EV71 3C protease induces apoptosis by cleavage of hnRNP A1 to promote apaf-1 translation

English version

Autoři: Mei-Ling Li ^aff001; Jing-Yi Lin ^aff002; Bo-Shiun Chen ^aff003; Kuo-Feng Weng ^aff003; Shin-Ru Shih ^aff003; Jesse Davila Calderon ^aff005; Blanton S. Tolbert ^aff005; Gary Brewer ^aff001
Působiště autorů: Department of Biochemistry and Molecular Biology, Rutgers Robert Wood Johnson Medical School, Piscataway, NJ, United States of America ^aff001; Department of Clinical Laboratory Sciences and Medical Biotechnology, College of Medicine, National Taiwan University, Taipei, Taiwan ^aff002; Research Center for Emerging Viral Infections, Chang Gung University, Tao-Yuan, Taiwan ^aff003; Department of Medical Biotechnology and Laboratory Science, Chang Gung University, Tao-Yuan, Taiwan ^aff004; Department of Chemistry, Case Western Reserve University, Cleveland, OH, United States of America ^aff005
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0221048

Souhrn

Enterovirus 71 (EV71) induces apoptosis to promote viral particle release. Earlier work showed that EV71 utilizes its 3C protease to induce apoptosis in a caspase-3-dependent pathway, though the mechanism is unknown. However, work from Vagner, Holcik and colleagues showed that host protein heterogeneous ribonucleoprotein A1 (hnRNP A1) binds the IRES of cellular apoptotic peptidase activating factor 1 (apaf-1) mRNA to repress its translation. In this work, we show that apaf-1 expression is essential for EV71-induced apoptosis. EV71 infection or ectopic expression of 3C protease cleaves hnRNP A1, which abolishes its binding to the apaf-1 IRES. This allows IRES-dependent synthesis of apaf-1, activation of caspase-3, and apoptosis. Thus, we reveal a novel mechanism that EV71 utilizes for virus release via a 3C protease–hnRNP A1–apaf-1–caspase-3–apoptosis axis.

Klíčová slova:

Biology and life sciences – Cell biology – Cell processes – Cell death – Apoptosis – Microbiology – Virology – Viral replication – Internal ribosome entry site – Biochemistry – Enzymology – Enzymes – Proteases – Proteins – Nucleic acids – RNA – Non-coding RNA – Genetics – Gene expression – Gene regulation – Small interfering RNAs – Protein translation – Molecular biology – Molecular biology techniques – Transfection – DNA construction – Plasmid construction – Research and analysis methods – Precipitation techniques – Immunoprecipitation

Zdroje

1. McMinn PC. An overview of the evolution of enterovirus 71 and its clinical and public health significance. FEMS MicrobiolRev. 2002;26(1):91–107.

2. Ooi MH, Wong SC, Lewthwaite P, Cardosa MJ, Solomon T. Clinical features, diagnosis, and management of enterovirus 71. Lancet Neurol. 2010;9(11):1097–105. Epub 2010/10/23. S1474-4422(10)70209-X [pii] doi: 10.1016/S1474-4422(10)70209-X 20965438.

3. Solomon T, Lewthwaite P, Perera D, Cardosa MJ, McMinn P, Ooi MH. Virology, epidemiology, pathogenesis, and control of enterovirus 71. Lancet Infect Dis. 2010;10(11):778–90. Epub 2010/10/22. S1473-3099(10)70194-8 [pii] doi: 10.1016/S1473-3099(10)70194-8 20961813.

4. Lee KY. Enterovirus 71 infection and neurological complications. Korean journal of pediatrics. 2016;59(10):395–401. Epub 2016/11/09. doi: 10.3345/kjp.2016.59.10.395 27826325; PubMed Central PMCID: PMC5099286.

5. Huang PN, Shih SR. Update on enterovirus 71 infection. Current opinion in virology. 2014;5:98–104. Epub 2014/04/15. doi: 10.1016/j.coviro.2014.03.007 24727707.

6. Chang SC, Lin JY, Lo LY, Li ML, Shih SR. Diverse apoptotic pathways in enterovirus 71-infected cells. JNeurovirol. 2004;10(6):338–49.

