Efficient cellular release of rift valley fever virus requires genomic RNA

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Piper, Mary E ^a   Sorenson, Dorothy R ^a   Gerrard, Sonja R ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC RNA; NUCLEOCAPSID PROTEIN; RNA DIRECTED RNA POLYMERASE; VIRUS GLYCOPROTEIN; PRIMER DNA; RNA;

ARTICLE; CONTROLLED STUDY; IMMUNOPRECIPITATION; NONHUMAN; PROTEIN BINDING; PROTEIN CROSS LINKING; RIFT VALLEY FEVER BUNYAVIRUS; RNA ANALYSIS; VIRUS ASSEMBLY; VIRUS ENVELOPE; VIRUS GENOME; VIRUS INFECTIVITY; VIRUS LIKE AGENT; VIRUS MORPHOLOGY; VIRUS PARTICLE; VIRUS RELEASE; VIRUS REPLICATION; ANIMAL; BIOCATALYSIS; CELL LINE; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; ULTRACENTRIFUGATION;

PHLEBOVIRUS; RIFT VALLEY FEVER VIRUS;

ANIMALS; BASE SEQUENCE; BIOCATALYSIS; CELL LINE; DNA PRIMERS; FLUORESCENT ANTIBODY TECHNIQUE; MICROSCOPY, ELECTRON, TRANSMISSION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIFT VALLEY FEVER VIRUS; RNA; RNA REPLICASE; ULTRACENTRIFUGATION; VIRUS REPLICATION;

EID: 79952843129     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018070     Document Type: Article

References (61)

