Regulation of stress granules and P-bodies during RNA virus infection

Wiley Interdisciplinary Reviews: RNA

Volumn 4, Issue 3, 2013, Pages 317-331

  Lloyd, Richard E ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HOST FACTOR; PEPTIDES AND PROTEINS; PROCESSING BODIES; PROTEIN KINASE R; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ENZYME ACTIVATION; GENE EXPRESSION; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN PROCESSING; PROTEIN SYNTHESIS; REVIEW; RNA TRANSLATION; RNA VIRUS; RNA VIRUS INFECTION; STRESS GRANULE;

CYTOPLASMIC GRANULES; HOST-PATHOGEN INTERACTIONS; MACROMOLECULAR SUBSTANCES; RNA VIRUSES; VIRAL PROTEINS; VIRUS REPLICATION;

MAMMALIA; RNA VIRUSES;

EID: 84876453384     PISSN: 17577004     EISSN: 17577012     Source Type: Journal    
DOI: 10.1002/wrna.1162     Document Type: Review

References (110)

1. Chang T-C, Yamashita A, Chen C-YA, Yamashita Y, Zhu W, Durdan S, Kahvejian A, Sonenberg N, Shyu A-B. UNR, a new partner of poly(A)-binding protein, plays a key role in translationally coupled mRNA turnover mediated by the c-fos major coding-region determinant. Genes Dev 2004, 18:2010-2023.
2. Shyu A-B, Wilkinson MF, van Hoof A. Messenger RNA regulation: to translate or to degrade. EMBO J 2008, 27:471-481.
3. Mao YS, Zhang B, Spector DL. Biogenesis and function of nuclear bodies. Trends Genet 2011, 27: 295-306.
4. Caudron-Herger M, Rippe K. Nuclear architecture by RNA. Curr Opin Genet Dev 2012, 22:179-187.
5. Reineke LC, Lloyd RE. Diversion of stress granules and P-bodies during viral infection. Virology 2013, 436:255-267.
6. Mokas S, Mills JR, Garreau C, Fournier M-J, Robert F, Arya P, Kaufman RJ, Pelletier J, Mazroui R. Uncoupling stress granule assembly and translation initiation inhibition. Mol Biol Cell 2009, 20:2673-2683.
7. Dang Y, Kedersha N, Low W-K, Romo D, Gorospe M, Kaufman R, Anderson P, Liu JO. Eukaryotic initiation factor 2α-independent pathway of stress granule induction by the natural product pateamine A. J Biol Chem 2006, 281:32870-32878.
8. Kedersha NL, Gupta M, Li W, Miller I, Anderson P. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 α to the assembly of mammalian stress granules. J Cell Biol 1999, 147:1431-1442.
9. Kedersha N, Stoecklin G, Ayodele M, Yacono P, Lykke-Andersen J, Fritzler MJ, Scheuner D, Kaufman RJ, Golan DE, Anderson P Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J Cell Biol 2005, 169:871-884.
10. Buchan JR, Parker R. Eukaryotic stress granules: the ins and outs of translation. Mol Cell 2009, 36:932-941.
11. Anderson P, Kedersha N. Stress granules: the Tao of RNA triage. Trends Biochem Sci 2008, 33:141-150.
12. Kedersha N, Anderson P. Mammalian stress granules and processing bodies. MethEnzymol 2007, 431:61-81.
13. Mazroui R, Sukarieh R, Bordeleau M-E, Kaufman RJ, Northcote P, Tanaka J, Gallouzi I, Pelletier J. Inhibition of ribosome recruitment induces stress granule formation independently of eukaryotic initiation factor 2α phosphorylation. Mol Biol Cell 2006, 17:4212-4219.
14. Emara MM, Fujimura K, Sciaranghella D, Ivanova V, Ivanov P, Anderson P. Hydrogen peroxide induces stress granule formation independent of eIF2α phosphorylation. Biochem Biophys Res Commun 2012, 423:763-769.
