Artículo

Tudisca, V.; Simpson, C.; Castelli, L.; Lui, J.; Hoyle, N.; Moreno, S.; Ashe, M.; Portela, P. "PKA isoforms coordinate mRNA fate during nutrient starvation" (2012) Journal of Cell Science. 125(21):5221-5232
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

A variety of stress conditions induce mRNA and protein aggregation into mRNA silencing foci, but the signalling pathways mediating these responses are still elusive. Previously we demonstrated that PKA catalytic isoforms Tpk2 and Tpk3 localise with processing and stress bodies in Saccharomyces cerevisiae. Here, we show that Tpk2 and Tpk3 are associated with translation initiation factors Pab1 and Rps3 in exponentially growing cells. Glucose starvation promotes the loss of interaction between Tpk and initiation factors followed by their accumulation into processing bodies. Analysis of mutants of the individual PKA isoform genes has revealed that the TPK3 or TPK2 deletion affects the capacity of the cells to form granules and arrest translation properly in response to glucose starvation or stationary phase. Moreover, we demonstrate that PKA controls Rpg1 and eIF4G1 protein abundance, possibly controlling cap-dependent translation. Taken together,our data suggest that the PKA pathway coordinates multiple stages in the fate of mRNAs in association with nutritional environment and growth status of the cell. © 2012.

Registro:

Documento: Artículo
Título:PKA isoforms coordinate mRNA fate during nutrient starvation
Autor:Tudisca, V.; Simpson, C.; Castelli, L.; Lui, J.; Hoyle, N.; Moreno, S.; Ashe, M.; Portela, P.
Filiación:Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Argentina
Faculty of Life Sciences, University of Manchester, The Michael Smith Building, Manchester, United Kingdom
Palabras clave:PKA; Saccharomyces cerevisiae; Translation; cyclic AMP dependent protein kinase; glucose; messenger RNA; tpk2 protein; tpk3 protein; unclassified drug; article; cell growth; controlled study; enzyme activity; gene deletion; gene mutation; nonhuman; priority journal; protein protein interaction; starvation; Culture Media; Cyclic AMP-Dependent Protein Kinase Catalytic Subunits; Cyclic AMP-Dependent Protein Kinases; Cytoplasmic Granules; Eukaryotic Initiation Factor-3; Eukaryotic Initiation Factor-4G; Gene Expression Regulation, Fungal; Glucose; Isoenzymes; Peptide Chain Initiation, Translational; Poly(A)-Binding Proteins; Protein Subunits; Protein Transport; Ribosomal Proteins; RNA, Messenger; Saccharomyces cerevisiae; Saccharomyces cerevisiae Proteins; Stress, Physiological; Saccharomyces cerevisiae
Año:2012
Volumen:125
Número:21
Página de inicio:5221
Página de fin:5232
DOI: http://dx.doi.org/10.1242/jcs.111534
Título revista:Journal of Cell Science
Título revista abreviado:J. Cell Sci.
ISSN:00219533
CODEN:JNCSA
CAS:glucose, 50-99-7, 84778-64-3; Culture Media; Cyclic AMP-Dependent Protein Kinase Catalytic Subunits, 2.7.11.11; Cyclic AMP-Dependent Protein Kinases, 2.7.11.11; Eukaryotic Initiation Factor-3; Eukaryotic Initiation Factor-4G; Glucose, 50-99-7; Isoenzymes; Poly(A)-Binding Proteins; Protein Subunits; RNA, Messenger; RPG1 protein, S cerevisiae; RPS3 protein, S cerevisiae; Ribosomal Proteins; Saccharomyces cerevisiae Proteins; TIF4631 protein, S cerevisiae; TPK2 protein, S cerevisiae, 2.7.1.-; Tpk1 protein, S cerevisiae, 2.7.1.11; Tpk3 protein, S cerevisiae, 2.7.11.11; pab1 protein, S cerevisiae
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00219533_v125_n21_p5221_Tudisca

Referencias:

