Modulation of innate immune responses by hantaviruses

Critical Reviews in Immunology

Volumn 30, Issue 6, 2010, Pages 515-527

  Rang, Andreas ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Antiviral state; Interferon lambda; Reassortment; TLR3; TRAF3

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; GAMMA INTERFERON; NUCLEOCAPSID PROTEIN;

ANTIVIRAL ACTIVITY; GENOME ANALYSIS; HANTAVIRUS; HANTAVIRUS INFECTION; HUMAN; IMMUNOMODULATION; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS INHIBITION; VIRUS REPLICATION; VIRUS VIRULENCE;

EID: 78650046006     PISSN: 10408401     EISSN: None     Source Type: Journal    
DOI: 10.1615/critrevimmunol.v30.i6.20     Document Type: Review

References (113)

1. Meyer BJ, Schmaljohn CS. Persistent hantavirus infections: characteristics and mechanisms. Trends Microbiol. 2000;8:61-7.
2. Krüger DH, Ulrich R, Lundkvist AA. Hantavirus infections and their prevention. Microbes Infect. 2001; 3:1129-44.
3. Schmaljohn C, Hjelle B. Hantaviruses: a global disease problem. Emerg. Infect. Dis. 1997; 3:95-104.
4. Schönrich G, Rang A, Lutteke N, Raftery MJ, Charbonnel N, Ulrich RG. Hantavirus-induced immunity in rodent reservoirs and humans. Immunol Rev. 2008; 225:163-89.
5. Khaiboullina SF, Morzunov SP, St Jeor SC. Hantaviruses: molecular biology, evolution and pathogenesis. Curr Mol Med. 2005; 5:773-90.
6. Peters CJ, Simpson GL, Levy H. Spectrum of hantavirus infection: hemorrhagic fever with renal syndrome and hantavirus pulmonary syndrome. Annu Rev Med. 1999; 50:531-45.
7. Vapalahti O, Mustonen J, Lundkvist A, Henttonen H, Plyusnin A, Vaheri A. Hantavirus infections in Europe. Lancet Infect Dis. 2003; 3:653-61.
8. Lee PW, Amyx HL, Gajdusek DC, Yanagihara RT, Goldgaber D, Gibbs CJ, Jr. New hemorrhagic fever with renal syndrome-related virus in rodents in the United States. Lancet. 1982; 2:1405.
9. Yanagihara R, Amyx HL, Lee PW, Asher DM, Gibbs CJ, Jr., Gajdusek DC. Experimental hantavirus infection in nonhuman primates. Arch Virol. 1988; 101:125-30.
10. Yanagihara R, Daum CA, Lee PW, Baek LJ, Amyx HL, Gajdusek DC, Gibbs CJ Jr. Serological survey of Prospect Hill virus infection in indigenous wild rodents in the USA. Trans R Soc Trop Med Hyg. 1987; 81:42-5.
11. Yanagihara R, Gajdusek DC, Gibbs CJ, Jr., Traub R. Prospect Hill virus: serologic evidence for infection in mammologists. N Engl J Med. 1984; 310:1325-6.
12. Klempa B, Meisel H, Rath S, Bartel J, Ulrich R, Krüger DH. Occurrence of renal and pulmonary syndrome in a region of northeast Germany where Tula hantavirus circulates. J Clin Microbiol. 2003; 41:4894-7.
13. Guhl S, Franke R, Schielke A, Johne R, Krüger DH, Babina M, Rang A. Infection of in vivo differentiated human mast cells with hantaviruses. J Gen Virol. 2010; 91:1256-61.
14. Raftery MJ, Kraus AA, Ulrich R, Krüger DH, Schonrich G. Hantavirus infection of dendritic cells. J Virol. 2002; 76:10724-33.
15. Zaki SR, Albers RC, Greer PW, Coffield LM, Armstrong LR, Khan AS, Khabbaz R, Peters CJ. Retrospective diagnosis of a 1983 case of fatal hantavirus pulmonary syndrome. Lancet. 1994; 343:1037-8.
16. Zaki SR, Greer PW, Coffield LM, Goldsmith CS, Nolte KB, Foucar K, Feddersen RM, Zumwalt RE, Miller GL, Khan AS, et al. Hantavirus pulmonary syndrome. Pathogenesis of an emerging infectious disease. Am J Pathol. 1995; 146:552-79.
