Assembly of ebola virus matrix protein VP40 is regulated by latch-like properties of N and C terminal tails

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Silva, Leslie P ^a   Vanzile, Michael ^b   Bavari, Sina ^b   Aman, J M Javad ^b,c   Schriemer, David C ^a  

^a UNIVERSITY OF CALGARY   (Canada)

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

^c Integrated BioTherapeutics Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MONOMER; PROTEIN VP40; VIRUS RNA;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; DEUTERIUM HYDROGEN EXCHANGE; EBOLA VIRUS; MASS SPECTROMETRY; NONHUMAN; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FUNCTION; PROTEIN STABILITY; REGULATORY MECHANISM; STRUCTURE ACTIVITY RELATION; VIRUS ASSEMBLY; VIRUS RELEASE;

EBOLAVIRUS; MODELS, MOLECULAR; NUCLEOPROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STABILITY; PROTEIN TRANSPORT; RNA, VIRAL; VIRAL CORE PROTEINS; VIRUS ASSEMBLY;

EBOLA VIRUS; RNA VIRUSES;

EID: 84863609124     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039978     Document Type: Article

References (39)

1. Pigott DC, (2005) Hemorrhagic fever viruses. Crit Care Clin 21: 765-783.
2. Wauquier N, Becquart P, Padilla C, Baize S, Leroy EM, (2010) Human fatal zaire ebola virus infection is associated with an aberrant innate immunity and with massive lymphocyte apoptosis. PLoS Negl Trop Dis 4.
3. Feldmann H, Geisbert TW, (2011) Ebola haemorrhagic fever. Lancet 377: 849-862.
4. He J, Kraft AJ, Fan JA, Van Dyke M, Wang LH, et al. (2009) Simultaneous Detection of CDC Category "A" DNA and RNA Bioterrorism Agents by Use of Multiplex PCR & RT-PCR Enzyme Hybridization Assays. Viruses-Basel 1: 441-459.
5. Warfield KL, Swenson DL, Olinger GG, Kalina WV, Aman MJ, et al. (2007) Ebola virus-like particle-based vaccine protects nonhuman primates against lethal Ebola virus challenge. Journal of Infectious Diseases 196: S430-S437.
6. Hoenen T, Groseth A, Feldmann H, (2012) Current ebola vaccines. Expert Opin Biol Ther.
7. Warren TK, Warfield KL, Wells J, Swenson DL, Donner KS, et al. (2010) Advanced antisense therapies for postexposure protection against lethal filovirus infections. Nat Med 16: 991-994.
8. Geisbert TW, Lee AC, Robbins M, Geisbert JB, Honko AN, et al. (2010) Postexposure protection of non-human primates against a lethal Ebola virus challenge with RNA interference: a proof-of-concept study. Lancet 375: 1896-1905.
9. Fabozzi G, Nabel CS, Dolan MA, Sullivan NJ, (2011) Ebola virus proteins supress the effects of small interfering RNA by direct interaction with the mammalian RNA interference pathway. Journal of Virology 85: 2512-2523.
10. Cote M, Misasi J, Ren T, Bruchez A, Lee K, et al. (2011) Small molecule inhibitors reveal Niemann-Pick C1 is essential for Ebola virus infection. Nature 477: 344-U122.
11. Kortepeter MG, Martin JW, Rusnak JM, Cieslak TJ, Warfield KL, et al. (2008) Managing potential laboratory exposure to ebola virus by using a patient biocontainment care unit. Emerg Infect Dis 14: 881-887.
12. Halfmann P, Kim JH, Ebihara H, Noda T, Neumann G, et al. (2008) Generation of biologically contained Ebola viruses. Proc Natl Acad Sci U S A 105: 1129-1133.
13. Noda T, Sagara H, Suzuki E, Takada A, Kida H, et al. (2002) Ebola virus VP40 drives the formation of virus-like filamentous particles along with GP. Journal of Virology 76: 4855-4865.
14. Sanchez A, Kiley MP, Holloway BP, Auperin DD, (1993) Sequence analysis of the Ebola virus genome: organization, genetic elements, and comparison with the genome of Marburg virus. Virus Res 29: 215-240.
15. Johnson RF, McCarthy SE, Godlewski PJ, Harty RN, (2006) Ebola virus VP35-VP40 interaction is sufficient for packaging 3E-5E minigenome RNA into virus-like particles. Journal of Virology 80: 5135-5144.
16. Mehedi M, Falzarano D, Seebach J, Hu X, Carpenter MS, et al. (2011) A new Ebola virus nonstructural glycoprotein expressed through RNA editing. J Virol 85: 5406-5414.
17. Warfield KL, Swenson DL, Demmin GL, Bavari S, (2005) Filovirus-like particles as vaccines and discovery tools. Expert Review of Vaccines 4: 429-440.
18. Licata JM, Johnson RF, Han Z, Harty RN, (2004) Contribution of Ebola virus glycoprotein, nucleoprotein, and VP24 to budding of VP40 virus-like particles. Journal of Virology 78: 7344-7351.
