Protein synthesis inhibition and GADD34 control IFN-β heterogeneous expression in response to dsRNA

EMBO Journal

Volumn 36, Issue 6, 2017, Pages 761-782

  Dalet, Alexandre ^a   Argüello, Rafael J ^a   Combes, Alexis ^a   Spinelli, Lionel ^a   Jaeger, Sebastien ^a   Fallet, Mathieu ^a   Vu Manh, Thien Phong ^a   Mendes, Andreia ^a   Perego, Jessica ^a   Reverendo, Marisa ^a   Camosseto, Voahirana ^a,b   Dalod, Marc ^a   Weil, Tobias ^c,d   Santos, Manuel A ^b,c   Gatti, Evelina ^a,b,c   Pierre, Philippe ^a,b,c  

^a CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^b International Assoc Lab (LIA)   (France)

^c UNIVERSITY OF AVEIRO   (Portugal)

^d RESEARCH AND INNOVATION CENTRE   (Italy)

Author keywords

cGAMP; integrated stress response; puromycin; RIG I like receptors; stress granules

Indexed keywords

BETA INTERFERON; BETA INTERFERON RECEPTOR; DOUBLE STRANDED RNA; INITIATION FACTOR 2ALPHA; INTERFERON; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 6; MESSENGER RNA; MITOCHONDRIAL ANTI VIRAL SIGNALING PROTEIN; MITOCHONDRIAL PROTEIN; PHOSPHATASE; PHOSPHATASE 1 C COFACTOR GADD34; PHOSPHOTRANSFERASE; PROTEIN KINASE R; STAT1 PROTEIN; TANK BINDING KINASE 1; UNCLASSIFIED DRUG; PHOSPHOPROTEIN PHOSPHATASE 1; PPP1R15A PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL CYCLE; ENZYME ACTIVITY; FLOW CYTOMETRY; GENE EXPRESSION; HERPES SIMPLEX VIRUS; HUMAN; HUMAN CELL; INNATE IMMUNITY; INTERFERON PRODUCTION; MATHEMATICAL MODEL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; RNA TRANSLATION; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; FIBROBLAST; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; IMMUNOLOGY; METABOLISM; PROTEIN SYNTHESIS; THEORETICAL MODEL; VIROLOGY;

ANIMALS; CELLS, CULTURED; FIBROBLASTS; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; IMMUNITY, INNATE; INTERFERON-BETA; MICE; MODELS, THEORETICAL; PROTEIN BIOSYNTHESIS; PROTEIN PHOSPHATASE 1; RNA, DOUBLE-STRANDED;

EID: 85010611998     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201695000     Document Type: Article

References (66)