17. Gavrilovskaya IN, Gorbunova EE, Mackow NA, Mackow ER. Hantaviruses direct endothelial cell permeability by sensitizing cells to the vascular permeability factor VEGF, while angiopoietin 1 and sphingosine 1-phosphate inhibit hantavirus-directed permeability. J Virol. 2008; 82:5797-806.
18. Gavrilovskaya IN, Peresleni T, Geimonen E, Mackow ER. Pathogenic hantaviruses selectively inhibit beta3 integrin directed endothelial cell migration. Arch Virol. 2002; 147:1913-31.
19. Gavrilovskaya IN, Brown EJ, Ginsberg MH, Mackow ER. Cellular entry of hantaviruses which cause hemorrhagic fever with renal syndrome is mediated by beta3 integrins. J Virol. 1999; 73:3951-9.
20. Gavrilovskaya IN, Shepley M, Shaw R, Ginsberg MH, Mackow ER. beta3 Integrins mediate the cellular entry of hantaviruses that cause respiratory failure. Proc Natl Acad Sci U S A. 1998; 95:7074-9.
21. Mackow ER, Gavrilovskaya IN. Cellular receptors and hantavirus pathogenesis. Curr Top Microbiol Immunol. 2001; 256:91-115.
22. Geimonen E, Neff S, Raymond T, Kocer SS, Gavrilovskaya IN, Mackow ER. Pathogenic and nonpathogenic hantaviruses differentially regulate endothelial cell responses. Proc Natl Acad Sci U S A. 2002; 99:13837-42.
23. Handke W, Oelschlegel R, Franke R, Krüger DH, Rang A. Hantaan virus triggers TLR3-dependent innate immune responses. J Immunol. 2009; 182:2849-58.
24. Linderholm M, Ahlm C, Settergren B, Waage A, Tarnvik A. Elevated plasma levels of tumor necrosis factor (TNF)-alpha, soluble TNF receptors, interleukin (IL)-6, and IL-10 in patients with hemorrhagic fever with renal syndrome. J Infect Dis. 1996; 173:38-43.
25. Sundstrom JB, McMullan LK, Spiropoulou CF, Hooper WC, Ansari AA, Peters CJ, Rollin PE. Hantavirus infection induces the expression of RANTES and IP-10 without causing increased permeability in human lung microvascular endothelial cells. J Virol. 2001; 75:6070-85.
26. Temonen M, Mustonen J, Helin H, Pasternack A, Vaheri A, Holthofer H. Cytokines, adhesion molecules, and cellular infiltration in nephropathia epidemica kidneys: an immunohistochemical study. Clin Immunol Immunopathol. 1996; 78:47-55.
27. Alff PJ, Gavrilovskaya IN, Gorbunova E, Endriss K, Chong Y, Geimonen E, Sen N, Reich NC, Mackow ER. The pathogenic NY-1 hantavirus G1 cytoplasmic tail inhibits RIG-I- and TBK-1-directed interferon responses. J Virol. 2006; 80:9676-86.
28. Alff PJ, Sen N, Gorbunova E, Gavrilovskaya IN, Mackow ER. The NY-1 hantavirus Gn cytoplasmic tail coprecipitates TRAF3 and inhibits cellular interferon responses by disrupting TBK1-TRAF3 complex formation. J Virol. 2008; 82:9115-22.
29. Khaiboullina SF, Rizvanov AA, Otteson E, Miyazato A, Maciejewski J, St Jeor S. Regulation of cellular gene expression in endothelial cells by sin nombre and prospect hill viruses. Viral Immunol. 2004; 17:234-51.
30. Kraus AA, Raftery MJ, Giese T, Ulrich R, Zawatzky R, Hippenstiel S, Suttorp N, Krüger DH, Schönrich G. Differential antiviral response of endothelial cells after infection with pathogenic and nonpathogenic hantaviruses. J Virol. 2004; 78:6143-50.
31. Spiropoulou CF, Albarino CG, Ksiazek TG, Rollin PE. Andes and Prospect Hill hantaviruses differ in early induction of interferon although both can downregulate interferon signaling. J Virol. 2007; 81:2769-76.
32. Elliott RM, Schmaljohn CS, Collett MS. Bunyaviridae genome structure and gene expression. Curr Top Microbiol Immunol. 1991; 169:91-141.
