Cytoplasmic hGle1A regulates stress granules by modulation of translation

Molecular Biology of the Cell

Volumn 26, Issue 8, 2015, Pages 1476-1490

  Aditi, ^a   Folkmann, Andrew W ^a   Wente, Susan R ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; CYCLOHEXIMIDE; DEAD BOX PROTEIN; ENHANCED GREEN FLUORESCENT PROTEIN; GLE1 PROTEIN; INITIATION FACTOR 2; MESSENGER RNA; NOCODAZOLE; PACLITAXEL; PUROMYCIN; RNA BINDING PROTEIN; SINGLE STRANDED DNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; GLE1 PROTEIN, HUMAN; ISOPROTEIN; NUCLEOCYTOPLASMIC TRANSPORT PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CELL GRANULE; CELL STRESS; CONTROLLED STUDY; CYTOPLASM; GENE EXPRESSION; HEAT SHOCK; HELA CELL LINE; HUMAN; HUMAN CELL; IN SITU HYBRIDIZATION; MICROSCOPY; MICROTUBULE; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RNA TRANSLATION; STRESS; TRANSLATION INITIATION; TRANSLATION REGULATION; CELL LINE; DOWN REGULATION; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

EUKARYOTA;

CELL LINE; CYTOPLASMIC GRANULES; DOWN-REGULATION; HUMANS; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; PROTEIN BIOSYNTHESIS; PROTEIN ISOFORMS; STRESS, PHYSIOLOGICAL;

EID: 84928136247     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E14-11-1523     Document Type: Article

References (78)