1. Argüello RJ, Rodriguez Rodrigues C, Gatti E, Pierre P (2015) Protein synthesis regulation, a pillar of strength for innate immunity? Curr Opin Immunol 32: 28–35
2. Balachandran S, Roberts PC, Brown LE, Truong H, Pattnaik AK, Archer DR, Barber GN (2000) Essential role for the dsRNA-dependent protein kinase PKR in innate immunity to viral infection. Immunity 13: 129–141
3. Balachandran S, Thomas E, Barber GN (2004) A FADD-dependent innate immune mechanism in mammalian cells. Nature 432: 401–405
4. Belgnaoui SM, Paz S, Hiscott J (2011) Orchestrating the interferon antiviral response through the mitochondrial antiviral signaling (MAVS) adapter. Curr Opin Immunol 23: 564–572
5. Brush MH, Shenolikar S (2008) Control of cellular GADD34 levels by the 26S proteasome. Mol Cell Biol 28: 6989–7000
6. Carpenter AE, Jones TR, Lamprecht MR, Clarke C, Kang IH, Friman O, Guertin DA, Chang JH, Lindquist RA, Moffat J, Golland P, Sabatini DM (2006) Cell Profiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 7: R100
7. Claudio N, Dalet A, Gatti E, Pierre P (2013) Mapping the crossroads of immune activation and cellular stress response pathways. EMBO J 32: 1214–1224
8. Clavarino G, Claudio N, Couderc T, Dalet A, Judith D, Camosseto V, Schmidt EK, Wenger T, Lecuit M, Gatti E, Pierre P (2012) Induction of GADD34 is necessary for dsRNA-dependent interferon-beta production and participates in the control of Chikungunya virus infection. PLoS Pathog 8: e1002708
9. Daffis S, Samuel MA, Keller BC, Gale M Jr, Diamond MS (2007) Cell-specific IRF-3 responses protect against West Nile virus infection by interferon-dependent and -independent mechanisms. PLoS Pathog 3: e106
10. Dalet A, Gatti E, Pierre P (2015) Integration of PKR-dependent translation inhibition with innate immunity is required for a coordinated anti-viral response. FEBS Lett 589: 1539–1545
11. Deng J, Lu PD, Zhang Y, Scheuner D, Kaufman RJ, Sonenberg N, Harding HP, Ron D (2004) Translational repression mediates activation of nuclear factor kappa B by phosphorylated translation initiation factor 2. Mol Cell Biol 24: 10161–10168
12. Elowitz MB, Leibler S (2000) A synthetic oscillatory network of transcriptional regulators. Nature 403: 335–338
13. Freaney JE, Kim R, Mandhana R, Horvath CM (2013) Extensive cooperation of immune master regulators IRF3 and NFkappaB in RNA Pol II recruitment and pause release in human innate antiviral transcription. Cell Rep 4: 959–973
14. Gabhann JN, Higgs R, Brennan K, Thomas W, Damen JE, Ben Larbi N, Krystal G, Jefferies CA (2010) Absence of SHIP-1 results in constitutive phosphorylation of tank-binding kinase 1 and enhanced TLR3-dependent IFN-beta production. J Immunol 184: 2314–2320
15. Gao D, Wu J, Wu YT, Du F, Aroh C, Yan N, Sun L, Chen ZJ (2013) Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 341: 903–906
16. Goubau D, Deddouche S, Reis e Sousa C (2013) Cytosolic sensing of viruses. Immunity 38: 855–869
17. Grandvaux N, Servant MJ, tenOever B, Sen GC, Balachandran S, Barber GN, Lin R, Hiscott J (2002) Transcriptional profiling of interferon regulatory factor 3 target genes: direct involvement in the regulation of interferon-stimulated genes. J Virol 76: 5532–5539
18. Han J, Back SH, Hur J, Lin YH, Gildersleeve R, Shan J, Yuan CL, Krokowski D, Wang S, Hatzoglou M, Kilberg MS, Sartor MA, Kaufman RJ (2013) ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat Cell Biol 15: 481–490
19. Honda K, Taniguchi T (2006) IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat Rev Immunol 6: 644–658
20. Hwang SY, Hur KY, Kim JR, Cho KH, Kim SH, Yoo JY (2013) Biphasic RLR-IFN-beta response controls the balance between antiviral immunity and cell damage. J Immunol 190: 1192–1200
21. Ishikawa H, Ma Z, Barber GN (2009) STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461: 788–792
22. Jefferies C, Wynne C, Higgs R (2011) Antiviral TRIMs: friend or foe in autoimmune and autoinflammatory disease? Nat Rev Immunol 11: 617–625