15. Reineke LC, Dougherty JD, Pierre P, Lloyd RE. Large G3BP-induced granules trigger eIF2α phosphorylation. Mol Biol Cell 2012, 23:3499-3510.
16. Ohn T, Kedersha N, Hickman T, Tisdale S, Anderson P. A functional RNAi screen links O-GlcNAc modification of ribosomal proteins to stress granule and processing body assembly. Nat Cell Biol 2008, 10:1224-1231.
17. White JP, Lloyd RE. Poliovirus unlinks TIA1 aggregation and mRNA stress granule formation. J Virol 2011, 85:12442-12454.
18. Tourrière H, Chebli K, Zekri L, Courselaud B, Blanchard JM, Bertrand E, Tazi J. The RasGAP-associated endoribonuclease G3BP assembles stress granules. J Cell Biol 2003, 160:823-831.
19. Gilks N, Kedersha N, Ayodele M, Shen L, Stoecklin G, Dember LM, Anderson P. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol Biol Cell 2004, 15:5383-5398.
20. Goulet I, Boisvenue S, Mokas S, Mazroui R, Côté J. TDRD3, a novel Tudor domain-containing protein, localizes to cytoplasmic stress granules. Human Molec Genet 2008, 17:3055-3074.
21. Kwon S, Zhang Y, Matthias P. The deacetylase HDAC6 is a novel critical component of stress granules involved in the stress response. Genes Dev 2007, 21:3381-3394.
22. Solomon S, Xu Y, Wang B, David MD, Schubert P, Kennedy D, Schrader JW. Distinct structural features of Caprin-1 mediate its interaction with G3BP-1 and its induction of phosphorylation of eukaryotic translation initiation factor 2, entry to cytoplasmic stress granules, and selective interaction with a subset of mRNAs. Mol Cell Biol 2007, 27:2324-2342.
23. Ariumi Y, Kuroki M, Kushima Y, Osugi K, Hijikata M, Maki M, Ikeda M, Kato N. Hepatitis C virus hijacks P-body and stress granule components around lipid droplets. J Virol 2011, 85:6882-6892.
24. Piotrowska J, Hansen SJ, Park N, Jamka K, Sarnow P, Gustin KE. Stable formation of compositionally unique stress granules in virus-infected cells. J Virol 2010, 84:3654-3665.
25. Fujimura K, Sasaki AT, Anderson P. Selenite targets eIF4E-binding protein-1 to inhibit translation initiation and induce the assembly of non-canonical stress granules. Nucl Acids Res 2012, 40:8099-8110.
26. Unsworth H, Raguz S, Edwards HJ, Higgins CF, Yagüe E. mRNA escape from stress granule sequestration is dictated by localization to the endoplasmic reticulum. FASEB J 2010, 24:3370-3380.
27. Nover L, Scharf KD, Neumann D. Cytoplasmic heat shock granules are formed from precursor particles and are associated with a specific set of mRNAs. Mol Cell Biol 1989, 9:1298-1308.
28. Eisinger-Mathason TSK, Andrade J, Groehler AL, Clark DE, Muratore-Schroeder TL, Pasic L, Smith JA, Shabanowitz J, Hunt DF, Macara IG, et al. Codependent functions of RSK2 and the apoptosis-promoting factor TIA-1 in stress granule assembly and cell survival. Mol Cell 2008, 31:722-736.
29. Loschi M, Leishman CC, Berardone N, Boccaccio GL. Dynein and kinesin regulate stress-granule and P-body dynamics. J Cell Sci 2009, 122:3973-3982.
30. Ohn T, Anderson P. The role of posttranslational modifications in the assembly of stress granules. WIREs RNA 2010, 1:486-493.