7. Chang YL, Ho BC, Sher S, Yu SL, Yang PC. miR-146a and miR-370 coordinate enterovirus 71-induced cell apoptosis through targeting SOS1 and GADD45beta. Cell Microbiol. 2015;17(6):802–18. Epub 2014/12/04. doi: 10.1111/cmi.12401 25469565.

8. Lu JR, Lu WW, Lai JZ, Tsai FL, Wu SH, Lin CW, et al. Calcium flux and calpain-mediated activation of the apoptosis-inducing factor contribute to enterovirus 71-induced apoptosis. J Gen Virol. 2013;94(Pt 7):1477–85. Epub 2013/03/22. doi: 10.1099/vir.0.047753-0 23515028.

9. Cong H, Du N, Yang Y, Song L, Zhang W, Tien P. Enterovirus 71 2B Induces Cell Apoptosis by Directly Inducing the Conformational Activation of the Proapoptotic Protein Bax. J Virol. 2016;90(21):9862–77. Epub 2016/08/26. doi: 10.1128/JVI.01499-16 27558414; PubMed Central PMCID: PMC5068536.

10. Kuo RL, Kung SH, Hsu YY, Liu WT. Infection with enterovirus 71 or expression of its 2A protease induces apoptotic cell death. JGenVirol. 2002;83(Pt 6):1367–76.

11. Li ML, Hsu TA, Chen TC, Chang SC, Lee JC, Chen CC, et al. The 3C protease activity of enterovirus 71 induces human neural cell apoptosis. Virology. 2002;293(2):386–95. doi: 10.1006/viro.2001.1310 11886259

12. Wu CC, Lee S, Malladi S, Chen MD, Mastrandrea NJ, Zhang Z, et al. The Apaf-1 apoptosome induces formation of caspase-9 homo- and heterodimers with distinct activities. Nature communications. 2016;7:13565. Epub 2016/11/25. doi: 10.1038/ncomms13565 27882936; PubMed Central PMCID: PMC5123071.

13. Coldwell MJ, Mitchell SA, Stoneley M, MacFarlane M, Willis AE. Initiation of Apaf-1 translation by internal ribosome entry. Oncogene. 2000;19(7):899–905. Epub 2000/03/07. doi: 10.1038/sj.onc.1203407 10702798.

14. Ungureanu NH, Cloutier M, Lewis SM, de Silva N, Blais JD, Bell JC, et al. Internal ribosome entry site-mediated translation of Apaf-1, but not XIAP, is regulated during UV-induced cell death. J Biol Chem. 2006;281(22):15155–63. Epub 2006/04/06. doi: 10.1074/jbc.M511319200 16595687.

15. Andreev DE, Dmitriev SE, Zinovkin R, Terenin IM, Shatsky IN. The 5' untranslated region of Apaf-1 mRNA directs translation under apoptosis conditions via a 5' end-dependent scanning mechanism. FEBS Lett. 2012;586(23):4139–43. Epub 2012/10/23. doi: 10.1016/j.febslet.2012.10.010 23085065.

16. Cammas A, Pileur F, Bonnal S, Lewis SM, Leveque N, Holcik M, et al. Cytoplasmic relocalization of heterogeneous nuclear ribonucleoprotein A1 controls translation initiation of specific mRNAs. MolBiolCell. 2007;18(12):5048–59.

17. Levengood JD, Tolbert M, Li ML, Tolbert BS. High-affinity interaction of hnRNP A1 with conserved RNA structural elements is required for translation and replication of enterovirus 71. RNA biology. 2013;10(7):1136–45. Epub 2013/06/04. doi: 10.4161/rna.25107 23727900.

18. Lin JY, Shih SR, Pan M, Li C, Lue CF, Stollar V, et al. hnRNP A1 interacts with the 5' untranslated regions of enterovirus 71 and Sindbis virus RNA and is required for viral replication. JVirol. 2009;83(12):6106–14.

19. Lin JY, Li ML, Brewer G. mRNA decay factor AUF1 binds the internal ribosomal entry site of enterovirus 71 and inhibits virus replication. PloS one. 2014;9(7):e103827. Epub 2014/08/01. doi: 10.1371/journal.pone.0103827 25077793; PubMed Central PMCID: PMC4117571.

