Glycoprotein-dependent acidification of vesicular stomatitis virus enhances release of matrix protein

Journal of Virology

Volumn 83, Issue 23, 2009, Pages 12139-12150

  Mire, Chad E ^a   Dube, Derek ^b   Delos, Sue E ^b   White, Judith M ^b   Whitt, Michael A ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BAFILOMYCIN A1; CYSTEINE; GLYCOPROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; MATRIX PROTEIN; RIBONUCLEOPROTEIN;

ACIDIFICATION; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFOCAL MICROSCOPY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISSOCIATION; ENDOCYTOSIS; FLUORESCENCE; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; VESICULAR STOMATITIS VIRUS; VIRION; VIRUS PARTICLE; VIRUS RECOMBINANT; WILD TYPE;

ANIMALS; CELL LINE; CRICETINAE; GLYCOPROTEINS; MICROSCOPY, CONFOCAL; RECOMBINANT PROTEINS; STAINING AND LABELING; TIME FACTORS; VESICULOVIRUS; VIRAL MATRIX PROTEINS; VIRAL PROTEINS; VIRUS INTERNALIZATION;

VESICULAR STOMATITIS VIRUS;

EID: 70450193087     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00955-09     Document Type: Article

References (57)

1. Adams, S. R., R. E. Campbell, L. A. Gross, B. R. Martin, G. K. Walkup, Y. Yao, J. Llopis, and R. Y. Tsien. 2002. New biarsenical ligands and tetracysteine motifs for protein labeling in vitro and in vivo: synthesis and biological applications. J. Am. Chem. Soc. 124:6063-6076.
2. Arhel, N., A. Genovesio, K. A. Kim, S. Miko, E. Perret, J. C. Olivo-Marin, S. Shorte, and P. Charneau. 2006. Quantitative four-dimensional tracking of cytoplasmic and nuclear HIV-1 complexes. Nat. Methods 3:817-824. (Pubitemid 44445829)
3. Blumenthal, R., A. Bali-Puri, A. Walter, D. Covell, and O. Eidelman. 1987. pH-dependent fusion of vesicular stomatitis virus with Vero cells. J. Biol. Chem. 262:13614-13619.
4. Boritz, E., J. Gerlach, J. E. Johnson, and J. K. Rose. 1999. Replication-competent rhabdoviruses with human immunodeficiency virus type 1 coats and green fluorescent protein: entry by a pH-independent pathway. J. Virol. 73:6937-6945. (Pubitemid 29327877)
5. Brown, J. C., W. W. Newcomb, and S. Lawrenz-Smith. 1988. pH-dependent accumulation of the vesicular stomatitis virus glycoprotein at the ends of intact virions. Virology 167:625-629.
6. Bui, M., G. Whittaker, and A. Helenius. 1996. Effect of M1 protein and low pH on nuclear transport of influenza virus ribonucleoproteins. J. Virol. 70:8391-8401. (Pubitemid 26378415)
7. Carrasco, L. 1981. Modification of membrane permeability induced by animal viruses early in infection. Virology 113:623-629. (Pubitemid 11056350)
8. Chong, L. D., and J. K. Rose. 1993. Membrane association of functional vesicular stomatitis virus matrix protein in vivo. J. Virol. 67:407-414.
9. Clinton, G. M., S. P. Little, F. S. Hagen, and A. S. Huang. 1978. The matrix (M) protein of vesicular stomatitis virus regulates transcription. Cell 15: 1455-1462.
10. Das, S. C., D. Panda, D. Nayak, and A. K. Pattnaik. 2009. Biarsenical labeling of vesicular stomatitis virus encoding tetracysteine-taggedMprotein allows dynamic imaging of M protein and virus uncoating in infected cells. J. Virol. 83:2611-2622.
11. De, B. P., G. B. Thornton, D. Luk, and A. K. Banerjee. 1982. Purified matrix protein of vesicular stomatitis virus blocks viral transcription in vitro. Proc. Natl. Acad. Sci. USA 79:7137-7141.
12. Flood, E. A., and D. S. Lyles. 1999. Assembly of nucleocapsids with cytosolic and membrane-derived matrix proteins of vesicular stomatitis virus. Virology 261:295-308.
13. Fuerst, T. R., P. L. Earl, and B. Moss. 1987. Use of a hybrid vaccinia virus-T7 RNA polymerase system for expression of target genes. Mol. Cell. Biol. 7:2538-2544.
14. Gaietta, G., T. J. Deerinck, S. R. Adams, J. Bouwer, O. Tour, D. W. Laird, G. E. Sosinsky, R. Y. Tsien, and M. H. Ellisman. 2002. Multicolor and electron microscopic imaging of connexin trafficking. Science 296:503-507. (Pubitemid 34408665)
