Coupling of replication and assembly in flaviviruses

Current Opinion in Virology

Volumn 9, Issue , 2014, Pages 134-142

  Apte Sengupta, Swapna ^a   Sirohi, Devika ^a   Kuhn, Richard J ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIPID; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; DENGUE VIRUS; ENDOPLASMIC RETICULUM MEMBRANE; FLAVIVIRUS; FLAVIVIRUS INFECTION; LIPID METABOLISM; MEMBRANE VESICLE; NONHUMAN; VIROGENESIS; VIRUS ASSEMBLY; VIRUS NUCLEOCAPSID; VIRUS REPLICATION; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; PHYSIOLOGY;

FLAVIVIRUS; HOST-PATHOGEN INTERACTIONS; HUMANS; LIPID METABOLISM; VIRAL PROTEINS; VIRUS ASSEMBLY; VIRUS REPLICATION;

EID: 84908416018     PISSN: 18796257     EISSN: 18796265     Source Type: Journal    
DOI: 10.1016/j.coviro.2014.09.020     Document Type: Review

References (85)

1. P. Avirutnan, A. Fuchs, R.E. Hauhart, P. Somnuke, S. Youn, M.S. Diamond, and J.P. Atkinson Antagonism of the complement component C4 by flavivirus nonstructural protein NS1 J Exp Med 207 2010 793 806
2. B.D. Lindenbach, C.L. Murray, H.-J. Thiel, and C.M. Rice Flaviviridae: the viruses and their replication D.M. Knipe, Fields Virology edn 6 2013 Lippincott Williams & Wilkins New York, NY (Chapter 26)
3. J.Y. Leung, G.P. Pijlman, N. Kondratieva, J. Hyde, J.M. Mackenzie, and A.A. Khromykh Role of nonstructural protein NS2A in flavivirus assembly J Virol 82 2008 4731 4741
4. X. Xie, S. Gayen, C. Kang, Z. Yuan, and P.-Y. Shi Membrane topology and function of dengue virus NS2A protein J Virol 87 2013 4609 4622
5. B.M. Kümmerer, and C.M. Rice Mutations in the yellow fever virus nonstructural protein NS2A selectively block production of infectious particles J Virol 76 2002 4773 4784
6. S. Miller, S. Kastner, J. Krijnse-Locker, S. Bühler, and R. Bartenschlager The non-structural protein 4A of dengue virus is an integral membrane protein inducing membrane alterations in a 2K-regulated manner J Biol Chem 282 2007 8873 8882
7. J. Roosendaal, E.G. Westaway, A. Khromykh, and J.M. Mackenzie Regulated cleavages at the West Nile Virus NS4A-2K-NS4B junctions play a major role in rearranging cytoplasmic membranes and Golgi trafficking of the NS4A protein J Virol 80 2006 4623 4632
8. J.E. McLean, A. Wudzinska, E. Datan, D. Quaglino, and Z. Zakeri Flavivirus NS4A-induced autophagy protects cells against death and enhances virus replication J Biol Chem 286 2011 22147 22159
9. J.L. Muñoz-Jordán, M. Laurent-Rolle, J. Ashour, L. Martínez-Sobrido, M. Ashok, W.I. Lipkin, and A. García-Sastre Inhibition of alpha/beta interferon signaling by the NS4B protein of flaviviruses J Virol 79 2005 8004 8013
10. I. Umareddy, A. Chao, A. Sampath, F. Gu, and S.G. Vasudevan Dengue virus NS4B interacts with NS3 and dissociates it from single-stranded RNA J Gen Virol 87 2006 2605 2614
11. L.K. Gillespie, A. Hoenen, G. Morgan, and J.M. Mackenzie The endoplasmic reticulum provides the membrane platform for biogenesis of the flavivirus replication complex J Virol 84 2010 10438 10447
12. J. Mackenzie Wrapping things up about virus RNA replication Traffic 6 2005 967 977
13. E.G. Westaway, J.M. Mackenzie, M.T. Kenney, M.K. Jones, and A.A. Khromykh Ultrastructure of Kunjin virus-infected cells: colocalization of NS1 and NS3 with double-stranded RNA, and of NS2B with NS3, in virus-induced membrane structures J Virol 71 1997 6650 6661
14. S. Welsch, S. Miller, I. Romero-Brey, A. Merz, C.K.E. Bleck, P. Walther, S.D. Fuller, C. Antony, J. Krijnse-Locker, and R. Bartenschlager Composition three-dimensional architecture of the dengue virus replication and assembly sites Cell Host Microbe 5 2009 365 375
