Casein kinase 2 is linked to stress granule dynamics through phosphorylation of the stress granule nucleating protein G3BP1

Molecular and Cellular Biology

Volumn 37, Issue 4, 2017, Pages

  Reineke, Lucas C ^a   Tsai, Wei Chih ^a   Jain, Antrix ^a   Kaelber, Jason T ^a   Jung, Sung Yun ^a   Lloyd, Richard E ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Casein kinase 2; G3BP1; Stress granule

Indexed keywords

ARSENIC TRIOXIDE; CASEIN KINASE II; PROTEIN; SERINE; SMALL INTERFERING RNA; STRESS GRANULE NUCLEATING PROTEIN G3BP1; UNCLASSIFIED DRUG; ARSENOUS ACID DERIVATIVE; CARRIER PROTEIN; G3BP PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR; PROTEIN SUBUNIT;

ARTICLE; CELL PROLIFERATION; CELL STRESS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DYNAMICS; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME LOCALIZATION; GENE LOSS; GENE OVEREXPRESSION; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; ANTAGONISTS AND INHIBITORS; CELL GRANULE; DOMINANT GENE; DRUG EFFECTS; HUMAN; METABOLISM; PHOSPHORYLATION; PHYSIOLOGICAL STRESS; PROTEIN SUBUNIT; TUMOR CELL LINE;

ARSENITES; CARRIER PROTEINS; CASEIN KINASE II; CELL LINE, TUMOR; CYTOPLASMIC GRANULES; GENES, DOMINANT; HUMANS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN SUBUNITS; STRESS, PHYSIOLOGICAL;

EID: 85012065276     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00596-16     Document Type: Article

References (61)