15. Green, T. J., X. Zhang, G. W. Wertz, and M. Luo. 2006. Structure of the vesicular stomatitis virus nucleoprotein-RNA complex. Science 313:357-360. (Pubitemid 44480961)
16. Griffin, B. A., S. R. Adams, and R. Y. Tsien. 1998. Specific covalent labeling of recombinant protein molecules inside live cells. Science 281:269-272.
17. Gruenberg, J., and F. R. Maxfield. 1995. Membrane transport in the endocytic pathway. Current Opinion in Cell Biology 7:552-563.
18. Han, Z., J. M. Licata, J. Paragas, and R. N. Harty. 2007. Permeabilization of the plasma membrane by Ebola virus GP2. Virus Genes 34:273-281. (Pubitemid 46474938)
19. Harrison, S. C. 2008. Viral membrane fusion. Nat. Struct. Mol. Biol. 15:690-698.
20. Helenius, A. 1992. Unpacking the incoming influenza virus. Cell 69:577-578.
21. Jayakar, H. R., K. G. Murti, and M. A. Whitt. 2000. Mutations in the PPPY motif of vesicular stomatitis virus matrix protein reduce virus budding by inhibiting a late step in virion release. J. Virol. 74:9818-9827.
22. Jeetendra, E., K. Ghosh, D. Odell, J. Li, H. P. Ghosh, and M. A. Whitt. 2003. The membrane-proximal region of vesicular stomatitis virus glycoprotein G ectodomain is critical for fusion and virus infectivity. J. Virol. 77:12807-12818. (Pubitemid 37430675)
23. Jeetendra, E., C. S. Robison, L. M. Albritton, and M. A. Whitt. 2002. The membrane-proximal domain of vesicular stomatitis virus G protein functions as a membrane fusion potentiator and can induce hemifusion. J. Virol. 76:12300-12311. (Pubitemid 35304328)
24. Johannsdottir, H. K., R. Mancini, J. Kartenbeck, L. Amato, and A. Helenius. 2009. Host cell factors and functions involved in vesicular stomatitis virus entry. J. Virol. 83:440-453.
25. Kahn, J. S., M. J. Schnell, L. Buonocore, and J. K. Rose. 1999. Recombinant vesicular stomatitis virus expressing respiratory syncytial virus (RSV) glycoproteins: RSV fusion protein can mediate infection and cell fusion. Virology 254:81-91.
26. Kasermann, F., and C. Kempf. 1996. Low pH-induced pore formation by spike proteins of enveloped viruses. J. Gen. Virol. 77:3025-3032.
27. Kemler, I., G. Whittaker, and A. Helenius. 1994. Nuclear import of microinjected influenza virus ribonucleoproteins. Virology 202:1028-1033. (Pubitemid 24254924)
28. Lamb, R. A., S. L. Zebedee, and C. D. Richardson. 1985. Influenza virus M2 protein is an integral membrane protein expressed on the infected-cell surface. Cell 40:627-633.
29. Lanzrein, M., N. Kasermann, and C. Kempf. 1992. Changes in membrane permeability during Semliki Forest virus induced cell fusion. Biosci. Rep. 12:221-236.
30. Lanzrein, M., A. Schlegel, and C. Kempf. 1994. Entry and uncoating of enveloped viruses. Biochem. J. 302:313-320.
31. Lanzrein, M., R. Weingart, and C. Kempf. 1993. pH-dependent pore formation in Semliki forest virus-infected Aedes albopictus cells. Virology 193: 296-302.
32. Lawson, N. D., E. A. Stillman, M. A. Whitt, and J. K. Rose. 1995. Recombinant vesicular stomatitis viruses from DNA. Proc. Natl. Acad. Sci. USA 92:4477-4481.
33. Lee, Y., and S. I. Chan. 1977. Effect of lysolecithin on the structure and permeability of lecithin bilayer vesicles. Biochemistry 16:1303-1309. (Pubitemid 8083095)
34. Lefrancois, L., and D. S. Lyles. 1982. The interaction of antibody with the major surface glycoprotein of vesicular stomatitis virus. I. Analysis of neutralizing epitopes with monoclonal antibodies. Virology 121:157-167.
35. Lenard, J., and R. Vanderoef. 1990. Localization of the membrane-associated region of vesicular stomatitis virus M protein at the N terminus, using the hydrophobic, photoreactive probe 125I-TID. J. Virol. 64:3486-3491. (Pubitemid 20219554)
36. Lyles, D. S., and M. O. McKenzie. 1998. Reversible and irreversible steps in assembly and disassembly and vesicular stomatitis virus: equilibria and kinetics of dissociation of nucleocapsid-M protein complexes assembled in vivo. Biochemistry 37:439-450.
