Vacuolar protein sorting pathway contributes to the release of marburg virus

Journal of Virology

Volumn 83, Issue 5, 2009, Pages 2327-2337

  Kolesnikova, Larissa ^a,b   Strecker, Thomas ^a   Morita, Eiji ^d   Zielecki, Florian ^a,b   Mittler, Eva ^a   Crump, Colin ^c   Becker, Stephan ^a,b  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b ROBERT KOCH INSTITUTE   (Germany)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; PROTEIN; PROTEIN VP40; SIGNAL PEPTIDE; UNCLASSIFIED DRUG; VPS4 PROTEIN; MATRIX PROTEIN; VP40 PROTEIN, VIRUS;

ARTICLE; BUDDING; CELL POPULATION; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; MARBURG VIRUS; MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN TARGETING; SEPARATION TECHNIQUE; SUPERNATANT; VIRUS EXPRESSION; VIRUS LIKE AGENT; CELL LINE; CELL VACUOLE; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; VIRION; VIRUS ASSEMBLY;

LAKE VICTORIA MARBURGVIRUS;

CELL LINE; HUMANS; MARBURGVIRUS; MUTATION; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; VACUOLES; VIRAL MATRIX PROTEINS; VIRION; VIRUS ASSEMBLY;

EID: 60049086612     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02184-08     Document Type: Article

References (63)

