Rift Valley fever virus NSs protein promotes post-transcriptional downregulation of protein kinase PKR and inhibits eIF2α phosphorylation

PLoS Pathogens

Volumn 5, Issue 2, 2009, Pages

  Ikegami, Tetsuro ^a,b   Narayanan, Krishna ^a   Won, Sungyong ^a,c   Kamitani, Wataru ^a   Peters, C J ^a,b   Makino, Shinji ^a,b  

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

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA AMANITIN; DACTINOMYCIN; DOUBLE STRANDED RNA; INITIATION FACTOR 2ALPHA; NSS PROTEIN; PROTEIN KINASE R; UNCLASSIFIED DRUG; VIRUS PROTEIN; INITIATION FACTOR 2; MESSENGER RNA; NUCLEIC ACID SYNTHESIS INHIBITOR; VIRULENCE FACTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; MESSENGER RNA SYNTHESIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; RIFT VALLEY FEVER BUNYAVIRUS; VIRUS REPLICATION; ANIMAL; CERCOPITHECUS; DRUG EFFECT; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; METABOLISM; PATHOGENICITY; PHOSPHORYLATION; PHYSIOLOGY; VERO CELL;

BUNYAVIRIDAE; EUKARYOTA; MAMMALIA; PHLEBOVIRUS; RIFT VALLEY FEVER VIRUS; RNA VIRUSES;

ANIMALS; CERCOPITHECUS AETHIOPS; DACTINOMYCIN; DOWN-REGULATION; EIF-2 KINASE; EUKARYOTIC INITIATION FACTOR-2; GENE EXPRESSION REGULATION, VIRAL; GENE KNOCKOUT TECHNIQUES; HOST-PATHOGEN INTERACTIONS; NUCLEIC ACID SYNTHESIS INHIBITORS; PHOSPHORYLATION; RIFT VALLEY FEVER VIRUS; RNA, MESSENGER; TRANSCRIPTION, GENETIC; VERO CELLS; VIRAL NONSTRUCTURAL PROTEINS; VIRULENCE FACTORS; VIRUS REPLICATION;

EID: 61449213995     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000287     Document Type: Article

References (65)