20. Cathcart AL, Rozovics JM, Semler BL. Cellular mRNA decay protein AUF1 negatively regulates enterovirus and human rhinovirus infections. J Virol. 2013. Epub 2013/08/02. doi: 10.1128/JVI.01049-13 23903828.

21. Weng KF, Li ML, Hung CT, Shih SR. Enterovirus 71 3C protease cleaves a novel target CstF-64 and inhibits cellular polyadenylation. PLoSPathog. 2009;5(9):e1000593.

22. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell. 1997;90(3):405–13. doi: 10.1016/s0092-8674(00)80501-2 9267021

23. Tolbert M, Morgan CE, Pollum M, Crespo-Hernandez CE, Li ML, Brewer G, et al. HnRNP A1 Alters the Structure of a Conserved Enterovirus IRES Domain to Stimulate Viral Translation. J Mol Biol. 2017. Epub 2017/06/20. doi: 10.1016/j.jmb.2017.06.007 28625847.

24. Shih SR, Chiang C, Chen TC, Wu CN, Hsu JT, Lee JC, et al. Mutations at KFRDI and VGK domains of enterovirus 71 3C protease affect its RNA binding and proteolytic activities. JBiomedSci. 2004;11(2):239–48.

25. Lei X, Liu X, Ma Y, Sun Z, Yang Y, Jin Q, et al. The 3C protein of enterovirus 71 inhibits retinoid acid-inducible gene I-mediated interferon regulatory factor 3 activation and type I interferon responses. J Virol. 2010;84(16):8051–61. Epub 2010/06/04. doi: 10.1128/JVI.02491-09 20519382; PubMed Central PMCID: PMC2916543.

26. Lei X, Sun Z, Liu X, Jin Q, He B, Wang J. Cleavage of the adaptor protein TRIF by enterovirus 71 3C inhibits antiviral responses mediated by Toll-like receptor 3. J Virol. 2011;85(17):8811–8. Epub 2011/06/24. doi: 10.1128/JVI.00447-11 21697485; PubMed Central PMCID: PMC3165803.

27. Lei X, Xiao X, Xue Q, Jin Q, He B, Wang J. Cleavage of interferon regulatory factor 7 by enterovirus 71 3C suppresses cellular responses. J Virol. 2013;87(3):1690–8. Epub 2012/11/24. doi: 10.1128/JVI.01855-12 23175366; PubMed Central PMCID: PMC3554134.

28. Wang YF, Wang XY, Ren Z, Qian CW, Li YC, Kaio K, et al. Phyllaemblicin B inhibits Coxsackie virus B3 induced apoptosis and myocarditis. Antiviral Res. 2009;84(2):150–8. Epub 2009/08/25. doi: 10.1016/j.antiviral.2009.08.004 19699238.

29. Xi X, Zhang X, Wang B, Wang T, Wang J, Huang H, et al. The interplays between autophagy and apoptosis induced by enterovirus 71. PloS one. 2013;8(2):e56966. Epub 2013/02/26. doi: 10.1371/journal.pone.0056966 23437282; PubMed Central PMCID: PMC3577684.

30. Shi W, Li X, Hou X, Peng H, Jiang Q, Shi M, et al. Differential apoptosis gene expressions of rhabdomyosarcoma cells in response to enterovirus 71 infection. BMC infectious diseases. 2012;12:327. Epub 2012/11/30. doi: 10.1186/1471-2334-12-327 23191987; PubMed Central PMCID: PMC3536580.

31. Li J, Yao Y, Chen Y, Xu X, Lin Y, Yang Z, et al. Enterovirus 71 3C Promotes Apoptosis through Cleavage of PinX1, a Telomere Binding Protein. J Virol. 2017;91(2). Epub 2016/11/17. doi: 10.1128/JVI.02016-16 27847364; PubMed Central PMCID: PMC5215332.

32. Song F, Yu X, Zhong T, Wang Z, Meng X, Li Z, et al. Caspase-3 Inhibition Attenuates the Cytopathic Effects of EV71 Infection. Frontiers in microbiology. 2018;9:817. Epub 2018/05/15. doi: 10.3389/fmicb.2018.00817 29755438; PubMed Central PMCID: PMC5932146.

EV71 3C protease induces apoptosis by cleavage of hnRNP A1 to promote apaf-1 translation

Souhrn

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