31. Weber SC, Brangwynne CP. Getting RNA and protein in phase. Cell 2012, 149:1188-1191.
32. Li P, Banjade S, Cheng H-C, Kim S, Chen B, Guo L, Llaguno M, Hollingsworth JV, King DS, Banani SF, et al. Phase transitions in the assembly of multivalent signalling proteins. Nature 2012, 483:336-340.
33. Kato M, Han TW, Xie S, Shi K, Du X, Wu LC, et al. Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 2012, 149:753-767.
34. Han TW, Kato M, Xie S, Wu LC, Mirzaei H, Pei J. Cell-free formation of RNA granules: bound RNAs identify features and components of cellular assemblies. Cell 2012, 149:768-779.
35. Bentmann E, Neumann M, Tahirovic S, Rodde R, Dormann D, Haass C. Requirements for stress granule recruitment of fused in sarcoma (FUS) and TAR DNA-binding protein of 43 kDa (TDP-43). J Biol Chem 2012, 287:23079-23094.
36. Aulas A, Stabile S, Vande Velde C. Endogenous TDP-43, but not FUS, contributes to stress granule assembly via G3BP. Mol Neurodegener 2012, 7:54.
37. Bikkavilli RK, Malbon CC. Arginine methylation of G3BP1 in response to Wnt3a regulates β-catenin mRNA. J Cell Sci 2011, 124:2310-2320.
38. Zou T, Rao JN, Liu L, Xiao L, Cui Y-H, Jiang Z, Ouyang M, Donahue JM, Wang J-Y. Polyamines inhibit the assembly of stress granules in normal intestinal epithelial cells regulating apoptosis. Am J Physiol, Cell Physiol 2012, 303:C102-C111.
39. Matsumoto K, Nakayama H, Yoshimura M, Masuda A, Dohmae N, Matsumoto S, Tsujimoto M. PRMT1 is required for RAP55 to localize to processing bodies. RNA Biol 2012, 9:610-623.
40. Dammer EB, Fallini C, Gozal YM, Duong DM, Rossoll W, Xu P, Lah JJ, Levey AI, Peng J, Bassell GJ, et al. Coaggregation of RNA-binding proteins in a model of TDP-43 Proteinopathy with selective RGG motif methylation and a role for RRM1 ubiquitination. PLoS ONE 2012, 7:e38658.
41. Arribere JA, Doudna JA, Gilbert WV. Reconsidering movement of eukaryotic mRNAs between polysomes and P bodies. Mol Cell 2011, 44:745-758.
42. Eulalio A, Behm-Ansmant I, Schweizer D, Izaurralde E. P-body formation is a consequence, not the cause, of RNA-mediated gene silencing. Mol Cell Biol 2007, 27:3970-3981.
43. Ernoult-Lange M, Baconnais S, Harper M, Minshall N, Souquere S, Boudier T, Bénard M, Andrey P, Pierron G, Kress M, Standart N, et al. Multiple binding of repressed mRNAs by the P-body protein Rck/ p54. RNA 2012, 18:1702-1715.
44. Teixeira D, Sheth U, Valencia-Sanchez MA, Brengues M, Parker R. Processing bodies require RNA for assembly and contain nontranslating mRNAs. RNA 2005, 11:371-382.
45. White JP, Cardenas AM, Marissen WE, Lloyd RE. Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. Cell Host Microbe 2007, 2:295-305.
46. White JP, Reineke LC, Lloyd RE. Poliovirus switches to an eIF2-independent mode of translation during infection. J Virol 2011, 85:8884-8893.
47. Borghese F, Michiels T. The leader protein of cardioviruses inhibits stress granule assembly. J Virol 2011, 85:9614-9622.
48. Khong A, Jan E. Modulation of stress granules and P bodies during dicistrovirus infection. J Virol 2011, 85:1439-1451.
49. Khaperskyy DA, Hatchette TF, McCormick C. Influenza A virus inhibits cytoplasmic stress granule formation. FASEB J 2012, 26:1629-1639.
