ORF3 of porcine circovirus 2 enhances the in vitro and in vivo spread of the of the virus

Virology

Volumn 410, Issue 1, 2011, Pages 248-256

  Karuppannan, Anbu K ^a   Kwang, Jimmy ^a,b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Apoptosis; ORF3; Pathogenesis; PCV2; Virus spread

Indexed keywords

CASPASE 3; CD11B ANTIGEN; RNA DIRECTED RNA POLYMERASE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CIRCOVIRIDAE INFECTION; CIRCOVIRUS; CONTROLLED STUDY; ENZYME ACTIVITY; EXPERIMENTAL INFECTION; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MOUSE; NONHUMAN; OPEN READING FRAME; PHAGOCYTOSIS; PORCINE CIRCOVIRUS 2; PRIORITY JOURNAL; VIRAL PHENOMENA AND FUNCTIONS; VIREMIA; VIRUS CELL INTERACTION; VIRUS REPLICATION; VIRUS SPREADING;

ANIMALS; CASPASES; CELL LINE; CELLS, CULTURED; CIRCOVIRIDAE INFECTIONS; CIRCOVIRUS; GENE EXPRESSION REGULATION, VIRAL; GENOME, VIRAL; MACROPHAGES; MICE; MICE, INBRED BALB C; SWINE; SWINE DISEASES; TIME FACTORS; VIRAL PROTEINS; VIRUS RELEASE;

MUS; PORCINE CIRCOVIRUS 2;

EID: 78650722964     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.11.009     Document Type: Article

References (60)

