Sindbis virus induces apoptosis through a caspase-dependent, CrmA- sensitive pathway

Journal of Virology

Volumn 72, Issue 1, 1998, Pages 452-459

  Nava, Victor E ^a   Rosen, Antony ^b   Veliuona, Michael A ^a   Clem, Rollie J ^a   Levine, Beth ^b   Hardwick, J Marie ^a,b,c  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c College of Physicians and Surgeons ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; APOPTOSIS; ARTICLE; DNA DAMAGE; ENZYME ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SINDBIS VIRUS; VIRUS CELL INTERACTION;

EID: 0031974917     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.1.452-459.1998     Document Type: Article

References (69)

1. Ahmad, M., S. M. Srinivasula, L. Wang, G. Litwack, T. Fernandes-Alnemri, and E. S. Alnemri. 1947. Spodoptera frugiperda caspase-1, a novel insect death protease that cleaves the nuclear immunophilin FKBP46, is the target of the baculovirus antiapoptotic protein p35. J. Biol. Chem. 272:1421-1424.
2. Bertin, J., S. M. Mendrysa, D. J. LaCount, S. Gaur, J. F. Krebs, R. C. Armstrong, K. J. Tomaselli, and P. D. Friesen. 1996. Apoptotic suppression of haculovirus P35 involves cleavage by and inhibition of a virus-induced CED-3/ICE-like prcitease. J. Virol. 70:6251-6259.
3. Boldin, M. P., T. M. Goncharov, Y. V. Goltsev, and D. Wallach. 1996. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell death. Cell 85:803-815.
4. Boulakia, C. A., G. Chen, F. W. Ng, J. G. Teodora, P. E. Branton, D. W. Nicholson, G. G. Poirier, and G. C. Shore. 1996. Bcl-2 and adenovirus E1B 19 kDa protein prevent E1A-induced processing of CPP32 and cleavage of poly(ADP-ribose) polymerase. Oncogene 12:529-535.
5. Casciola-Rosen, L., D. W. Nicholson, T. Chong, K. R. Rowan, N. A. Thornberry, D. K. Miller, and A. Rosen. 1996. Apopain/CPP32 cleaves proteins that are essential for cellular repair: a fundamental principle of apoptotic death. J. Exp. Med. 183:1957-1964.
6. Casciola-Rosen, L. A., G. J. Anhalt, and A. Rosen. 1995. DNA-dependent protein kinase is one of a subset of autoantigens specifically cleaved early during apoptosis. J. Exp. Med. 182:1625-1634.
7. Cheng, E. H.-Y., R. J. Clem, D. G. Kirsch, R. Ravi, M. B. Kastan, A. Bedi, K. Ueno, and J. M. Hardwick. Conversion of Bcl-2 to a Bax-like death effector by caspases. Submitted for publication.
8. L. Nature (London) 379:554-556.
9. Cheng, E. H.-Y., J. Nicholas, D. S. Bellows, G. S. Hayward, H.-G. Guo, M. S. Reitz, and J. M. Hardwick. 1997. A Bcl-2 homolog encoded by Kaposi's sarcoma-associated virus, human herpesvirus 8, inhibits apoptosis but does not heterodimerize with Bax or Bak. Proc. Natl. Acad. Sci. USA 94:690-694.
10. Chinnaiyan, A. M., K. Orth, K. O'Rourke, H. Duan, G. G. Poirier, and V. M. Dixit. 1996. Molecular ordering of the cell death pathway. J. Biol. Chem. 271:4573-4577.
11. Clem, R. J., and L. K. Miller. 1993. Apoptosis reduces both the in vitro replication and the in vivo infectivity of a baculovirus. J. Virol. 67:3730-3738.
12. Cryns, V. L., L. Bergeron, H. Zhu, H. Li, and J. Yuan. 1996. Specific cleavage of a-fodrin during Fas- and tumor necrosis factor-induced apoptosis is mediated by an interleukin-1β-converting enzyme/Ced-3 protease distinct from the polv(ADP-ribose) polymerase protease. J. Biol. Chem. 271:31277-31282.
13. Datta, R., H. Kojima, D. Banach, N. J. Bump, R. V. Talanian, E. S. Alnemri, R. R. Weichselbaum, W. W. Wong, and D. W. Kufe. 1997. Activation of a CrmA-insensitive, p35-sensitive pathway in ionizing radiation-induced apoptosis. J. Biol. Chem. 272:1965-1969.
