Porcine reproductive and respiratory syndrome virus induces autophagy to promote virus replication

Autophagy

Volumn 8, Issue 10, 2012, Pages 1434-1447

  Sun, Ming Xia ^a   Huang, Li ^a   Wang, Rui ^a   Yu, Ya Ling ^a   Li, Chen ^a   Li, Peng Peng ^a   Hu, Xiao Chun ^a   Hao, Hong Ping ^a   Ishag, Hassan A ^a   Mao, Xiang ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

Autophagosomes; Autophagy; Fusion; Lysosomes; Porcine reproductive and respiratory syndrome virus; Replication

Indexed keywords

3 METHYLADENINE; CHLOROQUINE; RAPAMYCIN; SHORT HAIRPIN RNA;

ANIMAL CELL; ARTERIVIRUS; ARTERIVIRUS INFECTION; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; DENSITY GRADIENT CENTRIFUGATION; HOST CELL; LYSOSOME; MEMBRANE VESICLE; NONHUMAN; ULTRASTRUCTURE; VIRUS REPLICATION;

EID: 84867250922     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.21159     Document Type: Article

References (67)

1. Cavanagh D. Nidovirales: a new order comprising Coronaviridae and Arteriviridae. Arch Virol 1997; 142:629-33; PMID:9349308
2. Neumann EJ, Kliebenstein JB, Johnson CD, Mabry JW, Bush EJ, Seitzinger AH, et al. Assessment of the economic impact of porcine reproductive and respiratory syndrome on swine production in the United States. J Am Vet Med Assoc 2005; 227:385-92; PMID:16121604; http://dx.doi.org/10.2460/javma.2005.227. 385
3. Kimman TG, Cornelissen LA, Moormann RJ, Rebel JMJ, Stockhofe-Zurwieden N. Challenges for porcine reproductive and respiratory syndrome virus (PRRSV) vaccinology. Vaccine 2009; 27:3704-18; PMID:19464553; http://dx.doi.org/10.1016/ j.vaccine.2009.04.022
4. Zhou L, Yang H. Porcine reproductive and respiratory syndrome in China. Virus Res 2010; 154:31- 7; PMID:20659506; http://dx.doi.org/10.1016/j.virusres. 2010.07.016
5. Tian K, Yu X, Zhao T, Feng Y, Cao Z, Wang C, et al. Emergence of fatal PRRSV variants: unparalleled outbreaks of atypical PRRS in China and molecular dissection of the unique hallmark. PLoS One 2007; 2:e526; PMID:17565379; http://dx.doi.org/10.1371/journal.pone.0000526
6. Feng Y, Zhao T, Nguyen T, Inui K, Ma Y, Nguyen TH, et al. Porcine respiratory and reproductive syndrome virus variants, Vietnam and China, 2007. Emerg Infect Dis 2008; 14:1774-6; PMID:18976568; http://dx.doi.org/10.3201/ eid1411.071676
7. Yoo D, Song C, Sun Y, Du Y, Kim O, Liu H-C. Modulation of host cell responses and evasion strategies for porcine reproductive and respiratory syndrome virus. Virus Res 2010; 154:48-60; PMID:20655963; http://dx.doi.org/10. 1016/j.virusres.2010.07.019
8. Luo R, Xiao S, Jiang Y, Jin H, Wang D, Liu M, et al. Porcine reproductive and respiratory syndrome virus (PRRSV) suppresses interferon-beta production by interfering with the RIG-I signaling pathway. Mol Immunol 2008; 45:2839-46; PMID:18336912; http://dx.doi.org/10.1016/j.molimm.2008.01.028
9. Lee YJ, Lee C. Porcine reproductive and respiratory syndrome virus replication is suppressed by inhibition of the extracellular signal-regulated kinase (ERK) signaling pathway. Virus Res 2010; 152:50-8; PMID:20540975; http://dx.doi.org/10.1016/j.virusres.2010.06.002
10. Zhang H, Wang X. A dual effect of porcine reproductive and respiratory syndrome virus replication on the phosphatidylinositol-3-kinase-dependent Akt pathway. Arch Virol 2010; 155:571-5; PMID:20213282; http://dx.doi.org/10.1007/ s00705-010-0611-6
11. Klionsky DJ. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 2007; 8:931-7; PMID:17712358; http://dx.doi.org/10.1038/nrm2245
12. Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science 2000; 290:1717-21; PMID:11099404; http://dx.doi.org/10. 1126/science.290.5497.1717