1. Allan G.M., McNeilly F., Kennedy S., Daft B., Clarke E.G., Ellis J.A., Haines D.M., Meehan B.M., Adair B.M. Isolation of porcine circovirus-like viruses from pigs with a wasting disease in the USA and Europe. J. Vet. Diagn. Invest. 1998, 10(1):3-10.
2. Allan G.M., McNeilly F., Ellis J., Krakowka S., Botner A., McCullough K., Nauwynck H., Kennedy S., Meehan B., Charreyre C. PMWS: experimental model and co-infections. Vet. Microbiol. 2004, 98(2):165-168.
3. An D.J., Song D.S., Park B.K. Systemic cytokine profiles of mice vaccinated with naked DNAs encoding six open reading frame antigens of porcine circovirus type 2 (PCV2). Res. Vet. Sci. 2008, 85(3):503-509.
4. Chang H.W., Jeng C.R., Lin T.L., Liu J.J., Chiou M.T., Tsai Y.C., Chia M.Y., Jan T.R., Pang V.F. Immunopathological effects of porcine circovirus type 2 (PCV2) on swine alveolar macrophages by in vitro inoculation. Vet. Immunol. Immunopathol. 2006, 110(3-4):207-219.
5. Cheung A.K. Transcriptional analysis of porcine circovirus type 2. Virology 2003, 305(1):168-180.
6. Cheung A.K., Lager K.M., Kohutyuk O.I., Vincent A.L., Henry S.C., Baker R.B., Rowland R.R., Dunham A.G. Detection of two porcine circovirus type 2 genotypic groups in United States swine herds. Arch. Virol. 2007, 152(5):1035-1044.
7. Cortey M., Pileri E., Sibila M., Pujols J., Balasch M., Plana J., Segales J. Genotypic shift of porcine circovirus type 2 from PCV-2a to PCV-2b in Spain from 1985 to 2008. Vet. J. 2010, doi:10.1016/j.tvjl.2009.12.023 (ISSN 1090-0233).
8. Darwich L., Segales J., Domingo M., Mateu E. Changes in CD4(+), CD8(+), CD4(+) CD8(+), and immunoglobulin M-positive peripheral blood mononuclear cells of postweaning multisystemic wasting syndrome-affected pigs and age-matched uninfected wasted and healthy pigs correlate with lesions and porcine circovirus type 2 load in lymphoid tissues. Clin. Diagn. Lab. Immunol. 2002, 9(2):236-242.
9. Darwich L., Segales J., Mateu E. Pathogenesis of postweaning multisystemic wasting syndrome caused by porcine circovirus 2: an immune riddle. Arch. Virol. 2004, 149(5):857-874.
10. Devireddy L.R., Jones C.J. Activation of caspases and p53 by bovine herpesvirus 1 infection results in programmed cell death and efficient virus release. J. Virol. 1999, 73(5):3778-3788.
11. Dey D., Dahl J., Cho S., Benjamin T.L. Induction and bypass of p53 during productive infection by polyomavirus. J. Virol. 2002, 76(18):9526-9532.
12. Dobner T., Horikoshi N., Rubenwolf S., Shenk T. Blockage by adenovirus E4orf6 of transcriptional activation by the p53 tumor suppressor. Science 1996, 272(5267):1470-1473.
13. Ellis J., Hassard L., Clark E., Harding J., Allan G., Willson P., Strokappe J., Martin K., McNeilly F., Meehan B., Todd D., Haines D. Isolation of circovirus from lesions of pigs with postweaning multisystemic wasting syndrome. Can. Vet. J. 1998, 39(1):44-51.
14. Emamaullee J.A., Stanton L., Schur C., Shapiro A.M. Caspase inhibitor therapy enhances marginal mass islet graft survival and preserves long-term function in islet transplantation. Diabetes 2007, 56(5):1289-1298.
15. Erwig L.P., Henson P.M. Clearance of apoptotic cells by phagocytes. Cell Death Differ. 2008, 15(2):243-250.
16. Everett H., McFadden G. Apoptosis: an innate immune response to virus infection. Trends Microbiol. 1999, 7(4):160-165.
17. Finsterbusch T., Mankertz A. Porcine circoviruses-small but powerful. Virus Res. 2009, 143(2):177-183.
18. Gagnon C.A., Tremblay D., Tijssen P., Venne M.H., Houde A., Elahi S.M. The emergence of porcine circovirus 2b genotype (PCV-2b) in swine in Canada. Can. Vet. J. 2007, 48(8):811-819.
19. Gillespie J., Opriessnig T., Meng X.J., Pelzer K., Buechner-Maxwell V. Porcine circovirus type 2 and porcine circovirus-associated disease. J. Vet. Intern. Med. 2009, 23(6):1151-1163.
20. Granja A.G., Nogal M.L., Hurtado C., Salas J., Salas M.L., Carrascosa A.L., Revilla Y. Modulation of p53 cellular function and cell death by African swine fever virus. J. Virol. 2004, 78(13):7165-7174.
21. Harding J.C., Baker C.D., Tumber A., McIntosh K.A., Parker S.E., Middleton D.M., Hill J.E., Ellis J.A., Krakowka S. 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. 2008, 20(3):274-282.
22. Jeurissen S.H., Wagenaar F., Pol J.M., van der Eb A.J., Noteborn M.H. Chicken anemia virus causes apoptosis of thymocytes after in vivo infection and of cell lines after in vitro infection. J. Virol. 1992, 66(12):7383-7388.
