Activation of the phosphatidylinositol 3-kinase/akt signaling pathway during porcine circovirus type 2 infection facilitates cell survival and viral replication

Journal of Virology

Volumn 86, Issue 24, 2012, Pages 13589-13597

  Wei, Li ^a   Zhu, Shanshan ^a   Wang, Jing ^a   Liu, Jue ^a  

^a INSTITUTE OF PLANT AND ENVIRONMENT PROTECTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; BIOTIN; CASPASE 3; DEOXYURIDINE TRIPHOSPHATE PYROPHOSPHATASE; DNA NUCLEOTIDYLEXOTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; VIRUS DNA; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CULTURE; CELL SURVIVAL; CIRCOVIRIDAE INFECTION; CIRCOVIRUS; CIRCOVIRUS 2; CONTROLLED STUDY; DISEASE COURSE; DNA FRAGMENTATION; DNA METABOLISM; DNA REPLICATION; ENZYME ACTIVATION; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME MECHANISM; ENZYME PHOSPHORYLATION; ENZYME REPRESSION; INTRACELLULAR SIGNALING; MOLECULAR MECHANICS; NICK END LABELING; NONHUMAN; POSTWEANING MULTISYSTEMIC WASTING SYNDROME; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; VIROGENESIS; VIRUS REPLICATION;

ANIMALS; APOPTOSIS; BASE SEQUENCE; CELL LINE; CELL SURVIVAL; CIRCOVIRIDAE INFECTIONS; CIRCOVIRUS; DNA PRIMERS; DNA REPLICATION; DNA, VIRAL; ENZYME ACTIVATION; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; IN SITU NICK-END LABELING; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SWINE; VIRUS REPLICATION;

PORCINE CIRCOVIRUS 2; SUIDAE;

EID: 84870697261     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01697-12     Document Type: Article

References (66)