1. Anderson P, Kedersha N. 2008. Stress granules: the tao of RNA triage. Trends Biochem Sci 33:141-150. https://doi.org/10.1016/j.tibs.2007.12.003.
2. McEwen E. 2005. Heme-regulated inhibitor kinase-mediated phosphorylation of eukaryotic translation initiation factor 2 inhibits translation, induces stress granule formation, and mediates survival upon arsenite exposure. J Biol Chem 280:16925-16933. https://doi.org/10.1074/jbc.M412882200.
3. Reineke LC, Lloyd RE. 2013. Diversion of stress granules and P-bodies during viral infection. Virology 436:255-267. https://doi.org/10.1016/j.virol.2012.11.017.
4. Farny NG, Kedersha NL, Silver PA. 2009. Metazoan stress granule assembly is mediated by P-eIF2-dependent and-independent mechanisms. RNA 15:1814-1821. https://doi.org/10.1261/rna.1684009.
5. Dang Y, Kedersha N, Low W-K, Romo D, Gorospe M, Kaufman R, Anderson P, Liu JO. 2006. Eukaryotic initiation factor 2alpha-independent pathway of stress granule induction by the natural product pateamine A. J Biol Chem 281:32870-32878. https://doi.org/10.1074/jbc.M606149200.
6. Mazroui R, Sukarieh R, Bordeleau M-E, Kaufman RJ, Northcote P, Tanaka J, Gallouzi I, Pelletier J. 2006. Inhibition of ribosome recruitment induces stress granule formation independently of eukaryotic initiation factor 2alpha phosphorylation. Mol Biol Cell 17:4212-4219. https://doi.org/10.1091/mbc.E06-04-0318.
7. Mokas S, Mills JR, Garreau C, Fournier M-J, Robert F, Arya P, Kaufman RJ, Pelletier J, Mazroui R. 2009. Uncoupling stress granule assembly and translation initiation inhibition. Mol Biol Cell 20:2673-2683. https://doi.org/10.1091/mbc.E08-10-1061.
8. Emara MM, Fujimura K, Sciaranghella D, Ivanova V, Ivanov P, Anderson P. 2012. Hydrogen peroxide induces stress granule formation independent of eIF2α phosphorylation. Biochem Biophys Res Commun 423: 763-769. https://doi.org/10.1016/j.bbrc.2012.06.033.
9. Kedersha N, Ivanov P, Anderson P. 2013. Stress granules and cell signaling: more than just a passing phase? Trends Biochem Sci 38: 494-506. https://doi.org/10.1016/j.tibs.2013.07.004.
10. Kedersha N, Anderson P. 2007. Mammalian stress granules and processing bodies. Methods Enzymol 431:61-81. https://doi.org/10.1016/S0076-6879(07)31005-7.
11. Kato M, Han TW, Xie S, Shi K, Du X, Wu LC, Mirzaei H, Goldsmith EJ, Longgood J, Pei J, Grishin NV, Frantz DE, Schneider JW, Chen S, Li L, Sawaya MR, Eisenberg D, Tycko R, McKnight SL. 2012. Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 149:753-767. https://doi.org/10.1016/j.cell.2012.04.017.
12. Tourriere H. 2003. The RasGAP-associated endoribonuclease G3BP assembles stress granules. J Cell Biol 160:823-831. https://doi.org/10.1083/jcb.200212128.
13. Gilks N, Kedersha N, Ayodele M, Shen L, Stoecklin G, Dember LM, Anderson P. 2004. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol Biol Cell 15:5383-5398. https://doi.org/10.1091/mbc.E04-08-0715.
14. Weber SC, Brangwynne CP. 2012. Getting RNA and protein in phase. Cell 149:1188-1191. https://doi.org/10.1016/j.cell.2012.05.022.
15. Li P, Banjade S, Cheng H-C, Kim S, Chen B, Guo L, Llaguno M, Hollingsworth JV, King DS, Banani SF, Russo PS, Jiang Q-X, Nixon BT, Rosen MK. 2012 Phase transitions in the assembly of multivalent signalling proteins. Nature 483:336-340. https://doi.org/10.1038/nature10879.
16. Nott TJ, Petsalaki E, Farber P, Jervis D, Fussner E, Plochowietz A, Craggs TD, Bazett-Jones DP, Pawson T, Forman-Kay JD, Baldwin AJ. 2015. Phase transition of a disordered nuage protein generates environmentally responsive membraneless organelles. Mol Cell 57:936-947. https://doi.org/10.1016/j.molcel.2015.01.013.
17. Sayed M. 2000. Stress-induced activation of protein kinase CK2 by direct interaction with p38 mitogen-activated protein kinase. J Biol Chem 275:16569-16573. https://doi.org/10.1074/jbc.M000312200.
18. Orlandini M, Semplici F, Ferruzzi R, Meggio F, Pinna LA, Oliviero S. 1998. Protein kinase CK2alpha= is induced by serum as a delayed early gene and cooperates with Ha-ras in fibroblast transformation. J Biol Chem 273:21291-21297. https://doi.org/10.1074/jbc.273.33.21291.
19. Meggio F, Boldyreff B, Marin O, Marchiori F, Perich JW, Issinger OG, Pinna LA. 1992. The effect of polylysine on casein-kinase-2 activity is influenced by both the structure of the protein/peptide substrates and the subunit composition of the enzyme. Eur J Biochem 205:939-945. https://doi.org/10.1111/j.1432-1033.1992.tb16860.x.