19. Harty RN, (2009) No exit: targeting the budding process to inhibit filovirus replication. Antiviral Res 81: 189-197.
20. Schmitt A, Lamb RA, (2004) Escaping from the cell: Assembly and budding of negative-strand RNA viruses. Biology of negative strand RNA viruses: the power of reverse genetics current topics in microbiology and immunology 283: 145-196.
21. Jasenosky L, Neumann G, Lukashevic I, Kawaoka Y, (2001) Ebola virus VP40-Induced Particle Formation and Association with Lipid Bilayer. Journal of Virology 75: 5205-5214.
22. Baize S, Leroy EM, Georges-Courbot M-C, Capron M, Lansoud-Soukate J, et al. (1999) Defective humoral responses and extensive intravascular apoptosis are associated with fatal outcome in Ebola virus-infected patients. Nature Medicine 5: 423-426.
23. Takimoto T, Murti KG, Bousse T, Scroggs RA, Portner A, (2001) Role of Matrix and Fusion Proteins in Budding of Sendai Virus. Journal of Virology 75: 11384-11391.
24. Panchal RG, Ruthel G, Kenny TA, Kallstrom GH, Lane D, et al. (2003) In vivo oligomerization and raft localization of Ebola virus protein VP40 during vesicular budding. Proceedings of the National Academy of Sciences 100: 15936-15941.
25. Scianimanico S, Schoehn G, Timmins J, Ruigrok RHW, Weissenhorn W, (2000) Membrane association induces a conformational change in the Ebola virus matrix protein. European Molecular Biology Organization Journal 19: 6732-6741.
26. Martin-Serrano J, Zang T, Bieniasz PD, (2001) HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nature Medicine 7: 1313-1319.
27. Ruigrok RWH, Schoehn G, Dessen A, Forest E, Volchkov V, et al. (2000) Structural characterization and membrane binding properties of the matrix protein VP40 of Ebola virus. Journal of Molecular Biology 300: 103-112.
28. Gomis-Ruth FX, Dessen A, Timmins J, Bracher A, Kolesnikova L, et al. (2003) The matrix protein VP40 from Ebola virus octamerizes into pore-like structures with specific RNA binding properties. Structure 11: 423-433.
29. Dessen A, Volchkov V, Dolnik O, Klenk H-D, Weissenhorn W, (2000) Crystal structure of the matrix protein VP40 from Ebola virus. European Molecular Biology Organization Journal 19: 4228-4236.
30. Timmins J, Schoehn G, Kohlhaas C, Klenk H-D, Ruigrok RWH, et al. (2003) Oligomerization and polymerization of the filovirus matrix protein VP40. Virology 312.
31. Hoenen T, Biedenkopf N, Zielecki F, Jung S, Groseth A, et al. (2010) Oligomerization of Ebola Virus VP40 Is Essential for Particle Morphogenesis and Regulation of Viral Transcription. Journal of Virology 84: 7053-7063.
32. Hoenen T, Jung S, Herwig A, Groseth A, Becker S, (2010) Both matrix proteins of Ebola virus contribute to the regulation of viral genome replication and transcription. Virology 403: 56-66.
33. Reynard O, Nemirov K, Page A, Mateo M, Raoul H, et al. (2011) Conserved proline-rich region of Ebola virus matrix protein VP40 is essential for plasma membrane targeting and virus-like particle release. J Infect Dis 204: S884-891.
34. Bennett MJ, Barakat K, Huzil JT, Tuszynski J, Schriemer DC, (2010) Discovery and Characterization of the Laulimalide-Microtubule Binding Mode by Mass Shift Perturbation Mapping. Chemistry & Biology 17: 725-734.
35. Pornillos O, Alam SL, Davis DR, Sundquist WI, (2002) Structure of the Tsg101 UEV domain in complex with the PTAP motif of the HIV-1 p6 protein. Nature Structural Biology 9: 812-817.
36. Slysz GW, Percy AJ, Schriemer DC, (2008) Restraining expansion of the peak envelope in H/D exchange-MS and its application in detecting perturbations of protein structure/dynamics. Analytical Chemistry 80: 7004-7011.
37. Chalmers MJ, Pascal BD, Willis S, Zhang J, Iturria SJ, et al. (2011) Methods for the analysis of high precision differential hydrogen-deuterium exchange data. International Journal of Mass Spectrometry 302: 59-68.
38. Arnold K, Bordoli L, Kopp J, Schwede T, (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201.
39. Leaver-Fay A, Tyka M, Lewis SM, Lange OF, Thompson J, et al. (2011) Rosetta3: An Object-Oriented Software Suite for the Simulation and Design of Macromolecules. Methods in Enzymology, Vol 487: Computer Methods, Pt C: 545-574.