Cytotoxicity of ORF3 proteins from a nonpathogenic and a pathogenic porcine circovirus

Journal of Virology

Volumn 84, Issue 21, 2010, Pages 11440-11447

  Chaiyakul, Mark ^a,b   Hsu, Karolynn ^a   Dardari, Rkia ^a   Marshall, Frank ^a,c   Czub, Markus ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c Marshall Swine Health Services   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CASPASE; GREEN FLUORESCENT PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PORCINE CIRCOVIRUS TYPE 1 OPEN READING FRAME 3 PROTEIN; PORCINE CIRCOVIRUS TYPE 2 OPEN READING FRAME 3 PROTEIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR; VIRUS PROTEIN;

APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CELL DEATH; CELL STRAIN HEK293; CELL VIABILITY; CIRCOVIRUS; CYTOTOXICITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; VIRUS VIRULENCE; ANIMAL; CELL LINE; CELL SHAPE; CHEMISTRY; CIRCOVIRIDAE INFECTION; PATHOGENICITY; PATHOLOGY; SWINE; SWINE DISEASE; TOXICITY; VIROLOGY;

PORCINE CIRCOVIRUS; PORCINE CIRCOVIRUS 2; SUIDAE;

ANIMALS; APOPTOSIS; CELL LINE; CELL SHAPE; CIRCOVIRIDAE INFECTIONS; CIRCOVIRUS; HUMANS; SWINE; SWINE DISEASES; VIRAL PROTEINS;

EID: 77957939289     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01030-10     Document Type: Article

References (35)

