Evolutionarily conserved 5'-3' exoribonuclease Xrn1 accumulates at plasma membrane-associated eisosomes in post-diauxic yeast
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
25811606
PubMed Central
PMC4374687
DOI
10.1371/journal.pone.0122770
PII: PONE-D-14-47490
Knihovny.cz E-zdroje
- MeSH
- buněčná membrána genetika metabolismus MeSH
- exoribonukleasy genetika metabolismus MeSH
- exprese genu MeSH
- glukosa metabolismus MeSH
- reakce na tepelný šok MeSH
- rekombinantní fúzní proteiny genetika metabolismus MeSH
- reportérové geny MeSH
- Saccharomyces cerevisiae - proteiny genetika metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- exoribonukleasy MeSH
- glukosa MeSH
- rekombinantní fúzní proteiny MeSH
- Saccharomyces cerevisiae - proteiny MeSH
- XRN1 protein, S cerevisiae MeSH Prohlížeč
Regulation of gene expression on the level of translation and mRNA turnover is widely conserved evolutionarily. We have found that the main mRNA decay enzyme, exoribonuclease Xrn1, accumulates at the plasma membrane-associated eisosomes after glucose exhaustion in a culture of the yeast S. cerevisiae. Eisosomal localization of Xrn1 is not achieved in cells lacking the main component of eisosomes, Pil1, or Sur7, the protein accumulating at the membrane compartment of Can1 (MCC) - the eisosome-organized plasma membrane microdomain. In contrast to the conditions of diauxic shift, when Xrn1 accumulates in processing bodies (P-bodies), or acute heat stress, in which these cytosolic accumulations of Xrn1 associate with eIF3a/Rpg1-containing stress granules, Xrn1 is not accompanied by other mRNA-decay machinery components when it accumulates at eisosomes in post-diauxic cells. It is important that Xrn1 is released from eisosomes after addition of fermentable substrate. We suggest that this spatial segregation of Xrn1 from the rest of the mRNA-decay machinery reflects a general regulatory mechanism, in which the key enzyme is kept separate from the rest of mRNA decay factors in resting cells but ready for immediate use when fermentable nutrients emerge and appropriate metabolism reprogramming is required. In particular, the localization of Xrn1 to the eisosome, together with previously published data, accents the relevance of this plasma membrane-associated compartment as a multipotent regulatory site.
Institute of Experimental Medicine Academy of Sciences of the Czech Republic Prague Czech Republic
Institute of Microbiology Academy of Sciences of the Czech Republic Prague Czech Republic
Zobrazit více v PubMed
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. 10.1016/j.cell.2013.05.012 PubMed DOI
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. 10.1016/j.bbagrm.2013.10.003 PubMed DOI PMC
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. PubMed
Parker R. RNA degradation in Saccharomyces cerevisae . Genetics. 2012;191(3): 671–702. 10.1534/genetics.111.137265 PubMed DOI PMC
Sheth U, Parker R. Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science. 2003;300(5620): 805–808. PubMed PMC
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. PubMed PMC
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. PubMed PMC
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. PubMed PMC
Parker R, Sheth U, P bodies and the control of mRNA translation and degradation. Mol Cell. 2007;25(5): 635–46. PubMed
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. 10.1016/j.ceb.2009.03.005 PubMed DOI PMC
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. PubMed PMC
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. PubMed PMC
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. PubMed
Anderson P, Kedersha N. Stress granules: the Tao of RNA triage. Trends Biochem Sci. 2008;33(3): 141–50. 10.1016/j.tibs.2007.12.003 PubMed DOI
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. PubMed PMC
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. PubMed PMC
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. PubMed PMC
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. 10.1242/jcs.078444 PubMed DOI PMC
Simons K, Gerl MJ. Revitalizing membrane rafts: new tools and insights. Nature reviews. Mol Cell Biol. 2010;11(10): 688–99. 10.1038/nrm2977 PubMed DOI
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. 10.1146/annurev-arplant-050312-120103 PubMed DOI
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. PubMed PMC
Malinsky J, Opekarova M, Tanner W. The lateral compartmentation of the yeast plasma membrane. Yeast. 2010;27(8): 473–8. 10.1002/yea.1772 PubMed DOI
Walther TC, Brickner JH, Aguilar PS, Bernales S, Pantoja C, Walter P. Eisosomes mark static sites of endocytosis. Nature. 2006;439(7079): 998–1003. PubMed
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. 10.1242/jcs.051227 PubMed DOI
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. 10.1091/mbc.E10-12-1021 PubMed DOI PMC
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. 10.1083/jcb.201104040 PubMed DOI PMC
Douglas LM, Konopka JB, Fungal Membrane Organization: The Eisosome Concept. Annu Rev Microbiol. 2014;68: 377–93. 10.1146/annurev-micro-091313-103507 PubMed DOI
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. PubMed PMC
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. PubMed PMC
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. 10.1083/jcb.200806035 PubMed DOI PMC
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. 10.1083/jcb.200811081 PubMed DOI PMC
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. 10.1016/j.bbamem.2010.01.015 PubMed DOI
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. 10.1038/ncb2480 PubMed DOI
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. PubMed
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. PubMed PMC
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. PubMed
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. PubMed
Mitchell SF, Jain S, She M, Parker R. Global analysis of yeast mRNPs. Nat Struct Mol Biol. 2013;20(1): 127–33. 10.1038/nsmb.2468 PubMed DOI PMC
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. 10.1016/j.molcel.2011.06.032 PubMed DOI PMC
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. 10.1534/genetics.112.146993 PubMed DOI PMC
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. 10.1242/jcs.045104 PubMed DOI
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. PubMed
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. PubMed
Balagopal V, Fluch L, Nissan T. Ways and means of eukaryotic mRNA decay. BBA. 2012;1819(6): 593–603. 10.1016/j.bbagrm.2012.01.001 PubMed DOI
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. PubMed
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. 10.1091/mbc.E08-05-0479 PubMed DOI PMC
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. PubMed
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. PubMed PMC
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. PubMed
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. 10.1074/jbc.M709972200 PubMed DOI PMC
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. 10.1074/jbc.M110.196030 PubMed DOI PMC
Arribere JA, Doudna JA, Gilbert WV. Reconsidering movement of eukaryotic mRNAs between polysomes and P bodies. Mol Cell. 2011;44(5): 745–58. 10.1016/j.molcel.2011.09.019 PubMed DOI PMC
Brengues M, Teixeira D, Parker R. Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science. 2005;310(5747): 486–9. PubMed PMC
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 PubMed PMC
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. 10.1073/pnas.1120181109 PubMed DOI PMC
Mackie GA. RNase E: at the interface of bacterial RNA processing and decay. Nature reviews. Microbiology. 2013;11(1): 45–57. 10.1038/nrmicro2930 PubMed DOI
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. 10.1091/mbc.E13-11-0639 PubMed DOI PMC
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 10.1371/journal.pone.0035132 PubMed DOI PMC
Buchan JR, Muhlrad D, Parker R. P bodies promote stress granule assembly in Saccharomyces cerevisiae . J Cell Biol. 2008;183(3): 441–55. 10.1083/jcb.200807043 PubMed DOI PMC
Conserved mechanism of Xrn1 regulation by glycolytic flux and protein aggregation
Live cell fluorescence microscopy-an end-to-end workflow for high-throughput image and data analysis
Plasma Membrane Protein Nce102 Modulates Morphology and Function of the Yeast Vacuole
Role of MCC/Eisosome in Fungal Lipid Homeostasis