20. Bibby AC, Litchfield DW. 2005. The multiple personalities of the regulatory subunit of protein kinase CK2: CK2 dependent and CK2 independent roles reveal a secret identity for CK2beta. Int J Biol Sci 1:67-79.
21. Arrigoni G, Pagano MA, Sarno S, Cesaro L, James P, Pinna LA. 2008. Mass spectrometry analysis of a protein kinase CK2beta subunit interactome isolated from mouse brain by affinity chromatography. J Proteome Res 7:990-1000. https://doi.org/10.1021/pr070500s.
22. Meggio F, Pinna LA. 2003. One-thousand-and-one substrates of protein kinase CK2? FASEB J 17:349-368. https://doi.org/10.1096/fj.02-0473rev.
23. Homma MK, Wada I, Suzuki T, Yamaki J, Krebs EG, Homma Y. 2005. CK2 phosphorylation of eukaryotic translation initiation factor 5 potentiates cell cycle progression. Proc Natl Acad Sci U S A 102:15688-15693. https://doi.org/10.1073/pnas.0506791102.
24. Lin Y, Protter DSW, Rosen MK, Parker R. 2015. Formation and maturation of phase-separated liquid droplets by RNA-binding proteins. Mol Cell 60:208-219. https://doi.org/10.1016/j.molcel.2015.08.018.
25. Bley N, Lederer M, Pfalz B, Reinke C, Fuchs T, Glaß M, Möller B, Hüttelmaier S. 2015. Stress granules are dispensable for mRNA stabilization during cellular stress. Nucleic Acids Res 43:e26. https://doi.org/10.1093/nar/gku1275.
26. 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. https://doi.org/10.1083/jcb.200502088.
27. Mollet S, Cougot N, Wilczynska A, Dautry F, Kress M, Bertrand E, Weil D. 2008 Translationally repressed mRNA transiently cycles through stress granules during stress. Mol Biol Cell 19:4469-4479. https://doi.org/10.1091/mbc.E08-05-0499.
28. Ong S-E, Mittler G, Mann M. 2004. Identifying and quantifying in vivo methylation sites by heavy methyl SILAC. Nat Methods 1:119-126. https://doi.org/10.1038/nmeth715.
29. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M. 2009. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325:834-840. https://doi.org/10.1126/science.1175371.
30. Bikkavilli RK, Malbon CC. 2011. Arginine methylation of G3BP1 in response to Wnt3a regulates catenin mRNA. J Cell Sci 124:2310-2320. https://doi.org/10.1242/jcs.084046.
31. Leung AKL, Vyas S, Rood JE, Bhutkar A, Sharp PA, Chang P. 2011. Poly(ADP-ribose) regulates stress responses and microRNA activity in the cytoplasm. Mol Cell 42:489-499. https://doi.org/10.1016/j.molcel.2011.04.015.
32. Wagner SA, Beli P, Weinert BT, Nielsen ML, Cox J, Mann M, Choudhary C. 2011 A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol Cell Proteomics 10: M111.013284. https://doi.org/10.1074/mcp.M111.013284.
33. Gallouzi IE, Parker F, Chebli K, Maurier F, Labourier E, Barlat I, Capony JP, Tocque B, Tazi J. 1998. A novel phosphorylation-dependent RNase activity of GAP-SH3 binding protein: a potential link between signal transduction and RNA stability. Mol Cell Biol 18:3956-3965. https://doi.org/10.1128/MCB.18.7.3956.
34. Annibaldi A, Dousse A, Martin S, Tazi J, Widmann C. 2011. Revisiting G3BP1 as a RasGAP binding protein: sensitization of tumor cells to chemotherapy by the RasGAP 317-326 sequence does not involve G3BP1. PLoS One 6:e29024. https://doi.org/10.1371/journal.pone.0029024.
35. Tsai W-C, Gayatri S, Reineke LC, Sbardella G, Bedford MT, Lloyd RE. 2016. Arginine demethylation of G3BP1 promotes stress granule assembly. J Biol Chem 291:22671-22685. https://doi.org/10.1074/jbc.M116.739573.
36. Tourriere H, Gallouzi IE, Chebli K, Capony JP, Mouaikel J, van der Geer P, Tazi J. 2001. RasGAP-associated endoribonuclease G3BP: selective RNA degradation and phosphorylation-dependent localization. Mol Cell Biol 21:7747-7760. https://doi.org/10.1128/MCB.21.22.7747-7760.2001.
37. Ortega AD, Willers IM, Sala S, Cuezva JM. 2010. Human G3BP1 interacts with-F1-ATPase mRNA and inhibits its translation. J Cell Sci 123: 2685-2696. https://doi.org/10.1242/jcs.065920.
38. Taniuchi K, Nishimori I, Hollingsworth MA. 2011. The N-terminal domain of G3BP enhances cell motility and invasion by posttranscriptional regulation of BART. Mol Cancer Res 9:856-866. https://doi.org/10.1158/1541-7786.MCR-10-0574.
39. Winslow S, Leandersson K, Larsson C. 2013. Regulation of PMP22 mRNA by G3BP1 affects cell proliferation in breast cancer cells. Mol Cancer 12:156. https://doi.org/10.1186/1476-4598-12-156.
40. 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. https://doi.org/10.1128/MCB.25.19.8703-8716.2005.
