Induction of apoptosis by sindbis virus occurs at cell entry and does not require virus replication

Journal of Virology

Volumn 73, Issue 12, 1999, Pages 10296-10302

  Jan, Jia Tsrong ^a,b   Griffin, Diane E ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIUM CHLORIDE; BAFILOMYCIN A1; CELL SURFACE RECEPTOR; CYCLOHEXIMIDE; DNA; HEPARAN SULFATE; MONENSIN; VIRUS FUSION PROTEIN; VIRUS GLYCOPROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL MEMBRANE; CHO CELL; CONTROLLED STUDY; DNA DEGRADATION; ENDOSOME; MOUSE; NEUROBLASTOMA CELL; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SINDBIS VIRUS; ULTRAVIOLET IRRADIATION; VIRUS CELL INTERACTION; VIRUS INACTIVATION; VIRUS REPLICATION;

EID: 0032710836     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.12.10296-10302.1999     Document Type: Article

References (50)

1. Agapov, E. V., I. Frolov, B. D. Lindenbach, B. M. Pragai, S. Schlesinger, and C. M. Rice. 1998. Noncytopathic Sindbis virus RNA vectors for heterologous gene expression. Proc. Natl. Acad. Sci. USA 95:12989-12994.
2. Amano, T., E. Richelson, and M. Nirenberg. 1972. Neurotransmitter synthesis by neuroblastoma clones. Proc. Natl. Acad. Sci. USA 69:258-263.
3. Bowman, E. M., A. Siebers, and K. Altendorf. 1988. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. USA 85:7972-7976.
4. Brojatsch, J., J. Naughton, M. M. Rolls, K. Zingler, and J. A. T. Young. 1996. CAR1, a TNFR-related protein, is a cellular receptor for cytopathic avian leukosis-sarcoma viruses and mediates apoptosis. Cell 87:845-855.
5. Bron, R., J. M. Wahlberg, H. Garoff, and J. Wilschut. 1993. Membrane fusion of Semliki Forest virus in a model system: correlation between fusion kinetics and structural changes in the envelope glycoprotein. EMBO J. 12:693-701.
6. Burge, B., and E. Pfefferkorn. 1966. Isolation and characterization of conditional lethal mutants of Sindbis virus. Virology 30:204-213.
7. Caillet-Fauquet, P., M. Perros, A. Brandenburger, P. Spegelaere, and J. Rommelaere. 1990. Programmed killing of human cells by means of an inducible clone of parvoviral genes encoding non-structural proteins. EMBO J. 9:2989-2995.
8. Cheng, E. H., B. Levine, L. H. Boise, C. B. Thompson, and J. M. Hardwick. 1996. Bax-independent inhibition of apoptosis by Bcl-xL. Nature 379:554-556.
9. Cleverley, D. Z., and J. Lenard. 1998. The transmembrane domain in viral fusion: essential role for a conserved glycine residue in vesicular stomatitis virus G protein. Proc. Natl. Acad. Sci. USA 95:3425-3430.
10. Dropulic, L. K., J. M. Hardwick, and D. E. Griffin. 1997. A single amino acid change in the E2 glycoprotein of Sindbis virus confers neurovirulence by altering an early step of virus replication. J. Virol. 71:6100-6105.
11. Dryga, S. A., O. A. Dryga, and S. Schlesinger. 1997. Identification of mutations in a Sindbis virus variant able to establish persistent infection in BHK cells: the importance of a mutation in the nsP2 gene. Virology 228:74-83.
12. Flynn, D. C., W. J. Meyer, J. M. Mackenzie, Jr., and R. E. Johnston. 1990. A conformational change in Sindbis virus glycoproteins E1 and E2 is detected at the plasma membrane as a consequence of early virus-cell interaction. J. Virol. 64:3643-3653.
13. Frolov, I., E. Agapov, T. A. Hoffman, Jr., B. M. Prágai, M. Lippa, S. Schlesinger, and C. M. Rice. 1999. Selection of RNA replicons capable of persistent noncytopathic replication in mammalian cells. J. Virol. 73:3854-3865.
14. Frolov, I., and S. Schlesinger. 1994. Comparison of the effects of Sindbis virus and Sindbis virus replicons on host cell protein synthesis and cytopathogenicity in BHK cells. J. Virol. 68:1721-1727.