13. Yorimitsu T, Klionsky DJ. Autophagy: molecular machinery for self-eating. Cell Death Differ 2005; 12(Suppl 2):1542-52; PMID:16247502; http://dx.doi.org/10.1038/sj.cdd.4401765
14. Levine B, Deretic V. Unveiling the roles of autophagy in innate and adaptive immunity. Nat Rev Immunol 2007; 7:767-77; PMID:17767194; http://dx.doi.org/10.1038/nri2161
15. Schmid D, Dengjel J, Schoor O, Stevanovic S, Münz C. Autophagy in innate and adaptive immunity against intracellular pathogens. J Mol Med (Berl) 2006; 84:194-202; PMID:16501849; http://dx.doi.org/10.1007/s00109-005-0014-4
16. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008; 451:1069-75; PMID:18305538; http://dx.doi.org/10.1038/nature06639
17. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008; 132:27-42; PMID:18191218; http://dx.doi.org/10.1016/j.cell.2007.12.018
18. Shintani T, Klionsky DJ. Autophagy in health and disease: a double-edged sword. Science 2004; 306:990-5; PMID:15528435; http://dx.doi.org/10.1126/ science.1099993
19. Tallóczy Z, Virgin HW 4th, Levine B. PKR-dependent autophagic degradation of herpes simplex virus type 1. Autophagy 2006; 2:24-9; PMID:16874088
20. Dreux M, Gastaminza P, Wieland SF, Chisari FV. The autophagy machinery is required to initiate hepatitis C virus replication. Proc Natl Acad Sci U S A 2009; 106:14046-51; PMID:19666601; http://dx.doi.org/10.1073/pnas.0907344106
21. Lee YR, Lei HY, Liu MT, Wang JR, Chen SH, Jiang-Shieh YF, et al. Autophagic machinery activated by dengue virus enhances virus replication. Virology 2008; 374:240-8; PMID:18353420; http://dx.doi.org/10.1016/j.virol.2008. 02.016
22. Tanida I, Fukasawa M, Ueno T, Kominami E, Wakita T, Hanada K. Knockdown of autophagyrelated gene decreases the production of infectious hepatitis C virus particles. Autophagy 2009; 5:937-45; PMID:19625776; http://dx.doi.org/10. 4161/auto.5.7.9243
23. Ke PY, Chen SS. Activation of the unfolded protein response and autophagy after hepatitis C virus infection suppresses innate antiviral immunity in vitro. J Clin Invest 2011; 121:37-56; PMID:21135505; http://dx.doi.org/10.1172/ JCI41474
24. Yoon SY, Ha YE, Choi JE, Ahn J, Lee H, Kweon HS, et al. Coxsackievirus B4 uses autophagy for replication after calpain activation in rat primary neurons. J Virol 2008; 82:11976-8; PMID:18799585; http://dx.doi.org/10.1128/JVI.01028-08
25. Zhou Z, Jiang X, Liu D, Fan Z, Hu X, Yan J, et al. Autophagy is involved in influenza A virus replication. Autophagy 2009; 5:321-8; PMID:19066474; http://dx.doi.org/10.4161/auto.5.3.7406
26. Gannagé M, Dormann D, Albrecht R, Dengjel J, Torossi T, Rämer PC, et al. Matrix protein 2 of influenza A virus blocks autophagosome fusion with lysosomes. Cell Host Microbe 2009; 6:367-80; PMID:19837376; http://dx.doi.org/10.1016/j.chom.2009.09.005
27. Wileman T. Aggresomes and autophagy generate sites for virus replication. Science 2006; 312:875-8; PMID:16690857; http://dx.doi.org/10.1126/science. 1126766
28. Wileman T. Aggresomes and pericentriolar sites of virus assembly: cellular defense or viral design? Annu Rev Microbiol 2007; 61:149-67; PMID:17896875; http://dx.doi.org/10.1146/annurev.micro.57.030502.090836
29. Ferraris P, Blanchard E, Roingeard P. Ultrastructural and biochemical analyses of hepatitis C virus-associated host cell membranes. J Gen Virol 2010; 91:2230-7; PMID:20484561; http://dx.doi.org/10.1099/vir.0.022186-0
30. Jackson WT, Giddings TH Jr., Taylor MP, Mulinyawe S, Rabinovitch M, Kopito RR, et al. Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol 2005; 3:e156; PMID:15884975; http://dx.doi.org/10.1371/ journal.pbio.0030156
31. Brabec-Zaruba M, Berka U, Blaas D, Fuchs R. Induction of autophagy does not affect human rhinovirus type 2 production. J Virol 2007; 81:10815-7; PMID:17670838; http://dx.doi.org/10.1128/JVI.00143-07
