The stress granule protein G3BP1 recruits protein kinase R to promote multiple innate immune antiviral responses

Journal of Virology

Volumn 89, Issue 5, 2015, Pages 2575-2589

  Reineke, Lucas C ^a   Lloyd, Richard E ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INITIATION FACTOR 2ALPHA; PROTEIN KINASE R; RAS GTPASE ACTIVATING PROTEIN BINDING PROTEIN 1; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; CARRIER PROTEIN; G3BP PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; EMBRYO; ENTEROVIRUS; GENE DELETION; INNATE IMMUNITY; MOUSE; NONHUMAN; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; TRANSCRIPTION INITIATION; VIRUS IMMUNITY; CELL LINE; HUMAN; IMMUNOLOGY; METABOLISM; PROTEIN ANALYSIS;

ENTEROVIRUS; POLIOVIRUS;

CARRIER PROTEINS; CELL LINE; EIF-2 KINASE; ENTEROVIRUS; HUMANS; IMMUNITY, INNATE; PROTEIN INTERACTION MAPPING;

EID: 84923066571     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02791-14     Document Type: Article

References (52)

1. Kedersha N, Chen S, Gilks N, Li W, Miller IJ, Stahl J, Anderson P. 2002. Evidence that ternary complex (eIF2-GTP-tRNA (i) (Met))-deficient preinitiation complexes are core constituents of mammalian stress granules. Mol Biol Cell 13:195-210. http://dx.doi.org/10.1091/mbc.01-05-0221.
2. Kedersha N, Stoecklin G, Ayodele M, Yacono P, Lykke-Andersen J, Fritzler MJ, Scheuner D, Kaufman RJ, Golan DE, Anderson P. 2005. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J Cell Biol 169:871-884. http://dx.doi.org/10.1083/jcb.200502088.
3. Ariumi Y, Kuroki M, Kushima Y, Osugi K, Hijikata M, Maki M, Ikeda M, Kato N. 2011. Hepatitis C virus hijacks P-body and stress granule components around lipid droplets. J Virol 85:6882-6892. http://dx.doi.org/10.1128/JVI.02418-10.
4. Cristea IM, Rozjabek H, Molloy KR, Karki S, White LL, Rice CM, Rout MP, Chait BT, MacDonald MR. 2010. Host factors associated with the Sindbis virus RNA-dependent RNA polymerase: role for G3BP1 and G3BP2 in virus replication. J Virol 84:6720-6732. http://dx.doi.org/10.1128/JVI.01983-09.
5. Pager CT, Schütz S, Abraham TM, Luo G, Sarnow P. 2013. Modulation of hepatitis C virus RNA abundance and virus release by dispersion of processing bodies and enrichment of stress granules. Virology 435:472-484. http://dx.doi.org/10.1016/j.virol.2012.10.027.
6. Reineke LC, Lloyd RE. 2013. Diversion of stress granules and P-bodies during viral infection. Virology 436:255-267. http://dx.doi.org/10.1016/j.virol.2012.11.017.
7. Ng CS, Jogi M, Yoo JS, Onomoto K, Koike S, Iwasaki T, Yoneyama M, Kato H, Fujita T. 2013. Encephalomyocarditis virus disrupts stress granules, the critical platform for triggering antiviral innate immune responses. J Virol 87:9511-9522. http://dx.doi.org/10.1128/JVI.03248-12.
8. Parker F, Maurier F, Delumeau I, Duchesne M, Faucher D, Debussche L, Dugue A, Schweighoffer F, Tocque B. 1996. A Ras-GTPase-activating protein SH3-domain-binding protein. Mol Cell Biol 16:2561-2569.
9. Panas MD, Varjak M, Lulla A, Eng Merits KEA, Karlsson Hedestam GB, McInerney GM. 2012. Sequestration of G3BP coupled with efficient translation inhibits stress granules in Semliki Forest virus infection. Mol Biol Cell 23:4701-4712. http://dx.doi.org/10.1091/mbc.E12-08-0619.
10. White JP, Cardenas AM, Marissen WE, Lloyd RE. 2007. Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. Cell Host Microbe 2:295-305. http://dx.doi.org/10.1016/j.chom.2007.08.006.
11. Bidet K, Dadlani D, Garcia-Blanco MA. 2014. G3BP1, G3BP2 and CAPRIN1 are required for translation of interferon stimulated mRNAs and are targeted by a Dengue virus non-coding RNA. PLoS Pathog 10: e1004242. http://dx.doi.org/10.1371/journal.ppat.1004242.
