virus from the brains of animals vaccinated with chimeric SIN/VEE viruses. J Virol 80: 2784-2796.
43. Asper M, Sternsdorf T, Hass M, Drosten C, Rhode A, et al. (2004) Inhibition of different Lassa virus strains by alpha and gamma interferons and comparison with a less pathogenic arenavirus. J Virol 78: 3162-3169.
44. Lucia HL, Coppenhaver DH, Baron S, (1989) Arenavirus infection in the guinea pig model: antiviral therapy with recombinant interferon-alpha, the immunomodulator CL246,738 and ribavirin. Antiviral Res 12: 279-292.
45. Stephen EL, Scott SK, Eddy GA, Levy HB, (1977) Effect of interferon on togavirus and arenavirus infections of animals. Tex Rep Biol Med 35: 449-454.
46. Peters CJ, Liu CT, Anderson GW Jr, Morrill JC, Jahrling PB, (1989) Pathogenesis of viral hemorrhagic fevers: Rift Valley fever and Lassa fever contrasted. Rev Infect Dis 11 (Suppl 4): S743-749.
47. Pozner RG, Ure AE, Jaquenod de Giusti C, D'Atri LP, Italiano JE, et al. (2010) Junin virus infection of human hematopoietic progenitors impairs in vitro proplatelet formation and platelet release via a bystander effect involving type I IFN signaling. PLoS Pathog 6: e1000847.
48. Zhang Z, Liu R, Noordhoek JA, Kauffman HF, (2005) Interaction of airway epithelial cells (A549) with spores and mycelium of Aspergillus fumigatus. J Infect 51: 375-382.
49. Zhou S, Cerny AM, Zacharia A, Fitzgerald KA, Kurt-Jones EA, et al. (2010) Induction and inhibition of type I interferon responses by distinct components of lymphocytic choriomeningitis virus. J Virol 84: 9452-9462.
50. Fan L, Briese T, Lipkin WI, (2010) Z proteins of New World arenaviruses bind RIG-I and interfere with type I interferon induction. J Virol 84: 1785-1791.
51. Marq JB, Hausmann S, Veillard N, Kolakofsky D, Garcin D, (2011) Short double-stranded RNAs with an overhanging 5′ ppp-nucleotide, as found in arenavirus genomes, act as RIG-I decoys. J Biol Chem 286: 6108-6116.
52. Marq JB, Kolakofsky D, Garcin D, (2010) Unpaired 5′ ppp-nucleotides, as found in arenavirus double-stranded RNA panhandles, are not recognized by RIG-I. J Biol Chem 285: 18208-18216.
53. Daffis S, Lazear HM, Liu WJ, Audsley M, Engle M, et al. (2011) The naturally attenuated Kunjin strain of West Nile virus shows enhanced sensitivity to the host type I interferon response. J Virol 85: 5664-5668.
54. Seo SH, Hoffmann E, Webster RG, (2002) Lethal H5N1 influenza viruses escape host anti-viral cytokine responses. Nat Med 8: 950-954.