Differential distribution of non-structural proteins of foot-and-mouth disease virus in BHK-21 cells

Virology

Volumn 349, Issue 2, 2006, Pages 409-421

  García Briones, Mercedes ^a,b   Rosas, María F ^a   González Magaldi, Mónica ^a   Martín Acebes, Miguel A ^a   Sobrino, Francisco ^a,b   Armas Portela, Rosario ^a,c  

^a CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^b Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria   (Spain)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

FMDV; Infection; Non structural proteins; Subcellular distribution; Transient expression

Indexed keywords

CALRETICULIN; NONSTRUCTURAL PROTEIN 2B; NONSTRUCTURAL PROTEIN 2BC; NONSTRUCTURAL PROTEIN 2C; NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 3A; NONSTRUCTURAL PROTEIN 3AB; NONSTRUCTURAL PROTEIN 3ABB; NONSTRUCTURAL PROTEIN 3ABBB; NONSTRUCTURAL PROTEIN 3B; NONSTRUCTURAL PROTEIN 3C; NONSTRUCTURAL PROTEIN 3CDPOL; NONSTRUCTURAL PROTEIN 3DPOL; PROTEIN PRECURSOR; PROTEIN VP1; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CELL FRACTIONATION; CELL NUCLEUS; CELL STRAIN BHK; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; FOOT AND MOUTH DISEASE VIRUS; GENETIC TRANSFECTION; IMMUNOFLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; VIRUS INFECTIVITY; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; CELL LINE; CYTOPATHOGENIC EFFECT; CYTOPLASM; ENDOPLASMIC RETICULUM; FLUORESCENCE MICROSCOPY; HAMSTER; METABOLISM; PHYSIOLOGY; TIME;

FOOT-AND-MOUTH DISEASE VIRUS;

ANIMALS; BLOTTING, WESTERN; CELL LINE; CELL NUCLEUS; CRICETINAE; CYTOPATHOGENIC EFFECT, VIRAL; CYTOPLASM; ENDOPLASMIC RETICULUM; FOOT-AND-MOUTH DISEASE VIRUS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; SUBCELLULAR FRACTIONS; TIME FACTORS; TRANSFECTION; VIRAL NONSTRUCTURAL PROTEINS;

EID: 33745892377     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2006.02.042     Document Type: Article

References (65)