1. Schmaljohn CS, Nichol ST, (2007) Bunyaviridae. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, editors. Fields Virology Philadelphia, PA Lippincott, Williams & Wilkins pp. 1741-1789.
2. Meegan JM, Bailey CL, (1988) Rift Valley Fever. In: Monath TP, editors. Arboviruses Epidemiology and Ecology Boca Raton, FL CRC pp. 51-76.
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. Meegan JM, Hoogstraal H, Moussa MI, (1979) An epizootic of Rift Valley fever in Egypt in 1977. Vet Rec 105: 124-125.
5. Philippe B, Jouan A, Riou O, Coulibaly I, Leguenno B, et al. (1989) Hemorrhagic forms of Rift Valley fever in Mauritania. Bull Soc Pathol Exot Filiales 82: 611-619.
6. 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.
7. 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.
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. Jin H, Elliott RM, (1993) Characterization of Bunyamwera virus S RNA that is transcribed and replicated by the L protein expressed from recombinant vaccinia virus. J Virol 67: 1396-1404.
10. Lopez N, Muller R, Prehaud C, Bouloy M, (1995) The L protein of Rift Valley fever virus can rescue viral ribonucleoproteins and transcribe synthetic genome-like RNA molecules. J Virol 69: 3972-3979.
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. Gerrard SR, Nichol ST, (2002) Characterization of the Golgi retention motif of Rift Valley fever virus GN glycoprotein. J Virol 76: 12200-12210.
13. Wasmoen TL, Kakach LT, Collett MS, (1988) Rift Valley fever virus M segment: cellular localization of M segment-encoded proteins. Virology 166: 275-280.
14. Piper ME, Gerrard SR, (2010) A novel system for identification of inhibitors of Rift Valley fever virus replication. Viruses 2: 731-747.
15. Kakach LT, Suzich JA, Collett MS, (1989) Rift Valley fever virus M segment: phlebovirus expression strategy and protein glycosylation. Virology 170: 505-510.
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. Ribeiro D, Borst JW, Goldbach R, Kormelink R, (2009) Tomato spotted wilt virus nucleocapsid protein interacts with both viral glycoproteins Gn and Gc in planta. Virology 383: 121-130.
18. Frese M, Kochs G, Feldmann H, Hertkorn C, Haller O, (1996) Inhibition of bunyaviruses, phleboviruses, and hantaviruses by human MxA protein. J Virol 70: 915-923.
19. Ramanathan HN, Chung DH, Plane SJ, Sztul E, Chu YK, et al. (2007) Dynein-dependent transport of the hantaan virus nucleocapsid protein to the endoplasmic reticulum-Golgi intermediate compartment. J Virol 81: 8634-8647.
20. Ravkov EV, Compans RW, (2001) Hantavirus nucleocapsid protein is expressed as a membrane-associated protein in the perinuclear region. J Virol 75: 1808-1815.
21. Shi X, Brauburger K, Elliott RM, (2005) Role of N-linked glycans on Bunyamwera virus glycoproteins in intracellular trafficking, protein folding, and virus infectivity. J Virol 79: 13725-13734.
22. Shi X, Kohl A, Li P, Elliott RM, (2007) Role of the cytoplasmic tail domains of Bunyamwera orthobunyavirus glycoproteins Gn and Gc in virus assembly and morphogenesis. J Virol 81: 10151-10160.
23. Raymond DD, Piper ME, Gerrard SR, Smith JL, (2010) Structure of the Rift Valley fever virus nucleocapsid protein reveals another architecture for RNA encapsidation. Proc Natl Acad Sci U S A 107: 11769-11774.
24. 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.
25. 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.
26. Simons JF, Hellman U, Pettersson RF, (1990) Uukuniemi virus S RNA segment: ambisense coding strategy, packaging of complementary strands into virions, and homology to members of the genus Phlebovirus. J Virol 64: 247-255.
27. Albarino CG, Bird BH, Nichol ST, (2007) A shared transcription termination signal on negative and ambisense RNA genome segments of Rift Valley fever, sandfly fever Sicilian, and Toscana viruses. J Virol 81: 5246-5256.
28. Ikegami T, Won S, Peters CJ, Makino S, (2007) Characterization of Rift Valley fever virus transcriptional terminations. J Virol 81: 8421-8438.
29. Flick K, Katz A, Overby A, Feldmann H, Pettersson RF, et al. (2004) Functional analysis of the noncoding regions of the Uukuniemi virus (Bunyaviridae) RNA segments. J Virol 78: 11726-11738.
30. Deng MY, Day SP, Cliver DO, (1994) Detection of hepatitis A virus in environmental samples by antigen-capture PCR. Appl Environ Microbiol 60: 1927-1933.
31. Flint SJ, (2004) Principles of virology: molecular biology, pathogenesis, and control of animal viruses. Washington, D.C. ASM Press.
32. Mohamadzadeh M, Coberley SS, Olinger GG, Kalina WV, Ruthel G, et al. (2006) Activation of triggering receptor expressed on myeloid cells-1 on human neutrophils by marburg and ebola viruses. J Virol 80: 7235-7244.
33. Wengler G, (1989) Cell-associated West Nile flavivirus is covered with E+pre-M protein heterodimers which are destroyed and reorganized by proteolytic cleavage during virus release. J Virol 63: 2521-2526.
34. Lowen AC, Elliott RM, (2005) Mutational analyses of the nonconserved sequences in the Bunyamwera Orthobunyavirus S segment untranslated regions. J Virol 79: 12861-12870.