33. Jin M, Park J, Lee S, Park B, Shin J, Song KJ, Ahn TI, Hwang SY, Ahn BY, Ahn K. Hantaan virus enters cells by clathrin-dependent receptor-mediated endocytosis. Virology. 2002; 294:60-9.
34. Garcin D, Lezzi M, Dobbs M, Elliott RM, Schmaljohn C, Kang CY, Kolakofsky D. The 5′ ends of Hantaan virus (Bunyaviridae) RNAs suggest a prime-and-realign mechanism for the initiation of RNA synthesis. J Virol. 1995; 69:5754-62.
35. Hutchinson KL, Peters CJ, Nichol ST. Sin Nombre virus mRNA synthesis. Virology. 1996; 224:139-49.
36. Mir MA, Brown B, Hjelle B, Duran WA, Panganiban AT. Hantavirus N protein exhibits genus-specific recognition of the viral RNA panhandle. J Virol. 2006; 80:11283-92.
37. Mir MA, Duran WA, Hjelle BL, Ye C, Panganiban AT. Storage of cellular 5′ mRNA caps in P bodies for viral cap-snatching. Proc Natl Acad Sci U S A. 2008; 105:19294-9.
38. Mir MA, Panganiban AT. A protein that replaces the entire cellular eIF4F complex. EMBO J. 2008; 2:3129-39.
39. Mir MA, Sheema S, Haseeb A, Haque A. Hantavirus nucleocapsid protein has distinct m7G cap and RNA binding sites. J Biol Chem. 2010; 285:11357-68.
40. Panganiban AT, Mir MA. Bunyavirus N: eIF4F surrogate and cap-guardian. Cell Cycle. 2009; 8:1332-7.
41. Hepojoki JM, Strandin T, Wang H, Vapalahti O, Vaheri A, Lankinen H. The Cytoplasmic Tails of Hantavirus Glyco-proteins Interact with the Nucleocapsid Protein. J Gen Virol. 2010; 91:2341-50.
42. Ravkov EV, Nichol ST, Compans RW. Polarized entry and release in epithelial cells of Black Creek Canal virus, a New World hantavirus. J Virol. 1997; 71:1147-54.
43. Henderson WW, Monroe MC, St Jeor SC, Thayer WP, Rowe JE, Peters CJ, Nichol ST. Naturally occurring Sin Nombre virus genetic reassortants. Virology. 1995; 214:602-10.
44. Klempa B, Schmidt HA, Ulrich R, Kaluz S, Labuda M, Meisel H, Hjelle B, Krüger DH. Genetic interaction between distinct Dobrava hantavirus subtypes in Apodemus agrarius and A. flavicollis in nature. J Virol. 2003; 77:804-9.
45. Li D, Schmaljohn AL, Anderson K, Schmaljohn CS. Complete nucleotide sequences of the M and S segments of two hantavirus isolates from California: evidence for reassortment in nature among viruses related to hantavirus pulmonary syndrome. Virology. 1995; 206:973-83.
46. Razzauti M, Plyusnina A, Sironen T, Henttonen H, Plyusnin A. 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. 2009; 90:1923-31.
47. Rizvanov AA, Khaiboullina SF, St Jeor S. Development of reassortant viruses between pathogenic hantavirus strains. Virology. 2004; 327:225-32.
48. Rodriguez LL, Owens JH, Peters CJ, Nichol ST. Genetic reassortment among viruses causing hantavirus pulmonary syndrome. Virology. 1998; 242:99-106.
49. Zou Y, Hu J, Wang ZX, Wang DM, Yu C, Zhou JZ, Fu ZF, Zhang YZ. Genetic characterization of hantaviruses isolated from Guizhou, China: evidence for spillover and reassortment in nature. J Med Virol. 2008; 80:1033-41.
50. McElroy AK, Smith JM, Hooper JW, Schmaljohn CS. Andes virus M genome segment is not sufficient to confer the virulence associated with Andes virus in Syrian hamsters. Virology. 2004; 326:130-9.
51. Handke W, Oelschlegel R, Franke R, Wiedemann L, Krüger DH, Rang A. Generation and characterisation of genetic reassortants between Puumala and Prospect Hill hantavirus in vitro. J Gen Virol. 2010; 91:2351-9.