1. Adams RL, Terry LJ, Wente SR (2014). Nucleoporin FG domains facilitate mRNP remodeling at the cytoplasmic face of the nuclear pore complex. Genetics 197, 1213-1224.
2. Alcazar-Roman AR, Tran EJ, Guo S, Wente SR (2006). Inositol hexakisphosphate and Gle1 activate the DEAD-box protein Dbp5 for nuclear mRNA export. Nat Cell Biol 8, 711-716.
3. Anderson P, Kedersha N (2008). Stress granules: the Tao of RNA triage. Trends Biochem Sci 33, 141-150.
4. Anderson P, Kedersha N (2009). RNA granules: post-transcriptional and epigenetic modulators of gene expression. Nat Rev Mol Cell Biol 10, 430-436.
5. Arimoto K, Fukuda H, Imajoh-Ohmi S, Saito H, Takekawa M (2008). Formation of stress granules inhibits apoptosis by suppressing stress-responsive MAPK pathways. Nat Cell Biol 10, 1324-1332.
6. 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.
7. Balagopal V, Parker R (2009). Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs. Curr Opin Cell Biol 21, 403-408.
8. Bolger TA, Folkmann AW, Tran EJ, Wente SR (2008). The mRNA export factor Gle1 and inositol hexakisphosphate regulate distinct stages of translation. Cell 134, 624-633.
9. Bolger TA, Wente SR (2011). Gle1 is a multifunctional DEAD-box protein regulator that modulates Ded1 in translation initiation. J Biol Chem 286, 39750-39759.
10. Bosco DA, Lemay N, Ko HK, Zhou H, Burke C, Kwiatkowski TJ Jr, Sapp P, McKenna-Yasek D, Brown RH Jr, Hayward LJ (2010). Mutant FUS proteins that cause amyotrophic lateral sclerosis incorporate into stress granules. Hum Mol Genet 19, 4160-4175.
11. Buchan JR, Kolaitis RM, Taylor J P, Parker R (2013). Eukaryotic stress granules are cleared by autophagy and Cdc48/VCP function. Cell 153, 1461-1474.
12. Buchan JR, Parker R (2009). Eukaryotic stress granules: the ins and outs of translation. Mol Cell 36, 932-941.
13. Chernov KG, Barbet A, Hamon L, Ovchinnikov L P, Curmi PA, Pastre D (2009). Role of microtubules in stress granule assembly: microtubule dynamical instability favors the formation of micrometric stress granules in cells. J Biol Chem 284, 36569-36580.
14. Chu WM, Ballard R, Carpick BW, Williams BR, Schmid CW (1998). Potential Alu function: regulation of the activity of double-stranded RNA-activated kinase PKR. Mol Cell Biol 18, 58-68.
15. Cuesta R, Laroia G, Schneider RJ (2000). Chaperone hsp27 inhibits translation during heat shock by binding eIF4G and facilitating dissociation of cap-initiation complexes. Genes Dev 14, 1460-1470.
16. Decker CJ, Parker R (2012). P-bodies and stress granules: possible roles in the control of translation and mRNA degradation. Cold Spring Harb Perspect Biol 4, a012286.
17. de Nadal E, Ammerer G, Posas F (2011). Controlling gene expression in response to stress. Nat Rev Genet 12, 833-845.
18. Dewey CM, Cenik B, Sephton CF, Dries DR, Mayer P III, Good SK, Johnson BA, Herz J, Yu G (2011). TDP-43 is directed to stress granules by sorbitol, a novel physiological osmotic and oxidative stressor. Mol Cell Biol 31, 1098-1108.
19. Dieterich DC, Lee JJ, Link AJ, Graumann J, Tirrell DA, Schuman EM (2007). Labeling, detection and identification of newly synthesized proteomes with bioorthogonal non-canonical amino-acid tagging. Nat Protoc 2, 532-540.
20. Dieterich DC, Link AJ, Graumann J, Tirrell DA, Schuman EM (2006). Selective identification of newly synthesized proteins in mammalian cells using bioorthogonal noncanonical amino acid tagging (BONCAT). Proc Natl Acad Sci USA 103, 9482-9487.
21. Folkmann AW, Collier SE, Zhan X, Aditi, Ohi MD, Wente SR (2013). Gle1 functions during mRNA export in an oligomeric complex that is altered in human disease. Cell 155, 582-593.
22. Folkmann AW, Dawson TR, Wente SR (2014). Insights into mRNA exportlinked molecular mechanisms of human disease through a Gle1 structure-function analysis. Adv Biol Regul 54, 74-91.
23. Gallouzi I-E, Brennan CM, Stenberg MG, Swanson MS, Eversole A, Maizels N, Steitz JA (2000). HuR binding to cytoplasmic mRNA is perturbed by heat shock. Proc Natl Acad Sci USA 97, 3073-3078.
24. Gebauer F, Hentze MW (2004). Molecular mechanisms of translational control. Nat Rev Mol Cell Biol 5, 827-835.
25. 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.
26. Grüter P, Tabernero C, von Kobbe C, Schmitt C, Saavedra C, Bachi A, Wilm M, Felber BK, Izaurralde E (1998). TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol Cell 1, 649-659.
27. Herold A, Suyama M, Rodrigues J P, Braun IC, Kutay U, Carmo-Fonseca M, Bork P, Izaurralde E (2000). TAP (NXF1) belongs to a multigene family of putative RNA export factors with a conserved modular architecture. Mol Cell Biol 20, 8996-9008.
