Viral and host proteins that modulate filovirus budding

Future Virology

Volumn 5, Issue 4, 2010, Pages 481-491

  Liu, Yuliang ^a   Harty, Ronald N ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

budding; Ebola; filovirus; Marburg; VLP

Indexed keywords

CYTOSKELETON PROTEIN; INTERFERON STIMULATED GENE 15; PROTEIN VP40; TRANSCRIPTION FACTOR; TUMOR SUSCEPTIBILITY GENE 101 PROTEIN; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ENDOCYTOSIS; FILOVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; REVIEW; RNA VIRUS; VIRUS CELL INTERACTION; VIRUS REPLICATION;

MAMMALIA; MARBURGVIRUS;

EID: 77954936778     PISSN: 17460794     EISSN: None     Source Type: Journal    
DOI: 10.2217/fvl.10.33     Document Type: Review

References (96)

1. Ascenzi P, Bocedi A, Heptonstall J et al.: Ebolavirus and Marburgvirus: insight the Filoviridae family. Mot. Aspects. Med. 29, 151-185 (2008).
2. Groseth A, Feldmann H, Strong JE: The ecology of Ebola virus. Trends Microbiol. 15, 408-416 (2007).
3. Martina BE, Osterhaus AD: "Filoviruses": a real pandemic threat? EMBO Mot. Med. 1, 10-18 (2009).
4. Towner JS, Sealy TK, Khristova ML et al.: Newly discovered Ebola virus associated with hemorrhagic fever outbreak in Uganda. PLoS Pathog. 4, e1000212 (2008).
5. Leroy EM, Kumulungui B, Pourrut X et al.: Fruit bats as reservoirs of Ebola virus. Nature 438, 575-576 (2005).
6. Swanepoel R, Smit SB, Rollin PE et al.: Studies of reservoir hosts for Marburg virus. Emerg. Infect. Dis. 13, 1847-1851 (2007).
7. Towner JS, Amman BR, Sealy TK et al.: Isolation of genetically diverse Marburg viruses from Egyptian fruit bats. PLoS Pathog. 5, e1000536 (2009).
8. Feldmann H, Jones S, Klenk HD, Schnittler HJ: Ebola virus: from discovery to vaccine. Nat. Rev. Immunol. 3, 677-685 (2003).
9. Diamond MS, Fremont DH: Ebola images emerge from the cave. Cell Host Microbe 4, 87-89 (2008).
10. Jasenosky LD, Neumann G, Lukashevich I, Kawaoka Y: Ebola virus VP40-induced particle formation and association with the lipid bilayer. J. Virol. 75, 5205-5214 (2001).
11. Warfield KL, Deal EM, Bavari S: Filovirus infections. J. Am. Vet. Med. Assoc. 234, 1130-1139 (2009).
12. Barrette, RW, Metwally SA, Rowland JM et al.: Discovery of swine as a host for the Reston Ebolavirus. Science 325, 204-246 (2009).
13. Sanchez A, Trappier SG, Mahy BW, Peters CJ, Nichol ST: The virion glycoproteins of Ebola viruses are encoded in two reading frames and are expressed through transcriptional editing. Proc. Natl Acad. Sci. USA 93, 3602-3607 (1996).
14. Volchkov VE, Becker S, Vochkova VA et al.: GP mRNA of Ebola virus is edited by the Ebola virus polymerase and by T7 and vaccinia virus polymerases. Virology 214, 421-430 (1995).
15. Harty RN, Brown ME, Wang G, Huibregtse J, Hayes FP: 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. USA 97, 13871-13876 (2000).
16. Timmins J, Scianimanico S, Schoehn G, Weissenhorn W: Vesicular release of Ebola virus matrix protein VP40. Virology 283, 1-6 (2001).
17. Noda T, Sagara H, Suzuki E et al.: Ebola virus VP40 drives the formation of virus-like filamentous particles along with GP. J. Virol. 76, 4855-4865 (2002).