1. Allan GM, et al. 1995. Pathogenesis of porcine circovirus: experimental infections of colostrum deprived piglets and examination of pig fetal material. Vet. Microbiol. 44:49-64.
2. Allan GM, et al. 1998. Isolation of porcine circovirus-like viruses from pigs with a wasting disease in the U. S. A. and Europe. J. Vet. Diagn. Invest. 10:3-10.
3. Autret A, et al. 2008. Early phosphatidylinositol-3-kinase/Akt pathway activation limits poliovirus-induced JNK-mediated cell death. J. Virol. 82:3796 -3802.
4. Bagchi P, et al. 2010. Rotavirus nonstructural protein 1 suppresses virusinduced cellular apoptosis to facilitate virus growth by activating the cell survival pathways during early stages of infection. J. Virol. 84:6834-6845.
5. s3 mutant virus but only at early times after infection with wild-type herpes simplex virus 1. J. Virol.80:3341-3348.
6. Bondar VM, Sweeney-Gotsch B, Andreeff M, Mills GB, McConkey DJ. 2002. Inhibition of the phosphatidylinositol 3=-kinase-AKT pathway induces apoptosis in pancreatic carcinoma cells in vitro and in vivo. Mol. Cancer Ther. 1:989 -997.
7. Chang HW, et al. 2007. The involvement of Fas/FasL interaction in porcine circovirus type 2 and porcine reproductive and respiratory syndrome virus co-inoculation-associated lymphocyte apoptosis in vitro. Vet. Microbiol. 122:72- 82.
8. Cheung AK. 2003. Transcriptional analysis of porcine circovirus type 2. Virology 305:168 -180.
9. Cooray S. 2004. The pivotal role of phosphatidylinositol 3-kinase-Akt signal transduction in virus survival. J. Gen. Virol. 85:1065-1076.
10. Darwich L, Segales J, Mateu E. 2004. Pathogenesis of postweaning multisystemic wasting syndrome caused by porcine circovirus 2: an immune riddle. Arch. Virol. 149:857- 874.
11. Datta SR, Brunet A, Greenberg ME. 1999. Cellular survival: a play in three Akts. Genes Dev. 13:2905-2927.
12. Dawson CW, Tramountanis G, Eliopoulos AG, Young LS. 2003. Epstein-Barr virus latent membrane protein 1 (LMP1) activates the phosphatidylinositol 3-kinase/Akt pathway to promote cell survival and induce actin filament remodeling. J. Biol. Chem. 278:3694 -3704.
13. Ehrhardt C, Ludwig S. 2009. A new player in a deadly game: influenza viruses and the PI3K/Akt signaling pathway. Cell. Microbiol. 11:863- 871.
14. Ehrhardt C, et al. 2006. Bivalent role of the phosphatidylinositol-3-kinase (PI3K) during influenza virus infection and host cell defence. Cell. Microbiol. 8:1336 -1348.
15. Ehrhardt C, et al. 2007. Influenza A virus NS1 protein activates the PI3K/Akt pathway to mediate antiapoptotic signaling responses. J. Virol. 81:3058 -3067.
16. Esfandiarei M, et al. 2004. Protein kinase B/Akt regulates coxsackievirus B3 replication through a mechanism which is not caspase dependent. J. Virol. 78:4289-4298.
17. Fothergill T, McMillan NAJ. 2006. Papillomavirus virus-like particles activate the PI3-kinase pathway via alpha-6 beta-4 integrin upon binding. Virology 352:319 -328.
18. + T lymphocytes and macrophages. J. Virol. 77:2539 -2549.
19. Fukuda M, Longnecker R. 2004. Latent membrane protein 2A inhibits transforming growth factor-beta 1-induced apoptosis through the phosphatidylinositol 3-kinase/Akt pathway. J. Virol. 78:1697-1705.
20. Galindo-Cardiel I, Grau-Roma L, Pérez-Maíllo M, Segalés J. 2011. Characterization of necrotizing lymphadenitis associated with porcine circovirus type 2 infection. J. Comp. Pathol. 144:63- 69.
21. Gratton JP, Morales-Ruiz M, Kureishi Y, Fulton D, Walsh K. 2001. Akt down-regulation of p38 signaling provides a novel mechanism of vascular endothelial growth factor-mediated cytoprotection in endothelial cells. J.Biol. Chem. 276:30359 -30365.
22. Guo HT, et al. 2007. Regulation of hepatitis B virus replication by the phosphatidylinositol 3-kinase-Akt signal transduction pathway. J. Virol. 81:10072-10080.
23. He Y, et al. 2002. Subversion of cell signaling pathways by hepatitis C virus nonstructural 5A protein via interaction with Grb2 and P85 phosphatidylinositol 3-kinase. J. Virol. 76:9207-9217.
24. Ji WT, Liu HJ. 2008. PI3K-Akt signaling and viral infection. Recent Pat. Biotechnol. 2:218 -226.
25. Johnson RA, Wang X, Ma XL, Huong SM, Huang ES. 2001. Human cytomegalovirus up-regulates the phosphatidylinositol 3-kinase (PI3-K) pathway: inhibition of PI3-K activity inhibits viral replication and virusinduced signaling. J. Virol. 75:6022- 6032.
26. Kiupel M, et al. 2005. Porcine circovirus type 2 (PCV2) causes apoptosis in experimentally inoculated BALB/c mice. BMC Vet. Res. 1:7.
27. Lee CJ, Liao CL, Lin YL. 2005. Flavivirus activates phosphatidylinositol 3-kinase signaling to block caspase-dependent apoptotic cell death at the early stage of virus infection. J. Virol. 79:8388-8399.
28. Li E, Stupack D, Bokoch GM, Nemerow GR. 1998. Adenovirus endocytosis requires actin cytoskeleton reorganization mediated by Rho family GTPases. J. Virol. 72:8806-8812.
29. vintegrins requires phosphoinositide- 3-OH kinase. J. Virol. 72:2055-2061.
30. kBBdependent mechanism. J. Immunol. 176:5529 -5537.
31. Liu J, Chen I, Du Q, Chua H, Kwang J. 2006. The ORF3 protein of porcine circovirus type 2 is involved in viral pathogenesis in vivo. J. Virol. 80:5065-5073.
32. Liu J, Chen I, Kwang J. 2005. Characterization of a previously unidentified viral protein of porcine circovirus type 2-infected cells and its role in virus-induced apoptosis. J. Virol. 79:8262- 8274.
33. Lu X, et al. 2010. The PI3K/Akt pathway inhibits influenza A virusinduced Bax-mediated apoptosis by negatively regulating the JNK pathway via ASK1. J. Gen. Virol. 91:1439 -1449.