1. Andree, H. A., C. P. Reutelingsperger, R. Hauptmann, H. C. Hemker, W. T. Hermens, and G. M. Willems. 1990. Binding of vascular anticoagulant alpha (VAC alpha) to planar phospholipid bilayers. J. Biol. Chem. 265:4923-4928.
2. Boulares, A. H., A. G. Yakovlev, V. Ivanova, B. A. Stoica, G. Wang, S. Iyer, and M. Smulson. 1999. Role of poly(ADP-ribose) polymerase (PARP) cleavage in apoptosis. Caspase 3-resistant PARP mutant increases rates of apoptosis in transfected cells. J. Biol. Chem. 274:22932-22940.
3. Duvall, E., A. H. Wyllie, and R. G. Morris. 1985. Macrophage recognition of cells undergoing programmed cell death (apoptosis). Immunology 56:351-358.
4. Ellis, J., L. Hassard, E. Clark, J. Harding, G. Allan, P. Willson, J. Strokappe, K. Martin, F. McNeilly, B. Meehan, D. Todd, and D. Haines. 1998. Isolation of circovirus from lesions of pigs with postweaning multisystemic wasting syndrome. Can. Vet. J. 39:44-51.
5. Finsterbusch, T., and A. Mankertz. 2009. Porcine circoviruses - small but powerful. Virus Res. 143:177-183.
6. Harding, J. C., C. D. Baker, A. Tumber, K. A. McIntosh, S. E. Parker, D. M. Middleton, J. E. Hill, J. A. Ellis, and S. Krakowka. 2008. Porcine circovirus-2 DNA concentration distinguishes wasting from nonwasting pigs and is correlated with lesion distribution, severity, and nucleocapsid staining intensity. J. Vet. Diagn. Invest. 20:274-282.
7. Hattermann, K., C. Roedner, C. Schmitt, T. Finsterbusch, T. Steinfeldt, and A. Mankertz. 2004. Infection studies on human cell lines with porcine circovirus type 1 and porcine circovirus type 2. Xenotransplantation 11:284-294. (Pubitemid 38623066)
8. Juhan, N. M., T. LeRoith, T. Opriessnig, and X. J. Meng. 2010. The open reading frame 3 (ORF3) of porcine circovirus type 2 (PCV2) is dispensable for virus infection but evidence of reduced pathogenicity is limited in pigs infected by an ORF3-null PCV2 mutant. Virus Res. 147:60-66.
9. Karuppannan, A. K., M. H. Jong, S. H. Lee, Y. Zhu, M. Selvaraj, J. Lau, Q. Jia, and J. Kwang. 2009. Attenuation of porcine circovirus 2 in SPF piglets by abrogation of ORF3 function. Virology 383:338-347.
10. Kiupel, M., G. W. Stevenson, E. J. Galbreath, A. North, H. HogenEsch, and S. K. Mittal. 2005. Porcine circovirus type 2 (PCV2) causes apoptosis in experimentally inoculated BALB/c mice. BMC Vet. Res. 1:7.
11. Krakowka, S., J. Ellis, F. McNeilly, B. Meehan, M. Oglesbee, S. Alldinger, and G. Allan. 2004. Features of cell degeneration and death in hepatic failure and systemic lymphoid depletion characteristic of porcine circovirus-2-associated postweaning multisystemic wasting disease. Vet. Pathol. 41:471-481.
12. Kroemer, G., L. Galluzzi, P. Vandenabeele, J. Abrams, E. S. Alnemri, E. H. Baehrecke, M. V. Blagosklonny, W. S. El-Deiry, P. Golstein, D. R. Green, M. Hengartner, R. A. Knight, S. Kumar, S. A. Lipton, W. Malorni, G. Nuñez, M. E. Peter, J. Tschopp, J. Yuan, M. Piacentini, B. Zhivotovsky, and G. Melino. 2009. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 16:3-11. (Pubitemid 41553979)
13. Liu, J., I. Chen, Q. Du, H. Chua, and J. Kwang. 2006. The ORF3 protein of porcine circovirus type 2 is involved in viral pathogenesis in vivo. J. Virol. 80:5065-5073.
14. Liu, J., I. Chen, and J. Kwang. 2005. Characterization of a previously unidentified viral protein in porcine circovirus type 2-infected cells and its role in virus-induced apoptosis. J. Virol. 79:8262-8274.
15. Lucas, K. C., D. A. Hart, and R. W. Becker. 2010. Porcine proximal tubular cells (LLC-PK1) are able to tolerate high levels of lithium chloride in vitro: assessment of the influence of 1-20 mM LiCl on cell death and alterations in cell biology and biochemistry. Cell Biol. Int. 34:225-233.
16. Mandrioli, L., G. Sarli, S. Panarese, S. Baldoni, and P. S. Marcato. 2004. Apoptosis and proliferative activity in lymph node reaction in postweaning multisystemic wasting syndrome (PMWS). Vet. Immunol. Immunopathol. 97:25-37.
17. Mankertz, A., J. Mankertz, K. Wolf, and H. J. Buhk. 1998. Identification of a protein essential for replication of porcine circovirus. J. Gen. Virol. 79: 381-384.
18. Martin, S. J., C. P. Reutelingsperger, A. J. McGahon, J. A. Rader, R. C. van Schie, D. M. LaFace, and D. R. Green. 1995. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med. 182:1545-1556.
19. Morris, R. G., A. D. Hargreaves, E. Duvall, and A. H. Wyllie. 1984. Hormone- induced cell death. 2. Surface changes in thymocytes undergoing apoptosis. Am. J. Pathol. 115:426-436.
20. 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 376:37-43.
21. Opriessnig, T., X. J. Meng, and P. G. Halbur. 2007. Porcine circovirus type 2 associated disease: update on current terminology, clinical manifestations, pathogenesis, diagnosis, and intervention strategies. J. Vet. Diagn. Invest. 19:591-615.
22. Raynal, P., and H. B. Pollard. 1994. Annexins: the problem of assessing the biological role for a gene family of multifunctional calcium- and phospholipid- binding proteins. Biochim. Biophys. Acta 1197:63-93.
23. Resendes, A. R., N. Majó, J. Segalés, E. Mateu, M. Calsamiglia, and M. Domingo. 2004. Apoptosis in lymphoid organs of pigs naturally infected by porcine circovirus type 2. J. Gen. Virol. 85:2837-2844.
24. Schotte, P., W. Declercq, S. Van Huffel, P. Vandenabeele, and R. Beyaert. 1999. Non-specific effects of methyl ketone peptide inhibitors of caspases. FEBS Lett. 442:117-121. (Pubitemid 29065390)
25. Shen, H. G., J. Y. Zhou, X. Zhang, Z. Y. Huang, J. L. He, and Y. Yan. 2009. Interference of porcine circovirus type 2 ORF2 immunogenicity by ORF1 and ORF3 mixed DNA immunizations in mice. Virology 393:104-111.
26. Shibahara, T., K. Sato, Y. Ishikawa, and K. Kadota. 2000. Porcine circovirus induces B lymphocyte depletion in pigs with wasting disease syndrome. J. Vet. Med. Sci. 62:1125-1131.
27. Simbulan-Rosenthal, C. M., D. S. Rosenthal, S. Iyer, H. Boulares, and M. E. Smulson. 1999. Involvement of PARP and poly(ADP-ribosyl)ation in the early stages of apoptosis and DNA replication. Mol. Cell. Biochem. 193:137-148.
28. Tait, J. F., D. Gibson, and K. Fujikawa. 1989. Phospholipid binding properties of human placental anticoagulant protein-I, a member of the lipocortin family. J. Biol. Chem. 264:7944-7949.
29. 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/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81:801-809.
30. Thiagarajan, P., and J. F. Tait. 1990. Binding of annexin V/placental anticoagulant protein I to platelets. Evidence for phosphatidylserine exposure in the procoagulant response of activated platelets. J. Biol. Chem. 265:17420-17423.
31. Timmusk, S., P. Wallgren, I. M. Brunborg, F. H. Wikström, G. Allan, B. Meehan, M. McMenamy, F. McNeilly, L. Fuxler, K. Belák, D. Põdersoo, T. Saar, M. Berg, and C. Fossum. 2008. Phylogenetic analysis of porcine circovirus type 2 (PCV2) pre- and post-epizootic postweaning multisystemic wasting syndrome (PMWS). Virus Genes 36:509-520.
32. Tischer, I., H. Gelderblom, W. Vettermann, and M. A. Koch. 1982. A very small porcine virus with circular single-stranded DNA. Nature 295:64-66.
33. Tischer, I., R. Rasch, and G. Tochtermann. 1974. Characterization of papovavirus- and picornavirus-like particles in permanent pig kidney cell lines. Zentralbl. Bakteriol. Orig. A 226:153-167.
34. Yang, Y., S. Zhao, and J. Song. 2004. Caspase-dependent apoptosis and -independent poly(ADP-ribose) polymerase cleavage induced by transforming growth factor beta1. Int. J. Biochem. Cell Biol. 36:223-234.
35. Zhang, W. V., M. Jüllig, A. R. Connolly, and N. S. Stott. 2005. Early gene response in lithium chloride induced apoptosis. Apoptosis 10:75-90.