18. Urata S, Noda T, Kawaoka Y, Morikawa S, Yokosawa H, Yasuda J: 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 (2007).
19. Martin-Serrano J, Zang T, Bieniasz PD: 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 (2001).
20. Timmins J, Schoehn G, Ricard-Blum S et al.: Ebola virus matrix protein VP40 interaction with human cellular factors Tsg101 and Nedd4. J. Mol. Biol. 326, 493-502 (2003).
21. Yasuda J, Nakao M, Kawaoka Y, Shida H: Nedd4 regulates egress of Ebola virus-like particles from host cells. J. Virol. 77, 9987-9992 (2003).
22. Kolesnikova L, Bugany H, Klenk HD, Becker S: VP40, the matrix protein of Marburg virus, is associated with membranes of the late endosomal compartment. J. Virol. 76, 1825-1838 (2002).
23. Kolesnikova L, Bamberg S, Berghofer B, Becker S: The matrix protein of Marburg virus is transported to the plasma membrane along cellular membranes: exploiting the retrograde late endosomal pathway. J. Virol. 78, 2382-2393 (2004).
24. Bavari S, Bosio CM, Wiegand E et al.: Lipid raft microdomains: a gateway for compartmentalized trafficking of Ebola and Marburg viruses. J. Exp. Med. 195, 593-602 (2002).
25. Johnson RF, McCarthy SE, Godlewski PJ, Harty RN: Ebola virus VP35-VP40 interaction is sufficient for packaging 3E-5E minigenome RNA into virus-like particles. J. Virol. 80, 5135-5144 (2006).
26. Swenson DL, Warfield KL, Kuehl K et al.: Generation of Marburg virus-like particles by coexpression of glycoprotein and matrix protein. FEMSImmunol. Med. Microbiol. 40, 27-31 (2004).
27. Wenigenrath J, Kolesnikova L, Hoenen T, Mittler E, Becker S: Establishment and application of an infectious virus-like particle system for Marburg virus. J. Gen. Virol. 91(Pt 5), 1325-1334 (2010).
28. Chen BJ, Lamb RA: Mechanisms for enveloped virus budding: can some viruses do without an ESCRT? Virology 372, 221-232 (2008).
29. Strack B, Calistri A, Craig S, Popova E, Gottlinger HG: AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 Functioning in virus budding. Cell 114, 689-699 (2003).
30. Licata JM, Simpson-Holley M, Wright NT, Han ZY, Paragas J, Harty RN: 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 (2003).
31. Urata S, Yasuda J: Regulation of Marburg virus (MARV) budding by Nedd4.1: a different WW domain of Nedd4.1 is critical for binding to MARV and Ebola virus VP40. J. Gen. Virol. 91, 228-234 (2010).
32. Hartlieb B, Weissenhorn W: Filovirus assembly and budding. Virology 344, 64-70 (2006).
33. Jasenosky LD, Kawaoka Y: Filovirus budding. Virus Res. 106, 181-188 (2004).
34. Harty RN, Pitha PM, Okumura A: Antiviral activity of innate immune protein ISG15. J. Innate. Immun. 1, 397-404 (2009).
35. Neumann G, Ebihara H, Takada A et al.: Ebola virus VP40 late domains are not essential for viral replication in cell culture. J. Virol. 79, 10300-10307 (2005).
36. Liu YL, Cocka L, Okumura A, Zhang YA, Sunyer JO, Harty RN: Conserved motifs within Ebola and Marburg virus VP40 proteins are important for stability, localization, and subsequent budding of virus-like particles. J. Virol. 84, 2294-2303 (2010).
37. Yamayoshi S, Kawaoka Y: Mapping of a region of Ebola virus VP40 that is important in the production of virus-like particles. J. Infect. Dis. 196(Suppl. 2), S291-S295 (2007).