15. J. Junjhon, J.G. Pennington, T.J. Edwards, R. Perera, J. Lanman, and R.J. Kuhn Ultrastructural characterization and three-dimensional architecture of replication sites in dengue virus-infected mosquito cells J Virol 88 2014 4687 4697
16. D.K. Offerdahl, D.W. Dorward, B.T. Hansen, and M.E. Bloom A three-dimensional comparison of tick-borne flavivirus infection in mammalian and tick cell lines PLoS ONE 7 2012 e47912
17. H.T. McMahon, and J.L. Gallop Membrane curvature and mechanisms of dynamic cell membrane remodelling Nature 438 2005 590 596
18. E.E. Kooijman, V. Chupin, B. de Kruijff, and K.N.J. Burger Modulation of membrane curvature by phosphatidic acid and lysophosphatidic acid Traffic 4 2003 162 174
19. P.F. Devaux, A. Herrmann, N. Ohlwein, and M.M. Kozlov How lipid flippases can modulate membrane structure Biochem Biophys Acta (BBA): Biomembr 1778 2008 1591 1600
20. P.H. Kaufusi, J.F. Kelley, R. Yanagihara, and V.R. Nerurkar Induction of endoplasmic reticulum-derived replication-competent membrane structures by West Nile Virus non-structural protein 4B PLoS ONE 9 2014 e84040
21. O. Stern, Y.-F. Hung, O. Valdau, Y. Yaffe, E. Harris, S. Hoffmann, D. Willbold, and E.H. Sklan An N-terminal amphipathic helix in dengue virus nonstructural protein 4A mediates oligomerization and is essential for replication J Virol 87 2013 4080 4085
22. C.S.H. Teo, and J.J.H. Chu Cellular vimentin regulates construction of dengue virus replication complexes through interaction with NS4A protein J Virol 88 2014 1897 1913
23. D.L. Akey, W.C. Brown, S. Dutta, J. Konwerski, J. Jose, T.J. Jurkiw, J. DelProposto, C.M. Ogata, G. Skiniotis, and R.J. Kuhn Flavivirus NS1 structures reveal surfaces for associations with membranes and the immune system Science 343 2014 881 885
24. J.M. Mackenzie, M.K. Jones, and P.R. Young Immunolocalization of the dengue virus nonstructural glycoprotein NS1 suggests a role in viral RNA replication Virology 220 1996 232 240
25. J.M. Mackenzie, A.A. Khromykh, M.K. Jones, and E.G. Westaway Subcellular localization and some biochemical properties of the flavivirus Kunjin nonstructural proteins NS2A and NS4A Virology 245 1998 203 215
26. J.M. Mackenzie, A.A. Khromykh, and R.G. Parton Cholesterol manipulation by West Nile Virus perturbs the cellular immune response Cell Host Microbe 2 2007 229 239
27. A.E. Matusan, M.J. Pryor, A.D. Davidson, and P.J. Wright Mutagenesis of the dengue virus type 2 NS3 protein within and outside helicase motifs: effects on enzyme activity and virus replication J Virol 75 2001 9633 9643
28. L. Yu, K. Takeda, and L. Markoff Protein-protein interactions among West Nile non-structural proteins and transmembrane complex formation in mammalian cells Virology 446 2013 365 377
29. S. Youn, T. Li, B.T. McCune, M.A. Edeling, D.H. Fremont, I.M. Cristea, and M.S. Diamond Evidence for a genetic and physical interaction between nonstructural proteins NS1 and NS4B that modulates replication of West Nile Virus J Virol 86 2012 7360 7371
30. B.D. Lindenbach, and C.M. Rice Genetic interaction of flavivirus nonstructural proteins NS1 and NS4A as a determinant of replicase function J Virol 73 1999 4611 4621
31. Z. Yi, Z. Yuan, C.M. Rice, and M.R. MacDonald Flavivirus replication complex assembly revealed by DNAJC14 functional mapping J Virol 86 2012 11815 11832
32. W.-L. Pong, Z.-S. Huang, P.-G. Teoh, C.-C. Wang, and H.-N. Wu RNA binding property and RNA chaperone activity of dengue virus core protein and other viral RNA-interacting proteins FEBS Lett 585 2011 2575 2581
33. P.-G. Teoh, Z.-S. Huang, W.-L. Pong, P.-C. Chen, and H.-N. Wu Maintenance of dimer conformation by the dengue virus core protein α4-α4′ helix pair is critical for nucleocapsid formation and virus production J Virol 88 2014 7998 8015