1. Peters CJ (1981) Rift Valley fever. Handbook Series of Zoonoses, Section B: Viral Zoonoses, Vol 1. CRC Press.
2. Morvan J, Rollin PE, Laventure S, Rakotoarivony I, Roux J (1992) Rift Valley fever epizootic in the central highlands of Madagascar. Res Virol 143: 407-415.
3. Meegan JM (1979) The Rift Valley fever epizootic in Egypt 1977-78. 1. Description of the epizootic and virological studies. Trans R Soc Trop Med Hyg 73: 618-623.
4. El-Akkad AM (1978) Rift Valley fever outbreak in Egypt. October-December 1977. The Journal of the Egyptian Public Health Association 53: 123-128.
5. Arthur RR, el-Sharkawy MS, Cope SE, Botros BA, Oun S, et al. (1993) Recurrence of Rift Valley fever in Egypt. Lancet 342: 1149-1150.
6. Shoemaker T, Boulianne C, Vincent MJ, Pezzanite L, Al-Qahtani MM, et al. (2002) Genetic analysis of viruses associated with emergence of Rift Valley fever in Saudi Arabia and Yemen, 2000-01. Emerg Infect Dis 8: 1415-1420.
7. Wilson ML (1994) Rift Valley fever virus ecology and the epidemiology of disease emergence. Ann N Y Acad Sci 740: 169-180.
8. Nichol ST (2001) Bunyaviruses: Fields Virology, 4th ed. Lippincott, Williams & Wilkins. pp 1603-1633.
9. Peters CJ (2000) Are hemorrhagic fever viruses practical agents for biological terrorism?: Emerging Infections, 1st ed. Vol. 4. ASM Press. pp 203-211.
10. Hoogstraal H, Meegan JM, Khalil GM, Adham FK (1979) The Rift Valley fever epizootic in Egypt 1977-78. 2. Ecological and entomological studies. Trans Roy Soc Trop Med Hyg 73: 624-629.
11. Brown JL, Dominik JW, Morrissey RL (1981) Respiratory infectivity of a recently isolated Egyptian strain of Rift Valley fever virus. Infect immun 33: 848-853.
12. Anderson GW Jr, Lee JO, Anderson AO, Powell N, Mangiafico JA, et al. (1991) Efficacy of a Rift Valley fever virus vaccine against an aerosol infection in rats. Vaccine 9: 710-714.
13. Caplen H, Peters CJ, Bishop DH (1985) Mutagen-directed attenuation of Rift Valley fever virus as a method for vaccine development. J Gen Virol 66: 2271-2277.
14. Schmaljohn C (2001) Bunyaviridae: the viruses and their replication. Fields Virology, 4th ed. Lippincott, Williams & Wilkins. pp 1581-1602.
15. Suzich JA, Collett MS (1988) Rift Valley fever virus M segment: cell-free transcription and translation of virus-complementary RNA. Virology 164: 478-486.
16. Suzich JA, Kakach LT, Collett MS (1990) Expression strategy of a phlebovirus: biogenesis of proteins from the Rift Valley fever virus M segment. J Virol 64: 1549-1555.
17. Won S, Ikegami T, Peters CJ, Makino S (2006) NSm and 78-kilodalton proteins of Rift Valley fever virus are nonessential for viral replication in cell culture. J Virol 80: 8274-8278.
18. Gerrard SR, Bird BH, Albarino CG, Nichol ST (2007) The NSm proteins of Rift Valley fever virus are dispensable for maturation, replication and infection. Virology 359: 459-465.
19. Ikegami T, Won S, Peters CJ, Makino S (2006) Rescue of infectious rift valley fever virus entirely from cDNA, analysis of virus lacking the NSs gene, and expression of a foreign gene. J Virol 80: 2933-2940.
20. Muller R, Saluzzo JF, Lopez N, Dreier T, Turell M, et al. (1995) 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 53: 405-411.
21. Bouloy M, Janzen C, Vialat P, Khun H, Pavlovic J, et al. (2001) Genetic evidence for an interferon-antagonistic function of Rift valley fever virus nonstructural protein NSs. J Virol 75: 1371-1377.
22. Bird BH, Albarino CG, Nichol ST (2007) Rift Valley fever virus lacking NSm proteins retains high virulence in vivo and may provide a model of human delayed onset neurologic disease. Virology 362: 10-15.
23. Won S, Ikegami T, Peters CJ, Makino S (2007) NSm protein of Rift Valley fever virus suppresses virus-induced apoptosis. J Virol 81: 13335-13345.