38. McCarthy SE, Johnson RF, Zhang YA, Sunyer JO, Harty RN: Role for amino acids 212KLR214 of Ebola virus VP40 in assembly and budding. J. Virol. 81, 11452-11460 (2007).
39. Dessen A, Volchkov V, Dolnik O, Klenk HD, Weissenhorn W: Crystal structure of the matrix protein VP40 from Ebola virus. EMBO J. 19, 4228-4236 (2000).
40. Patch JR, Han ZY, McCarthy SE et al.: The YPLGVG sequence of the Nipah virus matrix protein is required for budding. Virol. J. 5, 137 (2008).
41. Ruigrok RW, Schoehn G, Dessen A et al.: Structural characterization and membrane binding properties of the matrix protein VP40 of Ebola virus. J. Mol. Biol. 300, 103-112 (2000).
42. Scianimanico S, Schoehn G, Timmins J, Ruigrok RH, Klenk HD, Weissenhorn W: Membrane association induces a conformational change in the Ebola virus matrix protein. EMBO J. 19, 6732-6741 (2000).
43. Timmins J, Schoehn G, Kohlhaas C, Klenk HD, Ruigrok RW, Weissenhorn W: Oligomerization and polymerization of the filovirus matrix protein VP40. Virology 312, 59-68 (2003).
44. Nguyen TL, Schoehn G, Weissenhorn W et al.: An all-atom model of the pore-like structure of hexameric VP40 from Ebola: structural insights into the monomer-hexamer transition. J. Struct. Biol. 151, 30-40 (2005).
45. Gomis-Ruth FX, Dessen A, Timmins J et al.: The matrix protein VP40 from Ebola virus octamerizes into pore-like structures with specific RNA binding properties. Structure 11, 423-433 (2003).
46. Hoenen T, Volchkov V, Kolesnikova L et al.: VP40 octamers are essential for Ebola virus replication. J. Virol. 79, 1898-1905 (2005).
47. Mittler E, Kolesnikova L, Strecker T, Garten W, Becker S: Role of the transmembrane domain of marburg virus surface protein GP in assembly of the viral envelope. J. Virol 81, 3942-3948 (2007).
48. Bamberg S, Kolesnikova L, Moller P, Klenk HD, Becker S: VP24 of Marburg virus influences formation of infectious particles. J. Virol. 79, 13421-13433 (2005).
49. Licata JM, Johnson RF, Han ZY, Harty RN: Contribution of Ebola virus glycoprotein, nucleoprotein, and VP24 to budding of VP40 virus-like particles. J. Virol. 78, 7344-7351 (2004).
50. Johnson RF, Bell P, Harty RN: Effect of Ebola virus proteins GP, NP and VP35 on VP40 VLP morphology. Virol. J. 233, 31 (2006).
51. Li L, Cohen SN: Tsg101: a novel tumor susceptibility gene isolated by controlled homozygous functional knockout of allelic loci in mammalian cells. Cell 85, 319-329 (1996).
52. Williams RL, Urbe S: The emerging shape of the ESCRT machinery. Nat Rev. Mol. Cell. Biol. 8, 355-368 (2007).
53. Pornillos O, Garrus JE, Sundquist WI: Mechanisms of enveloped RNA virus budding. Trends Cell. Biol. 12, 569-579 (2002).
54. VerPlank L, Bouamr F, LaGarassa TJ et al.: Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55(Gag). Proc. Natl Acad. Sci. USA 98, 7724-7729 (2001).
55. Garrus JE, Schwedler UK, Pornillos OW et al.: Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107, 55-65 (2001).
56. Carter CA: Tsg101: HIV-1's ticket to ride. Trends Microbiol. 10, 203-205 (2002).
57. Kolesnikova L, Strecker T, Morita E et al.: Vacuolar protein sorting pathway contributes to the release of Marburg virus. J. Virol. 83, 2327-2337 (2009).