28. Hilliker A, Gao Z, Jankowsky E, Parker R (2011). The DEAD-box protein Ded1 modulates translation by the formation and resolution of an eIF4F-mRNA complex. Mol Cell 43, 962-972.
29. Hodge CA, Tran EJ, Noble KN, Alcazar-Roman AR, Ben-Yishay R, Scarcelli JJ, Folkmann AW, Shav-Tal Y, Wente SR, Cole CN (2011). The Dbp5 cycle at the nuclear pore complex during mRNA export I: dbp5 mutants with defects in RNA binding and ATP hydrolysis define key steps for Nup159 and Gle1. Genes Dev 25, 1052-1064.
30. Ivanov PA, Chudinova EM, Nadezhdina ES (2003). Disruption of microtubules inhibits cytoplasmic ribonucleoprotein stress granule formation. Exp Cell Res 290, 227-233.
31. Kaneb HM, Folkmann AW, Belzil VV, Jao LE, Leblond CS, Girard SL, Daoud H, Noreau A, Rochefort D, Hince P, et al. (2014). Deleterious mutations in the essential mRNA metabolism factor, hGle1, in amyotrophic lateral sclerosis. Hum Mol Genet 24, 1363-1373.
32. Kang Y, Cullen BR (1999). The human Tap protein is a nuclear mRNA export factor that contains novel RNA-binding and nucleocytoplasmic transport sequences. Genes Dev 13, 1126-1139.
33. Kedersha N, Anderson P (2002). Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem Soc Trans 30, 963-969.
34. Kedersha N, Anderson P (2007). Mammalian stress granules and processing bodies. Methods Enzymol 431, 61-81.
35. Kedersha N, Anderson P (2009). Regulation of translation by stress granules and processing bodies. Prog Mol Biol Transl Sci 90, 155-185.
36. 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.
37. 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.
38. Kedersha NL, Gupta M, Li W, Miller I, Anderson P (1999). RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J Cell Biol 147, 1431-1442.
39. Kendirgi F, Barry DM, Griffis ER, Powers MA, Wente SR (2003). An essential role for hGle1 nucleocytoplasmic shuttling in mRNA export. J Cell Biol 160, 1029-1040.
40. Kendirgi F, Rexer DJ, Alcazar-Roman AR, Onishko HM, Wente SR (2005). Interaction between the shuttling mRNA export factor Gle1 and the nucleoporin hCG1: a conserved mechanism in the export of Hsp70 mRNA. Mol Biol Cell 16, 4304-4315.
41. Khaperskyy DA, Hatchette TF, McCormick C (2012). Influenza A virus inhibits cytoplasmic stress granule formation. FASEB J 26, 1629-1639.
42. Kim WJ, Back SH, Kim V, Ryu I, Jang SK (2005). Sequestration of TRAF2 into stress granules interrupts tumor necrosis factor signaling under stress conditions. Mol Cell Biol 25, 2450-2462.
43. Kolobova E, Efimov A, Kaverina I, Rishi AK, Schrader JW, Ham AJ, Larocca MC, Goldenring JR (2009). Microtubule-dependent association of AKAP350A and CCAR1 with RNA stress granules. Exp Cell Res 315, 542-555.
44. Lai MC, Lee YH, Tarn WY (2008). The DEAD-box RNA helicase DDX3 associates with export messenger ribonucleoproteins as well as tip-associated protein and participates in translational control. Mol Biol Cell 19, 3847-3858.
45. Lloyd RE (2012). How do viruses interact with stress-associated RNA granules? PLoS Pathog 8, e1002741.
46. Lloyd RE (2013). Regulation of stress granules and P-bodies during RNA virus infection. Wiley Interdiscip Rev RNA 4, 317-331.
47. Lopez-Maury L, Marguerat S, Bahler J (2008). Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nat Rev Genet 9, 583-593.
48. Low WK, Dang Y, Schneider-Poetsch T, Shi Z, Choi NS, Merrick WC, Romo D, Liu JO (2005). Inhibition of eukaryotic translation initiation by the marine natural product pateamine A. Mol Cell 20, 709-722.
49. Mazroui R, Huot M-E, Tremblay S, Filion C, Labelle Y, Khandjian EW (2002). Trapping of messenger RNA by fragile X mental retardation protein into cytoplasmic granules induces translation repression. Hum Mol Genet 11, 3007-3017.
50. Mazroui R, Sukarieh R, Bordeleau ME, Kaufman RJ, Northcote P, Tanaka J, Gallouzi I, Pelletier J (2006). Inhibition of ribosome recruitment induces stress granule formation independently of eukaryotic initiation factor 2α phosphorylation. Mol Biol Cell 17, 4212-4219.
51. Montpetit B, Thomsen ND, Helmke KJ, Seeliger MA, Berger JM, Weis K (2011). A conserved mechanism of DEAD-box ATPase activation by nucleoporins and InsP6 in mRNA export. Nature 472, 238-242.
52. Mor A, Suliman S, Ben-Yishay R, Yunger S, Brody Y, Shav-Tal Y (2010). Dynamics of single mRNP nucleocytoplasmic transport and export through the nuclear pore in living cells. Nat Cell Biol 12, 543-552.
