Role of lipids on entry and exit of bluetongue virus, a complex non-enveloped virus

Viruses

Volumn 2, Issue 5, 2010, Pages 1218-1235

  Bhattacharya, Bishnupriya ^a   Roy, Polly ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

BTV; Entry; Exit; Lipid rafts; Non enveloped

Indexed keywords

LIPID; NONSTRUCTURAL PROTEIN 3; PROTEIN VP1; PROTEIN VP2; PROTEIN VP3; PROTEIN VP4; PROTEIN VP5; SMALL INTERFERING RNA; SYNAPTOTAGMIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

BLUETONGUE ORBIVIRUS; CELL FRACTIONATION; ENDOSOME; EXOCYTOSIS; GOLGI COMPLEX; HYDROPHOBICITY; LIPID RAFT; NONHUMAN; PICORNAVIRUS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REOVIRUS; REVIEW; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS INCLUSION; VIRUS MORPHOLOGY; VIRUS PARTICLE; VIRUS RELEASE; VIRUS REPLICATION; VIRUS UNCOATING;

BLUETONGUE VIRUS; PICORNAVIRIDAE; REOVIRIDAE; ROTAVIRUS;

EID: 79952086314     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v2051218     Document Type: Review

References (93)

1. Marsh, M.; Helenius, A. Virus entry: open sesame. Cell 2006, 124, 729-740.
2. Smith, A.E.; Helenius, A. How viruses enter animal cells. Science 2004, 304, 237-242.
3. Iwata, H.; Hirasawa, T.; Roy, P. Complete nucleotide sequence of segment 5 of epizootic haemorrhagic disease virus; the outer capsid protein VP5 is homologous to the VP5 protein of bluetongue virus. Virus Res. 1991, 20, 273-281.
4. Hogle, J.M. Poliovirus cell entry: common structural themes in viral cell entry pathways. Annu. Rev. Microbiol. 2002, 56, 677-702.
5. Roy, P.; Noad, R. Bluetongue virus assembly and morphogenesis. Curr. Top. Microbiol. Immunol. 2006, 309, 87-116.
6. Hewat, E.A.; Booth, T.F.; Loudon, P.T.; Roy, P. Three-dimensional reconstruction of baculovirus expressed bluetongue virus core-like particles by cryo-electron microscopy. Virology 1992, 189, 10-20.
7. Prasad, B.V.V.; Yamaguchi, S.; Roy, P. Three-dimensional structure of single-shelled bluetongue virus. J. Virol. 1992, 66, 2135-2142.
8. Grimes, J.M.; Jakana, J.; Ghosh, M.; Basak, A.K.; Roy, P.; Chiu, W.; Stuart, D.I.; Prasad, B.V. An atomic model of the outer layer of the bluetongue virus core derived from X-ray crystallography and electron cryomicroscopy. Structure 1997, 5, 885-893.
9. Grimes, J.M.; Burroughs, J.N.; Gouet, P.; Diprose, J.M.; Malby, R.; Zientara, S.; Mertens, P.P.C.; Stuart, D.I. The atomic structure of the bluetongue virus core. Nature 1998, 395, 470-478.
10. Hewat, E.A.; Booth, T.F.; Roy, P. Structure of bluetongue virus particles by cryoelectron microscopy. J. Struct. Biol. 1992, 109, 61-69.
11. Nason, E.; Rothnagel, R.; Muknerge, S.K.; Kar, A.K.; Forzan, M.; Prasad, B.V.V.; Roy, P. Interactions between the Inner and Outer Capsids of Bluetongue Virus. J. Virol. 2004, 78, 8059-8067.
12. Hassan, S.H.; Roy, P. Expression and functional characterization of bluetongue virus VP2 protein: role in cell entry. J. Virol. 1999, 73, 9832-9842.
13. Eaton, B.T.; Hyatt A.D.; Brookes, S.M. The replication of bluetongue virus. Curr. Top. Microbiol. Immunol. 1990, 162, 89-118.
14. Forzan, M.; Wirblich, C.; Roy, P. A capsid protein of nonenveloped Bluetongue virus exhibits membrane fusion activity. Proc. Natl. Acad. Sci. USA 2004, 101, 2100-2105.
15. Forzan, M.; Marsh, M.; Roy, P. Bluetongue virus entry into cells. J. Virol. 2007, 81, 4819-4827.
16. Fraile-Ramos, A.; Kohout, T.A.; Waldhoer, M.; Marsh, M. Endocytosis of the viral chemokine receptor US28 does not require beta-arrestins but is dependent on the clathrin-mediated pathway. Traffic 2003, 4, 243-253.
