The bovine viral diarrhea virus (BVDV) NS3 protein, when expressed alone in mammalian cells, induces apoptosis which correlates with caspase-8 and caspase-9 activation

Veterinary Research

Volumn 36, Issue 2, 2005, Pages 213-227

  St Louis, Marie Claude ^a   Massie, Bernard ^b,c,d   Archambault, Denis ^a  

^a UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^c INRS INSTITUT ARMAND FRAPPIER   (Canada)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Apoptosis; Bovine viral diarrhea virus; Caspases; NS3 protein

Indexed keywords

ADENOVIRUS VECTOR; CASPASE 8; CASPASE 9; CYTOCHROME C; DNA FRAGMENT; NONSTRUCTURAL PROTEIN 3; RIBONUCLEOTIDE REDUCTASE; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

ANIMAL CELL; APOPTOSIS; ARTICLE; CATTLE DISEASE; CHROMATIN CONDENSATION; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOPATHOGENIC EFFECT; ENZYME ACTIVATION; FLOW CYTOMETRY; GENE EXPRESSION; GENETIC CODE; HERPES SIMPLEX VIRUS 2; IMMUNOBLOTTING; IN VITRO STUDY; NICK END LABELING; NONHUMAN; NUCLEOTIDE SEQUENCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; VIRUS INFECTION; VIRUS STRAIN; WESTERN BLOTTING;

BOVINAE; BOVINE VIRAL DIARRHEA VIRUS 1; HERPES; HUMAN HERPESVIRUS 2; MAMMALIA;

EID: 14844346931     PISSN: 09284249     EISSN: None     Source Type: Journal    
DOI: 10.1051/vetres:2004059     Document Type: Article

References (48)