32. Prentice E, Jerome WG, Yoshimori T, Mizushima N, Denison MR. Coronavirus replication complex formation utilizes components of cellular autophagy. J Biol Chem 2004; 279:10136-41; PMID:14699140; http://dx.doi.org/10.1074/jbc.M306124200
33. Zhao Z, Thackray LB, Miller BC, Lynn TM, Becker MM, Ward E, et al. Coronavirus replication does not require the autophagy gene ATG5. Autophagy 2007; 3:581-5; PMID:17700057
34. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 2007; 282:24131-45; PMID:17580304; http://dx.doi.org/10.1074/jbc.M702824200
35. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4:151-75; PMID:18188003
36. Reggiori F, Monastyrska I, Verheije MH, Calì T, Ulasli M, Bianchi S, et al. Coronaviruses Hijack the LC3-Ipositive EDEMosomes, ER-derived vesicles exporting short-lived ERAD regulators, for replication. Cell Host Microbe 2010; 7:500-8; PMID:20542253; http://dx.doi.org/10.1016/j.chom.2010.05.013
37. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8:445-544; http://dx.doi.org/10.4161/auto. 19496
38. Deretic V, Levine B. Autophagy, immunity, and microbial adaptations. Cell Host Microbe 2009; 5:527-49; PMID:19527881; http://dx.doi.org/10.1016/j.chom. 2009.05.016
39. Kudchodkar SB, Levine B. Viruses and autophagy. Rev Med Virol 2009; 19:359-78; PMID:19750559; http://dx.doi.org/10.1002/rmv.630
40. Mizushima N, Yoshimori T. How to interpret LC3 immunoblotting. Autophagy 2007; 3:542-5; PMID:17611390
41. Tanida I, Minematsu-Ikeguchi N, Ueno T, Kominami E. Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 2005; 1:84-91; PMID:16874052; http://dx.doi.org/10.4161/auto.1.2.1697
42. Adler J, Parmryd I. Quantifying colocalization by correlation: the Pearson correlation coefficient is superior to the Mander's overlap coefficient. Cytometry A 2010; 77:733-42; PMID:20653013; http://dx.doi.org/10.1002/cyto.a. 20896
43. Pedersen KW, van der Meer Y, Roos N, Snijder EJ. Open reading frame 1a-encoded subunits of the arterivirus replicase induce endoplasmic reticulum-derived double-membrane vesicles which carry the viral replication complex. J Virol 1999; 73:2016-26; PMID:9971782
44. Calì T, Galli C, Olivari S, Molinari M. Segregation and rapid turnover of EDEM1 by an autophagy-like mechanism modulates standard ERAD and folding activities. Biochem Biophys Res Commun 2008; 371:405-10; PMID:18452703; http://dx.doi.org/10.1016/j.bbrc.2008.04.098
45. Kirkegaard K. Subversion of the cellular autophagy pathway by viruses. Curr Top Microbiol Immunol 2009; 335:323-33; PMID:19802573; http://dx.doi.org/ 10.1007/978-3-642-00302-8-16
46. Dales S, Eggers HJ, Tamm I, Palade GE. Electron microscopic study of the formation of poliovirus. Virology 1965; 26:379-89; PMID:14319710; http://dx.doi.org/10.1016/0042-6822(65)90001-2
47. Orvedahl A, Alexander D, Tallóczy Z, Sun Q, Wei Y, Zhang W, et al. HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe 2007; 1:23-35; PMID:18005679; http://dx.doi.org/10. 1016/j.chom.2006.12.001
48. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005; 122:927-39; PMID:16179260; http://dx.doi.org/10.1016/j.cell.2005.07.002
49. Ku B, Woo JS, Liang C, Lee KH, Hong HS, e X, et al. Structural and biochemical bases for the inhibition of autophagy and apoptosis by viral BCL-2 of murine gamma-herpesvirus 68. PLoS Pathog 2008; 4:e25; PMID:18248095; http://dx.doi.org/10.1371/journal.ppat.0040025
50. Sinha S, Colbert CL, Becker N, Wei Y, Levine B. Molecular basis of the regulation of Beclin 1-dependent autophagy by the gamma-herpesvirus 68 Bcl-2 homolog M11. Autophagy 2008; 4:989-97; PMID:18797192
