mRNA localization to P-bodies in yeast is bi-phasic with many mRNAs captured in a late Bfr1p-dependent wave

Journal of Cell Science

Volumn 127, Issue 6, 2014, Pages 1254-1262

  Simpson, Clare E ^a   Lui, Jennifer ^b   Kershaw, Christopher J ^b   Sims, Paul F G ^b   Ashe, Mark P ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Glucose regulation; MRNA localization; P bodies; Stress granules; Yeast

Indexed keywords

GREEN FLUORESCENT PROTEIN; INITIATION FACTOR 4E; MESSENGER RNA; RIBOSOME PROTEIN; RNA BINDING PROTEIN; BFR1 PROTEIN, S CEREVISIAE; FUNGAL RNA; REPRESSOR PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; BFR1P GENE; CELL STRESS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVE SITE; FLUORESCENCE MICROSCOPY; GENE; GENE LOCATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN PURIFICATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA DEGRADATION; RNA PROCESSING; RNA TRANSLATION; SACCHAROMYCES CEREVISIAE; TRANSLATION INITIATION; YEAST; YEAST CELL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; RNA STABILITY; RNA TRANSPORT;

GENE EXPRESSION REGULATION, FUNGAL; REPRESSOR PROTEINS; RNA STABILITY; RNA TRANSPORT; RNA, FUNGAL; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRESS, PHYSIOLOGICAL;

EID: 84903369142     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.139055     Document Type: Article

References (58)