53. Murphy R, Wente SR (1996). An RNA-export mediator with an essential nuclear export signal. Nature 383, 357-360.
54. Murtha-Riel P, Davies MV, Scherer BJ, Choi SY, Hershey JW, Kaufman RJ (1993). Expression of a phosphorylation-resistant eukaryotic initiation factor 2 alpha-subunit mitigates heat shock inhibition of protein synthesis. J Biol Chem 268, 12946-12951.
55. Nadezhdina ES, Lomakin AJ, Shpilman AA, Chudinova EM, Ivanov PA (2010). Microtubules govern stress granule mobility and dynamics. Biochim Biophys Acta 1803, 361-371.
56. Noble KN, Tran EJ, Alcazar-Roman AR, Hodge CA, Cole CN, Wente SR (2011). The Dbp5 cycle at the nuclear pore complex during mRNA export II: nucleotide cycling and mRNP remodeling by Dbp5 are controlled by Nup159 and Gle1. Genes Dev 25, 1065-1077.
57. Nousiainen HO, Kestila M, Pakkasjarvi N, Honkala H, Kuure S, Tallila J, Vuopala K, Ignatius J, Herva R, Peltonen L (2008). Mutations in mRNA export mediator GLE1 result in a fetal motoneuron disease. Nat Genet 40, 155-157.
58. Onishi H, Kino Y, Morita T, Futai E, Sasagawa N, Ishiura S (2008). MBNL1 associates with YB-1 in cytoplasmic stress granules. J Neurosci Res 86, 1994-2002.
59. Panniers R (1994). Translational control during heat shock. Biochimie 76, 737-747.
60. Parker R, Sheth U (2007). P bodies and the control of mRNA translation and degradation. Mol Cell 25, 635-646.
61. Parker SJ, Meyerowitz J, James JL, Liddell JR, Crouch PJ, Kanninen KM, White AR (2012). Endogenous TDP-43 localized to stress granules can subsequently form protein aggregates. Neurochem Int 60, 415-424.
62. Rayala HJ, Kendirgi F, Barry DM, Majerus PW, Wente SR (2004). The mRNA export factor human Gle1 interacts with the nuclear pore complex protein Nup155. Mol Cell Proteomics 3, 145-155.
63. Ruggieri A, Dazert E, Metz P, Hoffmann S, Bergeest JP, Mazur J, Bankhead P, Hiet MS, Kallis S, Alvisi G, et al. (2012). Dynamic oscillation of translation and stress granule formation mark the cellular response to virus infection. Cell Host Microbe 12, 71-85.
64. Shih JW, Wang WT, Tsai TY, Kuo CY, Li HK, Wu Lee YH (2012). Critical roles of RNA helicase DDX3 and its interactions with eIF4E/PABP1 in stress granule assembly and stress response. Biochem J 441, 119-129.
65. Sonenberg N, Hinnebusch AG (2009). Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136, 731-745.
66. Spriggs KA, Bushell M, Willis AE (2010). Translational regulation of gene expression during conditions of cell stress. Mol Cell 40, 228-237.
67. Stoecklin G, Stubbs T, Kedersha N, Wax S, Rigby WF, Blackwell TK, Anderson P (2004). MK2-induced tristetraprolin:14-3-3 complexes prevent stress granule association and ARE-mRNA decay. EMBO J 23, 1313-1324.
68. Thomas MG, Loschi M, Desbats MA, Boccaccio GL (2011). RNA granules: the good, the bad and the ugly. Cell Signal 23, 324-334.
69. Tourriere H, Chebli K, Zekri L, Courselaud B, Blanchard JM, Bertrand E, Tazi J (2003). The RasGAP-associated endoribonuclease G3BP assembles stress granules. J Cell Biol 160, 823-831.
70. Tran EJ, Zhou Y, Corbett AH, Wente SR (2007). The DEAD-box protein Dbp5 controls mRNA export by triggering specific RNA: protein remodeling events. Mol Cell 28, 850-859.
71. Vance C, Scotter EL, Nishimura AL, Troakes C, Mitchell JC, Kathe C, Urwin H, Manser C, Miller CC, Horthobagyi T, et al. (2013). ALS mutant FUS disrupts nuclear localization and sequesters wild-type FUS within cytoplasmic stress granules. Hum Mol Genet 22, 2676-2688.
72. Vanderweyde T, Youmans K, Liu-Yesucevitz L, Wolozin B (2013). Role of stress granules and RNA-binding proteins in neurodegeneration: a minireview. Gerontology 59, 524-533.
73. Weirich CS, Erzberger J P, Flick JS, Berger JM, Thorner J, Weis K (2006). Activation of the DExD/H-box protein Dbp5 by the nuclear-pore protein Gle1 and its coactivator InsP6 is required for mRNA export. Nat Cell Biol 8, 668-676.
74. Wek RC, Jiang HY, Anthony TG (2006). Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans 34, 7-11.
75. Williams BR (1999). PKR; a sentinel kinase for cellular stress. Oncogene 18, 6112-6120.
76. Wolozin B (2012). Regulated protein aggregation: stress granules and neurodegeneration. Mol Neurodegener 7, 56.
77. Yedavalli VSRK, Neuveut C, Chi Y-H, Kleiman L, Jeang K-T (2004). Requirement of DDX3 DEAD box RNA helicase for HIV-1 Rev-RRE export function. Cell 119, 381-392.
78. Zhang J, Okabe K, Tani T, Funatsu T (2011). Dynamic association-dissociation and harboring of endogenous mRNAs in stress granules. J Cell Sci 124, 4087-4095.