Rift Valley fever virus NSs protein functions and the similarity to other bunyavirus NSs proteins

Virology Journal

Volumn 13, Issue 1, 2016, Pages

  Ly, Hoai J ^a   Ikegami, Tetsuro ^a,b  

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

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Bunyavirus; E3 ligase; Interferon; NSs; p53; p62; Phlebovirus; PKR; Rift Valley fever virus; TFIIH; Ubiquitin

Indexed keywords

AMINO ACID; BETA INTERFERON; DNA; F BOX PROTEIN; PROTEIN KINASE R; PROTEIN P53; PROTEIN P62; STIMULATORY GUANINE NUCLEOTIDE BINDING PROTEIN; UBIQUITIN PROTEIN LIGASE E3; VIRUS PROTEIN; VIRAL PROTEIN;

ARTICLE; BIOLOGICAL FUNCTIONS; BUNYAVIRIDAE; CELL CYCLE ARREST; CHROMATIN; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DNA DAMAGE; GENE CONTROL; GENETIC VARIABILITY; HANTAVIRUS; HOST CELL; NAIROVIRUS; NONHUMAN; ORTHOBUNYAVIRUS; PHLEBOVIRUS; PROTEIN FUNCTION; RIFT VALLEY FEVER VIRUS; TOSPOVIRUS; ANIMAL; APOPTOSIS; CLASSIFICATION; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; PATHOPHYSIOLOGY; RIFT VALLEY FEVER; VIROLOGY;

ANIMALS; APOPTOSIS; HUMANS; INTERFERON-BETA; RIFT VALLEY FEVER; RIFT VALLEY FEVER VIRUS; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84976585846     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/s12985-016-0573-8     Document Type: Article

References (148)

1. Daubney R, Hudson JR. Enzootic hepatitis or Rift Valley fever: An undescribed virus disease of sheep cattle and man from east Africa. J Pathol Bacteriol. 1931;34:545-79.
2. Swanepoel R, Coetzer JAW. Rift Valley fever. In: Coetzer JAW, Tustin RC, editors. Infectious diseases of livestock with special reference to southern Africa. 2nd ed. Cape Town: Oxford University Press; 2004. p. 1037-70.
3. Shoemaker T, Boulianne C, Vincent MJ, Pezzanite L, Al-Qahtani MM, Al-Mazrou Y, et al. Genetic analysis of viruses associated with emergence of Rift Valley fever in Saudi Arabia and Yemen, 2000-01. Emerg Infect Dis. 2002;8:1415-20.
4. Carroll SA, Reynes JM, Khristova ML, Andriamandimby SF, Rollin PE, Nichol ST. Genetic evidence for Rift Valley fever outbreaks in Madagascar resulting from virus introductions from the East African mainland rather than enzootic maintenance. J Virol. 2011;85:6162-7.
5. Meegan JM. The Rift Valley fever epizootic in Egypt 1977-78. 1. Description of the epizzotic and virological studies. Trans R Soc Trop Med Hyg. 1979;73:618-23.
6. Bird BH, Khristova ML, Rollin PE, Ksiazek TG, Nichol ST. Complete genome analysis of 33 ecologically and biologically diverse Rift Valley fever virus strains reveals widespread virus movement and low genetic diversity due to recent common ancestry. J Virol. 2007;81:2805-16.
7. Schmaljohn C, Nichol ST. Bunyaviridae. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE, editors. Fields Virology. 5th ed. Philadelphia: Lippincott, Williams & Wilkins; 2007. p. 1741-89.
8. Coetzer JA, Barnard BJ. Hydrops amnii in sheep associated with hydranencephaly and arthrogryposis with wesselsbron disease and rift valley fever viruses as aetiological agents. Onderstepoort J Vet Res. 1977;44:119-26.
9. Easterday BC. Rift valley fever. Adv Vet Sci. 1965;10:65-127.
10. Ikegami T, Makino S. The Pathogenesis of Rift Valley Fever. Viruses. 2011;3:493-519.
11. CDC. Rift Valley fever outbreak - Kenya, November 2006-January 2007. MMWR Morb Mortal Wkly Rep. 2007;56:73-6.
12. Bird BH, Ksiazek TG, Nichol ST, Maclachlan NJ. Rift Valley fever virus. J Am Vet Med Assoc. 2009;234:883-93.
13. Linthicum KJ, Davies FG, Kairo A, Bailey CL. Rift Valley fever virus (family Bunyaviridae, genus Phlebovirus). Isolations from Diptera collected during an inter-epizootic period in Kenya. J Hyg (Lond). 1985;95:197-209.
