Evolutionarily conserved 5′-3′ exoribonuclease Xrn1 accumulates at plasma membrane-associated eisosomes in post-diauxic yeast

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Grousl, Tomas ^a   Opekarová, Miroslava ^b   Stradalova, Vendula ^b   Hasek, Jiri ^a   Malinsky, Jan ^b  

^a INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

5' 3' EXORIBONUCLEASE XRN1; EXORIBONUCLEASE; INITIATION FACTOR 3; MESSENGER RNA; PIL1 PROTEIN; SUR7 PROTEIN; UNCLASSIFIED DRUG; GLUCOSE; HYBRID PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; XRN1 PROTEIN, S CEREVISIAE;

ARTICLE; CELL ORGANELLE; CONTROLLED STUDY; CYTOSOL; EISOSOME; FUNGAL CELL CULTURE; FUNGUS GROWTH; GENETIC CONSERVATION; HEAT STRESS; MEMBRANE STRUCTURE; METABOLISM; NONHUMAN; PROCESSING BODY; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE; CELL MEMBRANE; GENE EXPRESSION; GENETICS; HEAT SHOCK RESPONSE; REPORTER GENE;

CELL MEMBRANE; EXORIBONUCLEASES; GENE EXPRESSION; GENES, REPORTER; GLUCOSE; HEAT-SHOCK RESPONSE; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84926483715     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0122770     Document Type: Article

References (59)