15. Griffin, D. E., and J. M. Hardwick. 1997. Regulators of apoptosis on the road to persistent alphavirus infection. Annu. Rev. Microbiol. 51:565-592.
16. Griffin, D. E., and R. T. Johnson. 1977. Role of the immune response in recovery from Sindbis virus encephalitis in mice. J. Immunol. 118:1070-1075.
17. Hanon, E., G. Meyer, A. Vanderplasschen, C. Dessy-Doizé, E. Thiry, and P.-P. Pastoret. 1998. Attachment but not penetration of bovine herpesvirus 1 is necessary to induce apoptosis in target cells. J. Virol. 72:7638-7641.
18. Hubbard, S. C., L. Walls, H. E. Ruley, and E. A. Muchmore. 1994 Generation of Chinese hamster ovary cell glycosylation mutants by retroviral insertional mutagenesis. J. Biol. Chem. 269:3717-3724.
19. Jackson, A. C., T. R. Moench, and D. E. Griffin. 1987. The pathogenesis of spinal cord involvement in the encephalomyelitis of mice caused by neuroadapted Sindbis virus infection. Lab. Investig. 56:418-423.
20. Jackson, A. C., T. R. Moench, B. D. Trapp, and D. E. Griffin. 1988. Basis of neurovirulence in Sindbis virus encephalomyelitis of mice. Lab. Investig. 58:503-509.
21. Jan, J.-T., A. P. Byrnes, and D. E. Griffin. 1999. Characterization of a Chinese hamster ovary cell line developed by retroviral insertional mutagenesis that is resistant to Sindbis virus infection. J. Virol. 73:4919-4924.
22. Joe, A. K., G. Ferrari, H. H. Jiang, X. H. Liang, and B. Levine. 1996. Dominant inhibitory Ras delays Sindbis virus-induced apoptosis in neuronal cells. J. Virol. 70:7744-7751.
23. Joe, A. K., H. H. Foo, L. Kleeman, and B. Levine. 1998. The transmembrane domains of Sindbis virus envelope glycoproteins induce cell death. J. Virol. 72:3935-3943.
24. Johnson, R. T., H. F. McFarland, and S. E. Levy. 1972. Age-dependent resistance to viral encephalitis: studies of infections due to Sindbis virus in mice. J. Infect. Dis. 125:257-262.
25. Legrand, C., J. Rommelaere, and P. Caillet-Fauquet. 1993. MVM(p) NS-2 protein expression is required with NS-1 for maximal cytotoxicity in human transformed cells. Virology 195:149-155.
26. Levine, B., J. E. Goldman, H. H. Jiang, D. E. Griffin, and J. M. Hardwick. 1996. Bcl-2 protects mice against fatal alphavirus encephalitis. Proc. Natl. Acad. Sci. USA 93:4810-4815.
27. Levine, B., Q. Huang, J. T. Isaacs, J. C. Reed, D. E. Griffin, and J. M. Hardwick. 1993. Conversion of lytic to persistent alphavirus infection by the bcl-2 cellular oncogene. Nature 361:739-742.
28. Lewis, J., S. L. Wesselingh, D. E. Griffin, and J. M. Hardwick. 1996. Alphavirus-induced apoptosis in mouse brains correlates with neurovirulence. J. Virol. 70:1828-1835.
29. Lin, K.-I., J. A. DiDonato, A. Hoffman, J. M. Hardwick, and R. R. Rattan. 1998. Suppression of steady-state, but not stimulus-induced NF-KB activity inhibits alphavirus-induced apoptosis. J. Cell Biol. 141:1479-1487.
30. Lin, K.-I., P. Pasinelli, R. H. Brown, J. M. Hardwick, and R. R. Rattan. 1999. Decreased intracellular superoxide levels activate Sindbis virus-induced apoptosis. J. Biol. Chem. 274:13650-13655.
31. Lin, K.-I., S. H. Lee, R. Narayanan, J. M. Baraban, J. M. Hardwick, and R. R. Ratan. 1995. Thiol agents and Bcl-2 identify an alphavirus-induced apoptotic pathway that requires activation of the transcription factor NF-kappa B. J. Cell Biol. 131:1-14.
32. Liu, Z. G., H. Hsu, D. V. Goeddel, and M. Karin. 1996. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-KB activation prevents cell death. Cell 87:565-576.
