Class II ADP-ribosylation factors are required for efficient secretion of dengue viruses

Journal of Biological Chemistry

Volumn 287, Issue 1, 2012, Pages 767-777

  Kudelko, Mateusz ^a   Brault, Jean Baptiste ^b   Kwok, Kevin ^a   Li, Ming Yuan ^a   Pardigon, Nathalie ^b   Peiris, J S Malik ^a   Bruzzone, Roberto ^a,b   Despre, Philippe ^b   Nal, Béatrice ^a,c,d   Wang, Pei Gang ^a,d  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b INSTITUT PASTEUR   (France)

^c BRUNEL UNIVERSITY   (United Kingdom)

^d Dexter H C Man Bldg ^*  (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

ADP-RIBOSYLATION FACTORS; CELLULAR FACTORS; CLASS II; CO-IMMUNOPRECIPITATIONS; DENGUE VIRUS; DISEASE PROGRESSION; FEVER VIRUS; HORSE-RADISH PEROXIDASE; HUMAN PATHOGENS; IMMUNOSTAINING; LATE STAGE; MOLECULAR MECHANISM; NOVEL FUNCTIONS; SECRETORY PATHWAYS; SEROTYPES; SIGNAL PEPTIDE; WEST NILE VIRUS;

LIFE CYCLE; PHYSIOLOGY; PROTEINS;

VIRUSES;

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 4; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 5; SMALL INTERFERING RNA;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ARTICLE; CONTROLLED STUDY; DENGUE VIRUS; GENE TARGETING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LIFE CYCLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SEROTYPE; VIRUS RELEASE; VIRUS REPLICATION; WEST NILE FLAVIVIRUS; YELLOW FEVER FLAVIVIRUS;

ADP-RIBOSYLATION FACTORS; AMINO ACID SEQUENCE; BASE SEQUENCE; CELL LINE; DENGUE VIRUS; DNA, RECOMBINANT; GENE SILENCING; HOST-PATHOGEN INTERACTIONS; HUMANS; MOLECULAR SEQUENCE DATA; RNA, SMALL INTERFERING; SPECIES SPECIFICITY; VIRAL PROTEINS; VIRION;

ARMORACIA RUSTICANA; DENGUE VIRUS; DENGUE VIRUS GROUP; WEST NILE VIRUS; YELLOW FEVER VIRUS GROUP;

EID: 84855290006     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.270579     Document Type: Article

References (49)