1. Alcalde J., Egea G., and Sandoval I.V. gp74 a membrane glycoprotein of the cis-Golgi network that cycles through the endoplasmic reticulum and intermediate compartment. J. Cell Biol. 124 5 (1994) 649-665
2. Aldabe R., and Carrasco L. Induction of membrane proliferation by poliovirus proteins 2C and 2BC. Biochem. Biophys. Res. Commun. 206 1 (1995) 64-76
3. Aminev A.G., Amineva S.P., and Palmenberg A.C. Encephalomyocarditis virus (EMCV) proteins 2A and 3BCD localize to nuclei and inhibit cellular mRNA transcription but not rRNA transcription. Virus Res. 95 1-2 (2003) 59-73
4. Amineva S.P., Aminev A.G., Palmenberg A.C., and Gern J.E. Rhinovirus 3C protease precursors 3CD and 3CD′ localize to the nuclei of infected cells. J. Gen. Virol. 85 Pt. 10 (2004) 2969-2979
5. Andino R., Boddeker N., Silvera D., and Gamarnik A.V. Intracellular determinants of picornavirus replication. Trends Microbiol. 7 2 (1999) 76-82
6. Arlinghaus R.B., and Polatnick J. The isolation of two enzyme-ribonucleic acid complexes involved in the synthesis of foot-and-mouth disease virus ribonucleic acid. Proc. Natl. Acad. Sci. U.S.A. 62 3 (1969) 821-828
7. Armas-Portela R., Parrales M.A., Albar J.P., Martinez A.C., and Avila J. Distribution and characteristics of betaII tubulin-enriched microtubules in interphase cells. Exp. Cell Res. 248 2 (1999) 372-380
8. Bachrach H.L. Foot-and-mouth disease virus, properties, molecular biology and immunogenicity. In: Romberger J.A. (Ed). Beltsville Symposia in Agricultural Research. Virology in Agriculture vol. 1 (1977), Allanheld, Osmun & Co., Montclair, NJ
9. Barteling S.J. Modern inactivated Foot-and-mouth disease (FMD) vaccines: historical background and key elements in production and use. In: Domingo F.S.a.E. (Ed). Foot-and-Mouth Disease: Current Perspectives (2004), Horizon Bioscience, Norfolk
10. Beard C.W., and Mason P.W. Genetic determinants of altered virulence of Taiwanese foot-and-mouth disease virus. J. Virol. 74 2 (2000) 987-991
11. Beck E., Forss S., Strebel K., Cattaneo R., and Feil G. Structure of the FMDV translation initiation site and of the structural proteins. Nucleic Acids Res. 11 22 (1983) 7873-7885
12. Belsham G.J. Translation and replication of FMDV RNA. Curr. Top. Microbiol. Immunol. 288 (2005) 43-70
13. Belsham G.J.a.M.-S., and E. Genome organization, translation and replication of foot-and-mouth disease virus. In: Domingo F.S.A.E. (Ed). Foot-and-mouth Disease. Current Perspectives (2004), Horizon Bioscience, Norfolk, UK 19-52
14. Bienz K., Egger D., and Pasamontes L. Association of polioviral proteins of the P2 genomic region with the viral replication complex and virus-induced membrane synthesis as visualized by electron microscopic immunocytochemistry and autoradiography. Virology 160 1 (1987) 220-226
15. Bienz K., Egger D., Pfister T., and Troxler M. Structural and functional characterization of the poliovirus replication complex. J. Virol. 66 5 (1992) 2740-2747
16. Bolten R., Egger D., Gosert R., Schaub G., Landmann L., and Bienz K. Intracellular localization of poliovirus plus- and minus-strand RNA visualized by strand-specific fluorescent in situ hybridization. J. Virol. 72 11 (1998) 8578-8585
17. Brown F. Problems with BHK 21 cells. Dev. Biol. Stand. 93 (1998) 85-88
18. Burrows R., Mann J.A., Garland A.J., Greig A., and Goodridge D. The pathogenesis of natural and simulated natural foot-and-mouth disease infection in cattle. J. Comp. Pathol. 91 4 (1981) 599-609
19. Capozzo A.V., Burke D.J., Fox J.W., Bergmann I.E., La Torre J.L., and Grigera P.R. Expression of foot and mouth disease virus non-structural polypeptide 3ABC induces histone H3 cleavage in BHK21 cells. Virus Res. 90 1-2 (2002) 91-99
20. Carrillo C., Tulman E.R., Delhon G., Lu Z., Carreno A., Vagnozzi A., Kutish G.F., and Rock D.L. Comparative genomics of foot-and-mouth disease virus. J. Virol. 79 10 (2005) 6487-6504
21. Cho M.W., Teterina N., Egger D., Bienz K., and Ehrenfeld E. Membrane rearrangement and vesicle induction by recombinant poliovirus 2C and 2BC in human cells. Virology 202 1 (1994) 129-145
22. Choe S.S., Dodd D.A., and Kirkegaard K. Inhibition of cellular protein secretion by picornaviral 3A proteins. Virology 337 1 (2005) 18-29
23. de Wet J.R., Wood K.V., DeLuca M., Helinski D.R., and Subramani S. Firefly luciferase gene: structure and expression in mammalian cells. Mol. Cell. Biol. 7 2 (1987) 725-737
