2,467
Views
57
CrossRef citations to date
0
Altmetric
Basic Research Papers

Absence of autophagy promotes apoptosis by modulating the ROS-dependent RLR signaling pathway in classical swine fever virus-infected cells

, , , , , , , , & show all
Pages 1738-1758 | Received 09 Oct 2015, Accepted 24 May 2016, Published online: 27 Jul 2016

References

  • Becher P, Avalos RR, Orlich M, Cedillo RS, König M, Schweizer M, Stalder H, Schirrmeier H, Thiel HJ. Genetic and antigenic characterization of novel pestivirus genotypes: implications for classification. Virology 2003; 311:96-104; PMID:12832207; http://dx.doi.org/10.1016/S0042-6822(03)00192-2
  • Lohse L, Nielsen J, Uttenthal A. Early pathogenesis of classical swine fever virus (CSFV) strains in Danish pigs. Vet Microbiol 2012; 159:327-36; PMID:22608103; http://dx.doi.org/10.1016/j.vetmic.2012.04.026
  • Kleiboeker SB. Swine fever: classical swine fever and African swine fever. Vet Clin North Am Food Anim Pract 2002; 18:431-51; PMID:12442576; http://dx.doi.org/10.1016/S0749-0720(02)00028-2
  • Bensaude E, Turner JL, Wakeley PR, Sweetman DA, Pardieu C, Drew TW, Wileman T, Powell PP. Classical swine fever virus induces proinflammatory cytokines and tissue factor expression and inhibits apoptosis and interferon synthesis during the establishment of long-term infection of porcine vascular endothelial cells. J Gen Virol 2004; 85:1029-37; PMID:15039545; http://dx.doi.org/10.1099/vir.0.19637-0
  • Knoetig SM, Summerfield A, Spagnuolo-Weaver M, McCullough KC. Immunopathogenesis of classical swine fever: role of monocytic cells. Immunology 1999; 97:359-66; PMID:10447754; http://dx.doi.org/10.1046/j.1365-2567.1999.00775.x
  • Tautz N, Meyers G, Thiel HJ. Pathogenesis of mucosal disease, a deadly disease of cattle caused by a pestivirus. Clin Diagn Virol 1998; 10:121-7; PMID:9741637; http://dx.doi.org/10.1016/S0928-0197(98)00037-3
  • Ressang AA. Studies on the pathogenesis of hog cholera. II. Virus distribution in tissue and the morphology of the immune response. Zentralbl Veterinarmed B 1973; 20:272-88; PMID:4751662; http://dx.doi.org/10.1111/j.1439-0450.1973.tb01127.x
  • Kurokawa M, Kornbluth S. Caspases and kinases in a death grip. Cell 2009; 138:838-54; PMID:19737514; http://dx.doi.org/10.1016/j.cell.2009.08.021
  • Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell 2004; 116:205-19; PMID:14744432; http://dx.doi.org/10.1016/S0092-8674(04)00046-7
  • Everett H, McFadden G. Apoptosis: an innate immune response to virus infection. Trends Microbiol 1999; 7:160-5; PMID:10217831; http://dx.doi.org/10.1016/S0966-842X(99)01487-0
  • Reggiori F. One. Membrane origin for autophagy. Curr Top Dev Biol 2006; 74:1-30; PMID:16860663; http://dx.doi.org/10.1016/S0070-2153(06)74001-7
  • Todde V, Veenhuis M, van der Klei IJ. Autophagy: principles and significance in health and disease. Biochim Biophys Acta 2009; 1792:3-13; PMID:19022377; http://dx.doi.org/10.1016/j.bbadis.2008.10.016
  • Alirezaei M, Kiosses WB, Flynn CT, Brady NR, Fox HS. Disruption of neuronal autophagy by infected microglia results in neurodegeneration. PLoS One 2008; 3:e2906; PMID:18682838; http://dx.doi.org/10.1371/journal.pone.0002906
  • Chen N, Karantza-Wadsworth V. Role and regulation of autophagy in cancer. Biochim Biophys Acta 2009; 1793:1516-23; PMID:19167434; http://dx.doi.org/10.1016/j.bbamcr.2008.12.013
  • 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
  • Schmid D, Münz C. Innate and adaptive immunity through autophagy. Immunity 2007; 27:11-21; PMID:17663981; http://dx.doi.org/10.1016/j.immuni.2007.07.004
  • 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
  • Lee YR, Lei HY, Liu MT, Wang JR, Chen SH, Jiang-Shieh YF, Lin YS, Yeh TM, Liu CC, Liu HS. 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