14. Pepin M, Bouloy M, Bird BH, Kemp A, Paweska J. Rift Valley fever virus (Bunyaviridae: Phlebovirus): an update on pathogenesis, molecular epidemiology, vectors, diagnostics and prevention. Vet Res. 2010;41:61.
15. Turell MJ, Dohm DJ, Fonseca DM. Comparison of the Potential for Different Genetic Forms in the Culex pipiens Complex in North America to Transmit Rift Valley Fever Virus. J Am Mosq Control Assoc. 2014;30:253-9.
16. Balenghien T, Cardinale E, Chevalier V, Elissa N, Failloux AB, Jean Jose Nipomichene TN, et al. Towards a better understanding of Rift Valley fever epidemiology in the south-west of the Indian Ocean. Vet Res. 2013;44:78.
17. CDC. Rift Valley fever with retinopathy-Canada. MMWR Morb Mortal Wkly Rep. 1979;28:607-8.
18. Mansfield KL, Banyard AC, McElhinney L, Johnson N, Horton DL, Hernandez-Triana LM, et al. Rift Valley fever virus: A review of diagnosis and vaccination, and implications for emergence in Europe. Vaccine. 2015;33:5520-31.
19. Miller MM, Bennett KE, Drolet BS, Lindsay R, Mecham JO, Reeves WK, et al. Evaluation of the efficacy, potential for vector transmission, and duration of immunity of MP-12, an attenuated Rift Valley fever virus vaccine candidate, in sheep. Clin Vaccine Immunol. 2015;22:930-7.
20. Peters CJ, Reynolds JA, Slone TW, Jones DE, Stephen EL. Prophylaxis of Rift Valley fever with antiviral drugs, immune serum, an interferon inducer, and a macrophage activator. Antiviral Res. 1986;6:285-97.
21. Kende M, Alving CR, Rill WL, Swartz Jr GM, Canonico PG. Enhanced efficacy of liposome-encapsulated ribavirin against Rift Valley fever virus infection in mice. Antimicrob Agents Chemother. 1985;27:903-7.
22. Huggins JW. Prospects for treatment of viral hemorrhagic fevers with ribavirin, a broad-spectrum antiviral drug. Rev Infect Dis. 1989;11 Suppl 4:S750-61.
23. Kende M, Lupton HW, Rill WL, Levy HB, Canonico PG. Enhanced therapeutic efficacy of poly(ICLC) and ribavirin combinations against Rift Valley fever virus infection in mice. Antimicrob Agents Chemother. 1987;31:986-90.
24. Kende M. Prophylactic and therapeutic efficacy of poly(I, C)-LC against Rift Valley fever virus infection in mice. J Biol Response Mod. 1985;4:503-11.
25. Morrill JC, Jennings GB, Cosgriff TM, Gibbs PH, Peters CJ. Prevention of Rift Valley fever in rhesus monkeys with interferon-alpha. Rev Infect Dis. 1989;11 Suppl 4:S815-25.
26. Manns MP, Wedemeyer H, Cornberg M. Treating viral hepatitis C: efficacy, side effects, and complications. Gut. 2006;55:1350-9.
27. Elliott RM. Orthobunyaviruses: recent genetic and structural insights. Nat Rev Microbiol. 2014;12:673-85.
28. Jaaskelainen KM, Kaukinen P, Minskaya ES, Plyusnina A, Vapalahti O, Elliott RM, et al. 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.
29. Altamura LA, Bertolotti-Ciarlet A, Teigler J, Paragas J, Schmaljohn CS, Doms RW. Identification of a novel C-terminal cleavage of Crimean-Congo hemorrhagic fever virus PreGN that leads to generation of an NSM protein. J Virol. 2007;81:6632-42.
30. Kormelink R, Storms M, Van Lent J, Peters D, Goldbach R. Expression and subcellular location of the NSM protein of tomato spotted wilt virus (TSWV), a putative viral movement protein. Virology. 1994;200:56-65.
31. Barnwal B, Karlberg H, Mirazimi A, Tan YJ. The Non-structural Protein of Crimean-Congo Hemorrhagic Fever Virus Disrupts the Mitochondrial Membrane Potential and Induces Apoptosis. J Biol Chem. 2016;291:582-92.
32. Reguera J, Weber F, Cusack S. Bunyaviridae RNA polymerases (L-protein) have an N-terminal, influenza-like endonuclease domain, essential for viral cap-dependent transcription. PLoS Pathog. 2010;6:e1001101.