52. Randall RE, Goodbourn S. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol. 2008; 89:1-47.
53. Garcia-Sastre A, Biron CA. Type 1 interferons and the virus-host relationship: a lesson in detente. Science. 2006; 312:879-82.
54. Versteeg GA, Garcia-Sastre A. Viral tricks to grid-lock the type I interferon system. Curr Opin Microbiol. 2010; 13:508-16.
55. Borden EC, Sen GC, Uze G, Silverman RH, Ransohoff RM, Foster GR, Stark GR. Interferons at age 50: past, current and future impact on biomedicine. Nat Rev Drug Discov. 2007; 6:975-90.
56. Ank N, West H, Paludan SR. IFN-lambda: novel antiviral cytokines. J Interferon Cytokine Res. 2006; 26:373-9.
57. Young HA. Unraveling the pros and cons of interferon-gamma gene regulation. Immunity. 2006; 24:506-7.
58. Platanias LC. Introduction: interferon signals: what is classical and what is nonclassical? J Interferon Cytokine Res. 2005; 25:732.
59. Platanias LC. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol. 2005; 5:375-86.
60. Uddin S, Platanias LC. Mechanisms of type-I interferon signal transduction. J Biochem Mol Biol. 2004; 37:635-41.
61. Stark GR. How cells respond to interferons revisited: from early history to current complexity. Cytokine Growth Factor Rev. 2007; 18:419-23.
62. Staeheli P. Interferon-induced proteins and the antiviral state. Adv Virus Res. 1990; 38:147-200.
63. Zhou A, Paranjape JM, Der SD, Williams BR, Silverman RH. Interferon action in triply deficient mice reveals the existence of alternative antiviral pathways. Virology. 1999; 258:435-40.
64. Rang A, Bruns M, Heise T, Will H. Antiviral activity of interferon-alpha against hepatitis B virus can be studied in non-hepatic cells and is independent of MxA. J Biol Chem. 2002; 277:7645-7.
65. Oelschlegel R, Krüger DH, Rang A. MxA-independent inhibition of Hantaan virus replication induced by type I and type II interferon in vitro. Virus Res. 2007; 127:100-5.
66. Elliott R, Weber F. Bunyaviruses and the Type I Interferon System. Viruses. 2009; 1:1003-21.
67. Levy DE, Marie IJ. RIGging an antiviral defense - it's in the CARDs. Nat Immunol. 2004; 5:699-701.
68. Medzhitov R, Janeway CA, Jr. Decoding the patterns of self and nonself by the innate immune system. Science. 2002; 296:298-300.
69. Janeway CA, Jr., Medzhitov R. Innate immune recognition. Annu Rev Immunol. 2002; 20:197-216.
70. Thompson AJ, Locarnini SA. Toll-like receptors, RIG-I-like RNA helicases and the antiviral innate immune response. Immunol Cell Biol. 2007;85:435-45.
71. Fitzgerald KA, McWhirter SM, Faia KL, Rowe DC, Latz E, Golenbock DT, Coyle AJ, Liao SM, Maniatis T. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol. 2003; 4:491-6.
72. Onoguchi K, Yoneyama M, Takemura A, Akira S, Taniguchi T, Namiki H, Fujita T. Viral infections activate types I and III interferon genes through a common mechanism. J Biol Chem. 2007; 282:7576-81.
73. Osterlund PI, Pietila TE, Veckman V, Kotenko SV, Julkunen I. IFN regulatory factor family members differentially regulate the expression of type III IFN (IFN-lambda) genes. J Immunol. 2007; 179:3434-42.
74. Hiscott J, Pitha P, Genin P, Nguyen H, Heylbroeck C, Mamane Y, Algarte M, Lin R. Triggering the interferon response: the role of IRF-3 transcription factor. J Interferon Cytokine Res. 1999; 19:1-13.
75. Sadler AJ, Williams BR. Interferon-inducible antiviral effectors. Nat Rev Immunol. 2008; 8:559-68.
76. Takeuchi O, Akira S. Recognition of viruses by innate immunity. Immunol Rev. 2007; 220:214-24.
77. Oganesyan G, Saha SK, Guo B, He JQ, Shahangian A, Zarnegar B, Perry A, Cheng G. Critical role of TRAF3 in the Toll-like receptor-dependent and -independent antiviral response. Nature. 2006; 439:208-11.