34. Mankertz A, Mankertz J, Wolf K, Buhk HJ. 1998. Identification of a protein essential for replication of porcine circovirus. J. Gen. Virol. 79: 381-383.
35. Mannova P, Beretta L. 2005. Activation of the N-Ras-PI3K-Akt-mTOR pathway by hepatitis C virus: control of cell survival and viral replication. J. Virol. 79:8742- 8749.
36. Misinzo G, et al. 2005. Binding and entry characteristics of porcine circovirus 2 in cells of the porcine monocytic line 3D4/31. J. Gen. Virol. 86: 2057-2068.
37. Nair P, Somasundaram K, Krishna S. 2003. Activated Notch1 inhibits p53-induced apoptosis and sustains transformation by human papillomavirus type 16 E6 and E7 oncogenes through a PI3K-PKB/Akt-dependent pathway. J. Virol. 77:7106 -7112.
38. Nawagitgul P, et al. 2000. Open reading frame 2 of porcine circovirus type 2 encodes a major capsid protein. J. Gen. Virol. 81:2281-2287.
39. Opriessnig T, Meng XJ, Halbur PG. 2007. Porcine circovirus type 2 associated disease: update on current terminology, clinical manifestations, pathogenesis, diagnosis, and intervention strategies. J. Vet. Diagn. Invest.19:571- 615.
40. O'Shea CC, Choi S, McCormick F, Stokoe D. 2005. Adenovirus overrides cellular checkpoints for protein translation. Cell Cycle 4:883- 888.
41. Pap M, Cooper GM. 1998. Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-kinase/Akt cell survival pathway. J. Biol. Chem. 273:19929 -19932.
42. Peruzzi F, et al. 1999. Multiple signaling pathways of the insulin-like growth factor 1 receptor in protection from apoptosis. Mol. Cell. Biol. 19:7203-7215.
43. Rajala MS, Rajala RVS, Astley RA, Buutt AL, Chodosh J. 2005. Corneal cell survival in adenovirus type 19 infection requires phosphoinositide 3-kinase/Akt activation. J. Virol. 79:12332-12341.
44. Resendes AR, et al. 2011. Apoptosis in postweaning multisystemic wasting syndrome (PMWS) hepatitis in pigs naturally infected with porcine circovirus type 2 (PCV2). Vet. J. 189:72-76.
45. Saeed MF, Kolokoltsov AA, Freiberg AN, Holbrook MR, Davey RA. 2008. Phosphoinositide-3 kinase-Akt pathway controls cellular entry of Ebola virus. PLoS Pathog. 4:e1000141. doi:10.1371/journal.ppat.1000141.
46. Sandra F, Matsuki NA, Takeuchi H, Ikebe T, Kanematsu T. 2002. TNF inhibited the apoptosis by activation of Akt serine/threonine kinase in the human head and neck squamous cell carcinoma. Cell Signal. 14:771-778.
47. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. 2005. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307:1098 -2101.
48. Seeliger FA, et al. 2007. Porcine circovirus type 2-associated cerebellar vasculitis in postweaning multisystemic wasting syndrome (PMWS)- affected pigs. Vet. Pathol. 44:621- 634.
49. Segalés J, Allan GM, Domingo M. 2005. Porcine circovirus diseases. Anim. Health Res. Rev. 6:119 -142.
50. Shih WL, Kuo ML, Chuang SE, Cheng AL, Doong SL. 2000. Hepatitis B virus X protein inhibits transforming growth factor-beta-induced apoptosis through the activation of phosphatidylinositol 3-kinase pathway. J.Biol. Chem. 275:25858 -25864.
51. Shin YK, et al. 2007. SH3 binding motif 1 in influenza A virus NS1 protein is essential for PI3K/Akt signaling pathway activation. J. Virol. 81:12730- 12739.
52. Shin YK, Liu Q, Tikoo SK, Babiuk LA, Zhou Y. 2007. Effect of the phosphatidylinositol 3-kinase/Akt pathway on influenza A virus propagation. J. Gen. Virol. 88:942-950.
53. Sinha A, Schalk S, Lager KM, Wang C, Opriessnig T. 2012. Singular PCV2a or PCV2b infection results in apoptosis of hepatocytes in clinically affected gnotobiotic pigs. Res. Vet. Sci. 92:151-156.
54. Soares JAP, et al. 2009. Activation of the PI3K/Akt pathway early during vaccinia and cowpox virus infections is required for both host survival and viral replication. J. Virol. 83:6883- 6899.
55. Sun M, et al. 2008. Akt plays a critical role in replication of nonsegmented negative-stranded RNA viruses. J. Virol. 82:105-114.
56. Thomas KW, et al. 2002. Respiratory syncytial virus inhibits apoptosis and induces NF-κB activity through a phosphatidylinositol 3-kinasedependent pathway. J. Biol. Chem. 277:492-501.
57. Tischer I, Mields W, Wolff D, Vagt M, Griem W. 1986. Studies on epidemiology and pathogenicity of porcine circovirus. Arch. Virol. 91: 271-276.
58. Tischer I, Peters D, Rasch R, Pociuli S. 1987. Replication of porcine circovirus: induction by glucosamine and cell cycle dependence. Arch. Virol. 96:39 -57.
59. Todd D, et al. 2005. Circoviridae, p 327-334. In Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (ed), Virus taxonomy, VIIIth report of the International Committee for the Taxonomy of Viruses. Elsevier/Academic Press, London, United Kingdom.
60. Tsuruta F, Masuyama N, Gotoh Y. 2002. The phosphatidylinositol 3-kinase (PI3K)-Akt pathway suppresses Bax translocation to mitochondria. J. Biol. Chem. 277:14040 -14047.
61. p85α subunit of PI3K. Virology 417:211-220.
62. Wei L, et al. 2008. Porcine circovirus type 2 induces the activation of nuclear factor kappa B by IκBα degradation. Virology 378:177-184.
63. Wei L, Zhu Z, Wang J, Liu J. 2009. JNK and p38 mitogen-activated protein kinase pathways contribute to porcine circovirus type 2 infection. J. Virol. 83:6039-6047.
64. Wong WR, Chen YY, Yang SM, Chen YL, Horng JT. 2005. Phosphorylation of PI3K/Akt and MAPK/ERK in an early entry step of enterovirus 71. Life Sci. 78:82-90.
65. Yao R, Cooper GM. 1995. Requirement for phosphatidylinostol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 267:2003- 2006.
66. Zhu L, et al. 2011. Biphasic activation of PI3K/Akt and MAPK/Erk1/2 signaling pathways in bovine herpesvirus type 1 infection of MDBK cells. BMC Vet. Res. 42:57.