33. Garcin D, Lezzi M, Dobbs M, Elliott RM, Schmaljohn C, Kang CY, et al. 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.
34. Klemm C, Reguera J, Cusack S, Zielecki F, Kochs G, Weber F. Systems to establish bunyavirus genome replication in the absence of transcription. J Virol. 2013;87:8205-12.
35. Morin B, Coutard B, Lelke M, Ferron F, Kerber R, Jamal S, et al. The N-terminal domain of the arenavirus L protein is an RNA endonuclease essential in mRNA transcription. PLoS Pathog. 2010;6:e1001038.
36. Ikegami T, Won S, Peters CJ, Makino S. Characterization of Rift Valley fever virus transcriptional terminations. J Virol. 2007;81:8421-38.
37. Albarino CG, Bird BH, Nichol ST. A shared transcription termination signal on negative and ambisense RNA genome segments of Rift Valley fever, sandfly fever Sicilian, and Toscana viruses. J Virol. 2007;81:5246-56.
38. Lara E, Billecocq A, Leger P, Bouloy M. Characterization of wild-type and alternate transcription termination signals in the Rift Valley fever virus genome. J Virol. 2011;85:12134-45.
39. Barr JN. Bunyavirus mRNA synthesis is coupled to translation to prevent premature transcription termination. RNA. 2007;13:731-6.
40. Barr JN, Rodgers JW, Wertz GW. Identification of the Bunyamwera bunyavirus transcription termination signal. J Gen Virol. 2006;87:189-98.
41. Gerrard SR, Nichol ST. Synthesis, proteolytic processing and complex formation of N-terminally nested precursor proteins of the Rift Valley fever virus glycoproteins. Virology. 2007;357:124-33.
42. Weingartl HM, Zhang S, Marszal P, McGreevy A, Burton L, Wilson WC. Rift Valley fever virus incorporates the 78 kDa glycoprotein into virions matured in mosquito C6/36 cells. PLoS ONE. 2014;9:e87385.
43. Kreher F, Tamietti C, Gommet C, Guillemot L, Ermonval M, Failloux AB, et al. The Rift Valley fever accessory proteins NSm and P78/NSm-Gn are determinants of virus propagation in vertebrate and invertebrate hosts. Emerg Microbes Infect. 2014;3:e71.
44. Kading RC, Crabtree MB, Bird BH, Nichol ST, Erickson BR, Horiuchi K, et al. Deletion of the NSm virulence gene of Rift Valley fever virus inhibits virus replication in and dissemination from the midgut of Aedes aegypti mosquitoes. PLoS Negl Trop Dis. 2014;8:e2670.
45. Crabtree MB, Kent Crockett RJ, Bird BH, Nichol ST, Erickson BR, Biggerstaff BJ, et al. Infection and transmission of Rift Valley fever viruses lacking the NSs and/or NSm genes in mosquitoes: potential role for NSm in mosquito infection. PLoS Negl Trop Dis. 2012;6:e1639.
46. Won S, Ikegami T, Peters CJ, Makino S. NSm protein of Rift Valley fever virus suppresses virus-induced apoptosis. J Virol. 2007;81:13335-45.
47. Terasaki K, Won S, Makino S. The C-terminal region of Rift Valley fever virus NSm protein targets the protein to the mitochondrial outer membrane and exerts anti-apoptotic function. J Virol. 2013;87:676-82.
48. Plyusnina A, Beaty BJ, Elliott RM, Goldbach R, Kormelink R, Lundkvist A, et al. Family Bunyaviridae. In: King AMQ, Adams MJ, Carsten EB, Lefkowitz EJ, editors. Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses. 1st ed. London: Elsevier; 2011. p. 725-41.
49. Dionisio D, Esperti F, Vivarelli A, Valassina M. Epidemiological, clinical and laboratory aspects of sandfly fever. Curr Opin Infect Dis. 2003;16:383-8.
50. Sabin AB. Experimental studies on Phlebotomus (pappataci, sandfly) fever during World War II. Arch Gesamte Virusforsch. 1951;4:367-410.
51. Tesh RB. The genus Phlebovirus and its vectors. Annu Rev Entomol. 1988;33:169-81.
52. Liu S, Chai C, Wang C, Amer S, Lv H, He H, et al. Systematic review of severe fever with thrombocytopenia syndrome: virology, epidemiology, and clinical characteristics. Rev Med Virol. 2014;24:90-102.
