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Research Article

Enterovirus 71 induces neural cell apoptosis and autophagy through promoting ACOX1 downregulation and ROS generation

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Pages 537-553 | Received 28 Jul 2019, Accepted 09 Dec 2019, Published online: 20 May 2020

References

  • Xing W, Liao Q, Viboud C, et al. Hand, foot, and mouth disease in China, 2008-12: an epidemiological study. Lancet Infect Dis. 2014;14(4):308–318.
  • Yang B, Liu F, Liao Q, et al. Epidemiology of hand, foot and mouth disease in China, 2008 to 2015 prior to the introduction of EV-A71 vaccine. Euro Surveill. 2017;22(50). DOI:https://doi.org/10.2807/1560-7917.ES.2017.22.50.16-00824.
  • Solomon T, Lewthwaite P, Perera D, et al. Virology, epidemiology, pathogenesis, and control of enterovirus 71. Lancet Infect Dis. 2010;10(11):778–790.
  • Wang W, Xiao F, Wan P, et al. EV71 3D protein binds with NLRP3 and enhances the assembly of inflammasome complex. PLoS Pathog. 2017;13(1):e1006123.
  • Kuo RL, Kung SH, Hsu YY, et al. Infection with enterovirus 71 or expression of its 2A protease induces apoptotic cell death. J Gen Virol. 2002;83(Pt 6):1367–1376.
  • Li J, Yao Y, Chen Y, et al. Enterovirus 71 3C promotes apoptosis through cleavage of PinX1, a telomere binding protein. J Virol. 2017;91(2). DOI:https://doi.org/10.1128/JVI.02016-16.
  • Cong H, Du N, Yang Y, et al. Enterovirus 71 2B induces cell apoptosis by directly inducing the conformational activation of the proapoptotic protein bax. J Virol. 2016;90(21):9862–9877.
  • Chen TC, Lai YK, Yu CK, et al. Enterovirus 71 triggering of neuronal apoptosis through activation of Abl-Cdk5 signalling. Cell Microbiol. 2007;9(11):2676–2688.
  • Chang YL, Ho BC, Sher S, et al. miR-146a and miR-370 coordinate enterovirus 71-induced cell apoptosis through targeting SOS1 and GADD45beta. Cell Microbiol. 2015;17(6):802–818.
  • Du X, Wang H, Xu F, et al. Enterovirus 71 induces apoptosis of SHSY5Y human neuroblastoma cells through stimulation of endogenous microRNA let-7b expression. Mol Med Rep. 2015;12(1):953–959.
  • Fu Y, Xu W, Chen D, et al. Enterovirus 71 induces autophagy by regulating has-miR-30a expression to promote viral replication. Antiviral Res. 2015;124:43–53.
  • Nordgren M, Fransen M. Peroxisomal metabolism and oxidative stress. Biochimie. 2014;98:56–62.
  • Trompier D, Vejux A, Zarrouk A, et al. Brain peroxisomes. Biochimie. 2014;98:102–110.
  • Berger J, Dorninger F, Forss-Petter S, et al. Peroxisomes in brain development and function. Biochim Biophys Acta. 2016;1863(5):934–955.
  • El Hajj HI, Vluggens A, Andreoletti P, et al. The inflammatory response in acyl-CoA oxidase 1 deficiency (pseudoneonatal adrenoleukodystrophy). Endocrinology. 2012;153(6):2568–2575.
  • Ferdinandusse S, Denis S, Hogenhout EM, et al. Clinical, biochemical, and mutational spectrum of peroxisomal acyl-coenzyme A oxidase deficiency. Hum Mutat. 2007;28(9):904–912.
  • Baarine M, Andreoletti P, Athias A, et al. Evidence of oxidative stress in very long chain fatty acid–treated oligodendrocytes and potentialization of ROS production using RNA interference-directed knockdown of ABCD1 and ACOX1 peroxisomal proteins. Neuroscience. 2012;213:1–18.
  • Wanders RJ, Waterham HR. Peroxisomal disorders: the single peroxisomal enzyme deficiencies. Biochim Biophys Acta. 2006;1763(12):1707–1720.
  • Eichler FS, Ren JQ, Cossoy M, et al. Is microglial apoptosis an early pathogenic change in cerebral X-linked adrenoleukodystrophy? Ann Neurol. 2008;63(6):729–742.