78. Handke W, Oelschlegel R, Franke R, Krüger DH, Rang A. Hantaan virus triggers TLR3-dependent innate immune responses. J Immunol. 2009; 182:2849-58.
79. Tissari J, Siren J, Meri S, Julkunen I, Matikainen S. IFN-alpha enhances TLR3-mediated antiviral cytokine expression in human endothelial and epithelial cells by up-regulating TLR3 expression. J Immunol. 2005; 174:4289-94.
80. Edelmann KH, Richardson-Burns S, Alexopoulou L, Tyler KL, Flavell RA, Oldstone MB. Does Toll-like receptor 3 play a biological role in virus infections? Virology. 2004; 322:231-8.
81. Takeuchi O, Akira S. Recognition of viruses by innate immunity. Immunol Rev. 2007; 220:214-24.
82. Lee HK, Lund JM, Ramanathan B, Mizushima N, Iwasaki A. Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science. 2007; 315:1398-401.
83. Guillot L, Le Goffic R, Bloch S, Escriou N, Akira S, Chignard M, et al. Involvement of toll-like receptor 3 in the immune response of lung epithelial cells to double-stranded RNA and influenza A virus. J. Biol. Chem. 2005; 280:5571-80.
84. Le Goffic R, Balloy V, Lagranderie M, Alexopoulou L, Escriou N, Flavell R, Chignard M, Si-Tahar M. Detrimental contribution of the Toll-like receptor (TLR)3 to influenza A virus-induced acute pneumonia. PLoS Pathog. 2006;2:e53.
85. Rudd BD, Burstein E, Duckett CS, Li X, Lukacs NW. Differential role for TLR3 in respiratory syncytial virus-induced chemokine expression. J Virol. 2005; 79:3350-7.
86. Rudd BD, Smit JJ, Flavell RA, Alexopoulou L, Schaller MA, Gruber A, Berlin AA, Lukacs NW. Deletion of TLR3 alters the pulmonary immune environment and mucus production during respiratory syncytial virus infection. J Immunol. 2006; 176:1937-42.
87. Wang T, Town T, Alexopoulou L, Anderson JF, Fikrig E, Flavell RA. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat Med. 2004; 10:1366-73.
88. Gowen BB, Hoopes JD, Wong MH, Jung KH, Isakson KC, Alexopoulou L, Flavell RA, Sidwell RW. TLR3 deletion limits mortality and disease severity due to Phlebovirus infection. J Immunol. 2006; 177:6301-7.
89. Hardarson HS, Baker JS, Yang Z, Purevjav E, Huang CH, Alexopoulou L, Li N, Flavell RA, Bowles NE, Vallejo JG. Toll-like receptor 3 is an essential component of the innate stress response in virus-induced cardiac injury. Am J Physiol Heart Circ Physiol. 2007; 292:H251-8.
90. Habjan M, Andersson I, Klingström J, Schümann M, Martin A, Zimmermann P, Wagner V, Pichlmair A, Schneider U, Mühlberger E, Mirazimi A, Weber F. Processing of genome 5′ termini as a strategy of negative-strand RNA viruses to avoid RIG-I-dependent interferon induction. PLoS ONE. 2008; 3:e2032.
91. Hornung V, Ellegast J, Kim S, Brzozka K, Jung A, Kato H, Poeck H, Akira S, Conzelmann KK, Schlee M, Endres S, Hartmann G. 5′-Triphosphate RNA is the ligand for RIG-I. Science. 2006; 314:994-7.
92. Pichlmair A, Schulz O, Tan CP, Näslund TI, Liljeström P, Weber F, Reis e Sousa C. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science. 2006; 314:997-1001.
93. Temonen M, Lankinen H, Vapalahti O, Ronni T, Julkunen I, Vaheri A. Effect of interferon-alpha and cell differentiation on Puumala virus infection in human monocyte/macrophages. Virology. 1995; 206:8-15.
94. Stoltz M, Ahlm C, Lundkvist A, Klingström J. Lambda interferon (IFN-lambda) in serum is decreased in hantavirus-infected patients, and in vitro-established infection is insensitive to treatment with all IFNs and inhibits IFN-gamma-induced nitric oxide production. J Virol. 2007; 81:8685-91.
95. Prescott J, Hall P, Acuna-Retamar M, Ye C, Wathelet MG, Ebihara H, Feldmann H, Hjelle B. New World Hantaviruses Activate IFNeλ Production in Type I IFN-Deficient Vero E6 Cells. Plos One. 2010; 5(6): e11159.