  • Wong J, Zhang J, Si X, Gao G, Mao I, McManus BM, Luo H. Autophagosome supports coxsackievirus B3 replication in host cells. J Virol 2008; 82:9143-53; PMID:18596087; http://dx.doi.org/10.1128/JVI.00641-08
  • Zhou Z, Jiang X, Liu D, Fan Z, Hu X, Yan J, Wang M, Gao GF. 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
  • 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
  • Pei J, Zhao M, Ye Z, Gou H, Wang J, Yi L, Dong X, Liu W, Luo Y, Liao M, et al. Autophagy enhances the replication of classical swine fever virus in vitro. Autophagy 2014; 10:93-110; PMID:24262968; http://dx.doi.org/10.4161/auto.26843
  • Zalckvar E, Yosef N, Reef S, Ber Y, Rubinstein AD, Mor I, Sharan R, Ruppin E, Kimchi A. A systems level strategy for analyzing the cell death network: implication in exploring the apoptosis/autophagy connection. Cell Death Differ 2010; 17:1244-53; PMID:20150916; http://dx.doi.org/10.1038/cdd.2010.7
  • Levine B, Sinha S, Kroemer G. Bcl-2 family members: dual regulators of apoptosis and autophagy. Autophagy 2008; 4:600-6; PMID:18497563; http://dx.doi.org/10.4161/auto.6260
  • Boya P, Gonzalez-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N, Métivier D, Meley D, Souquere S, Yoshimori T, et al. Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 2005; 25:1025-40; PMID:15657430; http://dx.doi.org/10.1128/MCB.25.3.1025-1040.2005
  • Eisenberg-Lerner A, Bialik S, Simon HU, Kimchi A. Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell Death Differ 2009; 16:966-75; PMID:19325568; http://dx.doi.org/10.1038/cdd.2009.33
  • Summerfield A, Knötig SM, McCullough KC. Lymphocyte apoptosis during classical swine fever: implication of activation-induced cell death. J Virol 1998; 72:1853-61; PMID:9499036
  • Heitman J, Movva NR, Hall MN. Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 1991; 253:905-9; PMID:1715094; http://dx.doi.org/10.1126/science.1715094
  • Sarkar S, Davies JE, Huang Z, Tunnacliffe A, Rubinsztein DC. Trehalose, a novel mTOR-independent autophagy enhancer, accelerates the clearance of mutant huntingtin and α-synuclein. J Biol Chem 2007; 282:5641-52; PMID:17182613; http://dx.doi.org/10.1074/jbc.M609532200
  • Thorburn A. Apoptosis and autophagy: regulatory connections between two supposedly different processes. Apoptosis 2008; 13:1-9; PMID:17990121; http://dx.doi.org/10.1007/s10495-007-0154-9
  • Khan SZ, Hand N, Zeichner SL. Apoptosis-induced activation of HIV-1 in latently infected cell lines. Retrovirology 2015; 12:42; PMID:25980942; http://dx.doi.org/10.1186/s12977-015-0169-1
  • Chen Y, Peng GF, Han XZ, Wang W, Zhang GQ, Li X. Apoptosis prediction via inhibition of AKT signaling pathway by neogrifolin. Int J Clin Exp Pathol 2015; 8:1154-64; PMID:25973001
  • Wu JR, Wang J, Zhou SK, Yang L, Yin JL, Cao JP, Cheng YB. Necrostatin-1 protection of dopaminergic neurons. Neural Regen Res 2015; 10:1120-4; PMID:26330837; http://dx.doi.org/10.4103/1673-5374.160108
  • Chang YJ, Hsu SL, Liu YT, Lin YH, Lin MH, Huang SJ, Ho JA, Wu LC. Gallic acid induces necroptosis via TNF-α signaling pathway in activated hepatic stellate cells. PLoS One 2015; 10:e0120713; PMID:25816210; http://dx.doi.org/10.1371/journal.pone.0120713
  • 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
  • Jounai N, Takeshita F, Kobiyama K, Sawano A, Miyawaki A, Xin KQ, Ishii KJ, Kawai T, Akira S, Suzuki K, et al. The Atg5 Atg12 conjugate associates with innate antiviral immune responses. Proc Natl Acad Sci U S A 2007; 104:14050-5; PMID:17709747; http://dx.doi.org/10.1073/pnas.0704014104
  • Takeshita F, Kobiyama K, Miyawaki A, Jounai N, Okuda K. The non-canonical role of Atg family members as suppressors of innate antiviral immune signaling. Autophagy 2008; 4:67-9; PMID:17921696; http://dx.doi.org/10.4161/auto.5055
  • Renson P, Blanchard Y, Le Dimna M, Felix H, Cariolet R, Jestin A, Le Potier MF. Acute induction of cell death-related IFN stimulated genes (ISG) differentiates highly from moderately virulent CSFV strains. Vet Res 2010; 41:7; PMID:19793538; http://dx.doi.org/10.1051/vetres/2009055
