Porcine circovirus type 2 induces autophagy via the AMPK/ERK/TSC2/mTOR signaling pathway in PK-15 cells

Journal of Virology

Volumn 86, Issue 22, 2012, Pages 12003-12012

  Zhu, Binglin ^a   Zhou, MYingshan ^a   Xu, Fei ^a   Shuai, Jiangbing ^b   Li, Xiaoliang ^a   Fang, Weihuan ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b Zhejiang Entry Exit Inspection and Quarantine Bureau   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; TUBERIN;

ANIMAL CELL; ARTICLE; AUTOPHAGY; CELL STRAIN; CELL VIABILITY; CIRCOVIRUS; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME REPRESSION; GENE INDUCTION; HOST CELL; IMMUNOPRECIPITATION; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; VIRUS CAPSID;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; AUTOPHAGY; CELL LINE; CIRCOVIRIDAE INFECTIONS; CIRCOVIRUS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, VIRAL; MODELS, BIOLOGICAL; PHOSPHORYLATION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SWINE; TOR SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEINS;

MAMMALIA; PORCINE CIRCOVIRUS 2;

EID: 84869147764     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01434-12     Document Type: Article

References (69)

1. Ballif BA, et al. 2005. Quantitative phosphorylation profiling of the ERK/ p90 ribosomal S6 kinase-signaling cassette and its targets, the tuberous sclerosis tumor suppressors. Proc. Natl. Acad. Sci. U. S. A. 102:667-672.
2. Beach NM, Meng XJ. 2012. Efficacy and future prospects of commercially available and experimental vaccines against porcine circovirus type 2 (PCV2). Virus Res. 164:33-42.
3. Bolin SR, Stoffregen WC, Nayar GP, Hamel AL. 2001. Postweaning multisystemic wasting syndrome induced after experimental inoculation of cesarean-derived, colostrum-deprived piglets with type 2 porcine circovirus. J. Vet. Diagn. Invest. 13:185-194.
4. Botti J, Djavaheri-Mergny M, Pilatte Y, Codogno P. 2006. Autophagy signaling and the cogwheels of cancer. Autophagy 2:67-73.
5. Cagnol S, Chambard JC. 2010. ERK and cell death: mechanisms of ERKinduced cell death-apoptosis, autophagy, and senescence. FEBS J. 277: 2-21.
6. Chaumorcel M, Souquère S, Pierron G, Codogno P, Esclatine A. 2008. Human cytomegalovirus controls a new autophagy-dependent cellular antiviral defense mechanism. Autophagy 4:46-53.
7. Chen HC, et al. 2002. Activation of the ERK pathway and atypical protein kinase C isoforms in exercise-and aminoimidazole-4-carboxamide-1-Β- D-riboside (AICAR)-stimulated glucose transport. J. Biol. Chem. 277: 23554-23562.
8. Chen Q, et al. 2012. Induction of autophagy enhances porcine reproductive and respiratory syndrome virus replication. Virus Res. 163:650-655.
9. Chianini F, Majó N, Segalés J, Domínguez J, Domingo M. 2003. Immunohistochemical characterisation of PCV2 associate lesions in lymphoid and non-lymphoid tissues of pigs with natural postweaning multisystemic wasting syndrome (PMWS). Vet. Immunol. Immunopathol. 94:63-75.
10. Corcelle E, et al. 2007. Control of the autophagy maturation step by the MAPK ERK and p38: lessons from environmental carcinogens. Autophagy 3:57-59.
11. Corradetti MN, Inoki K, Bardeesy N, DePinho RA, Guan KL. 2004. Regulation of the TSC pathway by LKB1: evidence of a molecular link between tuberous sclerosis co plex and Peutz-Jeghers syndrome. Genes Dev. 18:1533-1538.
12. Diaz-Troya S, Perez-Perez ME, Florencio FJ, Crespo JL. 2008. The role of TOR in autophagy regulation from yeast to plants and mammals. Autophagy 4:851-865.
13. kB transcription factor and reactive oxygen species. Autophagy 3:390-392.
14. Egan DF, et al. 2011. Phosphorylation of ULK1 (hATG1) by AMPactivated protein kinase connects energy sensing to mitophagy. Science 331:456-461.
15. Esclatine A, Chaumorcel M, Codogno P. 2009. Macroautophagy signaling and regulation. Curr. Top. Microbiol. Immunol. 335:33-70.
16. Fleming A, Noda T, Yoshimori T, Rubinsztein DC. 2011. Chemical modulators of autophagy as biological probes and potential therapeutics. Nat. Chem. Biol. 7:9-17.