51. Sir D, Chen WL, Choi J, Wakita T, Yen TS, Ou JH. Induction of incomplete autophagic response by hepatitis C virus via the unfolded protein response. Hepatology 2008; 48:1054-61; PMID:18688877; http://dx.doi.org/10.1002/hep.22464
52. Ding WX, Ni HM, Gao W, Yoshimori T, Stolz DB, Ron D, et al. Linking of autophagy to ubiquitinproteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am J Pathol 2007; 171:513-24; PMID:17620365; http://dx.doi.org/10.2353/ajpath.2007.070188
53. Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S, et al. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 2006; 26:9220-31; PMID:17030611; http://dx.doi.org/10.1128/MCB.01453- 06
54. Yorimitsu T, Klionsky DJ. Endoplasmic reticulum stress: a new pathway to induce autophagy. Autophagy 2007; 3:160-2; PMID:17204854
55. Qin L, Wang Z, Tao L, Wang Y. ER stress negatively regulates AKT/TSC/mTOR pathway to enhance autophagy. Autophagy 2010; 6:239-47; PMID:20104019; http://dx.doi.org/10.4161/auto.6.2.11062
56. Nguyen DH, Ludgate L, Hu J. Hepatitis B virus-cell interactions and pathogenesis. J Cell Physiol 2008; 216:289-94; PMID:18302164; http://dx.doi.org/10.1002/jcp.21416
57. Lépine S, Allegood JC, Park M, Dent P, Milstien S, Spiegel S. Sphingosine-1-phosphate phosphohydrolase- 1 regulates ER stress-induced autophagy. Cell Death Differ 2011; 18:350-61; PMID:20798685; http://dx.doi.org/10.1038/cdd.2010.104
58. He B. Viruses, endoplasmic reticulum stress, and interferon responses. Cell Death Differ 2006; 13:393-403; PMID:16397582; http://dx.doi.org/10.1038/sj. cdd.4401833
59. Lin JH, Walter P, Yen TSB. Endoplasmic reticulum stress in disease pathogenesis. Annu Rev Pathol 2008; 3:399-425; PMID:18039139; http://dx.doi.org/10.1146/annurev.pathmechdis.3.121806.151434
60. von dem Bussche A, Machida R, Li K, Loevinsohn G, Khander A, Wang J, et al. Hepatitis C virus NS2 protein triggers endoplasmic reticulum stress and suppresses its own viral replication. J Hepatol 2010; 53:797-804; PMID:20801537; http://dx.doi.org/10.1016/j.jhep.2010.05.022
61. Liu N, Kuang X, Kim HT, Stoica G, Qiang W, Scofield VL, et al. Possible involvement of both endoplasmic reticulum- and mitochondria-dependent pathways in MoMuLV-ts1-induced apoptosis in astrocytes. J Neurovirol 2004; 10:189-98; PMID:15204924; http://dx.doi.org/10.1080/13550280490448043
62. Dimcheff DE, Faasse MA, McAtee FJ, Portis JL. Endoplasmic reticulum (ER) stress induced by a neurovirulent mouse retrovirus is associated with prolonged BiP binding and retention of a viral protein in the ER. J Biol Chem 2004; 279:33782-90; PMID:15178688; http://dx.doi.org/10.1074/jbc.M403304200
63. Chan SW, Egan PA. Hepatitis C virus envelope proteins regulate CHOP via induction of the unfolded protein response. FASEB J 2005; 19:1510-2; PMID:16006626
64. Chan SW, Egan PA. Effects of hepatitis C virus envelope glycoprotein unfolded protein response activation on translation and transcription. Arch Virol 2009; 154:1631-40; PMID:19763778; http://dx.doi.org/10.1007/s00705-009- 0495-5
65. Li J, Liu Y, Wang Z, Liu K, Wang Y, Liu J, et al. Subversion of cellular autophagy machinery by hepatitis B virus for viral envelopment. J Virol 2011; 85:6319-33; PMID:21507968; http://dx.doi.org/10.1128/JVI.02627-10
66. Gosert R, Kanjanahaluethai A, Egger D, Bienz K, Baker SC. RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. J Virol 2002; 76:3697-708; PMID:11907209; http://dx.doi.org/10.1128/JVI.76.8.3697-3708.2002
67. Cottam EM, Maier HJ, Manifava M, Vaux LC, Chandra-Schoenfelder P, Gerner W, et al. Coronavirus nsp6 proteins generate autophagosomes from the endoplasmic reticulum via an omegasome intermediate. Autophagy 2011; 7:1335-47; PMID:21799305; http://dx.doi.org/10.4161/auto.7.11.16642