17. Conner, S.D.; Schmid, S.L. Regulated portals of entry into the cell. Nature 2003, 422, 37-44.
18. Smythe, E. Clathrin-coated vesicle formation: a paradigm for coated-vesicle formation. Biochem. Soc. Trans. 2003, 31, 736-739.
19. Meier, O.; Greber, U.F. Adenovirus endocytosis. J Gene Med. 2004, 6, S152-163.
20. Hyatt, A.D.; Eaton, B.T.; Brookes, S.M. The release of bluetongue virus from infected cells and their superinfection by progeny virus. Virology 1989, 173, 21-34.
21. Hassan, S.H.; Wirblich, C.; Forzan, M.; Roy, P. Expression and functional characterization of bluetongue virus VP5 protein: role in cellular permeabilization. J. Virol. 2001, 75, 8356-8367.
22. Colman, P.M.; Lawrence, M.C. The structural biology of type I viral membrane fusion. Nat. Rev. Mol. Cell Biol. 2003, 4, 309-319.
23. Hewat, E.A.; Booth, T.F.; Roy, P. Structure of correctly self-assembled bluetongue virus-like particles. J. Struct. Biol. 1994, 112, 183-191.
24. Zhang, X.; Boyce, M.; Bhattacharya, B.; Zhang, X.; Scheina, S.; Roy, P.; Zhou, Z.H. Bluetongue virus coat protein VP2 contains a sialic acid-binding domain and VP5 has similarities to enveloped virus fusion proteins. Proc. Natl. Academy. Sci. USA 2010, 107, 6292-6297.
25. Dormitzer, P.R.; Sun, Z.; Wagner, G.; Harrison, S.C. The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. Embo J. 2002, 21, 885-897.
26. Eaton, B.T.; Crameri, G.S. The site of bluetongue virus attachment to glycophorins from a number of animal erythrocytes. J. Gen. Virol. 1989, 70, 3347-3353.
27. Tan, K.; Liu, J.; Wang, J.; Shen, S.; Lu, M.; Atomic structure of a thermostable subdomain of HIV-1 gp41. Proc. Natl. Acad. Sci. USA 1997, 94, 12303-12308.
28. Weissenhorn, W.; Dessen, A.; Harrison, S.C.; Skehel, J.J.; Wiley, D.C. Atomic structure of the ectodomain from HIV-1 gp41. Nature. 1997, 387, 426-430.
29. Sauter, N.K.; Hanson, J.E.; Glick, G.D.; Brown, J.H.; Crowther, R.L.; Park, S.J.; Skehel, J.J.; Wiley, D.C. Binding of influenza virus hemagglutinin to analogs of its cell-surface receptor, sialic acid: analysis by proton nuclear magnetic resonance spectroscopy and X-ray crystallography. Biochemistry 1992, 31, 9609-9621.
30. Heldwein, E.E.; Lou, H.; Bender, F.C.; Cohen, G.H.; Eisenberg, R.J.; Harrison, S.C. Crystal structure of glycoprotein B from herpes simplex virus 1. Science 2006, 313, 217-220.
31. Roche, S.; Rey, F.A.; Gaudin, Y.; Bressanelli, S. Structure of the prefusion form of the vesicular stomatitis virus glycoprotein G. Science 2007, 315, 843-848.
32. Dormitzer, P.R.; Nason, E.B.; Prasad, B.V.; Harrison, S.C. Structural rearrangements in the membrane penetration protein of a non-enveloped virus. Nature 2004, 430, 1053-1058.
33. Van Dijk, A.A.; Huismans, H. The in vitro activation and further characterization of the bluetongue virus-associated transcriptase. Virology 1980, 104, 347-356.
34. Van Dijk, A.A.; Huismans, H. In vitro transcription and translation of bluetongue virus mRNA. J. Gen. Virol. 1988, 69, 573-581.
35. Stauber, N.; Martinez-Costas, J.; Sutton, G.; Monastyrskaya, K.; Roy, P. Bluetongue virus VP6 protein binds ATP and exhibits an RNA-dependent ATPase function and a helicase activity that catalyze the unwinding of double-stranded RNA substrates. J. Virol. 1997, 71, 7220-7226.
36. Costas, J.; Sutton, G.; Roy, P., Guanylyltransferase and RNA 5'-triphopatase activities of the purified expressed VP4 protein of bluetongue virus. J. Mol. Biol. 1998, 280, 859-866.