  • Feigenbaum V, Gelot A, Casanova P, et al. Apoptosis in the central nervous system of cerebral adrenoleukodystrophy patients. Neurobiol Dis. 2000;7(6 Pt B):600–612.
  • Odendall C, Dixit E, Stavru F, et al. Diverse intracellular pathogens activate type III interferon expression from peroxisomes. Nat Immunol. 2014;15(8):717–726.
  • Dixit E, Boulant S, Zhang Y, et al. Peroxisomes are signaling platforms for antiviral innate immunity. Cell. 2010;141(4):668–681.
  • Song Y, Cheng X, Yang X, et al. Early growth response-1 facilitates enterovirus 71 replication by direct binding to the viral genome RNA. Int J Biochem Cell Biol. 2015;62:36–46.
  • You J, Hou S, Malik-Soni N, et al. Flavivirus infection impairs peroxisome biogenesis and early antiviral signaling. J Virol. 2015;89(24):12349–12361.
  • Chu R, Varanasi U, Chu S, et al. Overexpression and characterization of the human peroxisomal acyl-CoA oxidase in insect cells. J Biol Chem. 1995;270(9):4908–4915.
  • Miyazawa S, Hayashi H, Hijikata M, et al. Complete nucleotide sequence of cDNA and predicted amino acid sequence of rat acyl-CoA oxidase. J Biol Chem. 1987;262(17):8131–8137.
  • Zhang X, Li K, Jones RA, et al. Structural characterization of acyl-CoA oxidases reveals a direct link between pheromone biosynthesis and metabolic state in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 2016;113(36):10055–10060.
  • Morita M, Imanaka T. Peroxisomal ABC transporters: structure, function and role in disease. Biochim Biophys Acta. 2012;1822(9):1387–1396.
  • Xu Z, Asahchop EL, Branton WG, et al. MicroRNAs upregulated during HIV infection target peroxisome biogenesis factors: implications for virus biology, disease mechanisms and neuropathology. PLoS Pathog. 2017;13(6):e1006360.
  • Mizushima N, Yoshimori T. How to interpret LC3 immunoblotting. Autophagy. 2007;3(6):542–545.
  • Bjorkoy G, Lamark T, Brech A, et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol. 2005;171(4):603–614.
  • Gotte K, Girzalsky W, Linkert M, et al. Pex19p, a farnesylated protein essential for peroxisome biogenesis. Mol Cell Biol. 1998;18(1):616–628.
  • Simon HU, Haj-Yehia A, Levi-Schaffer F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis. 2000;5(5):415–418.
  • Paine A, Eiz-Vesper B, Blasczyk R, et al. Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. Biochem Pharmacol. 2010;80(12):1895–1903.
  • Chan K, Han XD, Kan YW. An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen. Proc Natl Acad Sci U S A. 2001;98(8):4611–4616.
  • Clements CM, McNally RS, Conti BJ, et al. DJ-1, a cancer- and Parkinson’s disease-associated protein, stabilizes the antioxidant transcriptional master regulator Nrf2. Proc Natl Acad Sci U S A. 2006;103(41):15091–15096.
  • Shan Y, Lambrecht RW, Ghaziani T, et al. Role of Bach-1 in regulation of heme oxygenase-1 in human liver cells: insights from studies with small interfering RNAs. J Biol Chem. 2004;279(50):51769–51774.
  • Chang LY, Huang YC, Lin TY. Fulminant neurogenic pulmonary oedema with hand, foot, and mouth disease. Lancet. 1998;352(9125):367–368.
  • Hsueh C, Jung SM, Shih SR, et al. Acute encephalomyelitis during an outbreak of enterovirus type 71 infection in Taiwan: report of an autopsy case with pathologic, immunofluorescence, and molecular studies. Mod Pathol. 2000;13(11):1200–1205.
  • Lum LCS, Wong KT, Lam SK, et al. Fatal enterovirus 71 encephalomyelitis. J Paediatr. 1998;133(6):795–798.
  • Wang Z, Nicholls JM, Liu F, et al. Pulmonary and central nervous system pathology in fatal cases of hand foot and mouth disease caused by enterovirus A71 infection. Pathology. 2016;48(3):267–274.
  • Chen C, Wang Y, Shan C, et al. Crystal structure of enterovirus 71 RNA-dependent RNA polymerase complexed with its protein primer VPg: implication for a trans mechanism of VPg uridylylation. J Virol. 2013;87(10):5755–5768.