50. Onomoto K, Jogi M, Yoo J-S, Narita R, Morimoto S, Takemura A, Sambhara S, Kawaguchi A, Osari S, Nagata K, et al. Critical role of an antiviral stress granule containing RIG-I and PKR in viral detection and innate immunity. PLoS ONE 2012, 7:e43031.
51. Mok BW-Y, Song W, Wang P, Tai H, Chen Y, Zheng M, Wen X, Lau S-Y, Wu WL, Matsumoto K, et al. The NS1 protein of influenza a virus interacts with cellular processing bodies and stress granules through RNA-associated protein 55 (RAP55) during virus infection. J Virol 2012, 86:12695-12707.
52. Montero H, Rojas M, Arias CF, López S. Rotavirus infection induces the phosphorylation of eIF2α but prevents the formation of stress granules. J Virol 2008, 82:1496-1504.
53. Qin Q, Carroll K, Hastings C, Miller CL. Mammalian Orthoreovirus escape from host translational shutoff correlates with stress granule disruption and is independent of eIF2α phosphorylation and PKR. J Virol 2011, 85:8798-8810.
54. Qin Q, Hastings C, Miller CL. Mammalian orthoreovirus particles induce and are recruited into stress granules at early times postinfection. J Virol 2009, 83:11090-11101.
55. Ventoso I, Sanz MA, Molina S, Berlanga JJ, Carrasco L, Esteban M. Translational resistance of late alphavirus mRNA to eIF2α phosphorylation: a strategy to overcome the antiviral effect of protein kinase PKR. Genes Dev 2006, 20:87-100.
56. Terenin IM, Dmitriev SE, Andreev DE, Shatsky IN. Eukaryotic translation initiation machinery can operate in a bacterial-like mode without eIF2. Nat Struct Mol Biol 2008, 15:836-841.
57. Smith JA, Schmechel SC, Raghavan A, Abelson M, Reilly C, Katze MG, Kaufman RJ, Bohjanen PR, Schiff LA. Reovirus induces and benefits from an integrated cellular stress response. J Virol 2006, 80:2019-2033.
58. Ruggieri A, Dazert E, Metz P, Hofmann S, Bergeest J-P, Mazur J, Bankhead P, Hiet M-S, Kallis S, Alvisi G, et al. Dynamic oscillation of translation and stress granule formation mark the cellular response to virus infection. Cell Host Microbe 2012, 12:71-85.
59. Garaigorta U, Heim MH, Boyd B, Wieland S, Chisari FV. Hepatitis C virus induces the formation of stress granules whose proteins regulate HCV RNA replication, virus assembly and egress. J Virol 2012, 86:11043-11056.
60. Raaben M, Groot Koerkamp MJA, Rottier PJM, de Haan CAM. Mouse hepatitis coronavirus replication induces host translational shutoff and mRNA decay, with concomitant formation of stress granules and processing bodies. Cell Microbiol 2007, 9:2218-2229.
61. Sola I, Galán C, Mateos-Gómez PA, Palacio L, Zúñiga S, Cruz JL, Almazán F, Enjuanes L. The polypyrimidine tract-binding protein affects coronavirus RNA accumulation levels and relocalizes viral RNAs to novel cytoplasmic domains different from replication-transcription sites. J Virol 2011, 85:5136-5149.
62. Cristea IM, Rozjabek H, Molloy KR, Karki S, White LL, Rice CM, Rout MP, Chait BT, MacDonald MR. Host factors associated with the Sindbis virus RNA-dependent RNA polymerase: role for G3BP1 and G3BP2 in virus replication. J Virol 2010, 84: 6720-6732.
63. Frolova E, Gorchakov R, Garmashova N, Atasheva S, Vergara LA, Frolov I. Formation of nsP3-specific protein complexes during Sindbis virus replication. J Virol 2006, 80:4122-4134.