41. Sarno S, de Moliner E, Ruzzene M, Pagano MA, Battistutta R, Bain J, Fabbro D, Schoepfer J, Elliott M, Furet P, Meggio F, Zanotti G, Pinna LA. 2003 Biochemical and three-dimensional-structural study of the specific inhibition of protein kinase CK2 by [5-oxo-5, 6-dihydroindolo-(1, 2-a)quinazolin-7-yl]acetic acid (IQA). Biochem J 374:639-646. https://doi.org/10.1042/bj20030674.
42. Reineke LC, Kedersha N, Langereis MA, van Kuppeveld FJM, Lloyd RE. 2015 Stress granules regulate double-stranded RNA-dependent protein kinase activation through a complex containing G3BP1 and Caprin1. mBio 6:e02486. https://doi.org/10.1128/mBio.02486-14.
43. 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. https://doi.org/10.1128/JVI.03213-12.
44. Matsuki H, Takahashi M, Higuchi M, Makokha GN, Oie M, Fujii M. 2013. Both G3BP1 and G3BP2 contribute to stress granule formation. Genes Cells 18:135-146. https://doi.org/10.1111/gtc.12023.
45. Dougherty JD, Reineke LC, Lloyd RE. 2014. mRNA decapping enzyme 1a (Dcp1a)-induced translational arrest through protein kinase R (PKR) activation requires the N-terminal enabled vasodilator-stimulated protein homology 1 (EVH1) domain. J Biol Chem 289:3936-3949. https://doi.org/10.1074/jbc.M113.518191.
46. Ampofo E, Sokolowsky T, Götz C, Montenarh M. 2013. Functional interaction of protein kinase CK2 and activating transcription factor 4 (ATF4), a key player in the cellular stress response. Biochim Biophys Acta 1833:439-451. https://doi.org/10.1016/j.bbamcr.2012.10.025.
47. Obenauer JC, Cantley LC, Yaffe MB. 2003. Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res 31:3635-3641. https://doi.org/10.1093/nar/gkg584.
48. Burnett G, Kennedy EP. 1954. The enzymatic phosphorylation of proteins. J Biol Chem 211:969-980.
49. 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. https://doi.org/10.1016/j.ymeth.2008.06.014.
50. 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. https://doi.org/10.1038/nmeth947.
51. Gandin V, Masvidal L, Cargnello M, Gyenis L, McLaughlan S, Cai Y, Tenkerian C, Morita M, Balanathan P, Jean-Jean O, Stambolic V, Trost M, Furic L, Larose L, Koromilas AE, Asano K, Litchfield D, Larsson O, Topisirovic I. 2016. mTORC1 and CK2 coordinate ternary and eIF4F complex assembly. Nat Commun 7:11127. https://doi.org/10.1038/ncomms11127.
52. Wang C, Ye M, Bian Y, Liu F, Cheng K, Dong M, Dong J, Zou H. 2013. Determination of CK2 specificity and substrates by proteome-derived peptide libraries. J Proteome Res 12:3813-3821. https://doi.org/10.1021/pr4002965.
53. Lolli G, Pinna LA, Battistutta R. 2012. Structural determinants of protein kinase CK2 regulation by autoinhibitory polymerization. ACS Chem Biol 7:1158-1163. https://doi.org/10.1021/cb300054n.
54. Turowec JP, Duncan JS, French AC, Gyenis L, St Denis NA, Vilk G, Litchfield DW. 2010. Protein kinase CK2 is a constitutively active enzyme that promotes cell survival: strategies to identify CK2 substrates and manipulate its activity in mammalian cells. Methods Enzymol 484: 471-493. https://doi.org/10.1016/B978-0-12-381298-8.00023-X.
55. Reineke LC, Lloyd RE. 2015. The stress granule protein G3BP1 recruits PKR to promote multiple innate immune antiviral responses. J Virol 89:2575-2589. https://doi.org/10.1128/JVI.02791-14.
56. 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. https://doi.org/10.1016/j.chom.2007.08.006.
57. Pagano MA, Poletto G, Di Maira G, Cozza G, Ruzzene M, Sarno S, Bain J, Elliott M, Moro S, Zagotto G, Meggio F, Pinna LA. 2007. Tetrabromocinnamic acid (TBCA) and related compounds represent a new class of specific protein kinase CK2 inhibitors. Chembiochem 8:129-139. https://doi.org/10.1002/cbic.200600293.
58. Reineke LC, Dougherty JD, Pierre P, Lloyd RE. 2012. Large G3BP-induced granules trigger eIF2α phosphorylation. Mol Biol Cell 23:3499-3510. https://doi.org/10.1091/mbc.E12-05-0385.
59. Byrd MP. 2005. Translation of eukaryotic translation initiation factor 4GI (eIF4GI) proceeds from multiple mRNAs containing a novel capdependent internal ribosome entry site (IRES) that is active during poliovirus infection. J Biol Chem 280:18610-18622. https://doi.org/10.1074/jbc.M414014200.
60. Tang G, Peng L, Baldwin PR, Mann DS, Jiang W, Rees I, Ludtke SJ. 2007. EMAN2: an extensible image processing suite for electron microscopy. J Struct Biol 157:38-46. https://doi.org/10.1016/j.jsb.2006.05.009.
61. 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 CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 7:R100. https://doi.org/10.1186/gb-2006-7-10-r100.