53. Liu Q, He B, Huang SY, Wei F, Zhu XQ. Severe fever with thrombocytopenia syndrome, an emerging tick-borne zoonosis. Lancet Infect Dis. 2014;14:763-72.
54. Saito T, Fukushima K, Umeki K, Nakajima K. Severe fever with thrombocytopenia syndrome in Japan and public health communication. Emerg Infect Dis. 2015;21:487-9.
55. Yun SM, Lee WG, Ryou J, Yang SC, Park SW, Roh JY, et al. Severe fever with thrombocytopenia syndrome virus in ticks collected from humans, South Korea, 2013. Emerg Infect Dis. 2014;20:1358-61.
56. Vasconcelos PF, Calisher CH. Emergence of Human Arboviral Diseases in the Americas, 2000-2016. Vector Borne Zoonotic Dis. 2016;16:295-301.
57. Xu F, Chen H, Travassos da Rosa AP, Tesh RB, Xiao SY. Phylogenetic relationships among sandfly fever group viruses (Phlebovirus: Bunyaviridae) based on the small genome segment. J Gen Virol. 2007;88:2312-9.
58. Giorgi C, Accardi L, Nicoletti L, Gro MC, Takehara K, Hilditch C, et al. Sequences and coding strategies of the S RNAs of Toscana and Rift Valley fever viruses compared to those of Punta Toro, Sicilian Sandfly fever, and Uukuniemi viruses. Virology. 1991;180:738-53.
59. Yadani FZ, Kohl A, Prehaud C, Billecocq A, Bouloy M. The carboxy-terminal acidic domain of Rift Valley Fever virus NSs protein is essential for the formation of filamentous structures but not for the nuclear localization of the protein. J Virol. 1999;73:5018-25.
60. Billecocq A, Spiegel M, Vialat P, Kohl A, Weber F, Bouloy M, et al. NSs protein of Rift Valley fever virus blocks interferon production by inhibiting host gene transcription. J Virol. 2004;78:9798-806.
61. Cyr N, de la Fuente C, Lecoq L, Guendel I, Chabot PR, Kehn-Hall K, et al. A OmegaXaV motif in the Rift Valley fever virus NSs protein is essential for degrading p62, forming nuclear filaments and virulence. Proc Natl Acad Sci U S A. 2015;112:6021-6.
62. Le May N, Dubaele S, Proietti De Santis L, Billecocq A, Bouloy M, Egly JM. TFIIH transcription factor, a target for the Rift Valley hemorrhagic fever virus. Cell. 2004;116:541-50.
63. Iben S, Tschochner H, Bier M, Hoogstraten D, Hozak P, Egly JM, et al. TFIIH plays an essential role in RNA polymerase I transcription. Cell. 2002;109:297-306.
64. Kalveram B, Lihoradova O, Ikegami T. NSs Protein of Rift Valley Fever Virus Promotes Post-Translational Downregulation of the TFIIH Subunit p62. J Virol. 2011;85:6234-43.
65. Sorokin AV, Kim ER, Ovchinnikov LP. Proteasome system of protein degradation and processing. Biochemistry (Mosc). 2009;74:1411-42.
66. Hershko A, Ciechanover A. The ubiquitin system. Annu Rev Biochem. 1998;67:425-79.
67. Randow F, Lehner PJ. Viral avoidance and exploitation of the ubiquitin system. Nat Cell Biol. 2009;11:527-34.
68. Komander D, Rape M. The ubiquitin code. Annu Rev Biochem. 2012;81:203-29.
69. Kainulainen M, Habjan M, Hubel P, Busch L, Lau S, Colinge J, et al. Virulence factor NSs of rift valley fever virus recruits the F-box protein FBXO3 to degrade subunit p62 of general transcription factor TFIIH. J Virol. 2014;88:3464-73.
70. Petroski MD, Deshaies RJ. Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol. 2005;6:9-20.
71. Deshaies RJ, Joazeiro CA. RING domain E3 ubiquitin ligases. Annu Rev Biochem. 2009;78:399-434.
72. Chen M, Gerlier D. Viral hijacking of cellular ubiquitination pathways as an anti-innate immunity strategy. Viral Immunol. 2006;19:349-62.
73. Li T, Chen X, Garbutt KC, Zhou P, Zheng N. Structure of DDB1 in complex with a paramyxovirus V protein: viral hijack of a propeller cluster in ubiquitin ligase. Cell. 2006;124:105-17.
74. Wolfe LS, Stanley BJ, Liu C, Eliason WK, Xiong Y. Dissection of the HIV Vif interaction with human E3 ubiquitin ligase. J Virol. 2010;84:7135-9.
