Enterovirus 71 3C proteolytically processes the histone H3 N-terminal tail during infection

Meng Miao; Gang Deng; Xiaobei Xiong; Yang Qiu; Wenda Huang; Meng Yuan; Fei Yu; Shimei Bai; Xi Zhou; Xiaolu Zhao

doi:10.1016/j.virs.2022.02.006

April 2022

Meng Miao, Gang Deng, Xiaobei Xiong, Yang Qiu, Wenda Huang, Meng Yuan, Fei Yu, Shimei Bai, Xi Zhou and Xiaolu Zhao. Enterovirus 71 3C proteolytically processes the histone H3 N-terminal tail during infection[J]. Virologica Sinica, 2022, 37(2): 314-317. doi: 10.1016/j.virs.2022.02.006

Citation: Meng Miao, Gang Deng, Xiaobei Xiong, Yang Qiu, Wenda Huang, Meng Yuan, Fei Yu, Shimei Bai, Xi Zhou, Xiaolu Zhao. Enterovirus 71 3C proteolytically processes the histone H3 N-terminal tail during infection .VIROLOGICA SINICA, 2022, 37(2) : 314-317. http://dx.doi.org/10.1016/j.virs.2022.02.006

EV71 3C在感染过程中对宿主组蛋白H3进行N末端切割

苗蒙 ^a,b,, ,
邓港 ^a ,
熊晓蓓 ^c ,
邱洋 ^c ,
黄文达 ^a ,
袁梦 ^a ,
俞飞 ^a ,
白世梅 ^b ,
周溪 ^c,, ,
赵晓璐 ^a,,

a 武汉大学生命科学学院, 湖北省细胞稳态重点实验室
b 浙江理工大学生命科学与医药学院生物化学学科组
c 中国科学院武汉病毒研究所RNA病毒学实验室

通讯作者： 苗蒙, miaom@whu.edu.cn; 周溪, zhouxi@whu.edu.cn; 赵晓璐, zhaoxiaolu@whu.edu.cn
收稿日期： 2021-03-25
录用日期： 2022-02-16

摘要

3C蛋白酶是小核糖核酸病毒的重要组成部分，能够在病毒感染时劫持宿主细胞的翻译机器并蛋白酶解多种宿主因子进而帮助病毒复制。我们研究发现，肠道病毒71的3C蛋白酶在病毒感染时可以进入宿主细胞核，并在核内对宿主组蛋白H3进行N末端切割。我们的研究表明EV71感染能够改变宿主组蛋白，有可能是一种病毒调控宿主基因表达的新机制，将对病毒本身的复制以及宿主细胞产生全面影响。
- RNA病毒
- , EV71
- , 组蛋白H3
- , 蛋白酶切割
- , 组蛋白修饰

Enterovirus 71 3C proteolytically processes the histone H3 N-terminal tail during infection

Meng Miao ^a,b,, ,
Gang Deng ^a ,
Xiaobei Xiong ^c ,
Yang Qiu ^c ,
Wenda Huang ^a ,
Meng Yuan ^a ,
Fei Yu ^a ,
Shimei Bai ^b ,
Xi Zhou ^c,, ,
Xiaolu Zhao ^a,,

a Hubei Key Laboratory of Cell Homeostasis, College of Life Sciences, Wuhan University, Wuhan, 430072, China
b Institute of Biochemistry, College of Life Sciences and Medicine, Zhejiang Sci-Tech University, Hangzhou, 310018, China
c Laboratory of RNA Virology, Wuhan Institute of Virology, Chinese Academy of Science, Wuhan, 430071, China

Corresponding author: Meng Miao, miaom@whu.edu.cn Xi Zhou, zhouxi@whu.edu.cn Xiaolu Zhao, zhaoxiaolu@whu.edu.cn
Received Date: 25 March 2021
Accepted Date: 16 February 2022

Abstract

Highlights
1. The N-terminal tail of histone H3 is specifically cleaved during EV71 infection.
2. Viral protease 3C is identified as a protease responsible for proteolytically processing the N-terminal H3 tail.
3. Our finding reveals a new epigenetic regulatory mechanism for Enterovirus 71 in virus-host interactions.