1. Gubler, D. J. (2002) Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends Microbiol. 10, 100-103
2. Halstead, S. B. (1988) Pathogenesis of dengue: challenges to molecular biology. Science 239, 476-481
3. Halstead, S. B. (2007) Dengue. Lancet 370, 1644-1652
4. Lindenbach, B. D., and Rice, C. M. (2001) in Fields Virology (Knipe, D. M., and Howley, P. M., eds) 4th Ed., pp. 991-1041, Lippincott Williams & Wilkins, Philadelphia
5. Stadler, K., Allison, S. L., Schalich, J., and Heinz, F. X. (1997) Proteolytic activation of tick-borne encephalitis virus by furin. J. Virol. 71, 8475-8481 (Pubitemid 27446428)
6. Li, L., Lok, S. M., Yu, I. M., Zhang, Y., Kuhn, R. J., Chen, J., and Rossmann, M. G. (2008) The flavivirus precursor membrane-envelope protein complex: structure and maturation. Science 319, 1830-1834 (Pubitemid 351451591)
7. Yu, I. M., Zhang, W., Holdaway, H. A., Li, L., Kostyuchenko, V. A., Chipman, P. R., Kuhn, R. J., Rossmann, M. G., and Chen, J. (2008) Structure of the immature dengue virus at low pH primes proteolytic maturation. Science 319, 1834-1837 (Pubitemid 351451592)
8. Mukhopadhyay, S., Kuhn, R. J., and Rossmann, M. G. (2005) A structural perspective of the flavivirus life cycle. Nat. Rev. Microbiol. 3, 13-22 (Pubitemid 40028466)
9. Allison, S. L., Stadler, K., Mandl, C. W., Kunz, C., and Heinz, F. X. (1995) Synthesis and secretion of recombinant tick-borne encephalitis virus protein E in soluble and particulate form. J. Virol. 69, 5816-5820
10. Ferlenghi, I., Clarke, M., Ruttan, T., Allison, S. L., Schalich, J., Heinz, F. X., Harrison, S. C., Rey, F. A., and Fuller, S. D. (2001) Molecular organization of a recombinant subviral particle from tick-borne encephalitis virus. Mol. Cell 7, 593-602 (Pubitemid 32706351)
11. Hunt, A. R., Cropp, C. B., and Chang, G. J. (2001) A recombinant particulate antigen of Japanese encephalitis virus produced in stably transformed cells is an effective noninfectious antigen and subunit immunogen. J. Virol. Methods 97, 133-149 (Pubitemid 32718748)
12. Wang, P. G., Kudelko, M., Lo, J., Siu, L. Y., Kwok, K. T., Sachse, M., Nicholls, J. M., Bruzzone, R., Altmeyer, R. M., and Nal, B. (2009) Efficient assembly and secretion of recombinant subviral particles of the four dengue serotypes using native prM and E proteins. PLoS One 4, e8325
13. Chu, J. J., and Yang, P. L. (2007) c-Src protein kinase inhibitors block assembly and maturation of dengue virus. Proc. Natl. Acad. Sci. U.S.A. 104, 3520-3525 (Pubitemid 46364191)
14. Hirsch, A. J., Medigeshi, G. R., Meyers, H. L., DeFilippis, V., Früh, K., Briese, T., Lipkin, W. I., and Nelson, J. A. (2005) The Src family kinase c-Yes is required for maturation of West Nile virus particles. J. Virol. 79, 11943-11951 (Pubitemid 41279311)
15. Gillingham, A. K., and Munro, S. (2007) The small G proteins of the Arf family and their regulators. Annu. Rev. Cell Dev. Biol. 23, 579-611
16. Donaldson, J. G., Cassel, D., Kahn, R. A., and Klausner, R. D. (1992) ADP-ribosylation factor, a small GTP-binding protein, is required for binding of the coatomer protein β-COP to Golgi membranes. Proc. Natl. Acad. Sci. U.S.A. 89, 6408-6412
17. Stamnes, M. A., and Rothman, J. E. (1993) The binding of AP-1 clathrin adaptor particles to Golgi membranes requires ADP-ribosylation factor, a small GTP-binding protein. Cell 73, 999-1005 (Pubitemid 23165614)
18. Beck, R., Sun, Z., Adolf, F., Rutz, C., Bassler, J., Wild, K., Sinning, I., Hurt, E., Brügger, B., Béthune, J., and Wieland, F. (2008) Membrane curvature induced by Arf1-GTP is essential for vesicle formation. Proc. Natl. Acad. Sci. U.S.A. 105, 11731-11736
