P53 activation following rift valley fever virus infection contributes to cell death and viral production

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Austin, Dana ^a   Baer, Alan ^a   Lundberg, Lindsay ^a   Shafagati, Nazly ^a   Schoonmaker, Annalise ^a   Narayanan, Aarthi ^a   Popova, Taissia ^a   Panthier, Jean Jacques ^b   Kashanchi, Fatah ^a   Bailey, Charles ^a   Kehn Hall, Kylene ^a  

^a GEORGE MASON UNIVERSITY   (United States)

^b INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P53; SERINE; VIRUS PROTEIN;

APOPTOSIS; ARTICLE; CELL ASSAY; CELL CYCLE; CELL CYCLE ARREST; CELL VIABILITY; CONTROLLED STUDY; DNA DAMAGE; FATALITY; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; LIVESTOCK; NULL CELL; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RIFT VALLEY FEVER; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UPREGULATION; VIROGENESIS; VIRUS INFECTION; VIRUS REPLICATION; VIRUS STRAIN; ZOONOSIS; ACTIVE TRANSPORT; CELL LINE; CELL NUCLEUS; CHEMISTRY; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; RIFT VALLEY FEVER BUNYAVIRUS;

RIFT VALLEY FEVER VIRUS;

ACTIVE TRANSPORT, CELL NUCLEUS; APOPTOSIS; CELL LINE; CELL NUCLEUS; HUMANS; PHOSPHORYLATION; RIFT VALLEY FEVER VIRUS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84860522938     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036327     Document Type: Article

References (58)