24. Yadani FZ, Kohl A, Prehaud C, Billecocq A, Bouloy M (1999) 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 73: 5018-5025.
25. Le May N, Dubaele S, Proietti De Santis L, Billecocq A, et al. (2004) TFIIH transcription factor, a target for the Rift Valley hemorrhagic fever virus. Cell 116: 541-550.
26. Le May N, Mansuroglu Z, Leger P, Josse T, Blot G, et al. (2008) A SAP30 Complex Inhibits IFN-beta Expression in Rift Valley Fever Virus Infected Cells. PLoS Pathog 4: e13. doi:10.1371/journal.ppat.0040013.
27. Ikegami T, Peters CJ, Makino S (2005) Rift valley fever virus nonstructural protein NSs promotes viral RNA replication and transcription in a minigenome system. J Virol 79: 5606-5615.
28. Perry RP, Kelley DE (1970) Inhibition of RNA synthesis by actinomycin D: characteristic dose-response of different RNA species. J Cell Physiol 76: 127-139.
29. Nguyen VT, Giannoni F, Dubois MF, Seo SJ, Vigneron M, et al. (1996) In vivo degradation of RNA polymerase II largest subunit triggered by alpha-amanitin. Nucleic Acids Res 24: 2924-2929.
30. Garcia MA, Gil J, Ventoso I, Guerra S, Domingo E, et al. (2006) Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol Mol Biol Rev 70: 1032-1060.
31. Nallagatla SR, Hwang J, Toroney R, Zheng X, Cameron CE, et al. (2007) 5′-triphosphate-dependent activation of PKR by RNAs with short stem-loops. Science 318: 1455-1458.
32. Gale M Jr, Tan SL, Katze MG (2000) Translational control of viral gene expression in eukaryotes. Microbiol Mol Biol Rev 64: 239-280.
33. Saelens X, Kalai M, Vandenabeele P (2001) Translation inhibition in apoptosis: caspase-dependent PKR activation and eIF2-alpha phosphorylation. The Journal of Biological Chemistry 276: 41620-41628.
34. Clemens MJ, Bushell M, Jeffrey IW, Pain VM, Morley SJ (2000) Translation initiation factor modifications and the regulation of protein synthesis in apoptotic cells. Cell Death and Differentiation 7: 603-615.
35. Wek RC, Jiang HY, Anthony TG (2006) Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans 34: 7-11.
36. Li S, Koromilas AE (2001) Dominant negative function by an alternatively spliced form of the interferon-inducible protein kinase PKR. J Biol Chem 276: 13881-13890.
37. Yang YL, Reis LF, Pavlovic J, Aguzzi A, Schafer R, et al. (1995) Deficient signaling in mice devoid of double-stranded RNA-dependent protein kinase. EMBO J 14: 6095-6106.
38. Kuhen KL, Samuel CE (1997) Isolation of the interferon-inducible RNA-dependent protein kinase Pkr promoter and identification of a novel DNA element within the 5′-flanking region of human and mouse Pkr genes. Virology 227: 119-130.
39. Walters S, Burke DC, Skehel JJ (1967) Interferon production and RNA inhibitors. J Gen Virol 1: 349-362.
40. Thomis DC, Doohan JP, Samuel CE (1992) Mechanism of interferon action: cDNA structure, expression, and regulation of the interferon-induced, RNA-dependent P1/eIF-2 alpha protein kinase from human cells. Virology 188: 33-46.
41. Zhou Y, Chase BI, Whitmore M, Williams BR, Zhou A (2005) Double-stranded RNA-dependent protein kinase (PKR) is downregulated by phorbol ester. FEBS J 272: 1568-1576.
42. Mazroui R, Di Marco S, Kaufman RJ, Gallouzi IE (2007) Inhibition of the ubiquitin-proteasome system induces stress granule formation. Mol Bio Cell 18: 2603-2618.
43. Diaz MO, Ziemin S, Le Beau MM, Pitha P, Smith SD, et al. (1988) Homozygous deletion of the alpha- and beta 1-interferon genes in human leukemia and derived cell lines. Proc Nat Acad Sci U S A 85: 5259-5263.
44. Mosca JD, Pitha PM (1986) Transcriptional and posttranscriptional regulation of exogenous human beta interferon gene in simian cells defective in interferon synthesis. Mol Cell Biol 6: 2279-2283.
45. Billecocq A, Spiegel M, Vialat P, Kohl A, Weber F, et al. (2004) NSs protein of Rift Valley fever virus blocks interferon production by inhibiting host gene transcription. J Virol 78: 9798-9806.