58. Hu CD, Chinenov Y, Kerppola TK: Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell. 9, 789-798 (2002).
59. Magliery TJ, Wilson CGM, Pan W et al.: Detecting protein-protein interactions with a green fluorescent protein fragment reassembly trap: scope and mechanism. J. Am. Chem. Soc. 127, 146-157 (2005).
60. Kinch MS, Yunus A, Mao H et al.: FGI-104: a broad-spectrum small molecule inhibitor of viral infection. Am. J. Transl. Res. 1, 87-98 (2009).
61. Aman MJ, Kinch MS, Warfield K et al.: Development of a broad-spectrum antiviral with activity against Ebola virus. Antiviral Res. 83, 245-251 (2009).
62. Chen H, Liu X, Li Z, Zhan P, De Clercq E: TSG101: A novel anti-HIV-1 drug target. Curr. Med. Chem. 17(8), 750-758 (2010).
63. Rotin D, Kumar S: Physiological functions of the HECT family of ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 10, 398-409 (2009).
64. Irie T, Licata JM, McGettigan JP, Schnell MJ, Harty RN: Budding of PPxY-containing rhabdoviruses is not dependent on host proteins TGS101 and VPS4A. J. Virol. 78, 2657-2665 (2004).
65. Martin-Serrano J, Perez-Caballero D, Bieniasz PD: Context-dependent effects of L domains and ubiquitination on viral budding. J. Virol. 78, 5554-5563 (2004).
66. Okumura A, Pitha PM, Harty RN: ISG15 inhibits Ebola VP40 VLP budding in an L-domain-dependent manner by blocking Nedd4 ligase activity. Proc. Natl Acad. Sci. USA 105, 3974-3979 (2008).
67. Malakhova OA, Zhang DE: ISG15 inhibits Nedd4 ubiquitin E3 activity and enhances the innate antiviral response. J. Biol. Chem. 283, 8783-8787 (2008).
68. Irie T, Licata JM, Harty RN: Functional characterization of Ebola virus L-domains using VSV recombinants. Virology 336, 291-298 (2005).
69. Jadwin JA, Rudd V, Sette P, Challa S, Bouamr F: Late domain-independent rescue of a release-deficient Moloney murine leukemia virus by the ubiquitin ligase itch. J. Virol. 84, 704-715 (2010).
70. Yamayoshi S, Noda T, Ebihara H et al.: Ebola virus matrix protein VP40 uses the COPII transport system for its intracellular transport. Cell Host Microbe 3, 168-177 (2008).
71. Kolesnikova L, Bohil AB, Cheney RE, Becker S: Budding of Marburgvirus is associated with filopodia. Cell Microbiol. 9, 939-951 (2007).
72. Smith GA, Enquist LW: Break ins and break outs: viral interactions with the cytoskeleton of mammalian cells. Annu. Rev. Cell Dev. Biol. 18, 135-161 (2002).
73. Noda T: Assembly and budding of Ebolavirus. PloSPathog. 2, 864-872 (2006).
74. Ruthel G, Demmin GL, Kallstrom G et al.: Association of Ebola virus matrix protein VP40 with microtubules. J. Virol. 79, 4709-4719 (2005).
75. Wahl-Jensen VM, Afanasieva TA, Seebach J, Stroher U, Feldmann H, Schnittler HJ: Effects of Ebola virus glycoproteins on endothelial cell activation and barrier function. J. Virol. 79, 10442-10450 (2005).
76. Kolesnikova LH, Bugany H-D, Becker S: VP40, the matrix protein of Marburg virus, is associated with membranes of the late endosomal compartment. J. Virol. 76, 1825-1838 (2002).
77. Han Z, Harty RN: Packaging of actin into Ebola virus VLPs. Virol. J. 2, 92 (2005).
78. Han ZY, Harty RN: Influence of calcium/calmodulin on budding of Ebola VLPs: implications for the involvement of the Ras/Raf/MEK/ERK pathway. Virus Genes 35, 511-520 (2007).