1. Bouloy M, Weber F, (2010) Molecular biology of rift valley Fever virus. Open Virol J 4: 8-14.
2. Pepin M, Bouloy M, Bird BH, Kemp A, Paweska J, (2010) Rift Valley fever virus(Bunyaviridae: Phlebovirus): an update on pathogenesis, molecular epidemiology, vectors, diagnostics and prevention. Vet Res 41: 61.
3. Bird BH, Ksiazek TG, Nichol ST, Maclachlan NJ, (2009) Rift Valley fever virus. J Am Vet Med Assoc 234: 883-893.
4. Ikegami T, Makino S, (2011) The Pathogenesis of Rift Valley Fever. Viruses 3: 493-519.
5. Daubney R, Hudson JR, Garnham PC, (1931) Enzootic hepatitis or rift valley fever. An undescribed virus disease of sheep cattle and man from east africa. The Journal of Pathology and Bacteriology 34: 545-579.
6. Pepin M, Bouloy M, Bird BH, Kemp A, Paweska J, (2010) Rift Valley fever virus (Bunyaviridae: Phlebovirus): an update on pathogenesis, molecular epidemiology, vectors, diagnostics and prevention. Veterinary Research 41: 40-40.
7. Zamoto-Niikura A, Terasaki K, Ikegami T, Peters CJ, Makino S, (2009) Rift valley fever virus L protein forms a biologically active oligomer. Journal of Virology 83: 12779-12789.
8. 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.
9. 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.
10. 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.
11. Gerrard SR, Nichol ST, (2007) Synthesis, proteolytic processing and complex formation of N-terminally nested precursor proteins of the Rift Valley fever virus glycoproteins. Virology 357: 124-133.
12. Ikegami T, Peters CJ, Makino S, (2005) Rift valley fever virus nonstructural protein NSs promotes viral RNA replication and transcription in a minigenome system. Journal of Virology 79: 5606-5615.
13. 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. Journal of Virology 78: 9798-9806.
14. Habjan M, Pichlmair A, Elliott RM, Overby AK, Glatter T, et al. (2009) NSs protein of rift valley fever virus induces the specific degradation of the double-stranded RNA-dependent protein kinase. Journal of Virology 83: 4365-4375.
15. Ikegami T, Narayanan K, Won S, Kamitani W, Peters CJ, et al. (2009) Rift Valley fever virus NSs protein promotes post-transcriptional downregulation of protein kinase PKR and inhibits eIF2alpha phosphorylation. PLoS Pathogens 5: e1000287-e1000287.
16. 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. Journal of Virology 75: 1371-1377.
17. Won S, Ikegami T, Peters CJ, Makino S, (2007) NSm Protein of Rift Valley Fever Virus Suppresses Virus-Induced Apoptosis. Journal of Virology 81: 13335-13345.
18. Popova TG, Turell MJ, Espina V, Kehn-Hall K, Kidd J, et al. (2010) Reverse-phase phosphoproteome analysis of signaling pathways induced by Rift valley fever virus in human small airway epithelial cells. PloS One 5: e13805-e13805.
19. Moll UM, Wolff S, Speidel D, Deppert W, (2005) Transcription-independent pro-apoptotic functions of p53. Current Opinion in Cell Biology 17: 631-636.
20. Shieh SY, Ikeda M, Taya Y, Prives C, (1997) DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 91: 325-334.
21. Wang P, Reed M, Wang Y, Mayr G, Stenger JE, et al. (1994) p53 domains: structure, oligomerization, and transformation. Mol Cell Biol 14: 5182-5191.
22. Steegenga WT, van der Eb AJ, Jochemsen AG, (1996) How phosphorylation regulates the activity of p53. Journal of Molecular Biology 263: 103-113.
23. Shieh SY, Taya Y, Prives C, (1999) DNA damage-inducible phosphorylation of p53 at N-terminal sites including a novel site, Ser20, requires tetramerization. The EMBO Journal 18: 1815-1823.
24. Oda K, Arakawa H, Tanaka T, Matsuda K, Tanikawa C, et al. (2000) p53AIP1, a Potential Mediator of p53-Dependent Apoptosis, and Its Regulation by Ser-46-Phosphorylated p53. Cell 102: 849-862.
25. Meek DW, (1994) Post-translational modification of p53. Seminars in Cancer Biology 5: 203-210.
26. Kohn KW, (1999) Molecular interaction map of the mammalian cell cycle control and DNA repair systems. Molecular Biology of the Cell 10: 2703-2734.
27. Thakur VS, Ruhul Amin ARM, Paul RK, Gupta K, Hastak K, et al. (2010) p53-Dependent p21-mediated growth arrest pre-empts and protects HCT116 cells from PUMA-mediated apoptosis induced by EGCG. Cancer Letters 296: 225-232.
28. Haupt Y, Rowan S, Shaulian E, Vousden KH, Oren M, (1995) Induction of apoptosis in HeLa cells by trans-activation-deficient p53. Genes & Development 9: 2170-2183.
29. Kelekar A, Thompson CB, (1998) Bcl-2-family proteins: the role of the BH3 domain in apoptosis. Trends in Cell Biology 8: 324-330.
30. Myskiw C, Arsenio J, Hammett C, van Bruggen R, Deschambault Y, et al. (2011) Comparative analysis of poxvirus orthologues of the Vaccinia Virus E3 protein: Modulation of PKR activity, cytokine responses and virus pathogenicity. The Journal of Virology pp. JVI.05505-05511-JVI.05505-05511.
31. Sir D, Tian Y, Chen W-l, Ann DK, Yen T-SB, et al. (2010) The early autophagic pathway is activated by hepatitis B virus and required for viral DNA replication. Proc Natl Acad Sci U S A 107: 4383-4388.