23. Juhan N.M., LeRoith T., Opriessnig T., Meng X.J. 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. 2010, 147(1):60-66.
24. Karuppannan A.K., Jong M.H., Lee S.H., Zhu Y., Selvaraj M., Lau J., Jia Q., Kwang J. Attenuation of porcine circovirus 2 in SPF piglets by abrogation of ORF3 function. Virology 2009, 383(2):338-347.
25. Karuppannan A.K., Liu S., Jia Q., Selvaraj M., Kwang J. Porcine circovirus type 2 ORF3 protein competes with p53 in binding to Pirh2 and mediates the deregulation of p53 homeostasis. Virology 2010, 398(1):1-11.
26. Kim J., Ha Y., Chae C. Potentiation of porcine circovirus 2-induced postweaning multisystemic wasting syndrome by porcine parvovirus is associated with excessive production of tumor necrosis factor-alpha. Vet. Pathol. 2006, 43(5):718-725.
27. Kiupel M., Stevenson G.W., Choi J., Latimer K.S., Kanitz C.L., Mittal S.K. Viral replication and lesions in BALB/c mice experimentally inoculated with porcine circovirus isolated from a pig with postweaning multisystemic wasting disease. Vet. Pathol. 2001, 38(1):74-82.
28. Kiupel M., Stevenson G.W., Galbreath E.J., North A., HogenEsch H., Mittal S.K. Porcine circovirus type 2 (PCV2) causes apoptosis in experimentally inoculated BALB/c mice. BMC Vet. Res. 2005, 1:7.
29. Krakowka S., Ellis J.A., McNeilly F., Ringler S., Rings D.M., Allan G. Activation of the immune system is the pivotal event in the production of wasting disease in pigs infected with porcine circovirus-2 (PCV-2). Vet. Pathol. 2001, 38(1):31-42.
30. Krakowka S., Ellis J.A., McNeilly F., Gilpin D., Meehan B., McCullough K., Allan G. Immunologic features of porcine circovirus type 2 infection. Viral Immunol. 2002, 15(4):567-582.
31. Krakowka S., Ellis J., McNeilly F., Waldner C., Rings D.M., Allan G. Mycoplasma hyopneumoniae bacterins and porcine circovirus type 2 (PCV2) infection: induction of postweaning multisystemic wasting syndrome (PMWS) in the gnotobiotic swine model of PCV2-associated disease. Can. Vet. J. 2007, 48(7):716-724.
32. Ladekjaer-Mikkelsen A.S., Nielsen J., Stadejek T., Storgaard T., Krakowka S., Ellis J., McNeilly F., Allan G., Botner A. Reproduction of postweaning multisystemic wasting syndrome (PMWS) in immunostimulated and non-immunostimulated 3-week-old piglets experimentally infected with porcine circovirus type 2 (PCV2). Vet. Microbiol. 2002, 89(2-3):97-114.
33. Liu J., Chen I., Kwang J. Characterization of a previously unidentified viral protein in porcine circovirus type 2-infected cells and its role in virus-induced apoptosis. J. Virol. 2005, 79(13):8262-8274.
34. Liu J., Chen I., Du Q., Chua H., Kwang J. The ORF3 protein of porcine circovirus type 2 is involved in viral pathogenesis in vivo. J. Virol. 2006, 80(10):5065-5073.
35. Liu J., Zhu Y., Chen I., Lau J., He F., Lau A., Wang Z., Karuppannan A.K., Kwang J. The ORF3 protein of porcine circovirus type 2 interacts with porcine ubiquitin E3 ligase Pirh2 and facilitates p53 expression in viral infection. J. Virol. 2007, 81(17):9560-9567.
36. Lucas M., Stuart L.M., Savill J., Lacy-Hulbert A. Apoptotic cells and innate immune stimuli combine to regulate macrophage cytokine secretion. J. Immunol. 2003, 171:2610-2615.
37. Mandrioli L., Sarli G., Panarese S., Baldoni S., Marcato P.S. Apoptosis and proliferative activity in lymph node reaction in postweaning multisystemic wasting syndrome (PMWS). Vet. Immunol. Immunopathol. 2004, 97(1-2):25-37.
38. Misinzo G., Delputte P.L., Meerts P., Lefebvre D.J., Nauwynck H.J. Porcine circovirus 2 uses heparan sulfate and chondroitin sulfate B glycosaminoglycans as receptors for its attachment to host cells. J. Virol. 2006, 80(7):3487-3494.
39. Nielsen J., Vincent I.E., Botner A., Ladekaer-Mikkelsen A.S., Allan G., Summerfield A., McCullough K.C. Association of lymphopenia with porcine circovirus type 2 induced postweaning multisystemic wasting syndrome (PMWS). Vet. Immunol. Immunopathol. 2003, 92(3-4):97-111.
40. Noteborn M.H., Todd D., Verschueren C.A., de Gauw H.W., Curran W.L., Veldkamp S., Douglas A.J., McNulty M.S., van der E.A., Koch G. A single chicken anemia virus protein induces apoptosis. J. Virol. 1994, 68(1):346-351.
41. + T cells is unaffected by a pan-caspase inhibitor. J. Immunol. 2004, 173(11):6611-6618.