19. Brown, H. A., Gutowski, S., Moomaw, C. R., Slaughter, C., and Sternweis, P. C. (1993) ADP-ribosylation factor, a small GTP-dependent regulatory protein, stimulates phospholipase D activity. Cell 75, 1137-1144 (Pubitemid 24006110)
20. Cockcroft, S., Thomas, G. M., Fensome, A., Geny, B., Cunningham, E., Gout, I., Hiles, I., Totty, N. F., Truong, O., and Hsuan, J. J. (1994) Phospholipase D: a downstream effector of ARF in granulocytes. Science 263, 523-526
21. Kahn, R. A., Cherfils, J., Elias, M., Lovering, R. C., Munro, S., and Schurmann, A. (2006) Nomenclature for the human Arf family of GTP-binding proteins: ARF, ARL, and SAR proteins. J. Cell Biol. 172, 645-650
22. Bonifacino, J. S., and Glick, B. S. (2004) The mechanisms of vesicle budding and fusion. Cell 116, 153-166 (Pubitemid 38167309)
23. Donaldson, J. G. (2003) Multiple roles for Arf6: sorting, structuring, and signaling at the plasma membrane. J. Biol. Chem. 278, 41573-41576
24. Deretic, D., Williams, A. H., Ransom, N., Morel, V., Hargrave, P. A., and Arendt, A. (2005) Rhodopsin C terminus, the site of mutations causing retinal disease, regulates trafficking by binding to ADP-ribosylation factor 4 (ARF4). Proc. Natl. Acad. Sci. U.S.A. 102, 3301-3306 (Pubitemid 40328040)
25. Mazelova, J., Astuto-Gribble, L., Inoue, H., Tam, B. M., Schonteich, E., Prekeris, R., Moritz, O. L., Randazzo, P. A., and Deretic, D. (2009) Ciliary targeting motif VxPx directs assembly of a trafficking module through Arf4. EMBO J. 28, 183-192
26. Junjhon, J., Lausumpao, M., Supasa, S., Noisakran, S., Songjaeng, A., Saraithong, P., Chaichoun, K., Utaipat, U., Keelapang, P., Kanjanahaluethai, A., Puttikhunt, C., Kasinrerk, W., Malasit, P., and Sittisombut, N. (2008) Differential modulation of prM cleavage, extracellular particle distribution, and virus infectivity by conserved residues at nonfurin consensus positions of the dengue virus pr-M junction. J. Virol. 82, 10776-10791 (Pubitemid 352691150)
27. Desprès, P., Frenkiel, M. P., and Deubel, V. (1993) Differences between cell membrane fusion activities of two dengue type-1 isolates reflect modifications of viral structure. Virology 196, 209-219
28. Henchal, E. A., Gentry, M. K., McCown, J. M., and Brandt, W. E. (1982) Dengue virus-specific and flavivirus group determinants identified with monoclonal antibodies by indirect immunofluorescence. Am. J. Trop. Med. Hyg. 31, 830-836 (Pubitemid 12041595)
29. Volpicelli-Daley, L. A., Li, Y., Zhang, C. J., and Kahn, R. A. (2005) Isoform-selective effects of the depletion of ADP-ribosylation factors 1-5 on membrane traffic. Mol. Biol. Cell 16, 4495-4508 (Pubitemid 41416436)
30. Siu, Y. L., Teoh, K. T., Lo, J., Chan, C. M., Kien, F., Escriou, N., Tsao, S. W., Nicholls, J. M., Altmeyer, R., Peiris, J. S., Bruzzone, R., and Nal, B. (2008) The M, E, and N structural proteins of the severe acute respiratory syndrome coronavirus are required for efficient assembly, trafficking, and release of virus-like particles. J. Virol. 82, 11318-11330
31. Saraste, J., Palade, G. E., and Farquhar, M. G. (1986) Temperature-sensitive steps in the transport of secretory proteins through the Golgi complex in exocrine pancreatic cells. Proc. Natl. Acad. Sci. U.S.A. 83, 6425-6429 (Pubitemid 17174747)
32. Saraste, J., and Kuismanen, E. (1984) Pre- and post-Golgi vacuoles operate in the transport of Semliki Forest virus membrane glycoproteins to the cell surface. Cell 38, 535-549 (Pubitemid 14022046)
33. Misumi, Y., Misumi, Y., Miki, K., Takatsuki, A., Tamura, G., and Ikehara, Y. (1986) Novel blockade by brefeldin A of intracellular transport of secretory proteins in cultured rat hepatocytes. J. Biol. Chem. 261, 11398-11403 (Pubitemid 17216751)