  • Bantscheff M, Hopf C, Savitski MM, Dittmann A, Grandi P, Michon AM, Schlegl J, Abraham Y, Becher I, Bergamini G, et al. Chemoproteomics profiling of HDAC inhibitors reveals selective targeting of HDAC complexes. Nat Biotechnol 2011; 29:255-65; PMID:21258344; http://dx.doi.org/10.1038/nbt.1759
  • Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, Matsui K, Uematsu S, Jung A, Kawai T, Ishii KJ, et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006; 441:101-5; PMID:16625202; http://dx.doi.org/10.1038/nature04734
  • Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, Taira K, Akira S, Fujita T. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 2004; 5:730-7; PMID:15208624; http://dx.doi.org/10.1038/ni1087
  • Tal MC, Sasai M, Lee HK, Yordy B, Shadel GS, Iwasaki A. Absence of autophagy results in reactive oxygen species-dependent amplification of RLR signaling. Proc Natl Acad Sci U S A 2009; 106:2770-5; PMID:19196953; http://dx.doi.org/10.1073/pnas.0807694106
  • Zafarullah M, Li WQ, Sylvester J, Ahmad M. Molecular mechanisms of N-acetylcysteine actions. Cell Mol Life Sci 2003; 60:6-20; PMID:12613655; http://dx.doi.org/10.1007/s000180300001
  • Li N, Ragheb K, Lawler G, Sturgis J, Rajwa B, Melendez JA, Robinson JP. Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J Biol Chem 2003; 278:8516-25; PMID:12496265; http://dx.doi.org/10.1074/jbc.M210432200
  • Crotzer VL, Blum JS. Autophagy and adaptive immunity. Immunology 2010; 131:9-17; PMID:20586810; http://dx.doi.org/10.1111/j.1365-2567.2010.03309.x
  • 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
  • Rubinsztein DC, Gestwicki JE, Murphy LO, Klionsky DJ. Potential therapeutic applications of autophagy. Nat Rev Drug Discov 2007; 6:304-12; PMID:17396135; http://dx.doi.org/10.1038/nrd2272
  • Liu Y, Schiff M, Czymmek K, Tallóczy Z, Levine B, Dinesh-Kumar SP. Autophagy regulates programmed cell death during the plant innate immune response. Cell 2005; 121:567-77; PMID:15907470; http://dx.doi.org/10.1016/j.cell.2005.03.007
  • Liang XH, Kleeman LK, Jiang HH, Gordon G, Goldman JE, Berry G, Herman B, Levine B. Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J Virol 1998; 72:8586-96; PMID:9765397
  • Crighton D, Wilkinson S, O'Prey J, Syed N, Smith P, Harrison PR, Gasco M, Garrone O, Crook T, Ryan KM. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 2006; 126:121-34; PMID:16839881; http://dx.doi.org/10.1016/j.cell.2006.05.034
  • Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B. 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
  • Yousefi S, Perozzo R, Schmid I, Ziemiecki A, Schaffner T, Scapozza L, Brunner T, Simon HU. Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat Cell Biol 2006; 8:1124-32; PMID:16998475; http://dx.doi.org/10.1038/ncb1482
  • Kang R, Zeh HJ, Lotze MT, Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ 2011; 18:571-80; PMID:21311563; http://dx.doi.org/10.1038/cdd.2010.191
  • Sun J, Jiang Y, Shi Z, Yan Y, Guo H, He F, Tu C. Proteomic alteration of PK-15 cells after infection by classical swine fever virus. J Proteome Res 2008; 7:5263-9; PMID:19367723; http://dx.doi.org/10.1021/pr800546m
  • Grummer B, Fischer S, Depner K, Riebe R, Blome S, Greiser-Wilke I. Replication of classical swine fever virus strains and isolates in different porcine cell lines. Dtsch Tierarztl Wochenschr 2006; 113:138-42; PMID:16716048
  • Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, Baba M, Baehrecke EH, Bahr BA, Ballabio A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4:151-75; PMID:18188003; http://dx.doi.org/10.4161/auto.5338
  • Klionsky DJ, Cuervo AM, Seglen PO. Methods for monitoring autophagy from yeast to human. Autophagy 2007; 3:181-206; PMID:17224625; http://dx.doi.org/10.4161/auto.3678
  • Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, Levine B. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 1999; 402:672-6; PMID:10604474; http://dx.doi.org/10.1038/45257
  • Cao Y, Klionsky DJ. Physiological functions of Atg6/Beclin 1: a unique autophagy-related protein. Cell Res 2007; 17:839-49; PMID:17893711; http://dx.doi.org/10.1038/cr.2007.78
  • Joubert PE, Werneke SW, de la Calle C, Guivel-Benhassine F, Giodini A, Peduto L, Levine B, Schwartz O, Lenschow DJ, Albert ML. Chikungunya virus-induced autophagy delays caspase-dependent cell death. J Exp Med 2012; 209:1029-47; PMID:22508836; http://dx.doi.org/10.1084/jem.20110996
  • Shrivastava S, Raychoudhuri A, Steele R, Ray R, Ray RB. Knockdown of autophagy enhances the innate immune response in hepatitis C virus-infected hepatocytes. Hepatology 2011; 53:406-14; PMID:21274862; http://dx.doi.org/10.1002/hep.24073
  • Gannagé M, Dormann D, Albrecht R, Dengjel J, Torossi T, Rämer PC, Lee M, Strowig T, Arrey F, Conenello G, et al. Matrix protein 2 of influenza A virus blocks autophagosome fusion with lysosomes. Cell Host Microbe 2009; 6:367-80; http://dx.doi.org/10.1016/j.chom.2009.09.005
  • Bauhofer O, Summerfield A, Sakoda Y, Tratschin JD, Hofmann MA, Ruggli N. Classical swine fever virus Npro interacts with interferon regulatory factor 3 and induces its proteasomal degradation. J Virol 2007; 81:3087-96; PMID:17215286; http://dx.doi.org/10.1128/JVI.02032-06
  • Ruggli N, Bird BH, Liu L, Bauhofer O, Tratschin JD, Hofmann MA. N(pro) of classical swine fever virus is an antagonist of double-stranded RNA-mediated apoptosis and IFN-α/β induction. Virology 2005; 340:265-76; PMID:16043207; http://dx.doi.org/10.1016/j.virol.2005.06.033
  • Chawla-Sarkar M, Leaman DW, Jacobs BS, Borden EC. IFN-β pretreatment sensitizes human melanoma cells to TRAIL/Apo2 ligand-induced apoptosis. J Immunol 2002; 169:847-55; PMID:12097388; http://dx.doi.org/10.4049/jimmunol.169.2.847
  • Kaser A, Nagata S, Tilg H. Interferon α augments activation-induced T cell death by upregulation of Fas (CD95/APO-1) and Fas ligand expression. Cytokine 1999; 11:736-43; PMID:10525311; http://dx.doi.org/10.1006/cyto.1998.0484
  • Shigeno M, Nakao K, Ichikawa T, Suzuki K, Kawakami A, Abiru S, Miyazoe S, Nakagawa Y, Ishikawa H, Hamasaki K, et al. Interferon-α sensitizes human hepatoma cells to TRAIL-induced apoptosis through DR5 upregulation and NF-kappa B inactivation. Oncogene 2003; 22:1653-62; PMID:12642868; http://dx.doi.org/10.1038/sj.onc.1206139
  • Oshima K, Yanase N, Ibukiyama C, Yamashina A, Kayagaki N, Yagita H, Mizuguchi J. Involvement of TRAIL/TRAIL-R interaction in IFN-α-induced apoptosis of Daudi B lymphoma cells. Cytokine 2001; 14:193-201; PMID:11448118; http://dx.doi.org/10.1006/cyto.2001.0873
  • Warzych E, Wrenzycki C, Peippo J, Lechniak D. Maturation medium supplements affect transcript level of apoptosis and cell survival related genes in bovine blastocysts produced in vitro. Mol Reprod Dev 2007; 74:280-9; PMID:16955406; http://dx.doi.org/10.1002/mrd.20610
  • Flaws JA, Hirshfield AN, Hewitt JA, Babus JK, Furth PA. Effect of bcl-2 on the primordial follicle endowment in the mouse ovary. Biol Reprod 2001; 64:1153-9; PMID:11259262; http://dx.doi.org/10.1095/biolreprod64.4.1153
  • Kato H, Takahasi K, Fujita T. RIG-I-like receptors: cytoplasmic sensors for non-self RNA. Immunol Rev 2011; 243:91-8; PMID:21884169; http://dx.doi.org/10.1111/j.1600-065X.2011.01052.x
  • Kawai T, Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 2011; 34:637-50; PMID:21616434; http://dx.doi.org/10.1016/j.immuni.2011.05.006
  • Honda K, Takaoka A, Taniguchi T. Type I interferon gene induction by the interferon regulatory factor family of transcription factors. Immunity 2006; 25:349-60; PMID:16979567; http://dx.doi.org/10.1016/j.immuni.2006.08.009

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.