Identification of essential filovirion-associated host factors by serial proteomic analysis and RNAi screen

Molecular and Cellular Proteomics

Volumn 9, Issue 12, 2010, Pages 2690-2703

  Spurgers, Kevin B ^a   Alefantis, Tim ^b   Peyser, Brian D ^a   Ruthel, Gordon T ^a   Bergeron, Alison A ^a   Costantino, Julie A ^a   Enterlein, Sven ^c   Kota, Krishna P ^d   Dutch Boltz, R C ^d   Javad Aman, M ^c   DelVecchio, Vito G ^b   Bavari, Sina ^a  

^a UNITED STATES ARMY MEDICAL RESEARCH INSTITUTE OF INFECTIOUS DISEASES   (United States)

^b Vital Probes Inc   (United States)

^c PERKINELMER INC   (United States)

^d Integrated BioTherapeutics Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CELL PROTEIN; CHAPERONE; ENZYME; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE; RIBOSOME PROTEIN; RNA; SMALL INTERFERING RNA;

ARTICLE; CELL ADHESION; CELL COMMUNICATION; CELL MIGRATION; CYTOSKELETON; EBOLA VIRUS; FILOVIRUS INFECTION; GENE SILENCING; HUMAN IMMUNODEFICIENCY VIRUS 1; INFLUENZA VIRUS A; LIQUID CHROMATOGRAPHY; MARBURG VIRUS; MEMBRANE STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TANDEM MASS SPECTROMETRY; VIRION; VIRUS PARTICLE;

AMINO ACID SEQUENCE; CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FILOVIRIDAE; GENE KNOCKDOWN TECHNIQUES; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; PROTEOMICS; RNA INTERFERENCE; TANDEM MASS SPECTROMETRY; VIRAL PROTEINS; VIRION;

EBOLA VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MARBURGVIRUS;

EID: 78650139129     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M110.003418     Document Type: Article

References (76)