64. Gorchakov R, Garmashova N, Frolova E, Frolov I. Different types of nsP3-containing protein complexes in Sindbis virus-infected cells. J Virol 2008, 82:10088-10101.
65. Fros JJ, Domeradzka NE, Baggen J, Geertsema C, Flipse J, Vlak JM, Pijlman GP. Chikungunya virus nsP3 blocks stress granule assembly by recruitment of G3BP into cytoplasmic foci. J Virol 2012, 86: 10873-10879.
66. Atasheva S, Gorchakov R, English R, Frolov I, Frolova E. Development of Sindbis viruses encoding nsP2/ GFP chimeric proteins and their application for studying nsP2 functioning. J Virol 2007, 81:5046-5057.
67. McInerney GM, Kedersha NL, Kaufman RJ, Anderson P, Liljeström P. Importance of eIF2α phosphorylation and stress granule assembly in alphavirus translation regulation. Mol Biol Cell 2005, 16:3753-3763.
68. Panas MD, Varjak M, Lulla A, Eng KE, Merits A, Karlsson Hedestam GB, McInerney GM. Sequestration of G3BP coupled with efficient translation inhibits stress granules in Semliki Forest virus infection. Mol Biol Cell 2012, 23:4701-4712.
69. Ortega AD, Willers IM, Sala S, Cuezva JM. Human G3BP1 interacts with β-F1-ATPase mRNA and inhibits its translation. J Cell Sci 2010, 123: 2685-2696.
70. Emara MM, Brinton MA. Interaction of TIA-1/TIAR with West Nile and dengue virus products in infected cells interferes with stress granule formation and processing body assembly. Proc Natl Acad Sci U S A 2007, 104:9041-9046.
71. Emara MM, Liu H, Davis WG, Brinton MA. Mutation of mapped TIA-1/TIAR binding sites in the 3′ terminal stem-loop of West Nile virus minus-strand RNA in an infectious clone negatively affects genomic RNA amplification. J Virol 2008, 82:10657-10670.
72. Li W, Li Y, Kedersha N, Anderson P, Emara M, Swiderek KM, Moreno GT, Brinton MA. Cell proteins TIA-1 and TIAR interact with the 3′ stem-loop of the West Nile virus complementary minus-strand RNA and facilitate virus replication. J Virol 2002, 76: 11989-12000.
73. Ward AM, Bidet K, Yinglin A, Ler SG, Hogue K, Blackstock W, Gunaratne J, Garcia-Blanco MA Quantitative mass spectrometry of DENV-2 RNA-interacting proteins reveals that the DEAD-box RNA helicase DDX6 binds the DB1 and DB2 3′ UTR structures. RNA Biol 2011, 8:1173-1186.
74. Pager CT, Schütz S, Abraham TM, Luo G, Sarnow P. Modulation of hepatitis C virus RNA abundance and virus release by dispersion of processing bodies and enrichment of stress granules. Virology 2013, 435: 472-484.
75. Yi Z, Pan T, Wu X, Song W, Wang S, Xu Y, Rice CM, MacDonald MR, Yuan Z. Hepatitis C virus co-opts ras-GTPase-activating protein-binding protein 1 for its genome replication. J Virol 2011, 85:6996-7004.
76. Linero FN, Thomas MG, Boccaccio GL, Scolaro LA. Junin virus infection impairs stress-granule formation in Vero cells treated with arsenite via inhibition of eIF2α phosphorylation. J Gen Virol 2011, 92:2889-2899.
77. Baird NL, York J, Nunberg JH. Arenavirus infection induces discrete cytosolic structures for RNA replication. J Virol 2012, 86:11301-11310.
78. Legros S, Boxus M, Gatot JS, Van Lint C, Kruys V, Kettmann R, Twizere JC, Dequiedt F. The HTLV-1 tax protein inhibits formation of stress granules by interacting with histone deacetylase 6. Oncogene 2011, 30:4050-4062.