12. Onomoto K, Jogi M, Yoo J-S, Narita R, Morimoto S, Takemura A, Sambhara S, Kawaguchi A, Osari S, Nagata K, Matsumiya T, Namiki H, Yoneyama M, Fujita T. 2012. Critical role of an antiviral stress granule containing RIG-I and PKR in viral detection and innate immunity. PLoS One 7:e43031. http://dx.doi.org/10.1371/journal.pone.0043031.
13. Langereis MA, Feng Q, van Kuppeveld FJ. 2013. MDA5 localizes to stress granules, but this localization is not required for the induction of type I interferon. J Virol 87:6314-6325. http://dx.doi.org/10.1128/JVI.03213-12.
14. Takahashi M, Higuchi M, Matsuki H, Yoshita M, Ohsawa T, Oie M, Fujii M. 2013. Stress granules inhibit apoptosis by reducing reactive oxygen species production. Mol Cell Biol 33:815-829. http://dx.doi.org/10.1128/MCB.00763-12.
15. Reineke LC, Dougherty JD, Pierre P, Lloyd RE. 2012. Large G3BPinduced granules trigger eIF2α phosphorylation. Mol Biol Cell 23:3499-3510. http://dx.doi.org/10.1091/mbc.E12-05-0385.
16. Tourriere H, Chebli K, Zekri L, Courselaud B, Blanchard JM, Tazi J. 2003. The RasGAP-associated endoribonuclease G3BP assembles stress granules. J Cell Biol 160:823-831. http://dx.doi.org/10.1083/jcb.200212128.
17. Varshavsky A. 2011. The N-end rule pathway and regulation by proteolysis. Protein Sci 20:1298-1345. http://dx.doi.org/10.1002/pro.666.
18. Taghavi N, Samuel CE. 2012. Protein kinase PKR catalytic activity is required for the PKR-dependent activation of mitogen-activated protein kinases and amplification of interferon beta induction following virus infection. Virology 427:208-216. http://dx.doi.org/10.1016/j.virol.2012.01.029.
19. Patel RC, Stanton P, Sen GC. 1996. Specific mutations near the amino terminus of double-stranded RNA-dependent protein kinase (PKR) differentially affect its double-strandedRNAbinding and dimerization properties. J Biol Chem 271:25657-25663. http://dx.doi.org/10.1074/jbc.271.41.25657.
20. Wasserman T, Katsenelson K, Daniliuc S, Hasin T, Choder M, Aronheim A. 2010. A novel c-Jun N-terminal kinase (JNK)-binding protein WDR62 is recruited to stress granules and mediates a nonclassical JNK activation. Mol Biol Cell 21:117-130. http://dx.doi.org/10.1091/mbc.E09-06-0512.
21. Lee SH, Wang X, DeJong J. 2000. Functional interactions between an atypical NF-kappaB site from the rat CYP2B1 promoter and the transcriptional repressor RBP-Jkappa/CBF1. Nucleic Acids Res 28:2091-2098. http://dx.doi.org/10.1093/nar/28.10.2091.
22. Tabor-Godwin JM, Ruller CM, Bagalso N, An N, Pagarigan RR, Harkins S, Gilbert PE, Kiosses WB, Gude NA, Cornell CT, Doran KS, Sussman MA, Whitton JL, Feuer R. 2010. A novel population of myeloid cells responding to coxsackievirus infection assists in the dissemination of virus within the neonatal CNS. J Neurosci 30:8676-8691. http://dx.doi.org/10.1523/JNEUROSCI.1860-10.2010.
23. Zekri L, Chebli K, Tourriere H, Nielsen FC, Hansen TVO, Rami A, Tazi J. 2005. Control of fetal growth and neonatal survival by the RasGAPassociated endoribonuclease G3BP. Mol Cell Biol 25:8703-8716. http://dx.doi.org/10.1128/MCB.25.19.8703-8716.2005.
24. Kedersha N, Tisdale S, Hickman T, Anderson P. 2008. Real-time and quantitative imaging of mammalian stress granules and processing bodies RNA turnover in eukaryotes: nucleases, pathways and anaylsis of mRNA decay, 1st ed. Elsevier Inc., New York, NY.