23. Jiang HY, Wek SA, McGrath BC, Scheuner D, Kaufman RJ, Cavener DR, Wek RC (2003) Phosphorylation of the alpha subunit of eukaryotic initiation factor 2 is required for activation of NF-kappaB in response to diverse cellular stresses. Mol Cell Biol 23: 5651–5663
24. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, Kato H, Ishii KJ, Takeuchi O, Akira S (2005) MAVS, an adaptor triggering RIG-I and Mda5-mediated type I interferon induction. Nat Immunol 6: 981–988
25. Kawai T, Akira S (2006) Innate immune recognition of viral infection. Nat Immunol 7: 131–137
26. Kawai T, Akira S (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11: 373–384
27. Kedersha N, Cho MR, Li W, Yacono PW, Chen S, Gilks N, Golan DE, Anderson P (2000) Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J Cell Biol 151: 1257–1268
28. 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
29. Lazear HM, Lancaster A, Wilkins C, Suthar MS, Huang A, Vick SC, Clepper L, Thackray L, Brassil MM, Virgin HW, Nikolich-Zugich J, Moses AV, Gale M Jr, Fruh K, Diamond MS (2013) IRF-3, IRF-5, and IRF-7 coordinately regulate the type I IFN response in myeloid dendritic cells downstream of MAVS signaling. PLoS Pathog 9: e1003118
30. Li S, Wang L, Berman M, Kong YY, Dorf ME (2011) Mapping a dynamic innate immunity protein interaction network regulating type I interferon production. Immunity 35: 426–440
31. Lu B, Nakamura T, Inouye K, Li J, Tang Y, Lundback P, Valdes-Ferrer SI, Olofsson PS, Kalb T, Roth J, Zou Y, Erlandsson-Harris H, Yang H, Ting JP, Wang H, Andersson U, Antoine DJ, Chavan SS, Hotamisligil GS, Tracey KJ (2012) Novel role of PKR in inflammasome activation and HMGB1 release. Nature 488: 670–674
32. Ma A, Malynn BA (2012) A20: linking a complex regulator of ubiquitylation to immunity and human disease. Nat Rev Immunol 12: 774–785
33. Mangan S, Itzkovitz S, Zaslaver A, Alon U (2006) The incoherent feed-forward loop accelerates the response-time of the gal system of Escherichia coli. J Mol Biol 356: 1073–1081
34. McAllister CS, Taghavi N, Samuel CE (2012) Protein kinase PKR amplification of interferon beta induction occurs through initiation factor eIF-2alpha-mediated translational control. J Biol Chem 287: 36384–36392
35. Mesman AW, Zijlstra-Willems EM, Kaptein TM, de Swart RL, Davis ME, Ludlow M, Duprex WP, Gack MU, Gringhuis SI, Geijtenbeek TB (2014) Measles virus suppresses RIG-I-like receptor activation in dendritic cells via DC-SIGN-mediated inhibition of PP1 phosphatases. Cell Host Microbe 16: 31–42
36. Milo R, Shen-Orr S, Itzkovitz S, Kashtan N, Chklovskii D, Alon U (2002) Network motifs: simple building blocks of complex networks. Science 298: 824–827
37. Mohr I, Sonenberg N (2012) Host translation at the nexus of infection and immunity. Cell Host Microbe 12: 470–483
38. Mostafavi S, Yoshida H, Moodley D, LeBoite H, Rothamel K, Raj T, Ye CJ, Chevrier N, Zhang SY, Feng T, Lee M, Casanova JL, Clark JD, Hegen M, Telliez JB, Hacohen N, De Jager PL, Regev A, Mathis D, Benoist C (2016) Parsing the interferon transcriptional network and its disease associations. Cell 164: 564–578
39. Novoa I, Zeng H, Harding HP, Ron D (2001) Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J Cell Biol 153: 1011–1022
40. Obuchi M, Fernandez M, Barber GN (2003) Development of recombinant vesicular stomatitis viruses that exploit defects in host defense to augment specific oncolytic activity. J Virol 77: 8843–8856
41. Ourthiague DR, Birnbaum H, Ortenlof N, Vargas JD, Wollman R, Hoffmann A (2015) Limited specificity of IRF3 and ISGF3 in the transcriptional innate-immune response to double-stranded RNA. J Leukoc Biol 98: 119–128
42. Patil S, Fribourg M, Ge Y, Batish M, Tyagi S, Hayot F, Sealfon SC (2015) Single-cell analysis shows that paracrine signaling by first responder cells shapes the interferon-beta response to viral infection. Sci Signal 8: ra16
43. Pichlmair A, Reis e Sousa C (2007) Innate recognition of viruses. Immunity 27: 370–383