34. A.A. Khromykh, A.N. Varnavski, P.L. Sedlak, and E.G. Westaway Coupling between replication and packaging of flavivirus RNA: evidence derived from the use of DNA-based full-length cDNA clones of Kunjin virus J Virol 75 2001 4633 4640
35. G.A. Belov, V. Nair, B.T. Hansen, F.H. Hoyt, E.R. Fischer, and E. Ehrenfeld Complex dynamic development of poliovirus membranous replication complexes J Virol 86 2012 302 312
36. R.W. Limpens, H.M. van der Schaar, D. Kumar, A.J. Koster, E.J. Snijder, F.J. van Kuppeveld, and M. Barcena The transformation of enterovirus replication structures: a three-dimensional study of single- and double-membrane compartments MBio 2011 2
37. I. Romero-Brey, A. Merz, A. Chiramel, J.Y. Lee, P. Chlanda, U. Haselman, R. Santarella-Mellwig, A. Habermann, S. Hoppe, and S. Kallis Three-dimensional architecture and biogenesis of membrane structures associated with hepatitis C virus replication PLoS Pathog 8 2012 e1003056
38. Y.S. Chang, C.L. Liao, C.H. Tsao, M.C. Chen, C.I. Liu, L.K. Chen, and Y.L. Lin Membrane permeabilization by small hydrophobic nonstructural proteins of Japanese encephalitis virus J Virol 73 1999 6257 6264
39. M.M. Samsa, J.A. Mondotte, N.G. Iglesias, I. Assunção-Miranda, G. Barbosa-Lima, A.T. Da Poian, P.T. Bozza, and A.V. Gamarnik Dengue virus capsid protein usurps lipid droplets for viral particle formation PLoS Pathog 5 2009 e1000632
40. C. López, L. Gil, L. Lazo, I. Menéndez, E. Marcos, J. Sánchez, I. Valdés, V. Falcón, M. de la Rosa, and G. Márquez In vitro assembly of nucleocapsid-like particles from purified recombinant capsid protein of dengue-2 virus Arch Virol 154 2009 695 698
41. S. Kiermayr, R.M. Kofler, C.W. Mandl, P. Messner, and F.X. Heinz Isolation of capsid protein dimers from the tick-borne encephalitis flavivirus and in vitro assembly of capsid-like particles J Virol 78 2004 8078 8084
42. X. Zhang, P. Ge, X. Yu, J.M. Brannan, G. Bi, Q. Zhang, S. Schein, and Z.H. Zhou Cryo-EM structure of the mature dengue virus at 3.5-Å resolution Nat Struct Mol Biol 20 2013 105 110
43. S. Mukhopadhyay, B.S. Kim, P.R. Chipman, M.G. Rossmann, and R.J. Kuhn Structure of West Nile virus Science 302 2003 248
44. R.J. Kuhn, W. Zhang, M.G. Rossmann, S.V. Pletnev, J. Corver, E. Lenches, C.T. Jones, S. Mukhopadhyay, P.R. Chipman, and E.G. Strauss Structure of dengue virus: implications for flavivirus organization, maturation, and fusion Cell 108 2002 717 725
45. J. Schalich, S.L. Allison, K. Stiasny, C.W. Mandl, C. Kunz, and F.X. Heinz Recombinant subviral particles from tick-borne encephalitis virus are fusogenic and provide a model system for studying flavivirus envelope glycoprotein functions J Virol 70 1996 4549 4557
46. E. Lee, C.E. Stocks, S.M. Amberg, C.M. Rice, and M. Lobigs Mutagenesis of the signal sequence of yellow fever virus prM protein: enhancement of signalase cleavage in vitro is lethal for virus production J Virol 74 2000 24 32
47. M. Lobigs, and E. Lee Inefficient signalase cleavage promotes efficient nucleocapsid incorporation into budding flavivirus membranes J Virol 78 2004 178 186
48. M. Lobigs, E. Lee, M.L. Ng, M. Pavy, and P. Lobigs A flavivirus signal peptide balances the catalytic activity of two proteases and thereby facilitates virus morphogenesis Virology 401 2010 80 89
49. T.C. Pierson, and M.S. Diamond Degrees of maturity: the complex structure and biology of flaviviruses Curr Opin Virol 2 2012 168 175
50. I.A. Rodenhuis-Zybert, J. Wilschut, and J.M. Smit Partial maturation: an immune-evasion strategy of dengue virus? Trends Microbiol 19 2011 248 254