14. De Groot, R. J., W. R. Hardy, Y. Shirako, and J. H. Strauss. 1990. Cleavagesite preferences of Sindbis virus polyproteins containing the nonstructural proteinase: evidence for temporal regulation of polyprotein processing in vivo. EMBO J. 9:2631-2638.
15. Desprès, P., J. W. Griffin, and D. E. Griffin. 1995. Effects of anti-E2 monoclonal antibody on Sindbis virus replication in AT3 cells expressing bcl-2. J. Virol. 69:7006-7014.
16. 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.
17. Duckett, C. S., V. E. Nava, R. W. Gedrich, R. J. Clem, J. L. Van Dongen, M. C. Gilflllan, H. Shiels, J. M. Hardwick, and C. B. Thompson. 1996. A conserved family of apoptosis inhibitors related to the baculovirus iap gene. EMBO J. 15:2685-2694.
18. Emoto, Y., Y. Manome, G. Meinhardt, H. Kisaki, S. Kharbanda, M. Robertson, T. Ghayur, W. W. Wong, R. Kamen, R. Weichselbaum, et al. 1995. Proteolytic activation of protein kinase C delta by an ICE-like protease in apoptotic cells. EMBO J. 14:6148-6156.
19. Gagliardini, V., P.-A. Fernandez, R. K. K. Lee, H. C. A. Drexler, R. J. Rotello, M. C. Fishman, and Y. Yuan. 1994. Prevention of vertebrate neuronal death by the crmA gene. Science 263:826-828.
20. Greidinger, E. L., D. K. Miller, T.-T. Yamin, L. Casciola-Rosen, and A. Rosen. 1996. Sequential activation of three distinct ICE-like activities in Fas-ligated Jurkat cells. FEBS Lett. 390:299-303.
21. Griffin, D. E., B. Levine, W. R. Tyor, P. C. Tucker, and J. M. Hardwick. 1994. Age-dependent susceptibility to fatal encephalitis: alphavirus infection of neurons. Arch. Virol. 9:31-39.
22. Hardy, W. R., and J. H. Strauss. 1988. Processing the nonstructural polyproteins of Sindbis virus: study of the kinetics in vivo by using monospecific antibodies. J. Virol. 62:998-1007.
23. Henderson, S., D. Hue, M. Rowe, C. Dawson, G. Johnson, and A. Rickinson. 1993. Epstein-Barr virus-coded BHRFI protein, a viral homologue of bcl-2, protects human B cells from programmed cell death. Proc. Natl. Acad. Sci. USA 90:8479-8483.
24. Hengartner, M. O., R. E. Ellis, and H. R. Horvitz. 1992. Caenorhabditis elegans gene ced-9 protects cells from programmed cell death. Nature (London) 356:494-499.
25. Henkart, P. A. 1996. ICE family proteases: mediators of all apoptotic cell death? Immunity 4:195-201.
26. Komiyama, T., C. A. Ray, D. J. Pickup, A. D. Howard, N. A. Thornberry, E. P. Peterson, and G. Salvesen. 1994. Inhibition of the interleukin-1 beta converting enzyme by the cowpox virus sepin CrmA. An example of cross-class inhibition. J. Biol. Chem. 269:19331-19337.
27. Kuida, K., T. S. Zheng, S. Na, C. Kuan, D. Yang, H. Karasuyama, P. Rakic, and R. A. Flavell. 1996. Decreased apoptosis in the brain and premature lethality in CPP-32 deficient mice. Nature (London) 384:368-372.
28. Kumar, S. 1995. ICE-like proteases in apoptosis. Trends Biochem. Sci. 20:198-202.
29. Lazebnik, Y. A., S. H. Kaufmann, S. Desnoyers, G. G. Poirier, and W. C. Earnshaw. 1994. Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature (London) 371:346-347.
30. Lazebnik, Y. A., A. Takahashi, R. D. Moir, R. D. Goldman, G. G. Poirier, S. H. Kaufmann, and W. C. Earnshaw. 1995. Studies of the lamin proteinase reveal multiple parallel biochemical pathways during apoptotic execution. Proc. Natl. Acad. Sci. USA 92:9042-9046.
31. 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.
32. Levine, B., J. M. Hardwick, and D. E. Griffin. 1994. Persistence of alphavirus in vertebrate hosts. Trends Microbiol. 2:25-28.
33. 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 (London) 361:739-742.