75. Schrofelbauer B, Yu Q, Zeitlin SG, Landau NR. Human immunodeficiency virus type 1 Vpr induces the degradation of the UNG and SMUG uracil-DNA glycosylases. J Virol. 2005;79:10978-87.
76. Belzile JP, Duisit G, Rougeau N, Mercier J, Finzi A, Cohen EA. HIV-1 Vpr-mediated G2 arrest involves the DDB1-CUL4AVPRBP E3 ubiquitin ligase. PLoS Pathog. 2007;3:e85.
77. Le Rouzic E, Belaidouni N, Estrabaud E, Morel M, Rain JC, Transy C, et al. HIV1 Vpr arrests the cell cycle by recruiting DCAF1/VprBP, a receptor of the Cul4-DDB1 ubiquitin ligase. Cell Cycle. 2007;6:182-8.
78. Dallaire F, Blanchette P, Groitl P, Dobner T, Branton PE. Identification of integrin alpha3 as a new substrate of the adenovirus E4orf6/E1B 55-kilodalton E3 ubiquitin ligase complex. J Virol. 2009;83:5329-38.
79. Gori Savellini G, Weber F, Terrosi C, Habjan M, Martorelli B, Cusi MG. Toscana virus induces interferon although its NSs protein reveals antagonistic activity. J Gen Virol. 2011;92:71-9.
80. Simons JF, Persson R, Pettersson RF. Association of the nonstructural protein NSs of Uukuniemi virus with the 40S ribosomal subunit. J Virol. 1992;66:4233-41.
81. Wu X, Qi X, Liang M, Li C, Cardona CJ, Li D, et al. Roles of viroplasm-like structures formed by nonstructural protein NSs in infection with severe fever with thrombocytopenia syndrome virus. FASEB J. 2014;28:2504-16.
82. Wu X, Qi X, Qu B, Zhang Z, Liang M, Li C, et al. Evasion of antiviral immunity through sequestering of TBK1/IKKepsilon/IRF3 into viral inclusion bodies. J Virol. 2014;88:3067-76.
83. Santiago FW, Covaleda LM, Sanchez-Aparicio MT, Silvas JA, Diaz-Vizarreta AC, Patel JR, et al. Hijacking of RIG-I signaling proteins into virus-induced cytoplasmic structures correlates with the inhibition of type I interferon responses. J Virol. 2014;88:4572-85.
84. Kalveram B, Lihoradova O, Indran SV, Head JA, Ikegami T. Using click chemistry to measure the effect of viral infection on host-cell RNA synthesis. J Vis Exp. 2013;78:50809.
85. Lihoradova OA, Indran SV, Kalveram B, Lokugamage N, Head JA, Gong B, et al. Characterization of Rift Valley Fever Virus MP-12 Strain Encoding NSs of Punta Toro Virus or Sandfly Fever Sicilian Virus. PLoS Negl Trop Dis. 2013;7:e2181.
86. Indran SV, Lihoradova OA, Phoenix I, Lokugamage N, Kalveram B, Head JA, et al. Rift Valley fever virus MP-12 vaccine encoding Toscana virus NSs retains neuroinvasiveness in mice. J Gen Virol. 2013;94:1441-50.
87. Kalveram B, Ikegami T. Toscana Virus NSs Protein Promotes Degradation of Double-Stranded RNA-Dependent Protein Kinase. J Virol. 2013;87:3710-8.
88. Weber F, Dunn EF, Bridgen A, Elliott RM. The Bunyamwera virus nonstructural protein NSs inhibits viral RNA synthesis in a minireplicon system. Virology. 2001;281:67-74.
89. Thomas D, Blakqori G, Wagner V, Banholzer M, Kessler N, Elliott RM, et al. Inhibition of RNA polymerase II phosphorylation by a viral interferon antagonist. J Biol Chem. 2004;279:31471-7.
90. Leonard VH, Kohl A, Hart TJ, Elliott RM. Interaction of Bunyamwera Orthobunyavirus NSs protein with mediator protein MED8: a mechanism for inhibiting the interferon response. J Virol. 2006;80:9667-75.
91. Brower CS, Sato S, Tomomori-Sato C, Kamura T, Pause A, Stearman R, et al. Mammalian mediator subunit mMED8 is an Elongin BC-interacting protein that can assemble with Cul2 and Rbx1 to reconstitute a ubiquitin ligase. Proc Natl Acad Sci U S A. 2002;99:10353-8.