25. Byrd MP, Zamora M, Lloyd RE. 2005. Translation of eukaryotic translation initiation factor 4GI (eIF4GI) proceeds from multiple mRNAs containing a novel cap-dependent internal ribosome entry site (IRES) that is active during poliovirus infection. J Biol Chem 280:18610-18622. http://dx.doi.org/10.1074/jbc.M414014200.
26. White JP, Reineke LC, Lloyd RE. 2011. Poliovirus switches to an eIF2-independent mode of translation during infection. J Virol 85:8884-8893. http://dx.doi.org/10.1128/JVI.00792-11.
27. Vandermark ER, Deluca KA, Gardner CR, Marker DF, Schreiner CN, Strickland DA, Wilton KM, Mondal S, Woodworth CD. 2012. Human papillomavirus type 16 E6 and E7 proteins alter NF-κB in cultured cervical epithelial cells and inhibition of NF-κB promotes cell growth and immortalization. Virology 425:53-60. http://dx.doi.org/10.1016/j.virol.2011.12.023.
28. Nees M, Geoghegan JM, Hyman T, Frank S, Miller L, Woodworth CD. 2001. Papillomavirus type 16 oncogenes downregulate expression of interferon-responsive genes and upregulate proliferation-associated and NF-kappaB-responsive genes in cervical keratinocytes. J Virol 75:4283-4296. http://dx.doi.org/10.1128/JVI.75.9.4283-4296.2001.
29. Ronco LV, Karpova AY, Vidal M, Howley PM. 1998. Human papillomavirus 16 E6 oncoprotein binds to interferon regulatory factor-3 and inhibits its transcriptional activity. Gene Dev 12:2061-2072. http://dx.doi.org/10.1101/gad.12.13.2061.
30. Hebner CM, Wilson R, Rader J, Bidder M, Laimins LA. 2006. Human papillomaviruses target the double-stranded RNA protein kinase pathway. J Gen Virol 87:3183-3193. http://dx.doi.org/10.1099/vir.0.82098-0.
31. Martin S, Zekri L, Metz A, Maurice T, Chebli K, Vignes M, Tazi J. 2013. Deficiency of G3BP1, the stress granules assembly factor, results in abnormal synaptic plasticity and calcium homeostasis in neurons. J Neurochem 125:175-184. http://dx.doi.org/10.1111/jnc.12189.
32. Piotrowska J, Hansen SJ, Park N, Jamka K, Sarnow P, Gustin KE. 2010. Stable formation of compositionally unique stress granules in virus-infected cells. J Virol 84:3654-3665. http://dx.doi.org/10.1128/JVI.01320-09.
33. Yoo J-S, Takahasi K, Ng CS, Ouda R, Onomoto K, Yoneyama M, Lai JC, Lattmann S, Nagamine Y, Matsui T, Iwabuchi K, Kato H, Fujita T. 2014. DHX36 Enhances RIG-I signaling by facilitating PKR-mediated antiviral stress granule formation. PLoS Pathog 10:e1004012. http://dx.doi.org/10.1371/journal.ppat.1004012.
34. Zhang P, Langland JO, Jacobs BL, Samuel CE. 2009. Protein kinase PKR-dependent activation of mitogen-activated protein kinases occurs through mitochondrial adapter IPS-1 and is antagonized by vaccinia virus E3L. J Virol 83:5718-5725. http://dx.doi.org/10.1128/JVI.00224-09.
35. Söderberg O, Gullberg M, Jarvius M, Ridderstråle K, Leuchowius K-J, Jarvius J, Wester K, Hydbring P, Bahram F, Larsson L-G, Landegren U. 2006. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods 3:995-1000. http://dx.doi.org/10.1038/nmeth947.
36. Söderberg O, Leuchowius K-J, Gullberg M, Jarvius M, Weibrecht I, Larsson L-G, Landegren U. 2008. Characterizing proteins and their interactions in cells and tissues using the in situ proximity ligation assay. Methods 45:227-232. http://dx.doi.org/10.1016/j.ymeth.2008.06.014.
37. Fung G, Ng CS, Zhang J, Shi J, Wong J, Piesik P, Han L, Chu F, Jagdeo J, Jan E, Fujita T, Luo H. 2013. Production of a dominant-negative fragment Due to G3BP1 cleavage contributes to the disruption of mitochondria-associated protective stress granules during CVB3 infection. PLoS One 8:e79546. http://dx.doi.org/10.1371/journal.pone.0079546.
38. Bonnet MC, Weil R, Dam E, Hovanessian AG, Meurs EF. 2000. PKR stimulates NF-kappa B irrespective of its kinase function by interacting with the Ikappa B kinase complex. Mol Cell Biol 20:4532-4542. http://dx.doi.org/10.1128/MCB.20.13.4532-4542.2000.