35. Nugent CI, Johnson KL, Sarnow P, Kirkegaard K, (1999) Functional coupling between replication and packaging of poliovirus replicon RNA. J Virol 73: 427-435.
36. Venter PA, Krishna NK, Schneemann A, (2005) Capsid protein synthesis from replicating RNA directs specific packaging of the genome of a multipartite, positive-strand RNA virus. J Virol 79: 6239-6248.
37. Venter PA, Schneemann A, (2007) Assembly of two independent populations of flock house virus particles with distinct RNA packaging characteristics in the same cell. J Virol 81: 613-619.
38. Liu L, Celma CC, Roy P, (2008) Rift Valley fever virus structural proteins: expression, characterization and assembly of recombinant proteins. Virol J 5: 82.
39. Pantua HD, McGinnes LW, Peeples ME, Morrison TG, (2006) Requirements for the assembly and release of Newcastle disease virus-like particles. J Virol 80: 11062-11073.
40. Noda T, Ebihara H, Muramoto Y, Fujii K, Takada A, et al. (2006) Assembly and budding of Ebolavirus. PLoS Pathog 2: e99.
41. Gomez-Puertas P, Albo C, Perez-Pastrana E, Vivo A, Portela A, (2000) Influenza virus matrix protein is the major driving force in virus budding. J Virol 74: 11538-11547.
42. Nayak DP, Hui EK, Barman S, (2004) Assembly and budding of influenza virus. Virus Res 106: 147-165.
43. Sugahara F, Uchiyama T, Watanabe H, Shimazu Y, Kuwayama M, et al. (2004) Paramyxovirus Sendai virus-like particle formation by expression of multiple viral proteins and acceleration of its release by C protein. Virology 325: 1-10.
44. Irie T, Shimazu Y, Yoshida T, Sakaguchi T, (2007) The YLDL sequence within Sendai virus M protein is critical for budding of virus-like particles and interacts with Alix/AIP1 independently of C protein. J Virol 81: 2263-2273.
45. Coronel EC, Murti KG, Takimoto T, Portner A, (1999) Human parainfluenza virus type 1 matrix and nucleoprotein genes transiently expressed in mammalian cells induce the release of virus-like particles containing nucleocapsid-like structures. J Virol 73: 7035-7038.
46. Ciancanelli MJ, Basler CF, (2006) Mutation of YMYL in the Nipah virus matrix protein abrogates budding and alters subcellular localization. J Virol 80: 12070-12078.
47. Pohl C, Duprex WP, Krohne G, Rima BK, Schneider-Schaulies S, (2007) Measles virus M and F proteins associate with detergent-resistant membrane fractions and promote formation of virus-like particles. J Gen Virol 88: 1243-1250.
48. Iwasaki M, Takeda M, Shirogane Y, Nakatsu Y, Nakamura T, et al. (2009) The matrix protein of measles virus regulates viral RNA synthesis and assembly by interacting with the nucleocapsid protein. J Virol 83: 10374-10383.
49. Li M, Schmitt PT, Li Z, McCrory TS, He B, et al. (2009) Mumps virus matrix, fusion, and nucleocapsid proteins cooperate for efficient production of virus-like particles. J Virol 83: 7261-7272.
50. Jayakar HR, Jeetendra E, Whitt MA, (2004) Rhabdovirus assembly and budding. Virus Res 106: 117-132.
51. Hartlieb B, Weissenhorn W, (2006) Filovirus assembly and budding. Virology 344: 64-70.
52. Swenson DL, Warfield KL, Kuehl K, Larsen T, Hevey MC, et al. (2004) Generation of Marburg virus-like particles by co-expression of glycoprotein and matrix protein. FEMS Immunol Med Microbiol 40: 27-31.
53. Overby AK, Pettersson RF, Neve EP, (2007) The glycoprotein cytoplasmic tail of Uukuniemi virus (Bunyaviridae) interacts with ribonucleoproteins and is critical for genome packaging. J Virol 81: 3198-3205.
54. Kukkonen SK, Vaheri A, Plyusnin A, (2004) Tula hantavirus L protein is a 250 kDa perinuclear membrane-associated protein. J Gen Virol 85: 1181-1189.
55. Besselaar TG, Blackburn NK, (1992) The synergistic neutralization of Rift Valley fever virus by monoclonal antibodies to the envelope glycoproteins. Arch Virol 125: 239-250.
56. Garry CE, Garry RF, (2004) Proteomics computational analyses suggest that the carboxyl terminal glycoproteins of Bunyaviruses are class II viral fusion protein (beta-penetrenes). Theor Biol Med Model 1: 10.
57. Plassmeyer ML, Soldan SS, Stachelek KM, Martin-Garcia J, Gonzalez-Scarano F, (2005) California serogroup Gc (G1) glycoprotein is the principal determinant of pH-dependent cell fusion and entry. Virology 338: 121-132.
58. Plassmeyer ML, Soldan SS, Stachelek KM, Roth SM, Martin-Garcia J, et al. (2007) Mutagenesis of the La Crosse Virus glycoprotein supports a role for Gc (1066-1087) as the fusion peptide. Virology 358: 273-282.
59. Shi X, Goli J, Clark G, Brauburger K, Elliott RM, (2009) Functional analysis of the Bunyamwera orthobunyavirus Gc glycoprotein. J Gen Virol 90: 2483-2492.
60. Hoenen T, Groseth A, Kolesnikova L, Theriault S, Ebihara H, et al. (2006) Infection of naive target cells with virus-like particles: implications for the function of ebola virus VP24. J Virol 80: 7260-7264.
61. Jorba N, Coloma R, Ortin J, (2009) Genetic trans-complementation establishes a new model for influenza virus RNA transcription and replication. PLoS Pathog 5: e1000462.