1. Abed Y., St-Laurent G., Zhang H., Jacobs R.M., Archambault D., Development of a Western blot assay for detection of bovine immunodeficiency-like virus using capsid and transmembrane envelope proteins expressed from recombinant baculovirus, Clin. Diagn. Lab. Immunol. 6 (1999) 68-172.
2. Adler B., Adler H., Pfister H., Jungi T.W., Peterhans E., Macrophages infected with cytopathic bovine viral diarrhoea virus release a factor(s) capable of priming uninfected macrophages for activation-induced apoptosis, J. Virol. 71 (1997) 3255-3258.
3. Archambault D., St-Laurent G., Induction of apoptosis by equine arteritis virus infection, Virus Genes 20 (2000) 143-147.
4. Archambault D., Béliveau C., Couture Y., Carman S., Clinical response and immunomodulation following experimental challenge of calves with type 2 noncytopathogenic bovine viral diarrhea virus, Vet. Res. 31 (2000) 215-227.
5. Bendfeldt S., Grummer B., Greiser-Wilke I., No caspase activation but overexpression of Bcl-2 in bovine cells infected with noncytopathic bovine virus diarrhoea virus, Vet. Microbiol. 96 (2003) 313-326.
6. Bitzer M., Armeanu S., Prinz F., Ungerechts G., Wybranietz: W., Spiegel M., Bernlohr C., Cecconi F., Gregor M., Neubert W.J., Schulze-Osthoff K., Lauer U.M., Caspase-8 and Apaf-1-independent caspase-9 activation in Sendai virus-infected cells, J. Biol. Chem. 277 (2002) 29817-29824.
7. Breckenridge D.G., Nguyen M., Kuppig S., Reth M., Shore G.C., The procaspase-8 isoform, procaspase-8L, recruited to the BAP31 complex at the endoplasmic reticulum, Proc. Natl. Acad. Sci. USA 99 (2002) 4331-4336.
8. Bronfman M., Loyola G., Koenig C.S., Isolation of intact organelles by differential centrifugation of digitonin-treated hepatocytes using a table Eppendorf centrifuge, Anal. Biochem. 255 (1998) 252-256.
9. ms of pestiviruses induces apoptosis in lymphocytes of several species, J. Virol. 71 (1997) 6692-6696.
10. Drapier J.C., Hirling H., Wietzerbin J., Kaldy P., Kuhn L.C., Biosynthesis of nitric oxide activates iron regulatory factor in macrophages, EMBO J. 12 (1993) 3643-3649.
11. Grummer B., Bendfeldt S., Wagner B., Greiser-Wilke I., Induction of the intrinsic apoptotic pathway in cells infected with cytopathic bovine virus diarrhoea virus, Virus Res. 90 (2002) 143-153.
12. Gurbuxani S., Schmitt E., Cande C., Parcellier A., Hammann A., Daugas E., Kouranti I., Spahr C., Pance A., Kroemer G., Garrido C., Heat shock protein 70 binding inhibits the nuclear import of apoptosis-inducing factor, Oncogene 22 (2003) 6669-6678.
13. Hay S., Kannourakis G., A time to kill: viral manipulation of the cell death program, J. Gen. Virol. 83 (2002) 1547-1564.
14. Hoff H.S., Donis R.O., Induction of apoptosis and cleavage of poly(ADP-ribose) polymerase by cytopathic bovine viral diarrhea virus infection, Virus Res. 49 (1997) 101-113.
15. Jani A., Lochmuller H., Acsadi G., Simoneau M., Huard J., Garnier A., Karpati G., Massie B., Generation, validation, and large scale production of adenoviral recombinants with large size inserts such as 6.3 kb human distrophin cDNA, J. Virol. Methods 64 (1997) 111-124.
16. Jeronimo C., Archambault D., Importance of M-protein C terminus as substrate antigen for serodetection of equine arteritis virus infection, Clin. Diagn. Lab. Immunol. 9 (2002) 698-703.
17. Jimbo A., Fujita E., Kouroku Y., Ohnishi J., Inohara N., Kuida K., Sakamaki K., Yonehara S., Momoi T., ER stress induces caspase-8 activation, stimulating cytochrome c release and caspase-9 activation, Exp. Cell Res. 283 (2003) 156-166.
18. Jordan R., Wang L., Graczyk T.M., Block T.M., Romano P.R., Replication of a cytopathic strain of bovine viral diarrhea virus activates PERK and induces endoplasmic reticulum stress-mediated apoptosis of MDBK cells, J. Virol. 76 (2002) 9588-9599.
19. Jungi T.W., Schweizer M., Perler L., Peterhans E., Supernatants of virus-infected macrophages prime uninfected macrophages for lipopolysaccharide-induced apoptosis by both interferon-dependent and independent mechanism, Pathobiology 67 (1999) 294-297.
20. Kheyar A., Martin S., St-Laurent G., Timoney P.J., McCollum W.H., Archambault D., Expression cloning and humoral immune response to the nucleocapsid and membrane proteins of equine arteritis virus, Clin. Diagn. Lab. Immunol. 4 (1997) 648-652.
21. Klein S.D., Brüne B., Heat-shock protein 70 attenuates nitric oxide-induced apoptosis in RAW macrophages by preventing cytochrome c release, Biochem J. 362 (2002) 635-641.
22. Kummerer B.M., Tautz N., Becher P., Thiel H.-J., Meyers G., The genetic basis for cytopathogenicity of pestiviruses, Vet. Microbiol. 77 (2000) 117-128.
23. Kyte J., Doolittle R.F., A simple method for dysplaying the hydropathic character of a protein, J. Mol. Biol. 5 (1982) 105-132.
24. Langelier Y., Bergeron S., Chabaud S., Lippens J., Guilbault C., Sasseville A.M., Denis S., Mosser D.D., Massie B., The R1 subunit of herpes simplex virus ribonucleotide reductase protects cells against apoptosis at, or upstream of, caspase-8 activation, J. Gen. Virol. 83 (2002) 2779-2789.
