Viperin triggers ribosome collision-dependent translation inhibition to restrict viral replication

被引:26
作者
Hsu, Jack Chun-Chieh [1 ]
Laurent-Rolle, Maudry [2 ,3 ]
Pawlak, Joanna B. [1 ,2 ]
Xia, Hongjie [4 ]
Kunte, Amit [1 ]
Hee, Jia Shee [1 ]
Lim, Jaechul [1 ]
Harris, Lawrence D. [5 ,6 ]
Wood, James M. [5 ,6 ]
Evans, Gary B. [5 ,6 ]
Shi, Pei-Yong [4 ,7 ,8 ,9 ]
Grove, Tyler L. [10 ]
Almo, Steven C. [10 ]
Cresswell, Peter [1 ,11 ]
机构
[1] Yale Univ, Sch Med, Dept Immunobiol, 333 Cedar St, New Haven, CT 06520 USA
[2] Yale Univ, Sch Med, Dept Internal Med, Sect Infect Dis, 333 Cedar St, New Haven, CT 06520 USA
[3] Yale Sch Med, Dept Microbial Pathogenesis, New Haven, CT 06520 USA
[4] Univ Texas Med Branch, Dept Biochem & Mol Biol, Galveston, TX 77555 USA
[5] Victoria Univ Wellington, Ferrier Res Inst, Wellington 6012, New Zealand
[6] Univ Auckland, Maurice Wilkins Ctr Mol Biodiscovery, Auckland 1010, New Zealand
[7] Univ Texas Med Branch, Inst Human Infect & Immun, Galveston, TX 77555 USA
[8] Univ Texas Med Branch, Sealy Inst Vaccine Sci, Galveston, TX 77555 USA
[9] Sealy Inst Drug Discovery, Galveston, TX 77555 USA
[10] Albert Einstein Coll Med, Dept Biochem, Bronx, NY 10461 USA
[11] Yale Univ, Sch Med, Dept Cell Biol, 333 Cedar St, New Haven, CT 06520 USA
关键词
WEST-NILE-VIRUS; INTERFERON-INDUCIBLE PROTEIN; NS2B-NS3; PROTEASE; CRYSTAL-STRUCTURE; KINASE PKR; GCN2; IDENTIFICATION; INFECTION; CELLS;
D O I
10.1016/j.molcel.2022.02.031
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Innate immune responses induce hundreds of interferon-stimulated genes (ISGs). Viperin, a member of the radical S-adenosyl methionine (SAM) superfamily of enzymes, is the product of one such ISG that restricts the replication of a broad spectrum of viruses. Here, we report a previously unknown antiviral mechanism in which viperin activates a ribosome collision-dependent pathway that inhibits both cellular and viral RNA translation. We found that the radical SAM activity of viperin is required for translation inhibition and that this is mediated by viperin's enzymatic product, 3'-deoxy-3',4'-didehydro-CTP (ddhCTP). Viperin triggers ribosome collisions and activates the MAPKKK ZAK pathway that in turn activates the GCN2 arm of the integrated stress response pathway to inhibit translation. The study illustrates the importance of translational repression in the antiviral response and identifies viperin as a translation regulator in innate immunity.
引用
收藏
页码:1631 / +
页数:19
相关论文
共 62 条
[1]   Research paper Using recombination-dependent lethal mutations to stabilize reporter flaviviruses for rapid serodiagnosis and drug discovery [J].
Baker, Coleman ;
Xie, Xuping ;
Zou, Jing ;
Muruato, Antonio ;
Fink, Katja ;
Shi, Pei-Yong .
EBIOMEDICINE, 2020, 57
[2]   Essential role for the dsRNA-dependent protein kinase PKR in innate immunity to viral infection [J].
Balachandran, S ;
Roberts, PC ;
Brown, LE ;
Truong, H ;
Pattnaik, AK ;
Archer, DR ;
Barber, GN .
IMMUNITY, 2000, 13 (01) :129-141
[3]   Antiviral effect of the mammalian translation initiation factor 2α kinase GCN2 against RNA viruses [J].
Berlanga, Juan J. ;
Ventoso, Ivan ;
Harding, Heather P. ;
Deng, Jing ;
Ron, David ;
Sonenberg, Nahum ;
Carrasco, Luis ;
de Haro, Cesar .
EMBO JOURNAL, 2006, 25 (08) :1730-1740
[4]   Ribosome-associated protein quality control [J].
Brandman, Onn ;
Hegde, Ramanujan S. .
NATURE STRUCTURAL & MOLECULAR BIOLOGY, 2016, 23 (01) :7-15
[5]   Viperin, MTAP44, and Protein Kinase R Contribute to the Interferon-Induced Inhibition of Bunyamwera Orthobunyavirus Replication [J].
Carlton-Smith, Charles ;
Elliott, Richard M. .
JOURNAL OF VIROLOGY, 2012, 86 (21) :11548-11557
[6]   Receptor-Mediated Sorting of Typhoid Toxin during Its Export from Salmonella Typhi-Infected Cells [J].
Chang, Shu-Jung ;
Song, Jeongmin ;
Galan, Jorge E. .
CELL HOST & MICROBE, 2016, 20 (05) :682-689
[7]   Viperin (cig5), an IFN-inducible antiviral protein directly induced by human cytomegalovirus [J].
Chin, KC ;
Cresswell, P .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2001, 98 (26) :15125-15130
[8]  
De Nardo D, 2018, METHODS MOL BIOL, V1784, P35, DOI 10.1007/978-1-4939-7837-3_4
[9]   GCN2 Has Inhibitory Effect on Human Immunodeficiency Virus-1 Protein Synthesis and Is Cleaved upon Viral Infection [J].
del Pino, Javier ;
Luis Jimenez, Jose ;
Ventoso, Ivan ;
Castello, Alfredo ;
Angeles Munoz-Fernandez, Ma ;
de Haro, Cesar ;
Jose Berlanga, Juan .
PLOS ONE, 2012, 7 (10)
[10]   Activation of GCN2 in UV-irradiated cells inhibits translation [J].
Deng, J ;
Harding, HP ;
Raught, B ;
Gingras, AC ;
Berlanga, JJ ;
Scheuner, D ;
Kaufman, RJ ;
Ron, D ;
Sonenberg, N .
CURRENT BIOLOGY, 2002, 12 (15) :1279-1286