17. Gwinn DM, et al. 2008. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol. Cell 30:214-226.
18. He C, Klionsky DJ. 2009. Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 43:67-93.
19. Inoki K, Zhu T, Guan KL. 2003. TSC2 mediates cellular energy response to control cell growth and survival. Cell 115:577-590.
20. Juhan NM, LeRoith T, Opriessnig T, Meng XJ. 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 a ORF3-null PCV2 mutant. Virus Res. 147:60-66.
21. Jung CH, Ro SH, Cao J, Otto NM, Kim DH. 2010. mTOR regulation of autophagy. FEBS Lett. 584:1287-1295.
22. Kim EK, et al. 2012. Human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by AMP-activated protein kinase. J. Cell Physiol. 227:1680-1687.
23. Kim J, Kundu M, Viollet B, Guan KL. 2011. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 13: 132-141.
24. Klionsky DJ. 2005. The molecular machinery of autophagy: unanswered questions. J. Cell Sci. 118:7-18.
25. Kumar SH, Rangarajan A. 2009. Simian virus 40 small T antigen activates AMPK and triggers autophagy to protect cancer cells from nutrient deprivation. J. Virol. 83:8565-8574.
26. Lee JW, Park S, Takahashi Y, Wang HG. 2010. The association of AMPK with ULK1 regulates autophagy. PLoS One 5:e15394. doi:10.1371/ journal.pone.0015394.
27. Lempiäinen J, Finckenberg P, Levijoki J, Mervaala E. 2012. AMPK activator AICAR ameliorates ischemia reperfusion injury in the rat kidney. Br. J. Pharmacol. doi:10.1111/j.1476-5381.2012.01895.x.
28. Li J, et al. 2011. Subversion of cellular autophagy machinery by hepatitis B virus for viral envelopment. J. Virol. 85:6319-6333.
29. Li L, et al. 2012. The invasion of tobacco mosaic virus RNA induces endoplasmic reticulum stress-related autophagy in HeLa cells. Biosci. Rep. 32:171-186.
30. Li Y, Inoki K, Guan KL. 2004. Biochemical and functional characterizations of small GTPase Rheb and TSC2 GAP activity. Mol. Cell. Biol. 24: 7965-7975.
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 Q, et al. 2012. Autophagy sustains the replication of porcine reproductive and respiratory virus in host cells. Virology doi:org/10.1016/ j.virol.2012.03.022.
33. Ma L, Chen Z, Erdjument-Bromage H, Tempst P, Pandolfi PP. 2005. Phosphorylation and functional inactivation of TSC2 by Erk implications for tuberous sclerosis a d cancer pathogenesis. Cell 121:179-193.
34. Magnoni LJ, Vraskou Y, Palstra AP, Planas JV. 2012. AMP-activated protein kinase plays an important evolutionary conserved role in the regulation of glucose metabolism in fish skeletal muscle cells. PLoS One 7:e31219. doi:10.1371/journal.pone.0031219.
35. Mankertz A, Mankertz J, Wolf K, Buhk HJ. 1998. Identification of a protein essential for replication of porcine circovirus. J. Gen. Virol. 79(Pt 2):381-384.
36. McNeilly F, et al. 2001. Production, characterization and application of monoclonal antibodies to porcine circovirus 2. Arch. Virol. 146:909-922.
37. Meley D, et al. 2006. AMP-activated protein kinase and the regulation of autophagic proteolysis. J. Biol. Chem. 281:34870-34879.
38. Meng S, et al. 2012. Avian reovirus triggers autophagy in primary chicken fibroblast cells and Vero cells to promote virus production. Arch. Virol. doi:10.1007/s00705-012-1226-x.
39. Mizushima N, Yoshimori T, Levine B. 2010. Methods in mammalian autophagy research. Cell 140:313-326.
40. Morselli E, et al. 2009. Anti- and pro-tumor functions of autophagy. Biochim. Biophys. Acta 1793:1524-1532.
41. Nawagitgul P, et al. 2000. Open reading frame 2 of porcine circovirus type 2 encodes a major capsid protein. J. Gen. Virol. 81(Pt 9):2281-2287.
42. Opriessnig T, Meng MJ, Halbur PG. 2007. Porcine circovirus type 2 associated disease: update on current terminology, clinical manifestations, pathogenesis, diagnosis, and intervention strategies. J. Vet. Diagn. Invest. 19:591-615.
43. Pogranichnyy RM, et al. 2000. Characterization of immune response of young pigs to porcine circovirus type 2 infection. Viral Immunol. 13:143-153.