1. Chertova, E., Chertov, O., Coren, L. V., Roser, J. D., Trubey, C. M., Bess, J. W., Jr., Sowder, R. C., 2nd, Barsov, E., Hood, B. L., Fisher, R. J., Nagashima, K., Conrads, T. P., Veenstra, T. D., Lifson, J. D., and Ott, D. E. (2006) Proteomic and biochemical analysis of purified human immunodeficiency virus type 1 produced from infected monocyte-derived macrophages. J. Virol. 80, 9039-9052
2. Loret, S., Guay, G., and Lippé, R. (2008) Comprehensive characterization of extracellular herpes simplex virus type 1 virions. J. Virol. 82, 8605-8618
3. Shaw, M. L., Stone, K. L., Colangelo, C. M., Gulcicek, E. E., and Palese, P. (2008) Cellular proteins in influenza virus particles. PLoS Pathog 4, e1000085
4. Maxwell, K. L., and Frappier, L. (2007) Viral proteomics. Microbiol .Mol. Biol. Rev. 71, 398-411
5. Lawn, S. D., Roberts, B. D., Griffin, G. E., Folks, T. M., and Butera, S. T. (2000) Cellular compartments of human immunodeficiency virus type 1 replication in vivo: determination by presence of virion-associated host proteins and impact of opportunistic infection. J. Virol. 74, 139-145
6. Kuhn J. H., Filoviruses. A compendium of 40 years of epidemiological, clinical, and laboratory studies. 1st ed, C. H. Calisher (ed.) 2008, Springer-Wien, New York, 413
7. Warren, T. K., Warfield, K. L., Wells, J., Swenson, D. L., Donner, K. S., Van Tongeren, S. A., Garza, N. L., Dong, L., Mourich, D. V., Crumley, S., Nichols, D. K., Iversen, P. L., and Bavari, S. (2010) Advanced antisense therapies for postexposure protection against lethal filovirus infections. Nat. Med. 16, 991-994. Epub ahead of print
8. Burnett, J. C., Henchal, E. A., Schmaljohn, A. L., and Bavari, S. (2005) The evolving field of biodefence: therapeutic developments and diagnostics. Nat. Rev. Drug Discov. 4, 281-297
9. Bray, M. (2003) Defense against filoviruses used as biological weapons. Antiviral Res. 57, 53-60
10. Geisbert, T. W., and Jahrling, P. B. (1995) Differentiation of filoviruses by electron microscopy. Virus Res. 39, 129-150
11. Hoenen, T., Groseth, A., Falzarano, D., and Feldmann, H. (2006) Ebola virus: unravelling pathogenesis to combat a deadly disease. Trends Mol. Med. 12, 206-215 (Pubitemid 43728410)
12. Volchkov, V. E., Feldmann, H., Volchkova, V. A., and Klenk, H. D. (1998) Processing of the Ebola virus glycoprotein by the proprotein convertase furin. Proc. Natl. Acad. Sci. U.S.A. 95, 5762-5767
13. Volchkova, V. A., Feldmann, H., Klenk, H. D., and Volchkov, V. E. (1998) The nonstructural small glycoprotein sGP of Ebola virus is secreted as an antiparallel-orientated homodimer. Virology 250, 408-414
14. Hartlieb, B., and Weissenhor,n W. (2006) Filovirus assembly and budding. Virology 344, 64-70
15. Noda, T., Halfmann, P., Sagara, H., and Kawaoka, Y. (2007) Regions in Ebola virus VP24 that are important for nucleocapsid formation. J. Infect. Dis. 196 Suppl 2, S247-250
16. Hoenen, T., Groseth, A., Kolesnikova, L., Theriault, S., Ebihara, H., Hartlieb, B., Bamberg, S., Feldmann, H., Ströher, U., and Becker, S. (2006) Infection of naive target cells with virus-like particles: implications for the function of ebola virus VP24. J. Virol. 80, 7260-7264 (Pubitemid 44025222)
17. Huang, Y., Xu, L., Sun, Y., and Nabel, G. J. (2002) The assembly of Ebola virus nucleocapsid requires virion-associated proteins 35 and 24 and posttranslational modification of nucleoprotein. Mol. Cell. 10, 307-316 (Pubitemid 35007345)
18. Feldmann, H., Klenk, H. D., and Sanchez, A. (1993) Molecular biology and evolution of filoviruses. Arch. Virol. Suppl. 7, 81-100
19. Harty, R. N. (2009) No exit: targeting the budding process to inhibit filovirus replication. Antiviral Res. 81, 189-197
20. Becker, S., and Mühlberger, E. (1999) Co- and posttranslational modifications and functions of Marburg virus proteins. Curr. Top Microbiol. Immunol. 235, 23-34 (Pubitemid 28500193)
21. Sanchez, A. (2007) Analysis of filovirus entry into vero e6 cells, using inhibitors of endocytosis, endosomal acidification, structural integrity, and cathepsin (B and L) activity. J. Infect. Dis. 196, S251-258