  • Sun Y, Wang Y, Shan C, et al. Enterovirus 71 VPg uridylation uses a two-molecular mechanism of 3D polymerase. J Virol. 2012;86(24):13662–13671.
  • Wang LC, Chen SO, Chang SP, et al. Enterovirus 71 proteins 2A and 3D antagonize the antiviral activity of gamma interferon via signaling attenuation. J Virol. 2015;89(14):7028–7037.
  • Yu J, Zhang L, Ren P, et al. Enterovirus 71 mediates cell cycle arrest in S phase through non-structural protein 3D. Cell Cycle. 2015;14(3):425–436.
  • Leon S, Goodman JM, Subramani S. Uniqueness of the mechanism of protein import into the peroxisome matrix: transport of folded, co-factor-bound and oligomeric proteins by shuttling receptors. Biochim Biophys Acta. 2006;1763(12):1552–1564.
  • Wu Y, Lou Z, Miao Y, et al. Structures of EV71 RNA-dependent RNA polymerase in complex with substrate and analogue provide a drug target against the hand-foot-and-mouth disease pandemic in China. Protein Cell. 2010;1(5):491–500.
  • Tung WH, Hsieh HL, Lee IT, et al. Enterovirus 71 induces integrin beta1/EGFR-Rac1-dependent oxidative stress in SK-N-SH cells: role of HO-1/CO in viral replication. J Cell Physiol. 2011;226(12):3316–3329.
  • Cheng ML, Weng SF, Kuo CH, et al. Enterovirus 71 induces mitochondrial reactive oxygen species generation that is required for efficient replication. PLoS One. 2014;9(11):e113234.
  • Bonekamp NA, Volkl A, Fahimi HD, et al. Reactive oxygen species and peroxisomes: struggling for balance. Biofactors. 2009;35(4):346–355.
  • Fransen M, Nordgren M, Wang B, et al. Role of peroxisomes in ROS/RNS-metabolism: implications for human disease. Biochim Biophys Acta. 2012;1822(9):1363–1373.
  • Muller CC, Nguyen TH, Ahlemeyer B, et al. PEX13 deficiency in mouse brain as a model of Zellweger syndrome: abnormal cerebellum formation, reactive gliosis and oxidative stress. Dis Model Mech. 2011;4(1):104–119.
  • Schipper HM, Song W, Zukor H, et al. Heme oxygenase-1 and neurodegeneration: expanding frontiers of engagement. J Neurochem. 2009;110(2):469–485.
  • Gill AJ, Kovacsics CE, Cross SA, et al. Heme oxygenase-1 deficiency accompanies neuropathogenesis of HIV-associated neurocognitive disorders. J Clin Invest. 2014;124(10):4459–4472.
  • Cobley JN, Fiorello ML, Bailey DM. 13 reasons why the brain is susceptible to oxidative stress. Redox Biol. 2018;15:490–503.
  • Hill-Batorski L, Halfmann P, Neumann G, et al. The cytoprotective enzyme heme oxygenase-1 suppresses Ebola virus replication. J Virol. 2013;87(24):13795–13802.
  • Tseng CK, Lin CK, Wu YH, et al. Human heme oxygenase 1 is a potential host cell factor against dengue virus replication. Sci Rep. 2016;6(1):32176.
  • Espinoza JA, Leon MA, Cespedes PF, et al. Heme oxygenase-1 modulates human respiratory syncytial virus replication and lung pathogenesis during infection. J Immunol. 2017;199(1):212–223.
  • Schmidt WN, Mathahs MM, Zhu Z. Heme and HO-1 inhibition of HCV, HBV, and HIV. Front Pharmacol. 2012;3:129.
  • Chang SC, Lin JY, Lo LY, et al. Diverse apoptotic pathways in enterovirus 71-infected cells. J Neurovirol. 2004;10(6):338–349.
  • Wang C, Zhou R, Zhang Z, et al. Intrinsic apoptosis and proinflammatory cytokines regulated in human astrocytes infected with enterovirus 71. J Gen Virol. 2015;96(10):3010–3022.
  • Shih SR, Weng KF, Stollar V, et al. Viral protein synthesis is required for enterovirus 71 to induce apoptosis in human glioblastoma cells. J Neurovirol. 2008;14(1):53–61.
  • Li ML, Hsu TA, Chen TC, et al. The 3C protease activity of enterovirus 71 induces human neural cell apoptosis. Virology. 2002;293(2):386–395.