1. Haimovich G, Medina DA, Causse SZ, Garber M, Millán-Zambrano G, Barkai O, et al. Gene expression is circular: factors for mRNA degradation also foster mRNA synthesis. Cell. 2013; 153(5): 1000-11. doi: 10.1016/j.cell.2013.05.012 PMID: 23706738
2. Nagarajan VK, Jones CI, Newbury SF, Green PJ. XRN 5′->3′ exoribonucleases: structure, mechanisms and functions. Biochimica et biophysica acta. 2013; 1829(6-7): 590-603. doi: 10.1016/j.bbagrm.2013.10.003 PMID: 24185200
3. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, et al. Global analysis of protein expression in yeast. Nature. 2003; 425(6959): 737-41. PMID: 14562106
4. Parker R. RNA degradation in Saccharomyces cerevisae. Genetics. 2012; 191(3): 671-702. doi: 10.1534/genetics.111.137265 PMID: 22785621
5. Sheth U, Parker R. Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science. 2003; 300(5620): 805-808. PMID: 12730603
6. Bashkirov VI, Scherthan H, Solinger JA, Buerstedde JM, Heyer WD. A mouse cytoplasmic exoribonuclease (mXRN1p) with preference for G4 tetraplex substrates. J Cell Biol. 1997; 136(4): 761-73. PMID: 9049243
7. Ingelfinger D, Arndt-Jovin DJ, Lührmann R, Achsel T. The human LSm1-7 proteins colocalize with the mRNA-degrading enzymes Dcp1/2 and Xrnl in distinct cytoplasmic foci. RNA. 2002; 8(12): 1489-501. PMID: 12515382
8. Teixeira D, Sheth U, Valencia-Sanchez MA, Brengues M, Parker R. Processing bodies require RNA for assembly and contain nontranslating mRNAs. RNA. 2005; 11(4): 371-82. PMID: 15703442
9. Parker R, Sheth U, P bodies and the control of mRNA translation and degradation. Mol Cell. 2007; 25 (5): 635-46. PMID: 17349952
10. Balagopal V, Parker R. Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs. Curr Opin Cell Biol. 2009; 21(3): 403-8. doi: 10.1016/j.ceb.2009.03.005 PMID: 19394210
11. Kedersha NL, Gupta M, Li W, Miller I, Anderson P. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J Cell Biol. 1999; 147(7): 1431-42. PMID: 10613902
12. Kedersha N, Chen S, Gilks N, Li W, Miller IJ, Stahl J, et al. Evidence that ternary complex (eIF2-GTP-tRNA(i)(Met))-deficient preinitiation complexes are core constituents of mammalian stress granules. Mol Biol Cell. 2002; 13(1): 195-210. PMID: 11809833
13. Kimball SR, Horetsky RL, Ron D, Jefferson LS, Harding HP. Mammalian stress granules represent sites of accumulation of stalled translation initiation complexes. Am J Physiol Cell Physiol. 2003; 284 (2): C273-84. PMID: 12388085
14. Anderson P, Kedersha N. Stress granules: the Tao of RNA triage. Trends Biochem Sci. 2008; 33(3): 141-50. doi: 10.1016/j.tibs.2007.12.003 PMID: 18291657
15. Kedersha N, Cho MR, Li W, Yacono PW, Chen S, Gilks N, et al. Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J Cell Biol. 2000; 151(6): 1257-68. PMID: 11121440
16. Kedersha N, Stoecklin G, Ayodele M, Yacono P, Lykke-Andersen J, Fritzler MJ, et al. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J Cell Biol. 2005; 169(6): 871-84. PMID: 15967811
17. Hoyle NP, Castelli LM, Campbell SG, Holmes LE, Ashe MP. Stress-dependent relocalization of translationally primed mRNPs to cytoplasmic granules that are kinetically and spatially distinct from P-bodies. J Cell Biol. 2007; 179(1): 65-74. PMID: 17908917
18. Buchan JR, Yoon JH, Parker R. Stress-specific composition, assembly and kinetics of stress granules in Saccharomyces cerevisiae. J Cell Sci. 2011; 124(Pt 2): 228-39. doi: 10.1242/jcs.078444 PMID: 21172806
19. Simons K, Gerl MJ. Revitalizing membrane rafts: new tools and insights. Nature reviews. Mol Cell Biol. 2010; 11(10): 688-99. doi: 10.1038/nrm2977 PMID: 20861879
20. Malinsky J, Opekarová M, Grossmann G, Tanner W. Membrane microdomains, rafts, and detergent-resistant membranes in plants and fungi. Annu Review Plant Biol. 2013; 64: 501-29. doi: 10.1146/annurev-arplant-050312-120103 PMID: 23638827
21. Malínská K, Malínský J, Opekarová M, Tanner W. Visualization of protein compartmentation within the plasma membrane of living yeast cells. Mol Biol Cell. 2003; 14(11): 4427-36. PMID: 14551254