1. Babst, M. 2005. A protein's final ESCRT. Traffic 6:2-9.
2. Babst, M., T. K. Sato, L. M. Banta, and S. D. Emr. 1997. Endosomal transport function in yeast requires a novel AAA-type ATPase, Vps4p. EMBO J. 16:1820-1831.
3. Babst, M., B. Wendland, E. J. Estepa, and S. D. Emr. 1998. The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J. 17:2982-2993.
4. Bess, J. W., Jr., R. J. Gorelick, W. J. Bosche, L. E. Henderson, and L. O. Arthur. 1997. Microvesicles are a source of contaminating cellular proteins found in purified HIV-1 preparations. Virology 230:134-144.
5. Bieniasz, P. D. 2006. Late budding domains and host proteins in enveloped virus release. Virology 344:55-63.
6. Bishop, N., and P. Woodman. 2000. ATPase-defective mammalian VPS4 localizes to aberrant endosomes and impairs cholesterol trafficking. Mol. Biol. Cell 11:227-239.
7. Bishop, N., and P. Woodman. 2001. TSG101/mammalian VPS23 and mammalian VPS28 interact directly and are recruited to VPS4-induced endosomes. J. Biol. Chem. 276:11735-11742.
8. Chen, B. J., and R. A. Lamb. 2008. Mechanisms for enveloped virus budding: can some viruses do without an ESCRT? Virology 372:221-232.
9. Chen, H. I., and M. Sudol. 1995. The WW domain of Yes-associated protein binds a proline-rich ligand that differs from the consensus established for Src homology 3-binding modules. Proc. Natl. Acad. Sci. USA 92:7819-7823.
10. Coronel, E. C., K. G. Murti, T. Takimoto, and A. Portner. 1999. Human parainfluenza virus type 1 matrix and nucleoprotein genes transiently expressed in mammalian cells induce the release of virus-like particles containing nucleocapsid-like structures. J. Virol. 73:7035-7038.
11. Crump, C. M., C. Yates, and T. Minson. 2007. Herpes simplex virus type 1 cytoplasmic envelopment requires functional Vps4. J. Virol. 81:7380-7387.
12. Février, B., and G. Raposo. 2004. Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr. Opin. Cell Biol. 16:415-421.
13. Fraile-Ramos, A., A. Pelchen-Matthews, C. Risco, M. T. Rejas, V. C. Emery, A. F. Hassan-Walker, M. Esteban, and M. Marsh. 2007. The ESCRT machinery is not required for human cytomegalovirus envelopment. Cell. Microbiol. 9:2955-2967.
14. Freed, E. O. 2002. Viral late domains. J. Virol. 76:4679-4687.
15. Fujita, H., M. Yamanaka, K. Imamura, Y. Tanaka, A. Nara, T. Yoshimori, S. Yokota, and M. Himeno. 2003. A dominant negative form of the AAA ATPase SKD1/VPS4 impairs membrane trafficking out of endosomal/lyso- somal compartments: class E vps phenotype in mammalian cells. J. Cell Sci. 116:401-414.
16. Garrus, J. E., U. K. von Schwedler, O. W. Pornillos, S. G. Morham, K. H. Zavitz, H. E. Wang, D. A. Wettstein, K. M. Stray, M. Cote, R. L. Rich, D. G. Myszka, and W. I. Sundquist. 2001. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107:55-65.
17. Gluschankof, P., I. Mondor, H. R. Gelderblom, and Q. J. Sattentau. 1997. Cell membrane vesicles are a major contaminant of gradient-enriched human immunodeficiency virus type-1 preparations. Virology 230:125-133.
18. Geómez-Puertas, P., C. Albo, E. Perez-Pastrana, A. Vivo, and A. Portela. 2000. Influenza virus matrix protein is the major driving force in virus budding. J. Virol. 74:11538-11547.
19. Gottlinger, H. G., T. Dorfman, J. G. Sodroski, and W. A. Haseltine. 1991. Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release. Proc. Natl. Acad. Sci. USA 88:3195-3199.
20. Gruenberg, J., and H. Stenmark. 2004. The biogenesis of multivesicular endosomes. Nat. Rev. Mol. Cell Biol. 5:317-323.
21. Harrisson, F., C. Vanroelen, and L. Vakaet. 1988. Morphological and im- munocytochemical studies of fibronectin-coated, plasma membrane-limited vesicles in the early chicken embryo. Anat. Rec. 221:854-859.
22. Harty, R. N., M. E. Brown, G. Wang, J. Huibregtse, and F. P. Hayes. 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. USA 97:13871-13876.
23. Hierholzer, J. C., and R. A. Killington. 1996. Virus isolation and quantitation. Academic Press Limited, London, United Kingdom.
24. Hoenen, T., L. Kolesnikova, and S. Becker. 2007. Recent advances in filovirus- and arenavirus-like particles. Future Virol. 2:193.
25. Gag is required for particle production from full-length human immunodeficiency virus type 1 molecular clones expressing protease. J. Virol. 69:6810-6818.
26. Hurley, J. H., and S. D. Emr. 2006. The ESCRT complexes: structure and mechanism of a membrane-trafficking network. Annu. Rev. Biophys. Biomol. Struct. 35:277-298.
27. Irie, T., J. M. Licata, J. P. McGettigan, M. J. Schnell, and R. N. Harty. 2004. Budding of PPxY-containing rhabdoviruses is not dependent on host proteins TGS101 and VPS4A. J. Virol. 78:2657-2665.
28. Justice, P. A., W. Sun, Y. Li, Z. Ye, P. R. Grigera, and R. R. Wagner. 1995. Membrane vesiculation function and exocytosis of wild-type and mutant matrix proteins of vesicular stomatitis virus. J. Virol. 69:3156-3160.
29. Karacostas, V., K. Nagashima, M. A. Gonda, and B. Moss. 1989. Human immunodeficiency virus-like particles produced by a vaccinia virus expression vector. Proc. Natl. Acad. Sci. USA 86:8964-8967.
30. Kolesnikova, L., B. Berghofer, S. Bamberg, and S. Becker. 2004. Multivesicular bodies as a platform for formation of the Marburg virus envelope. J. Virol. 78:12277-12287.
31. Kolesnikova, L., A. B. Bohil, R. E. Cheney, and S. Becker. 2007. Budding of Marburg virus is associated with filopodia. Cell. Microbiol. 9:939-951.
32. Kolesnikova, L., H. Bugany, H. D. Klenk, and S. Becker. 2002. VP40, the matrix protein of Marburg virus, is associated with membranes of the late endosomal compartment. J. Virol. 76:1825-1838.