79. Dougherty JD, White JP, Lloyd RE. Poliovirus-mediated disruption of cytoplasmic processing bodies. J Virol 2011, 85:64-75.
80. Zheng D, Ezzeddine N, Chen C-YA, Zhu W, He X, Shyu A-B. Deadenylation is prerequisite for P-body formation and mRNA decay in mammalian cells. J Cell Biol 2008, 182:89-101.
81. Rzeczkowski K, Beuerlein K, Müller H, Dittrich-Breiholz O, Schneider H, Kettner-Buhrow D, Holtmann H, Kracht M. c-Jun N-terminal kinase phosphorylates DCP1a to control formation of P bodies. J Cell Biol 2011, 194:581-596.
82. Chahar HS, Chen S, Manjunath N. P-body components LSM1, GW182, DDX3, DDX6 and XRN1 are recruited to WNV replication sites and positively regulate viral replication. Virology 2013, 436:1-7.
83. Silva PAGC, Pereira CF, Dalebout TJ, Spaan WJM, Bredenbeek PJ. An RNA pseudoknot is required for production of yellow fever virus subgenomic RNA by the host nuclease XRN1. J Virol 2010, 84: 11395-11406.
84. Pijlman GP, Funk A, Kondratieva N, Leung J, Torres S, van der Aa L, Liu WJ, Palmenberg AC, Shi P-Y, Hall RA, et al. A highly structured, nuclease-resistant, noncoding RNA produced by flaviviruses is required for pathogenicity. Cell Host Microbe 2008, 4:579-591.
85. Moon SL, Anderson JR, Kumagai Y, Wilusz CJ, Akira S, Khromykh AA, Wilusz J. A noncoding RNA produced by arthropod-borne flaviviruses inhibits the cellular exoribonuclease XRN1 and alters host mRNA stability. RNA 2012, 18:2029-2040.
86. Schnettler E, Sterken MG, Leung JY, Metz SW, Geertsema C, Goldbach RW, Vlak JM, Kohl A, Khromykh AA, Pijlman GP. Noncoding flavivirus RNA displays RNA interference suppressor activity in insect and Mammalian cells. J Virol 2012, 86:13486-13500.
87. Mamiya N, Worman HJ. Hepatitis C virus core protein binds to a DEAD box RNA helicase. J Biol Chem 1999, 274:15751-15756.
88. You LR, Chen CM, Yeh TS, Tsai TY, Mai RT, Lin CH, Lee YH. Hepatitis C virus core protein interacts with cellular putative RNA helicase. J Virol 1999, 73:2841-2853.
89. Angus AGN, Dalrymple D, Boulant S, Mcgivern DR, Clayton RF, Scott MJ, Adair R, Graham S, Owsianka AM, Targett-Adams P, et al. Requirement of cellular DDX3 for hepatitis C virus replication is unrelated to its interaction with the viral core protein. J Gen Virol 2010, 91:122-132.
90. Ariumi Y, Kuroki M, Abe K-I, Dansako H, Ikeda M, Wakita T, Kato N. DDX3 DEAD-box RNA helicase is required for hepatitis C virus RNA replication. J Virol 2007, 81:13922-13926.
91. Scheller N, Mina LB, Galão RP, Chari A, Giménez-Barcons M, Noueiry A, Fischer U, Meyerhans A, Díez J. Translation and replication of hepatitis C virus genomic RNA depends on ancient cellular proteins that control mRNA fates. Proc Natl Acad Sci U S A 2009, 106:13517-13522.
92. Jangra RK, Yi M, Lemon SM. DDX6 (Rck/p54) is required for efficient hepatitis C virus replication but not for internal ribosome entry site-directed translation. J Virol 2010, 84:6810-6824.
93. Pérez-Vilaró G, Scheller N, Saludes V, Díez J. Hepatitis C virus infection alters P-body composition but is independent of P-body granules. J Virol 2012, 86:8740-8749.