22. Malinsky J, Opekarova M, Tanner W. The lateral compartmentation of the yeast plasma membrane. Yeast. 2010; 27(8): 473-8. doi: 10.1002/yea.1772 PMID: 20641012
23. Walther TC, Brickner JH, Aguilar PS, Bernales S, Pantoja C, Walter P. Eisosomes mark static sites of endocytosis. Nature. 2006; 439(7079): 998-1003. PMID: 16496001
24. Strádalová V, Stahlschmidt W, Grossmann G, Blazíková M, Rachel R, Tanner W, et al. Furrow-like invaginations of the yeast plasma membrane correspond to membrane compartment of Can1. J Cell Sci. 2009; 122(Pt 16): 2887-94. doi: 10.1242/jcs.051227 PMID: 19638406
25. Olivera-Couto A, Graña M, Harispe L, Aguilar PS. The eisosome core is composed of BAR domain proteins. Mol Biol Cell. 2011; 22(13): 2360-72. doi: 10.1091/mbc.E10-12-1021 PMID: 21593205
26. Karotki L, Huiskonen JT, Stefan CJ, Ziółkowska NE, Roth R, Surma MA, et al. Eisosome proteins assemble into a membrane scaffold. J Cell Biol. 2011; 195(5): 889-902. doi: 10.1083/jcb.201104040 PMID: 22123866
27. Douglas LM, Konopka JB, Fungal Membrane Organization: The Eisosome Concept. Annu Rev Microbiol. 2014; 68: 377-93. doi: 10.1146/annurev-micro-091313-103507 PMID: 25002088
28. Walther TC, Aguilar PS, Fröhlich F, Chu F, Moreira K, Burlingame AL et al. Pkh-kinases control eisosome assembly and organization. EMBO J. 2007; 26(24): 4946-55. PMID: 18034155
29. Grossmann G, Opekarová M, Malinsky J, Weig-Meckl I, Tanner W. Membrane potential governs lateral segregation of plasma membrane proteins and lipids in yeast. EMBO J. 2007; 26(1): 1-8. PMID: 17170709
30. Grossmann G, Malinsky J, Stahlschmidt W, Loibl M, Weig-Meckl I, Frommer WB et al. Plasma membrane microdomains regulate turnover of transport proteins in yeast. J Cell Biol. 2008; 183(6): 1075-1088. doi: 10.1083/jcb.200806035 PMID: 19064668
31. Fröhlich F, Moreira K, Aguilar PS, Hubner NC, Mann M, Walter P, et al. A genome-wide screen for genes affecting eisosomes reveals Nce102 function in sphingolipid signaling. J Cell Biol. 2009; 185(7): 1227-42. doi: 10.1083/jcb.200811081 PMID: 19564405
32. Dupont S, Beney L, Ritt JF, Lherminier J, Gervais P. Lateral reorganization of plasma membrane is involved in the yeast resistance to severe dehydration. BBA. 2010; 1798(5): 975-85. doi: 10.1016/j.bbamem.2010.01.015 PMID: 20116363
33. Berchtold D, Piccolis M, Chiaruttini N, Riezman I, Riezman H, Roux A, et al. Plasma membrane stress induces relocalization of Slm proteins and activation of TORC2 to promote sphingolipid synthesis. Nat Cell Biol. 2012; 14(5): 542-7. doi: 10.1038/ncb2480 PMID: 22504275
34. Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, Hieter P, et al. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast. 1998; 14(2): 115-32. PMID: 9483801
35. Robinson JS, Klionsky DJ, Banta LM, Emr SD. Protein sorting in Saccharomyces cerevisiae: isolation of mutants defective in the delivery and processing of multiple vacuolar hydrolases. Mol Cell Biol. 1988; 8(11): 4936-48. PMID: 3062374
36. Jorgensen P, Nishikawa JL, Breitkreutz BJ, Tyers M. Systematic identification of pathways that couple cell growth and division in yeast. Science. 2002; 297(5580): 395-400. PMID: 12089449
37. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS et al. Global analysis of protein localization in budding yeast. Nature. 2003; 425(6959): 686-91. PMID: 14562095
38. Mitchell SF, Jain S, She M, Parker R. Global analysis of yeast mRNPs. Nat Struct Mol Biol. 2013; 20(1): 127-33. doi: 10.1038/nsmb.2468 PMID: 23222640
39. Ramachandran V, Shah KH, Herman PK. The cAMP-dependent protein kinase signaling pathway is a key regulator of P body foci formation. Mol Cell. 2011; 43(6): 973-81. doi: 10.1016/j.molcel.2011.06.032 PMID: 21925385
40. Shah KH, Zhang B, Ramachandran V, Herman PK. Processing Body and Stress Granule Assembly Occur by Independent and Differentially Regulated Pathways in Saccharomyces cerevisiae. Genetics. 2013; 193(1): 109-23. doi: 10.1534/genetics.112.146993 PMID: 23105015