22. Martínez, M. J., Biedenkopf, N., Volchkova, V., Hartlieb, B., Alazard-Dany, N., Reynard, O., Becker, S., and Volchkov, V. (2008) Role of Ebola virus VP30 in transcription reinitiation. J. Virol. 82, 12569-12573
23. Weik, M., Enterlein, S., Schlenz, K., and Mühlberger, E. (2005) The Ebola virus genomic replication promoter is bipartite and follows the rule of six. J. Virol. 79, 10660-10671 (Pubitemid 41098605)
24. Aman, M. J., Bosio, C. M., Panchal, R. G., Burnett, J. C., Schmaljohn, A., and Bavari, S. (2003) Molecular mechanisms of filovirus cellular trafficking. Microbes Infect. 5, 639-649 (Pubitemid 36645124)
25. Dolnik, O., Kolesnikova, L., and Becker, S. (2008) Filoviruses: Interactions with the host cell. Cell Mol. Life Sci. 65, 756-776
26. Prins, K. C., Cárdenas, W. B., and Basler, C. F. (2009) Ebola virus protein VP35 impairs the function of interferon regulatory factor-activating kinases IKKepsilon and TBK-1. J. Virol. 83, 3069-3077
27. Kolesnikova, L., Bugany, H., Klenk, H. D., and Becker, S. (2002) VP40, the matrix protein of Marburg virus, is associated with membranes of the late endosomal compartment. J. Virol. 76, 1825-1838 (Pubitemid 34094630)
28. Kolesnikova, L., Bohil, A. B., Cheney, R. E., and Becker, S. (2007) Budding of Marburgvirus is associated with filopodia. Cell Microbiol. 9, 939-951
29. Thomas, P. D., Campbell, M. J., Kejariwal, A., Mi, H., Karlak, B., Daverman, R., Diemer, K., Muruganujan, A., and Narechania, A. (2003) PANTHER: a library of protein families and subfamilies indexed by function. Genome Res. 13, 2129-2141 (Pubitemid 37161770)
30. Thomas, P. D., Kejariwal, A., Guo, N., Mi, H., Campbell, M. J., Muruganujan, A., and Lazareva-Ulitsky, B. (2006) Applications for protein sequence-function evolution data: mRNA/protein expression analysis and coding SNP scoring tools. Nucleic Acids Res. 34, W645-650
31. Théry, C., Ostrowski, M., and Segura, E. (2009) Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9, 581-593
32. Théry, C., Zitvogel, L., and Amigorena, S. (2002) Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2, 569-579
33. Bavari, S., Bosio, C. M., Wiegand, E., Ruthel, G., Will, A. B., Geisbert, T. W., Hevey, M., Schmaljohn, C., Schmaljohn, A., and Aman, M. J. (2002) Lipid raft microdomains: a gateway for compartmentalized trafficking of Ebola and Marburg viruses. J. Exp. Med. 195, 593-602 (Pubitemid 34461504)
34. Panchal, R. G., Ruthel, G., Kenny, T. A., Kallstrom, G. H., Lane, D., Badie, S. S., Li, L., Bavari, S., and Aman, M. J. (2003) In vivo oligomerization and raft localization of Ebola virus protein VP40 during vesicular budding. Proc. Natl. Acad. Sci. U.S.A. 100, 15936-15941 (Pubitemid 38021093)
35. Jasenosky, L. D., Neumann, G., Lukashevich, I., and Kawaoka, Y. (2001) Ebola virus VP40-induced particle formation and association with the lipid bilayer. J. Virol. 75, 5205-5214 (Pubitemid 32448543)
36. Harty, R. N., Brown, M. E., Wang, G., Huibregtse, J., and Hayes, F. P. (2000) A PPxY motif within the VP40 protein of Ebola virus interacts physically and functionally with a ubiquitin ligase: implications for filovirus budding. Proc. Natl. Acad. Sci. U.S.A. 97, 13871-13876
37. Licata, J. M., Simpson-Holley, M., Wright, N. T., Han, Z., Paragas, J., and Harty, R. N. (2003) Overlapping motifs (PTAP and PPEY) within the Ebola virus VP40 protein function independently as late budding domains: involvement of host proteins TSG101 and VPS-4. J. Virol. 77, 1812-1819
38. Yasuda, J., Nakao, M., Kawaoka, Y., and Shida, H. (2003) Nedd4 regulates egress of Ebola virus-like particles from host cells. J. Virol. 77, 9987-9992 (Pubitemid 37122080)
39. Han, Z., and Harty, R. N. (2005) Packaging of actin into Ebola virus VLPs. Virol J. 2, 92
40. Kolesnikova, L., Strecker, T., Morita, E., Zielecki, F., Mittler, E., Crump, C., and Becker, S. (2009) Vacuolar protein sorting pathway contributes to the release of Marburg virus. J. Virol. 83, 2327-2337