92. Dunn EF, Pritlove DC, Elliott RM. The S RNA genome segments of Batai, Cache Valley, Guaroa, Kairi, Lumbo, Main Drain and Northway bunyaviruses: sequence determination and analysis. J Gen Virol. 1994;75:597-608.
93. Verbruggen P, Ruf M, Blakqori G, Overby AK, Heidemann M, Eick D, et al. Interferon antagonist NSs of La Crosse virus triggers a DNA damage response-like degradation of transcribing RNA polymerase II. J Biol Chem. 2011;286:3681-92.
94. Somesh BP, Reid J, Liu WF, Sogaard TM, Erdjument-Bromage H, Tempst P, et al. Multiple mechanisms confining RNA polymerase II ubiquitylation to polymerases undergoing transcriptional arrest. Cell. 2005;121:913-23.
95. Swanepoel R, Blackburn NK. Demonstration of nuclear immunofluorescence in Rift Valley fever infected cells. J Gen Virol. 1977;34:557-61.
96. Ikegami T, Narayanan K, Won S, Kamitani W, Peters CJ, Makino S. Rift Valley fever virus NSs protein promotes post-transcriptional downregulation of protein kinase PKR and inhibits eIF2alpha phosphorylation. PLoS Pathog. 2009;5:e1000287.
97. Habjan M, Pichlmair A, Elliott RM, Overby AK, Glatter T, Gstaiger M, et al. NSs protein of rift valley fever virus induces the specific degradation of the double-stranded RNA-dependent protein kinase. J Virol. 2009;83:4365-75.
98. Gale Jr M, Tan SL, Katze MG. Translational control of viral gene expression in eukaryotes. Microbiol Mol Biol Rev. 2000;64:239-80.
99. Langland JO, Cameron JM, Heck MC, Jancovich JK, Jacobs BL. Inhibition of PKR by RNA and DNA viruses. Virus Res. 2006;119:100-10.
100. Garcia MA, Gil J, Ventoso I, Guerra S, Domingo E, Rivas C, et al. Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol Mol Biol Rev. 2006;70:1032-60.
101. Kalveram B, Lihoradova O, Indran SV, Lokugamage N, Head JA, Ikegami T. Rift Valley fever virus NSs inhibits host transcription independently of the degradation of dsRNA-dependent protein kinase PKR. Virology. 2013;435:415-24.
102. Mudhasani R, Tran JP, Retterer C, Kota KP, Whitehouse CA, Bavari S. Protein Kinase R Degradation Is Essential for Rift Valley Fever Virus Infection and Is Regulated by SKP1-CUL1-F-box (SCF)FBXW11-NSs E3 Ligase. PLoS Pathog. 2016;12:e1005437.
103. Kainulainen M, Lau S, Samuel CE, Hornung V, Weber F. NSs virulence factor of Rift Valley fever virus engages the F-box proteins FBXW11 and beta-TRCP1 to degrade the antiviral protein kinase PKR. J Virol. 2016;90:6140-7.
104. Soucy TA, Smith PG, Rolfe M. Targeting NEDD8-activated cullin-RING ligases for the treatment of cancer. Clin Cancer Res. 2009;15:3912-6.
105. Bridgen A, Weber F, Fazakerley JK, Elliott RM. Bunyamwera bunyavirus nonstructural protein NSs is a nonessential gene product that contributes to viral pathogenesis. Proc Natl Acad Sci U S A. 2001;98:664-9.
106. Blakqori G, Weber F. Efficient cDNA-based rescue of La Crosse bunyaviruses expressing or lacking the nonstructural protein NSs. J Virol. 2005;79:10420-8.
107. Pettersson RF. Effect of Uukuniemi virus infection on host cell macromolecule synthesis. Med Biol. 1974;52:90-7.
108. Brennan B, Li P, Zhang S, Li A, Liang M, Li D, et al. Reverse genetics system for severe fever with thrombocytopenia syndrome virus. J Virol. 2015;89:3026-37.
109. Rezelj VV, Overby AK, Elliott RM. Generation of mutant Uukuniemi viruses lacking the nonstructural protein NSs by reverse genetics indicates that NSs is a weak interferon antagonist. J Virol. 2015;89:4849-56.
110. Eliseeva IA, Lyabin DN, Ovchinnikov LP. Poly(A)-binding proteins: structure, domain organization, and activity regulation. Biochemistry (Mosc). 2013;78:1377-91.