37. Ramadevi, N.; Burroughs, J.N.; Mertens, P.P.C.; Jones, I.M.; Roy, P. Capping and methylation of mRNA by purified recombinant VP4 protein of Bluetongue virus. Proc. Natl. Acad. Sci. 1998, 95, 13537-13542.
38. Ramadevi, N.; Roy, P. Bluetongue virus core protein VP4 has nucleoside triphosphate phosphohydrolase activity. J. Gen. Virol. 1998, 79, 2475-2480.
39. Boyce, M.; Wehrfritz, J.; Noad, R.; Roy, P. Purified recombinant bluetongue virus VP1 exhibits RNA replicase activity. J. Virol. 2004, 78, 3994-4002.
40. Thomas, C.P.; Booth, T.F.; Roy, P. Synthesis of bluetongue virus-encoded phosphoprotein and formation of inclusion bodies by recombinant baculovirus in insect cells: it binds the single-stranded RNA species. J. Gen. Virol. 1990, 71, 2073-2083.
41. Loudon, P.T.; Roy, P. Assembly of five bluetongue virus proteins expressed by recombinant baculoviruses: inclusion of the largest protein VP1 in the core and virus-like proteins. Virology 1991, 180, 798-802.
42. Lymperopoulos, K.; Wirblich, C.; Brierley, I.; Roy, P. Sequence specificity in the interaction of Bluetongue virus non-structural protein 2 (NS2) with viral RNA. J. Biol. Chem. 2003, 278, 31722-31730.
43. Kar, A.K.; Ghosh, M.; Roy, P. Mapping the assembly of Bluetongue virus scaffolding protein VP3. Virology 2004, 324, 387-399.
44. Kar, A.K.; Iwatani, N.; Roy, P. Assembly and intracellular localization of the bluetongue virus core protein VP3. J. Virol. 2005, 79, 11487-11495.
45. Modrof, J.; Lymperopoulos, K.; Roy, P. Phosphorylation of Bluetongue Virus Nonstructural Protein 2 Is Essential for Formation of Viral Inclusion Bodies. J. Virol. 2005, 79, 10023-10031.
46. Lymperopoulos, K.; Noad, R.; Tosi, S.; Nethisinghe, S.; Brierley, I.; Roy, P. Specific binding of Bluetongue virus NS2 to different viral plus-strand RNAs. Virology 2006, 353, 17-26.
47. Kar, A.K.; Bhattacharya, B.; Roy, P. Bluetongue virus RNA binding protein NS2 is a modulator of viral replication and assembly. BMC Mol. Biol. 2007, 8, 4.
48. Tanaka, S.; Roy, P. Identification of domains in bluetongue virus VP3 molecules essential for the assembly of virus cores. J. Virol. 1994, 68, 2795-2802.
49. Limn, C.H.; Staeuber, N.; Monastyrskaya, K.; Gouet, P.; Roy, P. Functional dissection of the major structural protein of bluetongue virus: identification of key residues within VP7 essential for capsid assembly. J. Virol. 2000, 74, 8658-8669.
50. Silvestri, L.S.; Taraporewala, Z.F.; Patton, J.T., Rotavirus replication: plus-sense templates for double-stranded RNA synthesis are made in viroplasms. J. Virol. 2004, 78, 7763-7774.
51. Broering, T.J.; Kim, J.; Miller, C.L.; Piggott, C.D.; Dinoso, J.B.; Nibert, M. L.; Parker, J. S. Reovirus nonstructural protein mu NS recruits viral core surface proteins and entering core particles to factory-like inclusions. J. Virol. 2004, 78, 1882-1892.
52. Miller, C.L.; Arnold, M.M.; Broering, T.J.; Hastings, C.E.; Nibert, M. L. Localization of mammalian orthoreovirus proteins to cytoplasmic factory-like structures via nonoverlapping regions of microNS. J. Virol. 2010, 84, 867-882.
53. Bhattacharya, B.; Roy, P. London School of Hygiene and Tripical Medicine, London, UK. Unpublished work, 2008.
54. Bhattacharya, B.; Roy, P. Bluetongue virus outer capsid protein VP5 interacts with membrane lipid rafts via a SNARE domain. J. Virol. 2008, 82, 10600-10612.
55. Harder, T.; Simons, K. Caveolae, DIGs and the dynamics of sphingolipid-cholesterol microdomains. Curr. Opin. Cell Biol. 1997, 9, 534-542.
56. Harder, T.; Scheiffele, P.; Verkade, P.; Simons, K. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 1998, 141, 929-942.