41. Martin-Serrano, J., Eastman, S. W., Chung, W., and Bieniasz, P. D. (2005) HECT ubiquitin ligases link viral and cellular PPXY motifs to the vacuolar protein-sorting pathway. J. Cell Biol. 168, 89-101
42. Silvestri, L. S., Ruthel, G., Kallstrom, G., Warfield, K. L., Swenson, D. L., Nelle, T., Iversen, P. L., Bavari, S., and Aman, M. J. (2007) Involvement of vacuolar protein sorting pathway in Ebola virus release independent of TSG101 interaction. J. Infect. Dis. 196, S264-270
43. Urata, S., Noda, T., Kawaoka, Y., Morikawa, S., Yokosawa, H., and Yasuda, J. (2007) Interaction of Tsg101 with Marburg virus VP40 depends on the PPPY motif, but not the PT/SAP motif as in the case of Ebola virus, and Tsg101 plays a critical role in the budding of Marburg virus-like particles induced by VP40, NP, and GP. J. Virol. 81, 4895-4899
44. Yamayoshi, S., Noda, T., Ebihara, H., Goto, H., Morikawa, Y., Lukashevich, I. S., Neumann, G., Feldmann, H., and Kawaoka, Y. (2008) Ebola virus matrix protein VP40 uses the COPII transport system for its intracellular transport. Cell Host Microbe. 3, 168-177
45. Ruthel, G., Demmin, G. L., Kallstrom, G., Javid, M. P., Badie, S. S., Will, A. B., Nelle, T., Schokman, R., Nguyen, T. L., Carra, J. H., Bavari, S., and Aman, M. J. (2005) Association of ebola virus matrix protein VP40 with microtubules. J. Virol. 79, 4709-4719
46. Martin-Serrano, J., Zang, T., and Bieniasz, P. D. (2001) HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nat. Med. 7, 1313-1319
47. Basler C. F., Mikulasova A., Martinez-Sobrido L., Paragas J., Mühlberger E., Bray M., Klenk H. D., Palese P., and Garcia-Sastre A. (2003) The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3. J. Virol. 77, 7945-7956
48. Feng, Z., Cerveny, M., Yan, Z., and He, B. (2007) The VP35 protein of Ebola virus inhibits the antiviral effect mediated by double-stranded RNA-dependent protein kinase PKR. J. Virol. 81, 182-192 (Pubitemid 44975159)
49. Reid, S. P., Leung, L. W., Hartman, A. L., Martinez, O., Shaw, M. L., Carbonnelle, C., Volchkov, V. E., Nichol, S. T., and Basler, C. F. (2006) Ebola virus VP24 binds karyopherin alpha1 and blocks STAT1 nuclear accumulation. J. Virol. 80, 5156-5167
50. Reid, S. P., Valmas, C., Martinez, O., Sanchez, F. M., and Basler, C. F. (2007) Ebola virus VP24 proteins inhibit the interaction of NPI-1 subfamily karyopherin alpha proteins with activated STAT1. J. Virol. 81, 13469-13477
51. Kaletsky, R. L., Francica, J. R., Agrawal-Gamse, C., and Bates, P. (2009) Tetherin-mediated restriction of filovirus budding is antagonized by the Ebola glycoprotein. Proc. Natl. Acad. Sci. U.S.A. 106, 2886-2891
52. Lindström, M. S. (2009) Emerging functions of ribosomal proteins in gene-specific transcription and translation. Biochem. Biophys. Res. Commun. 379, 167-170
53. Kovacs, D., Rakacs, M., Agoston, B., Lenkey, K., Semrad, K., Schroeder, R., and Tompa, P. (2009) Janus chaperones: assistance of both RNA-and protein-folding by ribosomal proteins. FEBS Lett. 583, 88-92
54. Wool, I. G. (1996) Extraribosomal functions of ribosomal proteins. Trends Biochem. Sci. 21, 164-165
55. Peltz, S. W., Hammell, A. B., Cui, Y., Yasenchak, J., Puljanowski, L., and Dinman, J. D. (1999) Ribosomal protein L3 mutants alter translational fidelity and promote rapid loss of the yeast killer virus. Mol. Cell. Biol. 19, 384-391
56. Schatz, O., Oft, M., Dascher, C., Schebesta, M., Rosorius, O., Jaksche, H., Dobrovnik, M., Bevec, D., and Hauber, J. (1998) Interaction of the HIV-1 rev cofactor eukaryotic initiation factor 5A with ribosomal protein L5. Proc. Natl. Acad. Sci. U.S.A. 95, 1607-1612 (Pubitemid 28103440)
57. Montgomery, S. A., Berglund, P., Beard, C. W., and Johnston, R. E. (2006) Ribosomal protein S6 associates with alphavirus nonstructural protein 2 and mediates expression from alphavirus messages. J. Virol. 80, 7729-7739
58. Leh, V., Yot, P., and Keller, M. (2000) The cauliflower mosaic virus translational transactivator interacts with the 60S ribosomal subunit protein L18 of Arabidopsis thaliana. Virology. 266, 1-7 (Pubitemid 30048630)