111. Copeland AM, Altamura LA, Van Deusen NM, Schmaljohn CS. Nuclear relocalization of polyadenylate binding protein during rift valley fever virus infection involves expression of the NSs gene. J Virol. 2013;87:11659-69.
112. Copeland AM, Van Deusen NM, Schmaljohn CS. Rift Valley fever virus NSS gene expression correlates with a defect in nuclear mRNA export. Virology. 2015;486:88-93.
113. Blakqori G, van Knippenberg I, Elliott RM. Bunyamwera orthobunyavirus S-segment untranslated regions mediate poly(A) tail-independent translation. J Virol. 2009;83:3637-46.
114. Hussein IT, Mir MA. How hantaviruses modulate cellular pathways for efficient replication? Front Biosci (Elite Ed). 2013;5:154-66.
115. McNab F, Mayer-Barber K, Sher A, Wack A, O'Garra A. Type I interferons in infectious disease. Nat Rev Immunol. 2015;15:87-103.
116. Witte K, Witte E, Sabat R, Wolk K. IL-28A, IL-28B, and IL-29: promising cytokines with type I interferon-like properties. Cytokine Growth Factor Rev. 2010;21:237-51.
117. de Weerd NA, Samarajiwa SA, Hertzog PJ. Type I interferon receptors: biochemistry and biological functions. J Biol Chem. 2007;282:20053-7.
118. Farrar MA, Schreiber RD. The molecular cell biology of interferon-gamma and its receptor. Annu Rev Immunol. 1993;11:571-611.
119. 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.
120. Muller R, Saluzzo JF, Lopez N, Dreier T, Turell M, Smith J, et al. Characterization of clone 13, a naturally attenuated avirulent isolate of Rift Valley fever virus, which is altered in the small segment. Am J Trop Med Hyg. 1995;53:405-11.
121. Bouloy M, Janzen C, Vialat P, Khun H, Pavlovic J, Huerre M, et al. Genetic evidence for an interferon-antagonistic function of rift valley fever virus nonstructural protein NSs. J Virol. 2001;75:1371-7.
122. Ermler ME, Yerukhim E, Schriewer J, Schattgen S, Traylor Z, Wespiser AR, et al. RNA helicase signaling is critical for type i interferon production and protection against Rift Valley fever virus during mucosal challenge. J Virol. 2013;87:4846-60.
123. Le May N, Mansuroglu Z, Leger P, Josse T, Blot G, Billecocq A, et al. A SAP30 complex inhibits IFN-beta expression in Rift Valley fever virus infected cells. PLoS Pathog. 2008;4:e13.
124. Weill L, Shestakova E, Bonnefoy E. Transcription factor YY1 binds to the murine beta interferon promoter and regulates its transcriptional capacity with a dual activator/repressor role. J Virol. 2003;77:2903-14.
125. Head JA, Kalveram B, Ikegami T. Functional analysis of Rift Valley fever virus NSs encoding a partial truncation. PLoS ONE. 2012;7:e45730.
126. Gori-Savellini G, Valentini M, Cusi MG. Toscana virus NSs protein inhibits the induction of type I interferon by interacting with RIG-I. J Virol. 2013;87:6660-7.
127. Brisbarre NM, Plumet S, de Micco P, Leparc-Goffart I, Emonet SF. Toscana virus inhibits the interferon beta response in cell cultures. Virology. 2013;442:189-94.
128. Pifat DY, Smith JF. Punta Toro virus infection of C57BL/6 J mice: a model for phlebovirus-induced disease. Microb Pathog. 1987;3:409-22.
129. Anderson Jr GW, Slayter MV, Hall W, Peters CJ. Pathogenesis of a phleboviral infection (Punta Toro virus) in golden Syrian hamsters. Arch Virol. 1990;114:203-12.
130. Perrone LA, Narayanan K, Worthy M, Peters CJ. The S segment of Punta Toro virus (Bunyaviridae, Phlebovirus) is a major determinant of lethality in the Syrian hamster and codes for a type I interferon antagonist. J Virol. 2007;81:884-92.
131. Mendenhall M, Wong MH, Skirpstunas R, Morrey JD, Gowen BB. Punta Toro virus (Bunyaviridae, Phlebovirus) infection in mice: strain differences in pathogenesis and host interferon response. Virology. 2009;395:143-51.
132. Ning YJ, Wang M, Deng M, Shen S, Liu W, Cao WC, et al. Viral suppression of innate immunity via spatial isolation of TBK1/IKKepsilon from mitochondrial antiviral platform. J Mol Cell Biol. 2014;6:324-37.