34. Bard, F., Casano, L., Mallabiabarrena, A., Wallace, E., Saito, K., Kitayama, H., Guizzunti, G., Hu, Y., Wendler, F., Dasgupta, R., Perrimon, N., and Malhotra, V. (2006) Functional genomics reveals genes involved in protein secretion and Golgi organization. Nature 439, 604-607 (Pubitemid 43185385)
35. Pepperkok, R., Scheel, J., Horstmann, H., Hauri, H. P., Griffiths, G., and Kreis, T. E. (1993) β-COP is essential for biosynthetic membrane transport from the endoplasmic reticulum to the Golgi complex in vivo. Cell 74, 71-82 (Pubitemid 23219879)
36. Peter, F., Plutner, H., Zhu, H., Kreis, T. E., and Balch, W. E. (1993) β-COP is essential for transport of protein from the endoplasmic reticulum to the Golgi in vitro. J. Cell Biol. 122, 1155-1167 (Pubitemid 23277286)
37. Courageot, M. P., Frenkiel, M. P., Dos Santos, C. D., Deubel, V., and Desprès, P. (2000) α-Glucosidase inhibitors reduce dengue virus production by affecting the initial steps of virion morphogenesis in the endoplasmic reticulum. J. Virol. 74, 564-572 (Pubitemid 30002943)
38. Zhang, Y., Corver, J., Chipman, P. R., Zhang, W., Pletnev, S. V., Sedlak, D., Baker, T. S., Strauss, J. H., Kuhn, R. J., and Rossmann, M. G. (2003) Structures of immature flavivirus particles. EMBO J. 22, 2604-2613 (Pubitemid 36712358)
39. Yu, I. M., Holdaway, H. A., Chipman, P. R., Kuhn, R. J., Rossmann, M. G., and Chen, J. (2009) Association of the pr peptides with dengue virus at acidic pH blocks membrane fusion. J. Virol. 83, 12101-12107
40. Welsch, S., Miller, S., Romero-Brey, I., Merz, A., Bleck, C. K., Walther, P., Fuller, S. D., Antony, C., Krijnse-Locker, J., and Bartenschlager, R. (2009) Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe 5, 365-375
41. D'Souza-Schorey, C., and Chavrier, P. (2006) ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 7, 347-358
42. Chun, J., Shapovalova, Z., Dejgaard, S. Y., Presley, J. F., and Melançon, P. (2008) Characterization of class I and II ADP-ribosylation factors (Arfs) in live cells: GDP-bound class II Arfs associate with the ER-Golgi intermediate compartment independently of GBF1. Mol. Biol. Cell 19, 3488-3500
43. Duijsings, D., Lanke, K. H., van Dooren, S. H., van Dommelen, M. M., Wetzels, R., de Mattia, F., Wessels, E., and van Kuppeveld, F. J. (2009) Differential membrane association properties and regulation of class I and class II Arfs. Traffic 10, 316-323
44. Kahn, R. A., Volpicelli-Daley, L., Bowzard, B., Shrivastava-Ranjan, P., Li, Y., Zhou, C., and Cunningham, L. (2005) Arf family GTPases: roles in membrane traffic and microtubule dynamics. Biochem. Soc. Trans. 33, 1269-1272 (Pubitemid 41779664)
45. Nie, Z., Hirsch, D. S., and Randazzo, P. A. (2003) Arf and its many interactors. Curr. Opin. Cell Biol. 15, 396-404 (Pubitemid 36928041)
46. Donaldson, J. G., and Jackson, C. L. (2000) Regulators and effectors of the ARF GTPases. Curr. Opin. Cell Biol. 12, 475-482 (Pubitemid 30453599)
47. Pastorino, B., Nougairède, A., Wurtz, N., Gould, E., and de Lamballerie, X. (2010) Role of host cell factors in flavivirus infection: Implications for pathogenesis and development of antiviral drugs. Antiviral Res. 87, 281-294
48. Krishnan, M. N., Ng, A., Sukumaran, B., Gilfoy, F. D., Uchil, P. D., Sultana, H., Brass, A. L., Adametz, R., Tsui, M., Qian, F., Montgomery, R. R., Lev, S., Mason, P. W., Koski, R. A., Elledge, S. J., Xavier, R. J., Agaisse, H., and Fikrig, E. (2008) RNA interference screen for human genes associated with West Nile virus infection. Nature 455, 242-245
49. Kuno, G., Chang, G. J., Tsuchiya, K. R., Karabatsos, N., and Cropp, C. B. (1998) Phylogeny of the genus Flavivirus. J. Virol. 72, 73-83 (Pubitemid 28048815)