44. Pierre P, Gatti E (2013) Loss of translation: a stealth weapon against pathogens? Nat Immunol 14: 1203–1205
45. Reineke LC, Dougherty JD, Pierre P, Lloyd RE (2012) Large G3BP-induced granules trigger eIF2alpha phosphorylation. Mol Biol Cell 23: 3499–3510
46. Reineke LC, Kedersha N, Langereis MA, van Kuppeveld FJ, Lloyd RE (2015) Stress granules regulate double-stranded RNA-dependent protein kinase activation through a complex containing G3BP1 and Caprin1. MBio 6: e02486
47. Reineke LC, Lloyd RE (2015) The stress granule protein G3BP1 recruits protein kinase R to promote multiple innate immune antiviral responses. J Virol 89: 2575–2589
48. Robert F, Carrier M, Rawe S, Chen S, Lowe S, Pelletier J (2009) Altering chemosensitivity by modulating translation elongation. PLoS One 4: e5428
49. Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8: 519–529
50. Ruggieri A, Dazert E, Metz P, Hofmann S, Bergeest JP, Mazur J, Bankhead P, Hiet MS, Kallis S, Alvisi G, Samuel CE, Lohmann V, Kaderali L, Rohr K, Frese M, Stoecklin G, Bartenschlager R (2012) Dynamic oscillation of translation and stress granule formation mark the cellular response to virus infection. Cell Host Microbe 12: 71–85
51. Saitoh T, Yamamoto M, Miyagishi M, Taira K, Nakanishi M, Fujita T, Akira S, Yamamoto N, Yamaoka S (2005) A20 is a negative regulator of IFN regulatory factor 3 signaling. J Immunol 174: 1507–1512
52. Schmidt EK, Clavarino G, Ceppi M, Pierre P (2009) SUnSET, a nonradioactive method to monitor protein synthesis. Nat Methods 6: 275–277
53. Schulz O, Pichlmair A, Rehwinkel J, Rogers NC, Scheuner D, Kato H, Takeuchi O, Akira S, Kaufman RJ, Reis e Sousa C (2010) Protein kinase R contributes to immunity against specific viruses by regulating interferon mRNA integrity. Cell Host Microbe 7: 354–361
54. Sekine Y, Zyryanova A, Crespillo-Casado A, Fischer PM, Harding HP, Ron D (2015) Stress responses. Mutations in a translation initiation factor identify the target of a memory-enhancing compound. Science 348: 1027–1030
55. Seth RB, Sun L, Ea CK, Chen ZJ (2005) Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122: 669–682
56. Sidrauski C, McGeachy AM, Ingolia NT, Walter P (2015) The small molecule ISRIB reverses the effects of eIF2alpha phosphorylation on translation and stress granule assembly. Elife 4: e05033
57. Starck SR, Tsai JC, Chen K, Shodiya M, Wang L, Yahiro K, Martins-Green M, Shastri N, Walter P (2016) Translation from the 5' untranslated region shapes the integrated stress response. Science 351: aad3867
58. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 102: 15545–15550
59. Whelan SP, Barr JN, Wertz GW (2000) Identification of a minimal size requirement for termination of vesicular stomatitis virus mRNA: implications for the mechanism of transcription. J Virol 74: 8268–8276
60. Wies E, Wang MK, Maharaj NP, Chen K, Zhou S, Finberg RW, Gack MU (2013) Dephosphorylation of the RNA sensors RIG-I and MDA5 by the phosphatase PP1 is essential for innate immune signaling. Immunity 38: 437–449
61. Williams BR (2001) Signal integration via PKR. Sci STKE 2001: re2
62. Yang YL, Reis LF, Pavlovic J, Aguzzi A, Schafer R, Kumar A, Williams BR, Aguet M, Weissmann C (1995) Deficient signaling in mice devoid of double stranded RNA-dependent protein kinase. EMBO J 14: 6095–6106
63. Zawatzky R, De Maeyer E, De Maeyer-Guignard J (1985) Identification of individual interferon-producing cells by in situ hybridization. Proc Natl Acad Sci USA 82: 1136–1140
64. Zhang P, Samuel CE (2008) Induction of protein kinase PKR-dependent activation of interferon regulatory factor 3 by vaccinia virus occurs through adapter MAVS signaling. J Biol Chem 283: 34580–34587
65. Zhang W, Tian T, Zou X (2015) Negative feedback contributes to the stochastic expression of the interferon-beta gene in virus-triggered type I interferon signaling pathways. Math Biosci 265: 12–27
66. Zhao M, Zhang J, Phatnani H, Scheu S, Maniatis T (2012) Stochastic expression of the interferon-beta gene. PLoS Biol 10: e1001249