59. Mayer, M. P. (2005) Recruitment of Hsp70 chaperones: a crucial part of viral survival strategies. Rev. Physiol. Biochem. Pharmacol. 153, 1-46
60. Kolegraff, K., Bostik, P., and Ansari, A. A. (2006) Characterization and role of lentivirus-associated host proteins. Exp. Biol. Med. (Maywood) 231(3), 252-263
61. Johannsen, E., Luftig, M., Chase, M. R., Weicksel, S., Cahir-McFarland, E., Illanes, D., Sarracino, D., and Kieff, E. (2004) Proteins of purified Epstein- Barr virus. Proc. Natl. Acad. Sci. U.S.A. 101, 16286-16291 (Pubitemid 39552837)
62. Varnum, S. M., Streblow, D. N., Monroe, M. E., Smith, P., Auberry, K. J., Pasa-Tolic, L., Wang, D., Camp, D. G., 2nd, Rodland, K., Wiley, S., Britt, W., Shenk, T., Smith, R. D., and Nelson, J. A. (2004) Identification of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. J. Virol. 78, 10960-10966
63. Resch, W., Hixson, K. K., Moore, R. J., Lipton, M. S., and Moss, B. (2007) Protein composition of the vaccinia virus mature virion. Virology 358, 233-247 (Pubitemid 46048878)
64. Awe, K., Lambert, C., and Prange, R. (2008) Mammalian BiP controls posttranslational ER translocation of the hepatitis B virus large envelope protein. FEBS Lett. 582, 3179-3184
65. Tomita, Y., Yamashita, T., Sato, H., and Taira, H. (1999) Kinetics of interactions of sendai virus envelope glycoproteins, F and HN, with endoplasmic reticulum-resident molecular chaperones, BiP, calnexin, and calreticulin. J. Biochem. 126, 1090-1100 (Pubitemid 30014456)
66. Earl, P. L., Moss, B., and Doms, R. W. (1991) Folding, interaction with GRP78-BiP, assembly, and transport of the human immunodeficiency virus type 1 envelope protein. J. Virol. 65, 2047-2055
67. Mulvey, M., and Brown, D. T. (1995) Involvement of the molecular chaperone BiP in maturation of Sindbis virus envelope glycoproteins. J. Virol. 69, 1621-1627
68. Jindadamrongwech, S., Thepparit, C., and Smith, D. R. (2004) Identification of GRP 78 (BiP) as a liver cell expressed receptor element for dengue virus serotype 2. Arch Virol. 149, 915-927
69. Cabrera-Hernandez, A., Thepparit, C., Suksanpaisan, L., and Smith, D. R. (2007) Dengue virus entry into liver (HepG2) cells is independent of hsp90 and hsp70. J. Med. Virol. 79, 386-392
70. Triantafilou, K., Fradelizi, D., Wilson, K., and Triantafilou, M. (2002) GRP78, a coreceptor for coxsackievirus A9, interacts with major histocompatibility complex class I molecules which mediate virus internalization. J. Virol. 76, 633-643 (Pubitemid 34033362)
71. Upanan, S., Kuadkitkan, A., and Smith, D. R. (2008) Identification of dengue virus binding proteins using affinity chromatography. J. Virol. Methods. 151, 325-328
72. Connor, J. H., McKenzie, M. O., Parks, G. D., and Lyles, D. S. (2007) Antiviral activity and RNA polymerase degradation following Hsp90 inhibition in a range of negative strand viruses. Virology 362, 109-119
73. Buchkovich, N. J., Maguire, T. G., Yu, Y., Paton, A. W., Paton, J. C., and Alwine, J. C. (2008) Human cytomegalovirus specifically controls the levels of the endoplasmic reticulum chaperone BiP/GRP78, which is required for virion assembly. J. Virol. 82, 31-39
74. Limjindaporn, T., Wongwiwat, W., Noisakran, S., Srisawat, C., Netsawang, J., Puttikhunt, C., Kasinrerk, W., Avirutnan, P., Thiemmeca, S., Sriburi, R., Sittisombut, N., Malasit, P., and Yenchitsomanus, P. T. (2009) Interaction of dengue virus envelope protein with endoplasmic reticulum-resident chaperones facilitates dengue virus production. Biochem. Biophys. Res. Commun. 379, 196-200
75. Huang, K. L., Lai, Y. K., Lin, C. C., and Chang, J. M. (2009) Involvement of GRP78 in inhibition of HBV secretion by Boehmeria nivea extract in human HepG2 2.2.15 cells. J. Viral Hepat. 16, 367-375
76. Ma, Y., Yu J., Chan, H. L., Chen, Y. C., Wang, H., Chen, Y., Chan, C. Y., Go, M. Y., Tsai, S. N., Ngai, S. M., To, K. F., Tong, J. H., He, Q. Y., Sung, J. J., Kung, H. F., Cheng, C. H., and He, M. L. (2009) Glucose-regulated protein 78 is an intracellular antiviral factor against hepatitis B virus. Mol. Cell. Proteomics 8, 2582-2594