57. Campbell, S.M.; Crowe, S.M.; Mak, J. Lipid rafts and HIV-1: from viral entry to assembly of progeny virions. J. Clin. Virol. 2001, 22, 217-227.
58. Briggs, J.A.; Wilk, T.; Fuller, S.D. Do lipid rafts mediate virus assembly and pseudotyping? J. Gen. Virol. 2003, 84, 757-768.
59. Ono, A.; Freed, E.O. Role of lipid rafts in virus replication. Adv Virus Res. 2005, 64, 311-358.
60. Kundu, A.; Avalos, R.T.; Sanderson, C.M.; Nayak, D.P. Transmembrane domain of influenza virus neuraminidase, a type II protein, possesses an apical sorting signal in polarized MDCK cells. J Virol. 1996, 70, 6508-6515.
61. Martin-Belmonte, F.; Lopez-Guerrero, J.A.; Carrasco, L.; Alonso, M.A. The amino-terminal nine amino acid sequence of poliovirus capsid VP4 protein is sufficient to confer N-myristoylation and targeting to detergent-insoluble membranes. Biochemistry 2000, 39, 1083-1090.
62. Fukuda, M.; Moreira, J. E.; Liu, V.; Sugimori, M.; Mikoshiba, K.; Llinas, R. R. Role of the conserved WHXL motif in the C terminus of synaptotagmin in synaptic vesicle docking. Proc. Natl. Acad. Sci. USA 2000, 97, 14715-14719.
63. Bhattacharya, B.; Noad, R. J.; Roy, P. Interaction between Bluetongue virus outer capsid protein VP2 and vimentin is necessary for virus egress. J. Virol. 2007, 4, 7.
64. Starkey, W.G.; Collins, J.; Wallis, T.S.; Clarke, G.J.; Spencer, A.J.; Haddon, S.J.; Osborne, M. P.; Candy, D. C.; Stephen, J. Kinetics, tissue specificity and pathological changes in murine rotavirus infection of mice. J Gen Virol. 1986, 67, 2625-2634.
65. Pesavento, J.B.; Crawford, S.E.; Estes, M.K.; Prasad, B.V. Rotavirus proteins: structure and assembly. Curr. Top. Microbiol. Immunol. 2006, 309, 189-219.
66. Storey, S.M.; Gibbons, T.F.; Williams, C.V.; Parr, R.D.; Schroeder, F.; Ball, J.M. Full-length, glycosylated NSP4 is localized to plasma membrane caveolae by a novel raft isolation technique. J. Virol. 2007, 81, 5472-5483.
67. Delmas, O.; Breton, M.; Sapin, C.; Le Bivic, A.; Colard, O.; Trugnan, G. Heterogeneity of Raft-type membrane microdomains associated with VP4, the rotavirus spike protein, in Caco-2 and MA 104 cells. J. Virol. 2007, 81, 1610-1618.
68. Mirre, C.; Monlauzeur, L.; Garcia, M.; Delgrossi, M.H.; Le Bivic, A. Detergent-resistant membrane microdomains from Caco-2 cells do not contain caveolin. Am. J. Physiol. 1996, 271, 887-894.
69. Chwetzoff, S.; Trugnan, G. Rotavirus assembly: an alternative model that utilizes an atypical trafficking pathway. Curr. Top. Microbiol. Immunol. 2006, 309, 245-261.
70. Sapin, C.; Colard, O.; Delmas, O.; Tessier, C.; Breton, M.; Enouf, V.; Chwetzoff, S.; Ouanich, J.; Cohen, J.; Wolf, C.; Trugnan, G. Rafts promote assembly and atypical targeting of a nonenveloped virus, rotavirus, in Caco-2 cells. J. Virol. 2002, 76, 4591-4602.
71. Cuadras, M.A.; Greenberg, H.B. Rotavirus infectious particles use lipid rafts during replication for transport to the cell surface in vitro and in vivo. Virology 2003, 313, 308-321.
72. Mohan, K.V.; Muller, J.; Atreya, C.D. Defective rotavirus particle assembly in lovastatin-treated MA104 cells. Arch. Virol. 2008, 153, 2283-2290.
73. Eaton, B.T.; Hyatt, A.D.; White, J. R. Association of bluetongue virus with the cytoskeleton. Virology 1987, 157, 107-116.
74. Hyatt, A.D.; Gould, A.R.; Coupar, B.; Eaton, B.T. Localization of the non-structural protein NS3 in bluetongue virus-infected cells. J. Gen. Virol. 1991, 72, 2263-2267.
75. Beaton, A.R.; Rodriguez, J.; Reddy, Y.K.; Roy, P. The membrane trafficking protein calpactin forms a complex with bluetongue virus protein NS3 and mediates virus release. Proc. Natl. Acad. Sci.USA 2002, 99, 13154-13159.