79. Panchal RG, Ruthel G, Kenny T et al.: In vivo oligomerization and raft localization of Ebola virus protein VP40 during vesicular budding. Proc. Natl Acad. Sci. USA 100, 15936-15941 (2003).
80. Aman MJ, Bosio CM, Panchal RG et al.: Molecular mechanisms of filovirus cellular trafficking. Microbes Infect. 5, 639-649 (2003).
81. Freitas MS, Gaspar LP, Lorenzoni M, et al.: Structure of the Ebola fusion peptide in a membrane-mimetic environment and the interaction with lipid rafts. J. Biol. Chem. 282, 27306-27314 (2007).
82. Jouvenet N, Neil SJ, Zhadina M et al.: Broad-spectrum inhibition of retroviral and filoviral particle release by tetherin. J. Virol. 83, 1837-1844 (2009).
83. Sakuma T, Sakurai A, Yasuda J: Dimerization of tetherin is not essential for its antiviral activity against Lassa and Marburg viruses. PLoS One 4, e6934 (2009).
84. Kaletsky RL, Francica JR, Agrawal-Gamse C, Bates P: Tetherin-mediated restriction of filovirus budding is antagonized by the Ebola glycoprotein. Proc. Natl Acad. Sci. USA 106, 2886-2891 (2009).
85. Tokarev A, Skasko M, Fitzpatrick K, Guatelli J: Antiviral activity of the interferon- induced cellular protein BST-2/tetherin. AIDS Res. Hum. Retroviruses 25, 1197-1210 (2009).
86. Neil SJ, Zang T, Bieniasz PD: Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451, 425-430 (2008).
87. Van Damme N, Goff D, Katsura C et al.: The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 3, 245-252 (2008).
88. Sakuma T, Noda T, Urata S, Kawaoka Y, Yasuda J: Inhibition of Lassa and Marburg virus production by tetherin. J. Virol. 83, 2382-2385 (2009).
89. Korant BD, Blomstrom DC, Jonak GJ et al.: Interferon-induced proteins. Purification and characterization of a 15,000-dalton protein from human and bovine cells induced by interferon. J. Biol. Chem. 259, 14835-14839 (1984).
90. Sridharan H, Zhao C, Krug RM: Species specificity of the NS1 protein of influenza B virus: It binds only human and non-human primate ubiquitin-like ISG15 proteins. J. Biol. Chem. 285(11), 7852-7856 (2010).
91. Zhao C, Hsiang TY, Kuo RL, Krug RM: ISG15 conjugation system targets the viral NS1 protein in influenza A virus-infected cells. Proc. Natl Acad. Sci. USA 107, 2253-2258 (2010)
92. Kallstrom G, Warfield KL, Swenson DL et al.: Analysis of Ebola virus and VLP release using an immunocapture assay. J. Virol. Methods 127, 1-9 (2005).
93. Shi W, Huang Y, Sutton-Smith M et al.: A filovirus-unique region of Ebola virus nucleoprotein confers aberrant migration and mediates its incorporation into virions. J. Virol. 82, 6190-6199 (2008).
94. Han ZY, Boshra H, Sunyer JO, Zwiers SH, Paragas J, Harty RN: Biochemical and functional characterization of the Ebola virus VP24 protein: implications for a role in virus assembly and budding. J. Virol. 77, 1793 - 1800 (2003).
95. Hoenen, T, Allison G, Larissa K et al.: Infection of naive target cells with virus-like particles: implications for the function of Ebola virus VP24. J. Virol. 80, 7260-7264 (2006).
96. Silvestri LS, Ruthel G, Kallstrom G et al.: Involvement of vacuolar protein sorting pathway in Ebola virus release independent of TSG101 interaction. J. Infect. Dis. 196(Suppl. 2), S264-S270 (2007).