25. Massie B., Couture F., Lamoureux L., Mosser D.D., Guilbault C., Jolicoeur P., Bélanger F., Langelier Y., Inducible overexpression of a toxic protein by an adenovirus vector with a tetracycline-regulatable expression cassette, J. Virol. 72 (1998) 2289-2298.
26. Massie B., Mosser D.D., Koutroumanis M., Vitté-Mony I, Lamoureux L., Couture F., Paquet L., Guilbault C., Dionne J., Chala D., Jolicoeur P., Langelier Y., New adenovirus vectors for protein production and gene transfer, Cytotechnology 28 (1998) 53-64.
27. Mendez E., Ruggli N., Collett M.S., Rice C.M., Infectious bovine viral diarrhea virus (strain NADL) RNA from stable cDNA clones: a cellular insert determines NS3 production and viral cytopathogenicity, J. Virol. 72 (1998) 4737-4745.
28. Meyers G., Thiel H.-J., Molecular characterization of pestiviruses, Adv. Virus Res. 47 (1996) 53-118.
29. Mignotte B., Vayssiere J.L., Mitochondria and apoptosis, Eur. J. Biochem. 252 (1998) 1-15.
30. Mosser D.D., Caron A.W., Bourget L., Meriin A.B., Sherman M.Y., Morimoto R.I., Massie B., The chaperone function of hsp70 is required for protection against stress-induced apoptosis, Mol. Cell. Biol. 20 (2000) 7146-7159.
31. Nakagawa T., Zhu H., Morishima N., Li E., Xu J., Yankner B.A., Yuan J., Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta, Nature 403 (2000) 98-103.
32. Nicholson D.W., Caspase structure, proteolytic substrates, and function during apoptotic cell death, Cell Death Differ. 6 (1999) 1028-1042.
33. Pataer A., Chadas S., Hunt K.K., Roth, J.A., Swisher S.G., Adenoviral melanoma differentiation-associated gene 7 induces apoptosis in lung cancer cells through mitochondrial permeability transition-independent cytochrome c release, J. Thorac. Cardiovasc. Surg. 125 (2003) 1328-1335.
34. Perler L., Schweizer M., Jungi T.W., Peterhans E., Bovine viral diarrhoea virus and bovine herpesvirus- 1 prime uninfected macrophages for lipopolysaccharide-triggered apoptosis by interferon-dependent and -independent pathways, J. Gen. Virol. 81 (2000) 881-887.
35. Prikbod'ko G.G., Prikhod'ko E.A., Pletnev A.G., Cohen J.I., Langat flavirvirus protease NS3 binds caspase-8 and induces apoptosis, J. Virol. 76 (2002) 5701-5710.
36. Rao R.V., Hermel E., Castro-Obregon S., del Rio G., Ellerby L.M., Ellerby H.M., Bredesen D.E., Coupling endoplasmic reticulum stress to the cell death program. Mechanism of caspase activation, J. Biol. Chem. 276 (2001) 33869-33874.
37. Rasper D.M., Vaillancourt J.P., Hadano S., Houtzager V.M., Seiden I., Keen S.L., Tawa P., Xanthoudakis S., Nasir J., Martindale D., Koop B.F., Peterson E.P., Thornberry N.A., Huang J., MacPherson D.P., Black S.C., Hornung F., Lenardo M.J., Hayden M,R., Roy S., Nicholson D.W., Cell death attenuation by "Usurpin", a mammalian DED-caspase homologue that precludes caspase-8 recruitment and activation by the CD-95 (Fas, APO-1) receptor complex, Cell Death Differ. 5 (1998) 271-288.
38. Scaffidi C., Krammer P.H., Peter M.E., Isolation and analysis of components of CD95 (APO-1/Fas) death-inducing signaling complex, Methods 17 (1999) 287-291.
39. Schulze-Osthoff K., Ferrari D., Los M., Wesselberg S., Peter M.E., Apoptosis signaling by death receptors, Eur. J. Biochem. 254 (1998) 439-459.
40. Schweizer M., Peterhans E., Oxydative stress in cells infected with bovine viral diarrhoea virus: a crucial step in the induction of apoptosis, J. Gen. Virol. 80 (1999) 1147-1155.
41. Shi Y., Mechanisms of caspase activation and inhibition during apoptosis, Mol. Cell 9 (2002) 459-470.
42. St-Laurent G., Morin G., Archambault D., Detection of equine arteritis virus following amplification of structural and nontructural viral genes by reverse transcription-PCR, J. Clin. Microbiol. 32 (1994) 658-665.
43. Thiel H.-J., Plagemann P.G.W., Moennig V., Pestiviruses, in: Fields B.N., Knipe D.M., Hewley P.M. (Eds.), Fields virology, Lippincott-Raven Publishers, 1996, pp. 1059-1073.
44. Vassilev V.B., Donis R.O., Bovine viral diarrhea virus induced apoptosis correlates with increased intracellular viral RNA accumulation, Virus Res. 69 (2000) 95-107.
45. Wolf B.B., Green D.R., Suicidal tendencies: apoptotic cell death by caspase family proteinases, J. Biol. Chem. 274 (1999) 20049-20052.
46. Zhang G., Aldridge S., Clarke M.C., McCauley J.W., Cell death induced by cytopathic bovine viral diarrhoea virus is mediated by apoptosis, J. Gen. Virol. 77 (1996) 1677-1681.
47. Zhang G., Flick-Smith H., McCauley J.W., Differences in membrane association and subcellular distribution between NS2-3 and NS3 of bovine viral diarrhoea virus, Virus Res. 97 (2003) 89-102.
48. Xu J., Mendez E., Caron P.R., Lin C., Murcko M.A., Collett M.S., Rice C.M., Bovine viral diarrhea virus NS3 serine proteinase: polyprotein cleavage sites, cofactor requirements, and molecular model of an enzyme essential for pestivirus replication, J. Virol. 71 (1997) 5312-5322.