32. Turpin E, Luke K, Jones J, Tumpey T, Konan K, et al. (2005) Influenza virus infection increases p53 activity: role of p53 in cell death and viral replication. Journal of Virology 79: 8802-8811.
33. Vialat P, Muller R, Vu TH, Prehaud C, Bouloy M, (1997) Mapping of the mutations present in the genome of the Rift Valley fever virus attenuated MP12 strain and their putative role in attenuation. Virus Res 52: 43-50.
34. 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.
35. Ikegami T, Narayanan K, Won S, Kamitani W, Peters CJ, et al. (2009) Rift Valley fever virus NSs protein promotes post-transcriptional downregulation of protein kinase PKR and inhibits eIF2alpha phosphorylation. PLoS Pathog 5: e1000287.
36. Milczarek GJ, Martinez J, Bowden GT, (1997) p53 Phosphorylation: biochemical and functional consequences. Life Sciences 60: 1-11.
37. Moll UM, Petrenko O, (2003) The MDM2-p53 Interaction. Molecular Cancer Research 1: 1001-1008.
38. Zhang Y, Xiong Y, (2001) A p53 amino-terminal nuclear export signal inhibited by DNA damage-induced phosphorylation. Science (New York, NY) 292: 1910-1915.
39. Vialat P, Billecocq A, Kohl A, Bouloy M, (2000) The S Segment of Rift Valley Fever Phlebovirus (Bunyaviridae) Carries Determinants for Attenuation and Virulence in Mice. Journal of Virology 74: 1538-1543.
40. Ikegami T, Narayanan K, Won S, Kamitani W, Peters CJ, et al. (2009) Dual Functions of Rift Valley Fever Virus NSs Protein: Inhibition of Host mRNA Transcription and Post-transcriptional Downregulation of Protein Kinase PKR. Ann N Y Acad Sci 1171: E75-E85-E75-E85.
41. Mansuroglu Z, Josse T, Gilleron J, Billecocq A, Leger P, et al. (2010) Nonstructural NSs protein of rift valley fever virus interacts with pericentromeric DNA sequences of the host cell, inducing chromosome cohesion and segregation defects. J Virol 84: 928-939.
42. Kalveram B, Lihoradova O, Ikegami T, (2011) NSs protein of rift valley fever virus promotes posttranslational downregulation of the TFIIH subunit p62. Journal of Virology 85: 6234-6243.
43. Baer A, Austin D, Narayanan A, Popova T, Kainulainen M, et al. (2012) Induction of DNA Damage Signaling upon Rift Valley Fever Virus Infection Results in Cell Cycle Arrest and Increased Viral Replication. J Biol Chem 287: 7399-7410.
44. Kurihara A, Nagoshi H, Yabuki M, Okuyama R, Obinata M, et al. (2007) Ser46 phosphorylation of p53 is not always sufficient to induce apoptosis: multiple mechanisms of regulation of p53-dependent apoptosis. Genes to Cells: Devoted to Molecular & Cellular Mechanisms 12: 853-861.
45. Popova TG, Turell MJ, Espina V, Kehn-Hall K, Kidd J, et al. (2010) Reverse-phase phosphoproteome analysis of signaling pathways induced by Rift valley fever virus in human small airway epithelial cells. PLoS ONE 5: e13805.
46. Le May N, Dubaele S, Proietti De Santis L, Billecocq A, Bouloy M, et al. (2004) TFIIH transcription factor, a target for the Rift Valley hemorrhagic fever virus. Cell 116: 541-550.
47. Di Lello P, Miller Jenkins LM, Mas C, Langlois C, Malitskaya E, et al. (2008) p53 and TFIIEα share a common binding site on the Tfb1/p62 subunit of TFIIH. Proceedings of the National Academy of Sciences 105: 106-111.
48. Chen X, Farmer G, Zhu H, Prywes R, Prives C, (1993) Cooperative DNA binding of p53 with TFIID (TBP): a possible mechanism for transcriptional activation. Genes & Development 7: 1837-1849.
49. Lazo PA, Santos CR, (2011) Interference with p53 functions in human viral infections, a target for novel antiviral strategies? Rev Med Virol.
50. Scheffner M, Werness BA, Huibregtse JM, Levine AJ, Howley PM, (1990) The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63: 1129-1136.
51. Werness BA, Levine AJ, Howley PM, (1990) Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science 248: 76-79.
52. Pise-Masison CA, Brady JN, (2005) Setting the stage for transformation: HTLV-1 Tax inhibition of p53 function. Front Biosci 10: 919-930.
53. Tabakin-Fix Y, Azran I, Schavinky-Khrapunsky Y, Levy O, Aboud M, (2006) Functional inactivation of p53 by human T-cell leukemia virus type 1 Tax protein: mechanisms and clinical implications. Carcinogenesis 27: 673-681.
54. Yang MR, Lee SR, Oh W, Lee EW, Yeh JY, et al. (2008) West Nile virus capsid protein induces p53-mediated apoptosis via the sequestration of HDM2 to the nucleolus. Cell Microbiol 10: 165-176.
55. Devireddy LR, Jones CJ, (1999) Activation of caspases and p53 by bovine herpesvirus 1 infection results in programmed cell death and efficient virus release. J Virol 73: 3778-3788.
56. Verbruggen P, Ruf M, Blakqori G, Overby AK, Heidemann M, et al. (2011) Interferon Antagonist NSs of La Crosse Virus Triggers a DNA Damage Response-like Degradation of Transcribing RNA Polymerase II. J Biol Chem 286: 3681-3692.
57. Blakqori G, Delhaye S, Habjan M, Blair CD, Sanchez-Vargas I, et al. (2007) La Crosse bunyavirus nonstructural protein NSs serves to suppress the type I interferon system of mammalian hosts. J Virol 81: 4991-4999.
58. Elliott RM, Weber F, (2009) Bunyaviruses and the type I interferon system. Viruses 1: 1003-1021.