39. Garcia MA, Gil J, Ventoso I, Guerra S, Domingo E, Rivas C, Esteban M. 2006. Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol Mol Biol Rev 70:1032-1060. http://dx.doi.org/10.1128/MMBR.00027-06.
40. Zerbini LF, Wang Y, Czibere A, Correa RG, Cho J-Y, Ijiri K, Wei W, Joseph M, Gu X, Grall F, Goldring MB, Zhou J-R, Libermann TA, Zhou J-R. 2004. NF-kappa B-mediated repression of growth arrest-and DNAdamage-inducible proteins 45alpha and gamma is essential for cancer cell survival. Proc Natl Acad Sci USA 101:13618-13623. http://dx.doi.org/10.1073/pnas.0402069101.
41. De Smaele E, Zazzeroni F, Papa S, Nguyen DU, Jin R, Jones J, Cong R, Franzoso G. 2001. Induction of gadd45beta by NF-kappaB downregulates pro-apoptotic JNK signalling. Nature 414:308-313. http://dx.doi.org/10.1038/35104560.
42. Arimoto K, Fukuda H, Imajoh-Ohmi S, Saito H, Takekawa M. 2008. Formation of stress granules inhibits apoptosis by suppressing stressresponsive MAPK pathways. Nat Cell Biol 10:1324-1332. http://dx.doi.org/10.1038/ncb1791.
43. Daher A, Laraki G, Singh M, Melendez-Peña CE, Bannwarth S, Peters AHFM, Meurs EF, Braun RE, Patel RC, Gatignol A. 2009. TRBP control of PACT-induced phosphorylation of protein kinaseRis reversed by stress. Mol Cell Biol 29:254-265. http://dx.doi.org/10.1128/MCB.01030-08.
44. Patel CV, Handy I, Goldsmith T, Patel RC. 2000. PACT, a stressmodulated cellular activator of interferon-induced double-stranded RNA-activated protein kinase, PKR. J Biol Chem 275:37993-37998. http://dx.doi.org/10.1074/jbc.M004762200.
45. Lemaire PA, Anderson E, Lary J, Cole JL. 2008. Mechanism of PKR activation by dsRNA. J Mol Biol 381:351-360. http://dx.doi.org/10.1016/j.jmb.2008.05.056.
46. Wen X, Huang X, Mok BW-Y, Chen Y, Zheng M, Lau S-Y, Wang P, Song W, Jin D-Y, Yuen K-Y, Chen H. 2014. NF90 exerts antiviral activity through regulation of PKR phosphorylation and stress granules in infected cells. J Immunol 192:3753-3764. http://dx.doi.org/10.4049/jimmunol.1302813.
47. Shiina N, Nakayama K. 2014. RNA granule assembly and disassembly modulated by nuclear factor associated with double-stranded RNA 2 and nuclear factor 45. J Biol Chem 289:21163-21180. http://dx.doi.org/10.1074/jbc.M114.556365.
48. Lee TG, Tomita J, Hovanessian AG, Katze MG. 1990. Purification and partial characterization of a cellular inhibitor of the interferon-induced protein kinase of Mr 68,000 from influenza virus-infected cells. Proc Natl Acad Sci USA 87:6208-6212. http://dx.doi.org/10.1073/pnas.87.16.6208.
49. Patel RC, Sen GC. 1998. PACT, a protein activator of the interferoninduced protein kinase, PKR. EMBO J 17:4379-4390. http://dx.doi.org/10.1093/emboj/17.15.4379.
50. Zhang P, Li Y, Xia J, He J, Pu J, Xie J, Wu S, Feng L, Huang X, Zhang P. 2014. IPS-1 plays an essential role in dsRNA-induced stress granule formation by interacting with PKR and promoting its activation. J Cell Sci 127:2471-2482. http://dx.doi.org/10.1242/jcs.139626.
51. Pataer A, Vorburger S, Chada S, Balachandran S, Barber G, Roth J, Hunt K, Swisher S. 2005. Melanoma differentiation-associated gene-7 protein physically associates with the double-stranded RNA-activated protein kinase PKR. Mol Ther 11:717-723. http://dx.doi.org/10.1016/j.ymthe.2005.01.018.
52. Mittelstadt M, Frump A, Khuu T, Fowlkes V, Handy I, Patel CV, Patel RC. 2008. Interaction of human tRNA-dihydrouridine synthase-2 with interferon-induced protein kinase PKR. Nucleic Acids Res 36:998-1008. http://dx.doi.org/10.1093/nar/gkm1129.