41. Grousl T, Ivanov P, Frýdlová I, Vasicová P, Janda F, Vojtová J, et al. Robust heat shock induces eIF2 alpha-phosphorylation-independent assembly of stress granules containing eIF3 and 40S ribosomal subunits in budding yeast, Saccharomyces cerevisiae. J Cell Sci. 2009; 122(12): 2078-2088. doi: 10.1242/jcs.045104 PMID: 19470581
42. Malinska K, Malinsky J, Opekarova M, Tanner W. Distribution of Can1p into stable domains reflects lateral protein segregation within the plasma membrane of living S. cerevisiae cells. J Cell Sci. 2004; 117 (Pt 25): 6031-41. PMID: 15536122
43. Eulalio A, Behm-Ansmant I, Izaurralde E. P bodies: at the crossroads of post-transcriptional pathways. Nature reviews. Mol Cell Biol. 2007; 8(1): 9-22.
44. Balagopal V, Fluch L, Nissan T. Ways and means of eukaryotic mRNA decay. BBA. 2012; 1819(6): 593-603. doi: 10.1016/j.bbagrm.2012.01.001 PMID: 22266130
45. Aizer A, Kalo A, Kafri P, Shraga A, Ben-Yishay R, Jacob A, et al. Quantifying mRNA targeting to P bodies in living human cells reveals a dual role in mRNA decay and storage. J Cell Sci. 2014; 127(20): 4443-56.
46. Alvarez FJ, Douglas LM, Rosebrock A, Konopka JB. The Sur7 protein regulates plasma membrane organization and prevents intracellular cell wall growth in Candida albicans. Mol Biol Cell. 2008; 19(12): 5214-25. doi: 10.1091/mbc.E08-05-0479 PMID: 18799621
47. Brach T, Specht T, Kaksonen M, Reassessment of the role of plasma membrane domains in the regulation of vesicular traffic in yeast. J Cell Sci. 2011; 124(3): 328-37.
48. Roelants FM, Torrance PD, Bezman N, Thorner J. Pkh1 and Pkh2 differentially phosphorylate and activate Ypk1 and Ykr2 and define protein kinase modules required for maintenance of cell wall integrity. Mol Biol Cell. 2002; 13(9): 3005-28. PMID: 12221112
49. Zhang X, Lester RL, Dickson RC. Pil1p and Lsp1p negatively regulate the 3-phosphoinositide-dependent protein kinase-like kinase Pkh1p and downstream signaling pathways Pkc1p and Ypk1p. J Biol Chem. 2004; 279(21): 22030-8. PMID: 15016821
50. Luo G, Gruhler A, Liu Y, Jensen ON, Dickson RC. The sphingolipid long-chain base-Pkh1/2-Ypk1/2 signaling pathway regulates eisosome assembly and turnover. J Biol Chem. 2008; 283(16): 10433-44. doi: 10.1074/jbc.M709972200 PMID: 18296441
51. Luo G, Costanzo M, Boone C, Dickson RC. Nutrients and the Pkh1/2 and Pkc1 protein kinases control mRNA decay and P-body assembly in yeast. J Biol Chem. 2011; 286(11): 8759-70. doi: 10.1074/jbc.M110.196030 PMID: 21163942
52. Arribere JA, Doudna JA, Gilbert WV. Reconsidering movement of eukaryotic mRNAs between polysomes and P bodies. Mol Cell. 2011; 44(5): 745-58. doi: 10.1016/j.molcel.2011.09.019 PMID: 22152478
53. Brengues M, Teixeira D, Parker R. Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science. 2005; 310(5747): 486-9. PMID: 16141371
54. Aragon AD, Quiñones GA, Thomas EV, Roy S, Werner-Washburne M. Release of extraction-resistant mRNA in stationary phase Saccharomyces cerevisiae produces a massive increase in transcript abundance in response to stress. Genome Biol. 2006; 7(2): R9. PMID: 16507144
55. Murashko ON, Kaberdin VR, Lin-Chao S. Membrane binding of Escherichia coli RNase E catalytic domain stabilizes protein structure and increases RNA substrate affinity. Proc Natl Acad Sci U S A. 2012; 109(18): 7019-24. doi: 10.1073/pnas.1120181109 PMID: 22509045
56. Mackie GA. RNase E: at the interface of bacterial RNA processing and decay. Nature reviews. Microbiology. 2013; 11(1): 45-57. doi: 10.1038/nrmicro2930 PMID: 23241849
57. Fröhlich F, Christiano R, Olson DK, Alcazar-Roman A, DeCamilli P, Walther TC. A role for eisosomes in maintenance of plasma membrane phosphoinositide levels. Mol Biol Cell. 2014; 25(18): 2797-806. doi: 10.1091/mbc.E13-11-0639 PMID: 25057013
58. Stradalova V, Blazikova M, Grossmann G, Opekarová M, Tanner W, Malinsky J. Distribution of cortical endoplasmic reticulum determines positioning of endocytic events in yeast plasma membrane. PLOS ONE. 2012; 7(4): e35132. doi: 10.1371/journal.pone.0035132 PMID: 22496901
59. Buchan JR, Muhlrad D, Parker R. P bodies promote stress granule assembly in Saccharomyces cerevisiae. J Cell Biol. 2008; 183(3): 441-55. doi: 10.1083/jcb.200807043 PMID: 18981231