37. Lyles, D. S., M. O. McKenzie, P. E. Daptur, K. W. Grant, and W. G. Jerome. 1996. Complementation of M gene mutants of vesicular stomatitis virus by plasmid-derived M protein converts spherical extracellular particles into native bullet shapes. Virology 217:76-87.
38. Martin, K., and A. Helenius. 1991. Nuclear transport of influenza virus ribonucleoproteins: The viral matrix protein (M1) promotes export and inhibits import. Cell 67:117-130.
39. Matlin, K., H. Reggio, A. Helenius, and K. Simons. 1982. The pathway of vesicular stomatitis entry leading to infection. J. Mol. Biol. 156:609-631.
40. McClure, M. O., M. A. Sommerfelt, M. Marsh, and R. A. Weiss. 1990. The pH independence of mammalian retrovirus infection. J. Gen. Virol. 71:767-773.
41. Mellman, I., R. Fuchs, and A. Helenius. 1986. Acidification of the endocytic and exocytic pathways. Annu. Rev. Biochem. 55:663-700.
42. Miller, M. R., J. J. Castellot, and A. B. Pardee. 1978. A permeable animal cell preparation for studying macromolecular synthesis. DNA synthesis and the role of deoxyribonucleotides in S phase initiation. Biochemistry 17:1073-1080.
43. Newcomb, W. W., and J. C. Brown. 1981. Role of the vesicular stomatitis virus matrix protein in maintaining the viral nucleocapsid in the condensed form found in native virions. J. Virol. 39:295-299.
44. Newcomb, W. W., G. J. Tobin, J. J. McGowan, and J. C. Brown. 1982. In vitro reassembly of vesicular stomatitis virus skeletons. J. Virol. 41:1055-1062.
45. Pinto, L. H., L. J. Holsinger, and R. A. Lamb. 1992. Influenza virus M2 protein has ion channel activity. Cell 69:517-528.
46. Rigaut, K. D., D. E. Birk, and J. Lenard. 1991. Intracellular distribution of input vesicular stomatitis virus proteins after uncoating. J. Virol. 65:2622-2628.
47. Robison, C. S., and M. A. Whitt. 2000. The membrane-proximal stem region of vesicular stomatitis virus G protein confers efficient virus assembly. J. Virol. 74:2239-2246.
48. Rose, J. K., L. Buonocore, and M. A. Whitt. 1991. A new cationic liposome reagent mediating nearly quantitative transfection of animal cells. Bio-Techniques 10:520-525.
49. Shimbo, K., D. L. Brassard, R. A. Lamb, and L. H. Pinto. 1996. Ion selectivity and activation of the M2 ion channel of influenza virus. Biophys. J. 70:1335-1346. (Pubitemid 26073046)
50. Sieczkarski, S. B., and G. R. Whittaker. 2003. Differential requirements of Rab5 and Rab7 for endocytosis of influenza and other enveloped viruses. Traffic 4:333-343.
51. Sun, X., V. K. Yau, B. J. Briggs, and G. R. Whittaker. 2005. Role of clathrin-mediated endocytosis during vesicular stomatitis virus entry into host cells. Virology 338:53-60. (Pubitemid 40835926)
52. Tatsuo, H., K. Okuma, K. Tanaka, N. Ono, H. Minagawa, A. Takade, Y. Matsuura, and Y. Yanagi. 2000. Virus entry is a major determinant of cell tropism of Edmonston and wild-type strains of measles virus as revealed by vesicular stomatitis virus pseudotypes bearing their envelope proteins. J. Virol. 74:4139-4145. (Pubitemid 30214419)
53. White, J., K. Matlin, and A. Helenius. 1981. Cell fusion by Semliki Forest, influenza and vesicular stomatitis virus. J. Cell Biol. 89:674-679. (Pubitemid 11035975)
54. White, J. M., S. E. Delos, M. Brecher, and K. Schornberg. 2008. Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit. Rev. Biochem. Mol. Biol. 43:189-219.
55. Wilson, T., and J. Lenard. 1981. Interaction of wild-type and mutant M protein vesicular stomatitis virus with nucleocapsids in vitro. Biochemistry 20:1349-1354. (Pubitemid 11115887)
56. Zakowski, J. J., and R. R. Wagner. 1980. Localization of membrane-associated proteins in vesicular stomatitis virus by use of hydrophobic membrane probes and cross-linking reagents. J. Virol. 36:93-102.
57. Zhirnov, O. P. 1990. Solubilization of matrix protein M1/M from virions occurs at different pH for orthomyxo- and paramyxoviruses. Virology 176: 274-279.