46. Morrill JC, Jennings GB, Johnson AJ, Cosgriff TM, Gibbs PH, et al. (1990) Pathogenesis of Rift Valley fever in rhesus monkeys: role of interferon response. Arch Virol 110: 195-212.
47. Unterholzner L, Bowie AG (2008) The interplay between viruses and innate immune signaling: recent insights and therapeutic opportunities. Biochem Pharmacol 75: 589-602.
48. Ikegami T, Won S, Peters CJ, Makino S (2005) Rift Valley fever virus NSs mRNA is transcribed from an incoming anti-viral-sense S RNA segment. J Virol 79: 12106-12111.
49. Harding HP, Calfon M, Urano F, Novoa I, Ron D (2002) Transcriptional and translational control in the Mammalian unfolded protein response. Ann Rev Cell Dev Biol 18: 575-599.
50. Ma Y, Hendershot LM (2003) Delineation of a negative feedback regulatory loop that controls protein translation during endoplasmic reticulum stress. J Biol Chem 278: 34864-34873.
51. Novoa I, Zeng H, Harding HP, Ron D (2001) Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J Cell Biol 153: 1011-1022.
52. Jang KL, Collins MK, Latchman DS (1992) The human immunodeficiency virus tat protein increases the transcription of human Alu repeated sequences by increasing the activity of the cellular transcription factor TFIIIC. J Acquire Immune Def Sym 5: 1142-1147.
53. Jang KL, Latchman DS (1992) The herpes simplex virus immediate-early protein ICP27 stimulates the transcription of cellular Alu repeated sequences by increasing the activity of transcription factor TFIIIC. Biochem J 284: 667-673.
54. Panning B, Smiley JR (1993) Activation of RNA polymerase III transcription of human Alu repetitive elements by adenovirus type 5: requirement for the E1b 58-kilodalton protein and the products of E4 open reading frames 3 and 6. Mol Cell Biol 13: 3231-3244.
55. Hasler J, Strub K (2006) Alu elements as regulators of gene expression. Nucleic Acids Res 34: 5491-5497.
56. Chu WM, Ballard R, Carpick BW, Williams BR, Schmid CW (1998) Potential Alu function: regulation of the activity of double-stranded RNA-activated kinase PKR. Mol Cell Biol 18: 58-68.
57. Lee TG, Tang N, Thompson S, Miller J, Katze MG (1994) The 58,000-dalton cellular inhibitor of the interferon-induced double-stranded RNA-activated protein kinase (PKR) is a member of the tetratricopeptide repeat family of proteins. Mol Cell Biol 14: 2331-2342.
58. Raine DA, Jeffrey IW, Clemens MJ (1998) Inhibition of the double-stranded RNA-dependent protein kinase PKR by mammalian ribosomes. FEBS Lett 436: 343-348.
59. Kumar KU, Srivastava SP, Kaufman RJ (1999) Double-stranded RNA-activated protein kinase (PKR) is negatively regulated by 60S ribosomal subunit protein L18. Mol Cell Biol 19: 1116-1125.
60. Black TL, Safer B, Hovanessian A, Katze MG (1989) The cellular 68,000-Mr protein kinase is highly autophosphorylated and activated yet significantly degraded during poliovirus infection: implications for translational regulation. J Virol 63: 2244-2251.
61. Black TL, Barber GN, Katze MG (1993) Degradation of the interferon-induced 68,000-M(r) protein kinase by poliovirus requires RNA. J Virol 67: 791-800.
62. Maggi LB Jr, Heitmeier MR, Scheuner D, Kaufman RJ, Buller RM, et al. (2000) Potential role of PKR in double-stranded RNA-induced macrophage activation. EMBO J 19: 3630-3638.
63. Ito N, Takayama-Ito M, Yamada K, Hosokawa J, Sugiyama M, et al. (2003) Improved recovery of rabies virus from cloned cDNA using a vaccinia virus-free reverse genetics system. Microbiol Immunol 47: 613-617.
64. Kamitani W, Narayanan K, Huang C, Lokugamage K, Ikegami T, et al. (2006) Severe acute respiratory syndrome coronavirus nsp1 protein suppresses host gene expression by promoting host mRNA degradation. Proc Nat Acad Sci U S A 103: 12885-12890.
65. Gunnery S, Mathews MB (1998) RNA binding and modulation of PKR activity. Methods 15: 189-198.