94. Yu SF, Lujan P, Jackson DL, Emerman M, Linial ML. The DEAD-box RNA helicase DDX6 is required for efficient encapsidation of a retroviral genome. PLoS Path 2011, 7:e1002303.
95. Mir MA, Duran WA, Hjelle BL, Ye C, Panganiban AT. Storage of cellular 5′ mRNA caps in P bodies for viral cap-snatching. Proc Natl Acad Sci U S A 2008, 105:19294-19299.
96. Mir MA, Panganiban AT. A protein that replaces the entire cellular eIF4F complex. EMBO J 2008, 27: 3129-3139.
97. Noueiry AO, Díez J, Falk SP, Chen J, Ahlquist P. Yeast Lsm1p-7p/Pat1p deadenylation-dependent mRNA-decapping factors are required for brome mosaic virus genomic RNA translation. Mol Cell Biol 2003, 23:4094-4106.
98. Beckham CJ, Light HR, Nissan TA, Ahlquist P, Parker R, Noueiry A. Interactions between brome mosaic virus RNAs and cytoplasmic processing bodies. J Virol 2007, 81:9759-9768.
99. Wang X, Lee W-M, Watanabe T, Schwartz M, Janda M, Ahlquist P. Brome mosaic virus 1a nucleoside triphosphatase/helicase domain plays crucial roles in recruiting RNA replication templates. J Virol 2005, 79:13747-13758.
100. Nakamura T, Furuhashi M, Li P, Cao H, Tuncman G, Sonenberg N, Gorgun CZ, Hotamisligil GS. Double-stranded RNA-dependent protein kinase links pathogen sensing with stress and metabolic homeostasis. Cell 2010, 140:338-348.
101. Yang X, Nath A, Opperman MJ, Chan C. The double-stranded RNA-dependent protein kinase differentially regulates insulin receptor substrates 1 and 2 in HepG2 cells. Mol Biol Cell 2010, 21:3449-3458.
102. Lu B, Nakamura T, Inouye K, Li J, Tang Y, Lundbäck P, Valdes-Ferrer SI, Olofsson PS, Kalb T, Roth J, et al. Novel role of PKR in inflammasome activation and HMGB1 release. Nature 2012, 488:670-674.
103. Taghavi N, Samuel CE. Protein kinase PKR catalytic activity is required for the PKR-dependent activation of mitogen-activated protein kinases and amplification of interferon β induction following virus infection. Virology 2012, 427:208-216.
104. Steele L, Errington F, Prestwich R, Ilett E, Harrington K, Pandha H, Coffey M, Selby P, Vile R, Melcher A. Pro-inflammatory cytokine/chemokine production by reovirus treated melanoma cells is PKR/NF-κB mediated and supports innate and adaptive anti-tumour immune priming. Mol Cancer 2011, 10:20.
105. Garcia MA, Gil J, Ventoso I, Guerra S, Domingo E, Rivas C, Esteban M. Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol Mol Biol Rev 2006, 70:1032-1060.
106. Ghosh S, May MJ, Kopp EB. NF-κB and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 1998, 16:225-260.
107. Gil J, Rullas J, Garcia MA, Alcamí J, Esteban M. The catalytic activity of dsRNA-dependent protein kinase, PKR, is required for NF-κB activation. Oncogene 2001, 20:385-394.
108. Bonnet MC, Weil R, Dam E, Hovanessian AG, Meurs EF. PKR stimulates NF-κB irrespective of its kinase function by interacting with the IκB kinase complex. Mol Cell Biol 2000, 20:4532-4542.
109. Hebner CM, Wilson R, Rader J, Bidder M, Laimins LA. Human papillomaviruses target the double-stranded RNA protein kinase pathway. J Gen Virol 2006, 87:3183-3193.
110. Wasserman T, Katsenelson K, Daniliuc S, Hasin T, Choder M, Aronheim A. 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 2010, 21:117-130.