34. Lewis, J., S. L. Wesselingh, D. E. Griffin, and J. M. Hardwick. 1996. Alpha-virus-induced apoptosis in mouse brains correlates with neurovirulence. J. Virol. 70:1828-1835.
35. Liu, X., C. N. Kim, J. Pohl, and X. Wang. 1996. Purification and characterization of an interleukin-1β-converting enzyme family protease that activates cysteine protease P32 (CPP32). J. Biol. Chcm. 271:13371-13376.
36. Liu, X., H. Zou, C. Slaughter, and X. Wang. 1997. DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89:175-184.
37. Martin, S. J., and D. R. Green. 1995. Protease activation during apoptosis: death by a thousand cuts? Cell 82:349-352.
38. Martin, S. J., G. A. O'Brien, W. K. Nishioka, A. J. McGahon, A. Mahboubi, T. C. Saido, and D. R. Green. 1995. Proteolysis of fodrin (non-erythroid spectrin) during apoptosis. J. Biol. Chem. 270:6425-6428.
39. Miura, M., R. M. Friedlander, and J. Yuan. 1995. Tumor necrosis factor-induced apoptosis is mediated by a CrmA-sensitive cell death pathway. Proc. Natl. Acad. Sci. USA 92:8318-8322.
40. Miura, M., and J. Yuan. 1996. Regulation of programmed cell death by interleukin-1 beta-converting enzyme family of proteases. Adv. Exp. Med. Biol. 389:165-172.
41. Muzio, M., A. M. Chinnaiyan, F. C. Kischkel, K. O'Rourke, A. Shevchenko, J. Ni, C. Scaffidi, J. D. Bretz, M. Zhang, R. Gentz, M. Mann, P. H. Krammer, M. E. Peter, and V. M. Dixit. 1996. FLICE, a novel FADD-homologous ICE/CED-3-like protease. is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell 85:817-827.
42. Muzio, M., G. S. Salvesen, and V. M. Dixit. 1997. FLICE induced apoptosis in a cell-free system. J. Biol. Chem. 272:2952-2956.
43. Nava, V. E., E. H.-Y. Cheng, M. Veliuona, S. Zou, R. J. Clem, M. L. Mayer, and J. M. Hardwick. 1997. Herpesvirus saimiri encodes a functional homolog of the human bcl-2 oncogene. J. Virol. 71:4118-4122.
44. Nava, V. E., and J. M. Hardwick. Unpublished data.
45. Nicholson, D. W., A. Ali, N. A. Thornberry, J. P. Vaillancourt, C. K. Ding, M. Gallant, Y. Gareau, P. R. Griffin, M. Labelle, Y. A. Lazebnik, N. A. Munday, S. M. Raju, M. E. Smulson, T.-T. Yamin, V. L. Yu, and D. K. Miller. 1995. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature (London) 376:37-43.
46. Olsen, C. W., J. C. Kehren, N. R. Dybdahl-Sissoko, and V. S. Hinshaw. 1996. bcl-2 alters influenza virus yield, spread, and hemagglutinin glycosylation. J. Virol. 70:663-666.
47. Orth, K., K. O'Rourke, G. S. Salvesen, and V. M. Dixit. 1996. Molecular ordering of apoptotic mammalian CED-3/ICE-like proteases. J. Biol. Chem. 271:20977-20980.
48. Rao, L., D. Perez, and E. White. 1996. Lamin proteolysis facilitates nuclear events during apoptosis. J. Cell Biol. 135:1441-1455.
49. Ray, C. A., R. A. Black, S. R. Kronheim, T. A. Greenstreet, P. R. Sleath, G. S. Salvesen, and D. J. Pickup. 1992. Viral inhibition of inflammation: cowpox virus encodes an inhibitor of the interleukin-1-beta converting enzyme. Cell 69:597-604.
50. Ray, C. A., and D. J. Pickup. 1996. The mode of death of pig kidney cells infected with cowpox virus is governed by the expression of the crmA gene. Virology 217:384-391.
51. Rosen, A., and L. Casciola-Rosen. 1997. Macromolecular substrates for the ICE-like proteases during apoptosis. J. Cell. Biochem. 64:50-54.
52. Scallan, M. F., T. E. Allsopp, and J. K. Fazakerley. 1997. bcl-2 acts early to restrict Semliki Forest virus replication and delays virus-induced programmed cell death. J. Virol. 71:1583-1590.