24. Deitz S.B., Dodd D.A., Cooper S., Parham P., and Kirkegaard K. MHC I-dependent antigen presentation is inhibited by poliovirus protein 3A. Proc. Natl. Acad. Sci. U.S.A. 97 25 (2000) 13790-13795
25. Doedens J.R., and Kirkegaard K. Inhibition of cellular protein secretion by poliovirus proteins 2B and 3A. EMBO J. 14 5 (1995) 894-907
26. Doedens J.R., Giddings Jr. T.H., and Kirkegaard K. Inhibition of endoplasmic reticulum-to-Golgi traffic by poliovirus protein 3A: genetic and ultrastructural analysis. J. Virol. 71 12 (1997) 9054-9064
27. Domingo E., Mateu M.G., Martínez M.A., Dopazo J., Moya A., and Sobrino F. Genetic variability and antigenic diversity of foot-and-mouth disease virus. In: Kurstak R.G.M.E., Murphy S.A., and Van-Regenmortel M.H.V. (Eds). Applied Virology Research. Virus Variation and Epidemiolgy vol. 2 (1990), Academic Press Inc., London
28. Egger D., Teterina N., Ehrenfeld E., and Bienz K. Formation of the poliovirus replication complex requires coupled viral translation, vesicle production, and viral RNA synthesis. J. Virol. 74 14 (2000) 6570-6580
29. Falk M.M., Grigera P.R., Bergmann I.E., Zibert A., Multhaup G., and Beck E. Foot-and-mouth disease virus protease 3C induces specific proteolytic cleavage of host cell histone H3. J. Virol. 64 2 (1990) 748-756
30. Falk M.M., Sobrino F., and Beck E. VPg gene amplification correlates with infective particle formation in foot-and-mouth disease virus. J. Virol. 66 4 (1992) 2251-2260
31. Follett E.A., Pringle C.R., and Pennington T.H. Virus development in enucleate cells: echovirus, poliovirus, pseudorabies virus, reovirus, respiratory syncytial virus and Semliki Forest virus. J. Gen. Virol. 26 2 (1975) 183-196
32. Forss S., Strebel K., Beck E., and Schaller H. Nucleotide sequence and genome organization of foot-and-mouth disease virus. Nucleic Acids Res. 12 16 (1984) 6587-6601
33. Gazina E.V., Mackenzie J.M., Gorrell R.J., and Anderson D.A. Differential requirements for COPI coats in formation of replication complexes among three genera of Picornaviridae. J. Virol. 76 21 (2002) 11113-11122
34. Gosert R., Egger D., and Bienz K. A cytopathic and a cell culture adapted hepatitis A virus strain differ in cell killing but not in intracellular membrane rearrangements. Virology 266 1 (2000) 157-169
35. Hope D.A., Diamond S.E., and Kirkegaard K. Genetic dissection of interaction between poliovirus 3D polymerase and viral protein 3AB. J. Virol. 71 12 (1997) 9490-9498
36. Jackson C.L., and Casanova J.E. Turning on ARF: the Sec7 family of guanine-nucleotide-exchange factors. Trends Cell Biol. 10 2 (2000) 60-67
37. Klausner R.D., Donaldson J.G., and Lippincott-Schwartz J. Brefeldin A: insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116 5 (1992) 1071-1080
38. Knox C., Moffat K., Ali S., Ryan M., and Wileman T. Foot-and-mouth disease virus replication sites form next to the nucleus and close to the Golgi apparatus, but exclude marker proteins associated with host membrane compartments. J. Gen. Virol. 86 Pt. 3 (2005) 687-696
39. Lama J., Paul A.V., Harris K.S., and Wimmer E. Properties of purified recombinant poliovirus protein 3aB as substrate for viral proteinases and as co-factor for RNA polymerase 3Dpol. J. Biol. Chem. 269 1 (1994) 66-70
40. Martinez-Salas E. Internal ribosome entry site biology and its use in expression vectors. Curr. Opin. Biotechnol. 10 5 (1999) 458-464
41. Martinez-Salas E., and Domingo E. Effect of expression of the aphthovirus protease 3C on viral infection and gene expression. Virology 212 1 (1995) 111-120
42. Mateu M.G., Rocha E., Vicente O., Vayreda F., Navalpotro C., Andreu D., Pedroso E., Giralt E., Enjuanes L., and Domingo E. Reactivity with monoclonal antibodies of viruses from an episode of foot-and-mouth disease. Virus Res. 8 3 (1987) 261-274
43. Moffat K., Howell G., Knox C., Belsham G.J., Monaghan P., Ryan M.D., and Wileman T. Effects of foot-and-mouth disease virus nonstructural proteins on the structure and function of the early secretory pathway: 2BC but not 3A blocks endoplasmic reticulum-to-Golgi transport. J. Virol. 79 7 (2005) 4382-4395
44. Monaghan P., Cook H., Jackson T., Ryan M., and Wileman T. The ultrastructure of the developing replication site in foot-and-mouth disease virus-infected BHK-38 cells. J. Gen. Virol. 85 Pt. 4 (2004) 933-946