76. Wu, X.; Chen, S.Y.; Iwata, H.; Compans, R.W.; Roy, P. Multiple glycoproteins synthesized by the smallest RNA segment (S10) of bluetongue virus. J. Virol. 1992, 66, 7104-7112.
77. Han, Z.; Harty, R.N. The NS3 protein of bluetongue virus exhibits viroporin-like properties. J. Biol. Chem. 2004, 279, 43092-43097.
78. Babst, M.; Katzmann, D.J.; Snyder, W.B.; Wendland, B.; Emr, S.D. Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting. Dev. Cell. 2002, 3, 271-282.
79. Gruenberg, J.; Stenmark, H. The biogenesis of multivesicular endosomes. Nat. Rev. Mol. Cell Biol. 2004, 5, 317-323.
80. Wirblich, C.; Bhattacharya, B.; Roy, P. Nonstructural protein 3 of bluetongue virus assists virus release by recruiting ESCRT-I protein Tsg101. J. Virol. 2006, 80, 460-473.
81. Celma, C.C.; Roy, P. A viral nonstructural protein regulates bluetongue virus trafficking and release. J. Virol. 2009, 83, 6806-6816.
82. Blanchette-Mackie, E.J.; Dwyer, N.K.; Amende, L.M.; Kruth, H.S.; Butler, J.D.; Sokol, J.; Comly, M.E.; Vanier, M.T.; August, J.T.; Brady, R.O. et al. Type-C Niemann-Pick disease: low density lipoprotein uptake is associated with premature cholesterol accumulation in the Golgi complex and excessive cholesterol storage in lysosomes. Proc Natl Acad Sci USA. 1988, 85, 8022-8026.
83. Coxey, R.A.; Pentchev, P.G.; Campbell, G.; Blanchette-Mackie, E.J. Differential accumulation of cholesterol in Golgi compartments of normal and Niemann-Pick type C fibroblasts incubated with LDL: a cytochemical freeze-fracture study. J. Lipid Res. 1993, 34, 1165-1176.
84. Simons, K.; Ikonen, E.; Functional rafts in cell membranes. Nature 1997, 387, 569-572.
85. Zimmer, G.; Zimmer, K.P.; Trotz, I.; Herrler, G. Vesicular stomatitis virus glycoprotein does not determine the site of virus release in polarized epithelial cells. J. Virol. 2002, 76, 4103-4107.
86. Bergmann, J.E.; Fusco, P.J. The M protein of vesicular stomatitis virus associates specifically with the basolateral membranes of polarized epithelial cells independently of the G protein. J. Cell Biol. 1988, 107, 1707-1715.
87. Maisner, A.; Klenk, H.; Herrler, G. Polarized budding of measles virus is not determined by viral surface glycoproteins. J. Virol. 1998, 72, 5276-5278.
88. Naim, H.Y.; Ehler, E.; Billeter, M.A. Measles virus matrix protein specifies apical virus release and glycoprotein sorting in epithelial cells. EMBO J. 2000, 19, 3576-3585.
89. Jourdan, N.; Maurice, M.; Delautier, D.; Quero, A.M.; Servin, A.L.; Trugnan, G. Rotavirus is released from the apical surface of cultured human intestinal cells through nonconventional vesicular transport that bypasses the Golgi apparatus. J. Virol. 1997, 71, 8268-8278.
90. Sapin, C.; Colard, O.; Delmas, O.; Tessier, C.; Breton, M.; Enouf, V.; Chwetzoff, S.; Ouanich, J.; Cohen, J.; Wolf, C.; Trugnan, G. Rafts promote assembly and atypical targeting of a nonenveloped virus, rotavirus, in Caco-2 cells. J. Virol. 2002, 76, 4591-4602.
91. Cuadras, M.A.; Greenberg, H. B. Rotavirus infectious particles use lipid rafts during replication for transport to the cell surface in vitro and in vivo. Virology 2003, 313, 308-321.
92. Trask, S.D.; Kim, I.S.; Harrison, S.C.; Dormitzer, P.R. A rotavirus spike protein conformational intermediate binds lipid bilayers. J. Virol. 2010, 84, 1764-1770.
93. Gibbons, D.L.; Vaney, M.C.; Roussel, A.; Vigouroux, A.; Reilly, B.; Lepault, J.; Kielian, M.; Rey, F.A. Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus. Nature 2004, 427, 320-325.