133. Ning YJ, Feng K, Min YQ, Cao WC, Wang M, Deng F, et al. Disruption of type I interferon signaling by the nonstructural protein of severe fever with thrombocytopenia syndrome virus via the hijacking of STAT2 and STAT1 into inclusion bodies. J Virol. 2015;89:4227-36.
134. Weber F, Bridgen A, Fazakerley JK, Streitenfeld H, Kessler N, Randall RE, et al. Bunyamwera bunyavirus nonstructural protein NSs counteracts the induction of alpha/beta interferon. J Virol. 2002;76:7949-55.
135. Kohl A, Clayton RF, Weber F, Bridgen A, Randall RE, Elliott RM. Bunyamwera virus nonstructural protein NSs counteracts interferon regulatory factor 3-mediated induction of early cell death. J Virol. 2003;77:7999-8008.
136. Mansuroglu Z, Josse T, Gilleron J, Billecocq A, Leger P, Bouloy M, et al. Non structural NSs protein of Rift Valley Fever Virus interacts with pericentromeric DNA sequences of the host cell inducing chromosome cohesion and segregation defects. J Virol. 2009;84:928-39.
137. Baer A, Austin D, Narayanan A, Popova T, Kainulainen M, Bailey C, et al. Induction of DNA damage signaling upon Rift Valley fever virus infection results in cell cycle arrest and increased viral replication. J Biol Chem. 2012;287:7399-410.
138. McElroy AK, Nichol ST. Rift Valley fever virus inhibits a pro-inflammatory response in experimentally infected human monocyte derived macrophages and a pro-inflammatory cytokine response may be associated with patient survival during natural infection. Virology. 2012;422:6-12.
139. Jansen van Vuren P, Shalekoff S, Grobbelaar AA, Archer BN, Thomas J, Tiemessen CT, et al. Serum levels of inflammatory cytokines in Rift Valley fever patients are indicative of severe disease. Virol J. 2015;12:159.
140. Benferhat R, Josse T, Albaud B, Gentien D, Mansuroglu Z, Marcato V, et al. Large-scale chromatin immunoprecipitation with promoter sequence microarray analysis of the interaction of the NSs protein of Rift Valley fever virus with regulatory DNA regions of the host genome. J Virol. 2012;86:11333-44.
141. Palacios G, Tesh R, Travassos da Rosa A, Savji N, Sze W, Jain K, et al. Characterization of the Candiru antigenic complex (Bunyaviridae: Phlebovirus), a highly diverse and reassorting group of viruses affecting humans in tropical America. J Virol. 2011;85:3811-20.
142. Palacios G, Wiley MR, Travassos da Rosa AP, Guzman H, Quiroz E, Savji N, et al. Characterization of the Punta Toro species complex (genus Phlebovirus, family Bunyaviridae). J Gen Virol. 2015;96:2079-85.
143. Palacios G, Savji N, Travassos da Rosa A, Desai A, Sanchez-Seco MP, Guzman H, et al. Characterization of the Salehabad virus species complex of the genus Phlebovirus (Bunyaviridae). J Gen Virol. 2013;94:837-42.
144. Palacios G, Tesh RB, Savji N, Travassos da Rosa AP, Guzman H, Bussetti AV, et al. Characterization of the Sandfly fever Naples species complex and description of a new Karimabad species complex (genus Phlebovirus, family Bunyaviridae). J Gen Virol. 2014;95:292-300.
145. Palacios G, Savji N, Travassos da Rosa A, Guzman H, Yu X, Desai A, et al. Characterization of the Uukuniemi virus group (Phlebovirus: Bunyaviridae): evidence for seven distinct species. J Virol. 2013;87:3187-95.
146. Matsuno K, Weisend C, Travassos da Rosa AP, Anzick SL, Dahlstrom E, Porcella SF, et al. Characterization of the Bhanja serogroup viruses (Bunyaviridae): a novel species of the genus Phlebovirus and its relationship with other emerging tick-borne phleboviruses. J Virol. 2013;87:3719-28.
147. Xu F, Liu D, Nunes MR, DA Rosa AP, Tesh RB, Xiao SY. Antigenic and genetic relationships among Rift Valley fever virus and other selected members of the genus Phlebovirus (Bunyaviridae). Am J Trop Med Hyg. 2007;76:1194-200.
148. Palacios G, da Rosa AT, Savji N, Sze W, Wick I, Guzman H, et al. Aguacate virus, a new antigenic complex of the genus Phlebovirus (family Bunyaviridae). J Gen Virol. 2011;92:1445-53.