44. Rodriguez-Rocha H, et al. 2011. Adenoviruses induce autophagy to promote virus replication and oncolysis. Virology 416:9-15.
45. Rosell C, et al. 2000. Identification of porcine circovirus in tissues of pigs with porcine dermatitis and nephropathy syndrome. Vet. Rec. 146:40-43.
46. Saiki S, et al. 2011. Caffeine induces apoptosis by enhancement of autophagy via PI3K/Akt/mTOR/p70S6K inhibition. Autophagy 7:176-187.
47. Sajan MP, et al. 2010. AICAR and metformin, but not exercise, increase muscle glucose transport through AMPK-, ERK-, and PDK1-dependent activation of atypical P C. Am. J. Physiol. Endocrinol. Metab. 298:E179-E192.
48. Shang L, Wang X. 2011. AMPK and mTOR coordinate the regulation of Ulk1 and mammalian autophagy initiation. Autophagy 7:924-926.
49. Shang L, et al. 2011. Nutrient starvation elicits an acute autophagic response mediated by Ulk1 dephosphorylation and its subsequent dissociation from AMPK. Proc. Natl. Acad. Sci. U. S. A. 108:4788-4793.
50. Shaw RJ, Cantley LC. 2006. Ras, PI(3)K, and mTOR signalling controls tumour cell growth. Nature 441:424-430.
51. Shelly S, Lukinova N, Bambina S, Berman A, Cherry S. 2009. Autophagy is an essential component of Drosophila immunity against vesicular stomatitis virus. Immunity 30 588-598.
52. Sir D, Ou JH. 2010. Autophagy in viral replication and pathogenesis. Mol. Cells 29:1-7.
53. Sir D, et al. 2008. Induction of incomplete autophagic response by hepatitis C virus via the unfolded protein response. Hepatology 48:1054-1061.
54. Steelman LS, et al. 2011. Roles of the Raf/MEK/ERK and PI3K/ PTEN/ Akt/mTOR pathways in controlling growth and sensitivity to therapyimplications for cancer and aging. Aging 3:192-222.
55. Su WC, et al. 2011. Rab5 and class III phosphoinositide 3-kinase Vps34 are involved in hepatitis C virus NS4B-induced autophagy. J. Virol. 85: 10561-10571.
56. Sun Y, et al. 2012. Inhibition of autophagy ameliorates acute lung injury caused by avian influenza A H5N1 infection. Sci. Signal. 5:ra16.
57. Tanida I. 2011. Autophagosome formation and molecular mechanism of autophagy. Antioxid. Redox Signal. 14:2201-2214.
58. Todd D, et al. 2005. Circoviridae, p 327-334. In Fauquet CM, et al. (ed), Virus taxonomy: VIIIth report of the International Committee on Taxonomy of Viruses, 2nd ed. Elsevier Academic Press, San Diego, CA.
59. In Fauquet CM, et al. (ed), Virus taxonomy: VIIIth report of the International Committee on Taxonomy of Viruses, 2nd ed. Elsevier Academic Press, San Diego, CA.
60. Van Grol J, et al. 2005. HIV-1 inhibits autophagy in bystander macrophage/ monocytic cells through Src-Akt and STAT3. PLoS One 5:e11733. doi:10.1371/journal.pone.0011733.
61. Wang J, et al. 2009. A non-canonical MEK/ERK signaling pathway regulates autophagy via regulating Beclin1. J. Biol. Chem. 284:21412-21424.
62. Wei L, Liu J. 2009. Porcine circovirus type 2 replication is impaired by inhibition of the extracellular signal-regulated kinase (ERK) signaling pathway. Virology 386:203-209.
63. Xiao G. 2007. Autophagy and NF-KB: fight for fate. Cytokine Growth Factor Rev. 18:233-243
64. Yang J, et al. 2011. Deficiency of hepatocystin induces autophagy through an mTOR-dependent pathway. Autophagy 7:748-759.
65. Yang ZF, Klionsky DJ. 2010. Mammalian autophagy: core molecular machinery and signaling regulation. Curr. Opin. Cell Biol. 22:124-131.
66. Yuk JM, Yoshimori T, Jo EK. 2012. Autophagy and bacterial infectious diseases. Exp. Mol. Med. 44:99-108.
67. Zhang Q, et al. 2012. Activation of the Ras/Raf/MEK pathway facilitates hepatitis C virus replication via attenuation of the interferon-JAK-STAT pathway. J. Virol. 86:1544-1554.
68. Zhang YN, Li ZC, Ge XN, Guo X, Yang HC. 2011. Autophagy promotes the replication of encephalomyocarditis virus in host cells. Autophagy 7:1-16.
69. Zhu BL, et al. 2012. Porcine circovirus type 2 explores the autophagic machinery for replication in PK-15 cells. Virus Res. 163:476-485.