1. Aoh, Q. L., Graves, L. M. and Duncan, M. C. (2011). Glucose regulates clathrin adaptors at the trans-Golgi network and endosomes. Mol. Biol. Cell 22, 3671-3683.
2. Arribere, J. A., Doudna, J. A. and Gilbert, W. V. (2011). Reconsidering movement of eukaryotic mRNAs between polysomes and P bodies. Mol. Cell 44, 745-758.
3. Ashe, M. P., De Long, S. K. and Sachs, A. B. (2000). Glucose depletion rapidly inhibits translation initiation in yeast. Mol. Biol. Cell 11, 833-848.
4. Balagopal, V. and Parker, R. (2009). Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs. Curr. Opin. Cell Biol. 21, 403-408.
5. Balagopal, V., Fluch, L. and Nissan, T. (2012). Ways and means of eukaryotic mRNA decay. Biochim. Biophys. Acta 1819, 593-603.
6. Beckham, C. J. and Parker, R. (2008). P bodies, stress granules, and viral life cycles. Cell Host Microbe 3, 206-212.
7. Brengues, M., Teixeira, D. and Parker, R. (2005). Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310, 486-489.
8. Buchan, J. R., Muhlrad, D. and Parker, R. (2008). P bodies promote stress granule assembly in Saccharomyces cerevisiae. J. Cell Biol. 183, 441-455.
9. Buchan, J. R., Nissan, T. and Parker, R. (2010). Analyzing P-bodies and stress granules in Saccharomyces cerevisiae. Methods Enzymol. 470, 619-640.
10. Buchan, J. R., Yoon, J. H. and Parker, R. (2011). Stress-specific composition, assembly and kinetics of stress granules in Saccharomyces cerevisiae. J. Cell Sci. 124, 228-239.
11. Campbell, S. G. and Ashe, M. P. (2007). An approach to studying the localization and dynamics of eukaryotic translation factors in live yeast cells. Meth. Enzymol. 431, 33-45.
12. Castelli, L. M., Lui, J., Campbell, S. G., Rowe, W., Zeef, L. A. H., Holmes, L. E. A., Hoyle, N. P., Bone, J., Selley, J. N., Sims, P. F. G. et al. (2011). Glucose depletion inhibits translation initiation via eIF4A loss and subsequent 48S preinitiation complex accumulation, while the pentose phosphate pathway is coordinately up-regulated. Mol. Biol. Cell 22, 3379-3393.
13. Decker, C. J., Teixeira, D. and Parker, R. (2007). Edc3p and a glutamine/ asparagine-rich domain of Lsm4p function in processing body assembly in Saccharomyces cerevisiae. J. Cell Biol. 179, 437-449.
14. Durand, S., Cougot, N., Mahuteau-Betzer, F., Nguyen, C. H., Grierson, D. S., Bertrand, E., Tazi, J. and Lejeune, F. (2007). Inhibition of nonsense-mediated mRNA decay (NMD) by a new chemical molecule reveals the dynamic of NMD factors in P-bodies. J. Cell Biol. 178, 1145-1160.
15. Duttagupta, R., Tian, B., Wilusz, C. J., Khounh, D. T., Soteropoulos, P., Ouyang, M., Dougherty, J. P. and Peltz, S. W. (2005). Global analysis of Pub1p targets reveals a coordinate control of gene expression through modulation of binding and stability. Mol. Cell. Biol. 25, 5499-5513.
16. Fenger-Grøn, M., Fillman, C., Norrild, B. and Lykke-Andersen, J. (2005). Multiple processing body factors and the ARE binding protein TTP activate mRNA decapping. Mol. Cell 20, 905-915.
17. Franks, T. M. and Lykke-Andersen, J. (2007). TTP and BRF proteins nucleate processing body formation to silence mRNAs with AU-rich elements. Genes Dev. 21, 719-735.
18. Grousl, T., Ivanov, P., Frýdlová, I., Vasicová, P., Janda, F., Vojtová, J., Malínská, K., Malcová, I., Nováková, L., Janosková, D. et al. (2009). Robust heat shock induces eIF2alpha-phosphorylation-independent assembly of stress granules containing eIF3 and 40S ribosomal subunits in budding yeast, Saccharomyces cerevisiae. J. Cell Sci. 122, 2078-2088.
19. Grousl, T., Ivanov, P., Malcova, I., Pompach, P., Frydlova, I., Slaba, R., Senohrabkova, L., Novakova, L. and Hasek, J. (2013). Heat shock-induced accumulation of translation elongation and termination factors precedes assembly of stress granules in S. cerevisiae. PLoS ONE 8, e57083.
20. Guthrie, C. and Fink, G. R. (1991). Guide to Yeast Genetics and Molecular Biology. San Diego, CA: Academic Press.
21. Haim, L., Zipor, G., Aronov, S. and Gerst, J. E. (2007). A genomic integration method to visualize localization of endogenous mRNAs in living yeast. Nat. Methods 4, 409-412.
22. Haim-Vilmovsky, L. and Gerst, J. E. (2009). m-TAG: a PCR-based genomic integration method to visualize the localization of specific endogenous mRNAs in vivo in yeast. Nat. Protoc. 4, 1274-1284.
23. Hamada, S., Ishiyama, K., Choi, S. B., Wang, C., Singh, S., Kawai, N., Franceschi, V. R. and Okita, T. W. (2003). The transport of prolamine RNAs to prolamine protein bodies in living rice endosperm cells. Plant Cell 15, 2253-2264.
24. Hogan, D. J., Riordan, D. P., Gerber, A. P., Herschlag, D. and Brown, P. O. (2008). Diverse RNA-binding proteins interact with functionally related sets of RNAs, suggesting an extensive regulatory system. PLoS Biol. 6, e255.
25. Hoyle, N. P., Castelli, L. M., Campbell, S. G., Holmes, L. E. and Ashe, M. P. (2007). Stress-dependent relocalization of translationally primed mRNPs to cytoplasmic granules that are kinetically and spatially distinct from P-bodies. J. Cell Biol. 179, 65-74.
26. Huh, W.-K., Falvo, J. V., Gerke, L. C., Carroll, A. S., Howson, R. W., Weissman, J. S. and O'Shea, E. K. (2003). Global analysis of protein localization in budding yeast. Nature 425, 686-691.
27. Jackson, C. L. and Képès, F. (1994). BFR1, a multicopy suppressor of brefeldin A-induced lethality, is implicated in secretion and nuclear segregation in Saccharomyces cerevisiae. Genetics 137, 423-437.