96. Stoltz M, Klingström J. Alpha/Beta Interferon (IFN-{alpha}/{beta})- Independent Induction of IFN-{lambda}1 (Interleukin-29) in Response to Hantaan Virus Infection. J Virol. 2010; 84:9140-8.
97. Kirsanovs S, Klempa B, Franke R, Lee M, Schönrich G, Rang A, Krüger DH. Genetic reassortment between high-virulent and low-virulent Dobrava-Belgrade virus strains. Virus Genes. 2010; 41(3):319-28.
98. Tamura M, Asada H, Kondo K, Takahashi M, Yamanishi K. Effects of human and murine interferons against hemorrhagic fever with renal syndrome (HFRS) virus (Hantaan virus). Antiviral Res. 1987; 8:171-8.
99. Wichmann D, Gröne HJ, Frese M, Pavlovic J, Anheier B, Haller O, Klenk HD, Feldmann H. Hantaan virus infection causes an acute neurological disease that is fatal in adult laboratory mice. J Virol. 2002; 76:8890-9.
100. Haller O, Staeheli P, Kochs G. Interferon-induced Mx proteins in antiviral host defense. Biochimie. 2007; 89:812-8.
101. Honda K, Taniguchi T. IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat Rev Immunol. 2006; 6:644-58.
102. Taylor SL, Frias-Staheli N, Garcia-Sastre A, Schmaljohn CS. Hantaan virus nucleocapsid protein binds to importin alpha proteins and inhibits tumor necrosis factor alpha-induced activation of nuclear factor kappa B. J Virol. 2009; 83:1271-9.
103. Taylor SL, Krempel RL, Schmaljohn CS. Inhibition of TNF-alpha-induced activation of NF-kappaB by hantavirus nucleocapsid proteins. Ann N Y Acad Sci. 2009; 1171 Suppl. 1:E86-93.
104. Jääskeläinen KM, Kaukinen P, Minskaya ES, Plyusnina A, Vapalahti O, Elliott RM, Weber F, Vaheri A, Plyusnin A. Tula and Puumala hantavirus NSs ORFs are functional and the products inhibit activation of the interferon-beta promoter. J Med Virol. 2007; 79:1527-36.
105. Rang A, Heider H, Ulrich R, Krüger DH. A novel method for cloning of non-cytolytic viruses. J Virol Meth. 2006; 135:26-31.
106. Mackow ER, Gavrilovskaya IN. Hantavirus regulation of endothelial cell functions. Thromb Haemost. 2009; 102:1030-41.
107. Sen N, Sen A, Mackow ER. Degrons at the C terminus of the pathogenic but not the nonpathogenic hantavirus G1 tail direct proteasomal degradation. J Virol. 2007; 81:4323-30.
108. Geimonen E, Fernandez I, Gavrilovskaya IN, Mackow ER. Tyrosine residues direct the ubiquitination and degradation of the NY-1 hantavirus G1 cytoplasmic tail. J Virol. 2003; 77:10760-868.
109. Alff PJ, Sen N, Gorbunova E, Gavrilovskaya IN, Mackow ER. The NY-1 hantavirus Gn cytoplasmic tail coprecipitates TRAF3 and inhibits cellular interferon responses by disrupting TBK1-TRAF3 complex formation. J Virol. 2008; 82:9115-22.
110. Wang H, Strandin T, Hepojoki J, Lankinen H, Vaheri A. Degradation and aggresome formation of the Gn tail of the apathogenic Tula hantavirus. J Gen Virol. 2009; 90:2995-3001.
111. Briese T, Bird B, Kapoor V, Nichol ST, Lipkin WI. Batai and Ngari viruses: M segment reassortment and association with severe febrile disease outbreaks in East Africa. J Virol. 2006; 80:5627-30.
112. Li XL, Boyanapalli M, Weihua X, Kalvakolanu DV, Hassel BA. Induction of interferon synthesis and activation of interferon-stimulated genes by liposomal transfection reagents. J Interferon Cytokine Res. 1998; 18:947-52.
113. Zhu FG, Reich CF, Pisetsky DS. Effect of cytofectins on the immune response of murine macrophages to mammalian DNA. Immunology. 2003; 109:255-62.