51. J. Peña, and E. Harris Early dengue virus protein synthesis induces extensive rearrangement of the endoplasmic reticulum independent of the UPR and SREBP-2 pathway PLoS ONE 7 2012 e38202
52. N.S. Heaton, R. Perera, K.L. Berger, S. Khadka, D.J. LaCount, R.J. Kuhn, and G. Randall Dengue virus nonstructural protein 3 redistributes fatty acid synthase to sites of viral replication and increases cellular fatty acid synthesis Proc Natl Acad Sci U S A 107 2010 17345 17350
53. W.-C. Tang, R.-J. Lin, C.-L. Liao, and Y.-L. Lin Rab18 facilitates dengue virus infection by targeting fatty acid synthase to sites of viral replication J Virol 88 2014 6793 6804
54. M.A. Martín-Acebes, A.-B. Blázquez, N. Jiménez de Oya, E. Escribano-Romero, and J.-C. Saiz West Nile Virus replication requires fatty acid synthesis but is independent on phosphatidylinositol-4-phosphate lipids PLoS ONE 6 2011 e24970
55. N.S. Heaton, and G. Randall Dengue virus-induced autophagy regulates lipid metabolism Cell Host Microbe 8 2010 422 432
56. R. Perera, C. Riley, G. Isaac, A.S. Hopf-Jannasch, R.J. Moore, K.W. Weitz, L. Pasa-Tolic, T.O. Metz, J. Adamec, and R.J. Kuhn Dengue virus infection perturbs lipid homeostasis in infected mosquito cells PLoS Pathog 8 2012 e1002584
57. S. Das, S. Chakraborty, and A. Basu Critical role of lipid rafts in virus entry and activation of phosphoinositide 3′ kinase/Akt signaling during early stages of Japanese encephalitis virus infection in neural stem/progenitor cells J Neurochem 115 2010 537 549
58. R. Soto-Acosta, C. Mosso, M. Cervantes-Salazar, H. Puerta-Guardo, F. Medina, L. Favari, J.E. Ludert, and R.M. del Angel The increase in cholesterol levels at early stages after dengue virus infection correlates with an augment in LDL particle uptake and HMG-CoA reductase activity Virology 442 2013 132 147
59. M. Kalia, R. Khasa, M. Sharma, M. Nain, and S. Vrati Japanese encephalitis virus infects neuronal cells through a clathrin-independent endocytic mechanism J Virol 87 2013 148 162
60. G.R. Medigeshi, A.J. Hirsch, D.N. Streblow, J. Nikolich-Zugich, and J.A. Nelson West Nile Virus entry requires cholesterol-rich membrane microdomains and is independent of αvβ3 integrin J Virol 82 2008 5212 5219
61. Y.-Z. Zhu, M.-M. Cao, W.-B. Wang, W. Wang, H. Ren, P. Zhao, and Z.-T. Qi Association of heat-shock protein 70 with lipid rafts is required for Japanese encephalitis virus infection in Huh7 cells J Gen Virol 93 2012 61 71
62. E. Zaitseva, S.-T. Yang, K. Melikov, S. Pourmal, and L.V. Chernomordik Dengue virus ensures its fusion in late endosomes using compartment-specific lipids PLoS Pathog 6 2010 e1001131
63. C. Rothwell, A. LeBreton, Ng.C. Young, J.Y.H. Lim, W. Liu, S. Vasudevan, M. Labow, F. Gu, and L.A. Gaither Cholesterol biosynthesis modulation regulates dengue viral replication Virology 389 2009 8 19
64. C.-J. Lee, H.-R. Lin, C.-L. Liao, and Y.-L. Lin Cholesterol effectively blocks entry of flavivirus J Virol 82 2008 6470 6480
65. M. Martinez-Gutierrez, L.A. Correa-Londoño, J.E. Castellanos, J.C. Gallego-Gómez, and J.E. Osorio Lovastatin delays infection and increases survival rates in AG129 mice infected with dengue virus serotype 2 PLoS ONE 9 2014 e28741
66. H. Tani, M. Shiokawa, Y. Kaname, H. Kambara, Y. Mori, T. Abe, K. Moriishi, and Y. Matsuura Involvement of ceramide in the propagation of Japanese encephalitis virus J Virol 84 2010 2798 2807
67. M.A. Martín-Acebes, T. Merino-Ramos, A.-B. Blázquez, J. Casas, E. Escribano-Romero, F. Sobrino, and J.-C. Saiz The composition of West Nile virus lipid envelope unveils a role of sphingolipid metabolism on flavivirus biogenesis J Virol 2014