28. Janke, C., Magiera, M. M., Rathfelder, N., Taxis, C., Reber, S., Maekawa, H., Moreno-Borchart, A., Doenges, G., Schwob, E., Schiebel, E. et al. (2004). A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21, 947-962.
29. Kato, K., Yamamoto, Y. and Izawa, S. (2011). Severe ethanol stress induces assembly of stress granules in Saccharomyces cerevisiae. Yeast 28, 339-347.
30. Kedersha, N. and Anderson, P. (2009). Regulation of translation by stress granules and processing bodies. Prog. Mol. Biol. Transl. Sci. 90, 155-185.
31. Kedersha, N. L., Gupta, M., Li, W., Miller, I. and Anderson, P. (1999). RNAbinding 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.
32. Kedersha, N., Stoecklin, G., Ayodele, M., Yacono, P., Lykke-Andersen, J., Fritzler, M. J., Scheuner, D., Kaufman, R. J., Golan, D. E. and Anderson, P. (2005). Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 169, 871-884.
33. Krogan, N. J., Cagney, G., Yu, H., Zhong, G., Guo, X., Ignatchenko, A., Li, J., Pu, S., Datta, N., Tikuisis, A. P. et al. (2006). Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440, 637-643.
34. Lang, B. D., Li Am, Black-Brewster, H. D. and Fridovich-Keil, J. L. (2001). The brefeldin A resistance protein Bfr1p is a component of polyribosome-associated mRNP complexes in yeast. Nucleic Acids Res. 29, 2567-2574.
35. Lavut, A. and Raveh, D. (2012). Sequestration of highly expressed mRNAs in cytoplasmic granules, P-bodies, and stress granules enhances cell viability. PLoS Genet. 8, e1002527.
36. Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408.
37. Lui, J., Campbell, S. G. and Ashe, M. P. (2010). Inhibition of translation initiation following glucose depletion in yeast facilitates a rationalization of mRNA content. Biochem. Soc. Trans. 38, 1131-1136.
38. Mitchell, S. F., Jain, S., She, M. and Parker, R. (2013). Global analysis of yeast mRNPs. Nat. Struct. Mol. Biol. 20, 127-133.
39. Parker, R. and Sheth, U. (2007). P bodies and the control of mRNA translation and degradation. Mol. Cell 25, 635-646.
40. Pichon, X., Wilson, L. A., Stoneley, M., Bastide, A., King, H. A., Somers, J. and Willis, A. E. (2012). RNA binding protein/RNA element interactions and the control of translation. Curr. Protein Pept. Sci. 13, 294-304.
41. Pillai, R. S., Bhattacharyya, S. N., Artus, C. G., Zoller, T., Cougot, N., Basyuk, E., Bertrand, E. and Filipowicz, W. (2005). Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science 309, 1573-1576.
42. Ramachandran, V., Shah, K. H. and Herman, P. K. (2011). The cAMP-dependent protein kinase signaling pathway is a key regulator of P body foci formation. Mol. Cell 43, 973-981.
43. Reijns, M. A., Alexander, R. D., Spiller, M. P. and Beggs, J. D. (2008). A role for Q/N-rich aggregation-prone regions in P-body localization. J. Cell Sci. 121, 2463-2472.
44. Scheuner, D., Song, B., McEwen, E., Liu, C., Laybutt, R., Gillespie, P., Saunders, T., Bonner-Weir, S. and Kaufman, R. J. (2001). Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7, 1165-1176.
45. Sezen, B., Seedorf, M. and Schiebel, E. (2009). The SESA network links duplication of the yeast centrosome with the protein translation machinery. Genes Dev. 23, 1559-1570.
46. Sheth, U. and Parker, R. (2006). Targeting of aberrant mRNAs to cytoplasmic processing bodies. Cell 125, 1095-1109.
47. Simpson, C. E. and Ashe, M. P. (2012). Adaptation to stress in yeast: to translate or not? Biochem. Soc. Trans. 40, 794-799.
48. Spriggs, K. A., Bushell, M. and Willis, A. E. (2010). Translational regulation of gene expression during conditions of cell stress. Mol. Cell 40, 228-237.
49. Thomas, M. G., Loschi, M., Desbats, M. A. and Boccaccio, G. L. (2011). RNA granules: the good, the bad and the ugly. Cell. Signal. 23, 324-334.
50. Toone, W. M. and Jones, N. (1998). Stress-activated signalling pathways in yeast. Genes Cells 3, 485-498.
51. Tudisca, V., Simpson, C., Castelli, L., Lui, J., Hoyle, N., Moreno, S., Ashe, M. and Portela, P. (2012). PKA isoforms coordinate mRNA fate during nutrient starvation. J. Cell Sci. 125, 5221-5232.
52. Uesono, Y., Ashe, M. P. and Toh-E, A. (2004). Simultaneous yet independent regulation of actin cytoskeletal organization and translation initiation by glucose in Saccharomyces cerevisiae. Mol. Biol. Cell 15, 1544-1556.
53. Updike, D. and Strome, S. (2010). P granule assembly and function in Caenorhabditis elegans germ cells. J. Androl. 31, 53-60.
54. Wach, A., Brachat, A., Pöhlmann, R. and Philippsen, P. (1994). New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10, 1793-1808.
55. Weil, T. T., Parton, R. M., Herpers, B., Soetaert, J., Veenendaal, T., Xanthakis, D., Dobbie, I. M., Halstead, J. M., Hayashi, R., Rabouille, C. et al. (2012). Drosophila patterning is established by differential association of mRNAs with P bodies. Nat. Cell Biol. 14, 1305-1313.
56. Welch, W. J. (1987). The mammalian heat shock (or stress) response: a cellular defense mechanism. Adv. Exp. Med. Biol. 225, 287-304.
57. Whitney, M. L., Hurto, R. L., Shaheen, H. H. and Hopper, A. K. (2007). Rapid and reversible nuclear accumulation of cytoplasmic tRNA in response to nutrient availability. Mol. Biol. Cell 18, 2678-2686.
58. Xu, D., Suenaga, N., Edelmann, M. J., Fridman, R., Muschel, R. J. and Kessler, B. M. (2008). Novel MMP-9 substrates in cancer cells revealed by a label-free quantitative proteomics approach. Mol. Cell. Proteomics 7, 2215-2228.