42. O'Dea M.A., Hughes A.P., Davies L.J., Muhling J., Buddle R., Wilcox G.E. Thermal stability of porcine circovirus type 2 in cell culture. J. Virol. Methods 2008, 147(1):61-66.
43. Perez-Martin E., Rovira A., Calsamiglia M., Mankertz A., Rodriguez F., Segales J. A new method to identify cell types that support porcine circovirus type 2 replication in formalin-fixed, paraffin-embedded swine tissues. J. Virol. Methods 2007, 146(1-2):86-95.
44. Resendes A.R., Majo N., Segales J., Mateu E., Calsamiglia M., Domingo M. Apoptosis in lymphoid organs of pigs naturally infected by porcine circovirus type 2. J. Gen. Virol. 2004, 85(Pt 10):2837-2844.
45. Roulston A., Marcellus R.C., Branton P.E. Viruses and apoptosis. Annu. Rev. Microbiol. 1999, 53:577-628.
46. Sanchez R.E., Meerts P., Nauwynck H.J., Ellis J.A., Pensaert M.B. Characteristics of porcine circovirus-2 replication in lymphoid organs of pigs inoculated in late gestation or postnatally and possible relation to clinical and pathological outcome of infection. J. Vet. Diagn. Invest. 2004, 16(3):175-185.
47. Sarkar A., Hall M.W., Exline M., Hart J., Knatz N., Gatson N.T., Wewers M.D. Caspase-1 regulates Escherichia coli sepsis and splenic B cell apoptosis independently of interleukin-1beta and interleukin-18. Am. J. Respir. Crit. Care Med. 2006, 174(9):1003-1010.
48. Segales J., Domingo M. Postweaning multisystemic wasting syndrome (PMWS) in pigs. A review. Vet. Q. 2002, 24(3):109-124.
49. Segales J., Domingo M., Chianini F., Majo N., Dominguez J., Darwich L., Mateu E. Immunosuppression in postweaning multisystemic wasting syndrome affected pigs. Vet. Microbiol. 2004, 98(2):151-158.
50. Shi K.C., Guo X., Ge X.N., Liu Q., Yang H.C. Cytokine mRNA expression profiles in peripheral blood mononuclear cells from piglets experimentally co-infected with porcine reproductive and respiratory syndrome virus and porcine circovirus type 2. Vet. Microbiol. 2010, 140(1-2):155-160.
51. Shibahara T., Sato K., Ishikawa Y., Kadota K. Porcine circovirus induces B lymphocyte depletion in pigs with wasting disease syndrome. J. Vet. Med. Sci. 2000, 62(11):1125-1131.
52. Sipos W., Duvigneau J.C., Pietschmann P., Schilcher F., Hofbauer G., Hartl R.T., Schmoll F. Porcine dermatitis and nephropathy syndrome (PDNS) is associated with a systemic cytokine expression profile indicative of proinflammation and a Th1 bias. Vet. Immunol. Immunopathol. 2005, 107(3-4):303-313.
53. Stevenson G.W., Kiupel M., Mittal S.K., Kanitz C.L. Ultrastructure of porcine circovirus in persistently infected PK-15 cells. Vet. Pathol. 1999, 36(5):368-378.
54. Stevenson G.W., Kiupel M., Mittal S.K., Choi J., Latimer K.S., Kanitz C.L. Tissue distribution and genetic typing of porcine circoviruses in pigs with naturally occurring congenital tremors. J. Vet. Diagn. Invest. 2001, 13(1):57-62.
55. Timmusk S., Wallgren P., Brunborg I.M., Wikstrom F.H., Allan G., Meehan B., McMenamy M., McNeilly F., Fuxler L., Belak K., Podersoo D., Saar T., Berg M., Fossum C. Phylogenetic analysis of porcine circovirus type 2 (PCV2) pre- and post-epizootic postweaning multisystemic wasting syndrome (PMWS). Virus Genes 2008, 36(3):509-520.
56. Victoria J.G., Wang C., Jones M.S., Jaing C., McLoughlin K., Gardner S., Delwart E.L. Viral nucleic acids in live-attenuated vaccines: detection of minority variants and an adventitious virus. J. Virol. 2010, 84(12):6033-6040.
57. Vincent I.E., Carrasco C.P., Herrmann B., Meehan B.M., Allan G.M., Summerfield A., McCullough K.C. Dendritic cells harbor infectious porcine circovirus type 2 in the absence of apparent cell modulation or replication of the virus. J. Virol. 2003, 77(24):13288-13300.
58. Wallgren P., Brunborg I.M., Blomqvist G., Bergstrom G., Wikstrom F., Allan G., Fossum C., Jonassen C.M. The index herd with PMWS in Sweden: presence of serum amyloid A, circovirus 2 viral load and antibody levels in healthy and PMWS-affected pigs. Acta Vet. Scand. 2009, 51:13.
59. Wiederkehr D.D., Sydler T., Buergi E., Haessig M., Zimmermann D., Pospischil A., Brugnera E., Sidler X. A new emerging genotype subgroup within PCV-2b dominates the PMWS epizooty in Switzerland. Vet. Microbiol. 2009, 136(1-2):27-35.
60. Yu S., Opriessnig T., Kitikoon P., Nilubol D., Halbur P.G., Thacker E. Porcine circovirus type 2 (PCV2) distribution and replication in tissues and immune cells in early infected pigs. Vet. Immunol. Immunopathol. 2007, 115(3-4):261-272.