References
1. Amineva, S.P., Aminev, A.G., Palmenberg, A.C., Gern, J.E., 2004. Rhinovirus 3C protease precursors 3CD and 3CD' localize to the nuclei of infected cells. J. Gen. Virol. 85, 2969–2979.
2. Bhaumik, S.R., Smith, E., Shilatifard, A., 2007. Covalent modifications of histones during development and disease pathogenesis. Nat. Struct. Mol. Biol. 14, 1008–1016.
3. Britton, L.M., Sova, P., Belisle, S., Liu, S., Chan, E.Y., Katze, M.G., Garcia, B.A., 2014. A proteomic glimpse into the initial global epigenetic changes during HIV infection. Proteomics 14, 2226–2230.
4. Clark, M.E., Hammerle, T., Wimmer, E., Dasgupta, A., 1991. Poliovirus proteinase 3C converts an active form of transcription factor IIIC to an inactive form: a mechanism for inhibition of host cell polymerase III transcription by poliovirus. EMBO J. 10, 2941–2947.
5. Clark, M.E., Lieberman, P.M., Berk, A.J., Dasgupta, A., 1993. Direct cleavage of human TATA-binding protein by poliovirus protease 3C in vivo and in vitro. Mol. Cell Biol. 13, 1232–1237.
6. Etchison, D., Milburn, S.C., Edery, I., Sonenberg, N., Hershey, J.W., 1982. Inhibition of HeLa cell protein synthesis following poliovirus infection correlates with the proteolysis of a 220,000-dalton polypeptide associated with eucaryotic initiation factor 3 and a cap binding protein complex. J. Biol. Chem. 257, 14806–14810.
7. Fonseca, G.J., Thillainadesan, G., Yousef, A.F., Ablack, J.N., Mossman, K.L., Torchia, J., Mymryk, J.S., 2012. Adenovirus evasion of interferon-mediated innate immunity by direct antagonism of a cellular histone posttranslational modification. Cell Host Microbe 11, 597–606.
8. Genin, P., Lin, R., Hiscott, J., Civas, A., 2012. Recruitment of histone deacetylase 3 to the interferon-A gene promoters attenuates interferon expression. PLoS One 7, e38336.
9. Guo, Q., Sidoli, S., Garcia, B.A., Zhao, X., 2018. Assessment of quantification precision of histone post-translational modifications by using an ion trap and down to 50 000 cells as starting material. J. Proteome Res. 17, 234–242. Jan 5.
10. Han, X., Li, X., Yue, S.C., Anandaiah, A., Hashem, F., Reinach, P.S., Koziel, H., Tachado, S.D., 2012. Epigenetic regulation of tumor necrosis factor alpha (TNFalpha) release in human macrophages by HIV-1 single-stranded RNA (ssRNA) is dependent on TLR8 signaling. J. Biol. Chem. 287, 13778–13786.
11. Horwitz, G.A., Zhang, K., McBrian, M.A., Grunstein, M., Kurdistani, S.K., Berk, A.J., 2008. Adenovirus small e1a alters global patterns of histone modification. Science 321, 1084–1085.
12. Huang, H., Sabari, B.R., Garcia, B.A., Allis, C.D., Zhao, Y., 2014. SnapShot: histone modifications. Cell 159, 458–458.e1.
13. Kitamura, N., Semler, B.L., Rothberg, P.G., Larsen, G.R., Adler, C.J., et al., 1981. Primary structure, gene organization and polypeptide expression of poliovirus RNA. Nature 291, 547–553.
14. Kouzarides, T., 2007. Chromatin modifications and their function. Cell 128, 693–705.
15. Lieberman, P.M., 2006. Chromatin regulation of virus infection. Trends Microbiol. 14, 132–140.
16. Matthews, D.A., Smith, W.W., Ferre, R.A., Condon, B., Budahazi, G., et al., 1994. Structure of human rhinovirus 3C protease reveals a trypsin-like polypeptide fold, RNA-binding site, and means for cleaving precursor polyprotein. Cell 77, 761–771.
17. McMinn, P.C., 2002. An overview of the evolution of enterovirus 71 and its clinical and public health significance. FEMS Microbiol. Rev. 26, 91–107.
18. Murata, T., Kondo, Y., Sugimoto, A., et al., 2012. Epigenetic histone modification of Epstein-Barr virus BZLF1 promoter during latency and reactivation in Raji cells. J. Virol. 86, 4752–4761.
19. O'Connor, C.M., DiMaggio Jr., P.A., Shenk, T., Garcia, B.A., 2014. Quantitative proteomic discovery of dynamic epigenome changes that control human cytomegalovirus(HCMV) infection. Mol. Cell. Proteomics 13, 2399–2410.
20. Oberste, M.S., Maher, K., Kilpatrick, D.R., Pallansch, M.A., 1999. Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J. Virol. 73, 1941–1948.
21. Placek, B.J., Huang, J., Kent, J.R., Dorsey, J., Rice, L., Fraser, N.W., Berger, S.L., 2009. The histone variant H3.3 regulates gene expression during lytic infection with herpes simplex virus type 1. J. Virol. 83, 1416–1421.
22. Rose, J.K., Trachsel, H., Leong, K., Baltimore, D., 1978. Inhibition of translation by poliovirus: inactivation of a specific initiation factor. Proc. Natl. Acad. Sci. U.S.A. 75, 2732–2736.
23. Schmidt, N.J., Lennette, E.H., Ho, H.H., 1974. An apparently new enterovirus isolated from patients with disease of the central nervous system. J. Infect. Dis. 129, 304–309.
24. Sharma, R., Raychaudhuri, S., Dasgupta, A., 2004. Nuclear entry of poliovirus protease polymerase precursor 3CD: implications for host cell transcription shutoff. Virology 320, 195–205.
25. Shih, S.R., Chiang, C., Chen, T.C., Wu, C.N., Hsu, J.T., Lee, J.C., Hwang, M.J., Li, M.L., Chen, G.W., Ho, M.S., 2004. Mutations at KFRDI and VGK domains of enterovirus 71 3C protease affect its RNA binding and proteolytic activities. J. Biomed. Sci. 11, 239–248.
26. Solomon, T., Lewthwaite, P., Perera, D., Cardosa, M.J., McMinn, P., Ooi, M.H., 2010. Virology, epidemiology, pathogenesis, and control of enterovirus 71. Lancet Infect. Dis. 10, 778–790.
27. Weidman, M.K., Yalamanchili, P., Ng, B., Tsai, W., Dasgupta, A., 2001. Poliovirus 3C protease-mediated degradation of transcriptional activator p53 requires a cellular activity. Virology 291, 260–271.
28. Weng, K.F., Li, M.L., Hung, C.T., Shih, S.R., 2009. Enterovirus 71 3C protease cleaves a novel target CstF-64 and inhibits cellular polyadenylation. PLoS Pathog. 5, e1000593.
Proportional views
Electronic Supplementary Material

10.1016j.virs.2022.02.006-ESM.docx