33. Langelier, C., U. K. von Schwedler, R. D. Fisher, I. De Domenico, P. L. White, C. P. Hill, J. Kaplan, D. Ward, and W. I. Sundquist. 2006. Human ESCRT-II complex and its role in human immunodeficiency virus type 1 release. J. Virol. 80:9465-9480.
34. Licata, J. M., M. Simpson-Holley, N. T. Wright, Z. Han, J. Paragas, and R. N. Harty. 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.
35. Martin-Serrano, J., A. Yarovoy, D. Perez-Caballero, and P. D. Bieniasz. 2003. Divergent retroviral late-budding domains recruit vacuolar protein sorting factors by using alternative adaptor proteins. Proc. Natl. Acad. Sci. USA 100:12414-12419.
36. Martin-Serrano, J., T. Zang, and P. D. Bieniasz. 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.
37. Martin-Serrano, J., T. Zang, and P. D. Bieniasz. 2003. Role ofESCRT-I in retroviral budding. J. Virol. 77:4794-4804.
38. Medina, G., Y. Zhang, Y. Tang, E. Gottwein, M. L. Vana, F. Bouamr, J. Leis, and C. A. Carter. 2005. The functionally exchangeable L domains in RSV and HIV-1 Gag direct particle release through pathways linked by Tsg101. Traffic 6:880-894.
39. Mittler, E., L. Kolesnikova, T. Strecker, W. Garten, and S. Becker. 2007. Role of the transmembrane domain of Marburg virus surface protein GP in assembly of the viral envelope. J. Virol. 81:3942-3948.
40. Moller, P., N. Pariente, H. D. Klenk, and S. Becker. 2005. Homo-oligomerization of Marburg virus VP35 is essential for its function in replication and transcription. J. Virol. 79:14876-14886.
41. Nayak, D. P., E. K. Hui, and S. Barman. 2004. Assembly and budding of influenza virus. Virus Res. 106:147-165.
42. Perez, M., R. C. Craven, and J. C. de la Torre. 2003. The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies. Proc. Natl. Acad. Sci. USA 100:12978-12983.
43. Piccin, A., W. G. Murphy, and O. P. Smith. 2007. Circulating microparticles: pathophysiology and clinical implications. Blood Rev. 21:157-171.
44. Pushko, P., T. M. Tumpey, N. Van Hoeven, J. A. Belser, R. Robinson, M. Nathan, G. Smith, D. C. Wright, and R. A. Bright. 2007. Evaluation of influenza virus-like particles and Novasome adjuvant as candidate vaccine for avian influenza. Vaccine 25:4283-4290.
45. Scheuring, S., R. A. Rohricht, B. Schoning-Burkhardt, A. Beyer, S. Muller, H. F. Abts, and K. Kohrer. 2001. Mammalian cells express two VPS4 proteins both of which are involved in intracellular protein trafficking. J. Mol. Biol. 312:469-480.
46. Schmitt, A. P., G. P. Leser, E. Morita, W. I. Sundquist, and R. A. Lamb. 2005. Evidence for a new viral late-domain core sequence, FPIV, necessary for budding of a paramyxovirus. J. Virol. 79:2988-2997.
47. Strack, B., A. Calistri, S. Craig, E. Popova, and H. G. Gottlinger. 2003. AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 114:689-699.
48. Strecker, T., R. Eichler, J. Meulen, W. Weissenhorn, H. Dieter Klenk, W. Garten, and O. Lenz. 2003. Lassa virus Z protein is a matrix protein and sufficient for the release of virus-like particles. J. Virol. 77:10700-10705. (Corrected.)
49. Swenson, D. L., K. L. Warfield, K. Kuehl, T. Larsen, M. C. Hevey, A. Schmaljohn, S. Bavari, and M. J. Aman. 2004. Generation of Marburg virus-like particles by co-expression of glycoprotein and matrix protein. FEMS Immunol. Med. Microbiol. 40:27-31.
50. Taylor, G. M., P. I. Hanson, and M. Kielian. 2007. Ubiquitin depletion and dominant-negative VPS4 inhibit rhabdovirus budding without affecting alphavirus budding. J. Virol. 81:13631-13639.
51. Théry, C., L. Zitvogel, and S. Amigorena. 2002. Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2:569-579.
52. Timmins, J., S. Scianimanico, G. Schoehn, and W. Weissenhorn. 2001. Vesicular release of Ebola virus matrix protein VP40. Virology 283:1-6.
53. Trubey, C. M., E. Chertova, L. V. Coren, J. M. Hilburn, C. V. Hixson, K. Nagashima, J. D. Lifson, and D. E. Ott. 2003. Quantitation of HLA class II protein incorporated into human immunodeficiency type 1 virions purified by anti-CD45 immunoaffinity depletion of microvesicles. J. Virol. 77:12699-12709.
54. Urata, S., T. Noda, Y. Kawaoka, S. Morikawa, H. Yokosawa, and J. Yasuda. 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.
55. Urata, S., T. Noda, Y. Kawaoka, H. Yokosawa, and J. Yasuda. 2006. Cellular factors required for Lassa virus budding. J. Virol. 80:4191-4195.
56. van Niel, G., I. Porto-Carreiro, S. Simoes, and G. Raposo. 2006. Exo- somes: a common pathway for a specialized function. J. Biochem. (Tokyo) 140:13-21.
57. Gag Proc. Natl. Acad. Sci. USA 98:7724-7729.
58. von Schwedler, U. K., M. Stuchell, B. Muller, D. M. Ward, H. Y. Chung, E. Morita, H. E. Wang, T. Davis, G. P. He, D. M. Cimbora, A. Scott, H. G. Krausslich, J. Kaplan, S. G. Morham, and W. I. Sundquist. 2003. The protein network of HIV budding. Cell 114:701-713.
59. Warfield, K. L., D. L. Swenson, G. Demmin, and S. Bavari. 2005. Filovirus- like particles as vaccines and discovery tools. Expert Rev. Vaccines 4:429-440.
60. Welsch, S., B. Muller, and H. G. Krausslich. 2007. More than one door: budding of enveloped viruses through cellular membranes. FEBS Lett. 581: 2089-2097.
61. Williams, R. L., and S. Urbe. 2007. The emerging shape of the ESCRT machinery. Nat. Rev. Mol. Cell Biol. 8:355-368.
62. Wills, J. W., and R. C. Craven. 1991. Form, function, and use of retroviral gag proteins. AIDS 5:639-654.
63. Yang, C., L. Ye, and R. W. Compans. 2008. Protection against filovirus infection: virus-like particle vaccines. Expert Rev. Vaccines 7:333-344.