53. Shaham, S., and H. R. Horvitz. 1996. An alternatively spliced C. elegans ced-4 RNA encodes a novel cell death inhibitor. Cell 86:201-208.
54. Srinivasula, S. M., M. Ahmad, T. Fernandes-Alnemri, G. Litwack, and E. S. Alnemri. 1996. Molecular ordering of the Fas-apoptotic pathway: the Fas/APO-1 protease Mch5 is a CrmA-inhibitable protease that activates multiple Ced-3/ICE-like cysteine proteases. Proc. Natl. Acad. Sci. USA 93:14486-14491.
55. Strack, P. R., M. W. Frey, C. J. Rizzo, B. Cordova, H. J. George, R. Meade, S. P. Ho, J. Corman, R. Tritch, and B. D. Korant. 1996. Apoptosis mediated by HIV protease is preceded by cleavage of Bcl-2. Proc. Natl. Acad. Sci. USA 93:9571-9576.
56. Strauss, J. H., and E. G. Strauss. 1994. The alphaviruses: gene expression, replication and evolution. Microbiol. Rev. 58:491-562.
57. Tan, X. Q., S. J. Martin, D. R. Green, and J. Y. J. Wang. 1997. Degradation of retinoblastoma protein in tumor necrosis factor- and CD95-induced cell death. J. Biol. Chem. 272:9613-9616.
58. Tewari M., L. T. Quan, K. O'Rourke, S. Desnoyers, Z. Zeng, D. R. Beidler, G. G. Poirier, G. S. Salvesen, and V. M. Dixit. 1995. Yama/CPP32β, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81:1-20.
59. Thornberry, N. A., H. G. Bull, J. R. Calaycay, K. T. Chapman, A. D. Howard, M. J. Kostura, D. K. Miller, S. M. Molineaux, J. R. Weidner, J. Aunins, K. O. Elliston, J. M. Ayala, F. J. Casano, J. Chin, G. J.-F. Ding, L. A. Egger, E. P. Gaffhey, G. Limjuco, O. C. Palyha, S. M. Raju, A. M. Rolando, J. P. Salley, T.-T. Yamin, T. D. Lee, J. E. Shively, M. MacCross, R. A. Mumford, J. A. Schmidt, and M. J. Tocci. 1992. A novel heterodimeric cysteine protease is required for interleukin-1-beta processing in monocytes. Nature (London) 356:768-774.
60. Trgovcich, J., K. Ryman, P. Extrom, C. Eldridge, J. F. Aronson, and R. E. Johnston. 1997. Sindbis virus infection of neonatal mice results in a severe stress response. Virology 227:234-238.
61. Ubol, S., S. Park, I. Budihardjo, S. Desnoyers, M. H. Montrose, G. G. Poirier, S. H. Kaufmann, and D. E. Griffin. 1996. Temporal changes in chromatin, intracellular calcium, and poly(ADP-ribose) polymerase during Sindbis virus-induced apoptosis of neuroblastoma cells. J. Virol. 70:2215-2220.
62. 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.
63. Vincenz, C., and V. M. Dixit. 1997. Fas-associated death domain protein interleukin-1β-converting enzyme 2 (FLICE2), an ICE/Ced-3 homologue, is proximally involved in CD95- and p55-mediated death signaling. J. Biol. Chem. 272:6578-6583.
64. Wesselingh, S. L., B. Levine, R. J. Fox, S. Choi, and D. E. Griffin. 1994. Intracerebral cytokine mRNA expression during fatal and nonfatal alphavirus encephalitis suggests a predominant type 2 T cell response. J. Immunol. 152:1289-1297.
65. White, E. 1994. Function of the adenovirus E1B oncogene in infected and transformed cells. Semin. Virol. 5:341-348.
66. White, E. 1996. Life, death, and the pursuit of apoptosis. Genes Dev. 10:1-15.
67. Yuan, J., S. Shaham, S. Ledoux, H. M. Ellis, and H. R. Horvitz. 1993. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1-beta-converting enzyme. Cell 75:641-652.
68. Zhivotovsky, B., A. Gahm, M. Ankarcrona, P. Nicotera, and S. Orrenius. 1995. Multiple proteases are involved in thymocyte apoptosis. Exp. Cell Res. 221:404-412.
69. Zhou, Q., S. Snipas, K. Orth, M. Muzio, V. M. Dixit, and G. S. Salvesen. 1997. Target protease specificity of the viral serpin CrmA. J. Biol. Chem. 272:7797-7800.