68. D. Luo, T. Xu, C. Hunke, G. Grüber, S.G. Vasudevan, and J. Lescar Crystal structure of the NS3 protease-helicase from dengue virus J Virol 82 2008 173 183
69. M.P. Egloff, D. Benarroch, B. Selisko, J.L. Romette, and B. Canard An RNA cap (nucleoside-2′-O-)-methyltransferase in the flavivirus RNA polymerase NS5: crystal structure and functional characterization EMBO 21 2002 2757 2768
70. T.L. Yap, T. Xu, Y.-L. Chen, H. Malet, M.-P. Egloff, B. Canard, S.G. Vasudevan, and J. Lescar Crystal structure of the dengue virus RNA-dependent RNA polymerase catalytic domain at 1.85-Angstrom resolution J Virol 81 2007 4753 4765
71. E.R. Winkelmann, D.G. Widman, R. Suzuki, and P.W. Mason Analyses of mutations selected by passaging a chimeric flavivirus identify mutations that alter infectivity and reveal an interaction between the structural proteins and the nonstructural glycoprotein NS1 Virology 421 2011 96 104
72. W.J. Liu, H.B. Chen, and A.A. Khromykh Molecular and functional analyses of Kunjin virus infectious cDNA clones demonstrate the essential roles for NS2A in virus assembly and for a nonconservative residue in NS3 in RNA replication J Virol 77 2003 7804 7813
73. A.A. Khromykh, P.L. Sedlak, and E.G. Westaway Cis- and trans-acting elements in flavivirus RNA replication J Virol 74 2000 3253 3263
74. W.J. Liu, P.L. Sedlak, N. Kondratieva, and A.A. Khromykh Complementation analysis of the flavivirus Kunjin NS3 and NS5 proteins defines the minimal regions essential for formation of a replication complex and shows a requirement of NS3 in cis for virus assembly J Virol 76 2002 10766 10775
75. G.P. Pijlman, N. Kondratieva, and A.A. Khromykh Translation of the flavivirus Kunjin NS3 gene in cis but not its RNA sequence or secondary structure is essential for efficient RNA packaging J Virol 80 2006 11255 11264
76. C.T. Jones, C.G. Patkar, and R.J. Kuhn Construction and applications of yellow fever virus replicons Virology 331 2005 247 259
77. C.G. Patkar, and R.J. Kuhn Yellow fever virus NS3 plays an essential role in virus assembly independent of its known enzymatic functions J Virol 82 2008 3342 3352
78. L.N. Carpp, R. Galler, and M.C. Bonaldo Interaction between the yellow fever virus nonstructural protein NS3 and the host protein Alix contributes to the release of infectious particles Microbes Infect 13 2011 85 95
79. Z. Xu, R. Anderson, and T.C. Hobman The capsid-binding nucleolar helicase DDX56 is important for infectivity of West Nile Virus J Virol 85 2011 5571 5580
80. Z. Xu, and T.C. Hobman The helicase activity of DDX56 is required for its role in assembly of infectious West Nile virus particles Virology 433 2012 226 235
81. C.A. Balinsky, H. Schmeisser, S. Ganesan, K. Singh, T.C. Pierson, and K.C. Zoon Nucleolin interacts with the dengue virus capsid protein and plays a role in formation of infectious virus particles J Virol 87 2013 13094 13106
82. M.K. Poh, G. Shui, X. Xie, P.-Y. Shi, M.R. Wenk, and F. Gu U18666A, an intra-cellular cholesterol transport inhibitor, inhibits dengue virus entry and replication Antiviral Res 93 2012 191 198
83. A.C. Carro, and E.B. Damonte Requirement of cholesterol in the viral envelope for dengue virus infection Virus Res 174 2013 78 87
84. A. Anwar, T. Hosoya, K.M. Leong, H. Onogi, Y. Okuno, T. Hiramatsu, H. Koyama, M. Suzuki, M. Hagiwara, and M.A. Garcia-Blanco The kinase inhibitor SFV785 dislocates dengue virus envelope protein from the replication complex and blocks virus assembly PLoS ONE 6 2011 e62324
85. R. Mateo, C.M. Nagamine, J. Spagnolo, E. Méndez, M. Rahe, M. Gale, J. Yuan, and K. Kirkegaard Inhibition of cellular autophagy deranges dengue virion maturation J Virol 87 2013 1312 1321