45. Nayak A., Goodfellow I.G., and Belsham G.J. Factors required for the uridylylation of the foot-and-mouth disease virus 3B1, 3B2, and 3B3 peptides by the RNA-dependent RNA polymerase (3Dpol) in vitro. J. Virol. 79 12 (2005) 7698-7706
46. Newman J.F., Cartwright B., Doel T.R., and Brown F. Purification and identification of the RNA-dependent RNA polymerase of foot-and-mouth disease virus. J. Gen. Virol. 45 2 (1979) 497-507
47. Nunez J.I., Baranowski E., Molina N., Ruiz-Jarabo C.M., Sanchez C., Domingo E., and Sobrino F. A single amino acid substitution in nonstructural protein 3A can mediate adaptation of foot-and-mouth disease virus to the guinea pig. J. Virol. 75 8 (2001) 3977-3983
48. O'Donnell V.K., Pacheco J.M., Henry T.M., and Mason P.W. Subcellular distribution of the foot-and-mouth disease virus 3A protein in cells infected with viruses encoding wild-type and bovine-attenuated forms of 3A. Virology 287 1 (2001) 151-162
49. Pacheco J.M., Henry T.M., O'Donnell V.K., Gregory J.B., and Mason P.W. Role of nonstructural proteins 3A and 3B in host range and pathogenicity of foot-and-mouth disease virus. J. Virol. 77 24 (2003) 13017-13027
50. Pereira H.G. Foot-and-mouth disease. In: Gibbs E.P.J. (Ed). Virus Disease of Food Animals vol. 2 (1981), Academic Press Inc, London
51. Porter A.G. Picornavirus nonstructural proteins: emerging roles in virus replication and inhibition of host cell functions. J. Virol. 67 12 (1993) 6917-6921
52. Ryan M.D., Donelly M.L.L., Flint M., Cowton V.M., Luke G., Hughes L.E., Knox C., and de Felipe P. Foot-and-mouth disease proteinases. In: Domingo F.S.a.E. (Ed). Foot-and-Mouth Disease. Current Perspectives (2004), Horizon Bioscience, Norfolk, UK 53-76
53. Sandoval I.V., and Carrasco L. Poliovirus infection and expression of the poliovirus protein 2B provoke the disassembly of the Golgi complex, the organelle target for the antipoliovirus drug Ro-090179. J. Virol. 71 6 (1997) 4679-4693
54. Sanz-Parra A., Sobrino F., and Ley V. Infection with foot-and-mouth disease virus results in a rapid reduction of MHC class I surface expression. J. Gen. Virol. 79 Pt. 3 (1998) 433-436
55. Schlegel A., Giddings Jr. T.H., Ladinsky M.S., and Kirkegaard K. Cellular origin and ultrastructure of membranes induced during poliovirus infection. J. Virol. 70 10 (1996) 6576-6588
56. Sobrino F., Palma E.L., Beck E., Davila M., de la Torre J.C., Negro P., Villanueva N., Ortin J., and Domingo E. Fixation of mutations in the viral genome during an outbreak of foot-and-mouth disease: heterogeneity and rate variations. Gene 50 1-3 (1986) 149-159
57. Sobrino F., Saiz M., Jimenez-Clavero M.A., Nunez J.I., Rosas M.F., Baranowski E., and Ley V. Foot-and-mouth disease virus: a long known virus, but a current threat. Vet. Res. 32 1 (2001) 1-30
58. Strebel K., Beck E., Strohmaier K., and Schaller H. Characterization of foot-and-mouth disease virus gene products with antisera against bacterially synthesized fusion proteins. J. Virol. 57 3 (1986) 983-991
59. Suhy D.A., Giddings Jr. T.H., and Kirkegaard K. Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: an autophagy-like origin for virus-induced vesicles. J. Virol. 74 19 (2000) 8953-8965
60. Tesar M., and Marquardt O. Foot-and-mouth disease virus protease 3C inhibits cellular transcription and mediates cleavage of histone H3. Virology 174 2 (1990) 364-374
61. Toja M., Escarmis C., and Domingo E. Genomic nucleotide sequence of a foot-and-mouth disease virus clone and its persistent derivatives. Implications for the evolution of viral quasispecies during a persistent infection. Virus Res. 64 2 (1999) 161-171
62. Towner J.S., Ho T.V., and Semler B.L. Determinants of membrane association for poliovirus protein 3AB. J. Biol. Chem. 271 43 (1996) 26810-26818
63. Whitton J.L., Cornell C.T., and Feuer R. Host and virus determinants of picornavirus pathogenesis and tropism. Nat. Rev., Microbiol. 3 10 (2005) 765-776
64. Xiang W., Harris K.S., Alexander L., and Wimmer E. Interaction between the 5′-terminal cloverleaf and 3AB/3CDpro of poliovirus is essential for RNA replication. J. Virol. 69 6 (1995) 3658-3667
65. Xiang W., Cuconati A., Hope D., Kirkegaard K., and Wimmer E. Complete protein linkage map of poliovirus P3 proteins: interaction of polymerase 3Dpol with VPg and with genetic variants of 3AB. J. Virol. 72 8 (1998) 6732-6741