33. Lowe, S. W., and H. E. Ruley. 1993. Stabilization of the p53 tumor suppressor is induced by adenoviras 5 E1A and accompanies apoptosis. Genes Dev. 7:535-545.
34. Marsh, M., J. Wellsteed, H. Kern, E. Harms, and A. Helenius. 1982. Monensin inhibits Semliki Forest virus penetration into culture cells. Proc. Natl. Acad. Sci. USA 79:5297-5301.
35. Mattson, M. P., and K. Furukawa. 1997. Anti-apoptotic actions of cycloheximide: blockade of programmed cell death or induction of programmed cell life? Apoptosis 2:257-264.
36. Nava, V. E., A. Rosen, M. A. Veliuona, R. J. Clem, B. Levine, and J. M. Hardwick. 1998. Sindbis virus induces apoptosis through a caspase-dependent, CrmA-sensitive pathway. J. Virol. 72:452-459.
37. Nieva, J.-L., R. Bron, J. Corver, and J. Wilschut. 1994. Membrane fusion of Semliki Forest virus requires sphingolipids in the target membrane. EMBO J. 13:2797-2804.
38. Noteborn, M. H. M., D. Todd, C. A. J. Verschueren, H. W. F. M. de Gauw, W. L. Curran, S. Veldkamp, A. J. Douglas, M. S. McNulty, A. J. van der Eb, and G. Koch. 1994. A single chicken anemia virus protein induces apoptosis. J. Virol. 68:346-351.
39. Pesonen, M., and L. Kaariainen. 1982. Incomplete complex oligosaccharides in Semliki Forest virus envelope proteins arrested within the cell in the presence of monensin. J. Mol. Biol. 158:213-230.
40. Ramsey-Ewing, A., and B. Moss. 1998. Apoptosis induced by a postbinding step of vaccinia virus entry into Chinese hamster ovary cells. Virology 242: 138-149.
41. Rao, L., M. Debbas, P. Sabbatini, D. Hockenberry, S. Korsmeyer, and E. White. 1992. The adenovirus E1A proteins induce apoptosis, which is inhibited by the E1B 19-kDa and Bcl-2 proteins. Proc. Natl. Acad. Sci. USA 89:7742-7746.
42. Schmaljohn, A. L. 1983. Protective monoclonal antibodies define maturational and pH-dependent antigenic changes in Sindbis virus E1 glycoprotein. Virology 130:144-154.
43. Stewart, S. A., B. Poon, J. B. M. Jowett, and I. S. Y. Chen. 1997. Human immunodeficiency virus type 1 Vpr induces apoptosis following cell cycle arrest. J. Virol. 71:5579-5592.
44. Strauss, J. H., and E. G. Strauss. 1994. The alphaviruses: gene expression, replication, and evolution. Microbiol. Rev. 58:491-562.
45. Taylor, R. M., H. S. Hurlbut, T. H. Work, J. R. Kingsbury, and T. E. Frothingham. 1955. Sindbis virus: a newly recognized arthropod-transmitted virus. Am. J. Trop. Med. Hyg. 4:844-846.
46. Tucker, P. C., and D. E. Griffin. 1991. Mechanism of altered Sindbis virus neurovirulence associated with a single-amino-acid change in the E2 glycoprotein. J. Virol. 65:1551-1557.
47. Tucker, P. C., S. H. Lee, N. Bui, D. Martinie, and D. E. Griffin. 1997. Amino acid changes in the Sindbis virus E2 glycoprotein that increase neurovirulence improve entry into neuroblastoma cells. J. Virol. 71:6106-6112.
48. Tyler, K. L., M. K. T. Squier, S. E. Rodgers, B. E. Schneider, S. M. Oberhaus, T. A. Grdina, J. J. Cohen, and T. S. Dermody. 1995. Differences in the capacity of reovirus strains to induce apoptosis are determined by the viral attachment protein σ1. J. Virol. 69:6972-6979.
49. Ubol, S., P. C. Tucker, D. E. Griffin, and J. M. Hardwick. 1994. Neurovirulent strains of alphavirus induce apoptosis in bcl-2-expressing cells; role of a single amino acid change in the E2 glycoprotein. Proc. Natl. Acad. Sci. USA 91:5202-5206.
50. Wahlberg, J. M., and H. Garoff. 1992. Membrane fusion process of Semliki Forest virus. I. Low pH-induced rearrangement in spike protein quaternary structure precedes virus penetration into cells. J. Cell Biol. 116:339-348.