  • Anderson, P., Kedersha, N., RNA granules (2006) J. Cell Biol., 172, pp. 803-808
  • Ashe, M.P., De Long, S.K., Sachs, A.B., Glucose depletion rapidly inhibits translation initiation in yeast (2000) Mol. Biol. Cell, 11, pp. 833-848
  • Berset, C., Trachsel, H., Altmann, M., The TOR (target of rapamycin) signal transduction pathway regulates the stability of translation initiation factor eIF4G in the yeast Saccharomyces cerevisiae (1998) Proc. Natl. Acad. Sci., 95, pp. 4264-4269. , USA
  • Beullens, M., Mbonyi, K., Geerts, L., Gladines, D., Detremerie, K., Jans, A.W., Thevelein, J.M., Studies on the mechanism of the glucose-induced cAMP signal in glycolysis and glucose repression mutants of the yeast Saccharomyces cerevisiae (1988) Eur. J. Biochem., 172, pp. 227-231
  • Braun, J.E., Tritschler, F., Haas, G., Igreja, C., Truffault, V., Weichenrieder, O., Izaurralde, E., The C-terminal alpha-alpha superhelix of Pat is required for mRNA decapping in metazoa (2010) EMBO J., 29, pp. 2368-2380
  • Brengues, M., Parker, R., Accumulation of polyadenylated mRNA, Pab1p, eIF4E, and eIF4G with P-bodies in Saccharomyces cerevisiae (2007) Mol. Biol. Cell, 18, pp. 2592-2602
  • Buchan, J.R., Muhlrad, D., Parker, R., P bodies promote stress granule assembly in Saccharomyces cerevisiae (2008) J. Cell Biol., 183, pp. 441-455
  • Buchan, J.R., Yoon, J.H., Parker, R., Stress-specific composition, assembly and kinetics of stress granules in Saccharomyces cerevisiae (2011) J. Cell Sci., 124, pp. 228-239
  • Castelli, L.M., Lui, J., Campbell, S.G., Rowe, W., Zeef, L.A., Holmes, L.E., Hoyle, N.P., Sims, P.F., Glucose depletion inhibits translation initiation via eIF4A loss and subsequent 48S preinitiation complex accumulation, while the pentose phosphate pathway is coordinately up-regulated (2011) Mol. Biol. Cell, 22, pp. 3379-3393
  • Chevtzoff, C., Vallortigara, J., Avéret, N., Rigoulet, M., Devin, A., The yeast cAMP protein kinase Tpk3p is involved in the regulation of mitochondrial enzymatic content during growth (2005) Biochim. Biophys. Acta, 1706, pp. 117-125
  • Chiu, W.L., Wagner, S., Herrmannová, A., Burela, L., Zhang, F., Saini, A.K., Valásek, L., Hinnebusch, A.G., The C-terminal region of eukaryotic translation initiation factor 3a (eIF3a) promotes mRNA recruitment, scanning, and, together with eIF3j and the eIF3b RNA recognition motif, selection of AUG start codons (2010) Mol. Cell. Biol., 30, pp. 4415-4434
  • Davidson, G.S., Joe, R.M., Roy, S., Meirelles, O., Allen, C.P., Wilson, M.R., Tapia, P.H., Chakraborty, S., The proteomics of quiescent and nonquiescent cell differentiation in yeast stationary-phase cultures (2011) Mol. Biol. Cell, 22, pp. 988-998
  • Dechant, R., Peter, M., Nutrient signals driving cell growth (2008) Curr. Opin. Cell Biol., 20, pp. 678-687
  • Decker, C.J., Teixeira, D., Parker, R., Edc3p and a glutamine/asparagine-rich domain of Lsm4p function in processing body assembly in Saccharomyces cerevisiae (2007) J. Cell Biol., 179, pp. 437-449
  • Ferrero, P.V., Layana, C., Paulucci, E., Gutiérrez, P., Hernández, G., Rivera-Pomar, R.V., Cap binding-independent recruitment of eIF4E to cytoplasmic foci (2012) Biochim. Biophys. Acta, 1823, pp. 1217-1224
  • Grousl, T., Ivanov, P., Frỳdlová, I., Vasicová, P., Janda, F., Vojtová, J., Malínská, K., Janosková, D., Robust heat shock induces eIF2alpha-phosphorylation-independent assembly of stress granules containing eIF3 and 40S ribosomal subunits in budding yeast, Saccharomyces cerevisiae (2009) J. Cell Sci., 122, pp. 2078-2088
  • Haim, L., Zipor, G., Aronov, S., Gerst, J.E., A genomic integration method to visualize localization of endogenous mRNAs in living yeast (2007) Nat. Methods, 4, pp. 409-412
  • Herman, P.K., Stationary phase in yeast (2002) Curr. Opin. Microbiol., 5, pp. 602-607
  • Hilliker, A., Parker, R., Stressed out? Make some modifications! (2008) Nat. Cell Biol., 10, pp. 1129-1130
  • Hoyle, N.P., Castelli, L.M., Campbell, S.G., Holmes, L.E., Ashe, M.P., Stress-dependent relocalization of translationally primed mRNPs to cytoplasmic granules that are kinetically and spatially distinct from P-bodies (2007) J. Cell Biol., 179, pp. 65-74
  • Huh, W.K., Falvo, J.V., Gerke, L.C., Carroll, A.S., Howson, R.W., Weissman, J.S., O'Shea, E.K., Global analysis of protein localization in budding yeast (2003) Nature, 425, pp. 686-691
  • Jackson, R.J., Hellen, C.U., Pestova, T.., The mechanism of eukaryotic translation initiation and principles of its regulation (2010) Nat. Rev. Mol. Cell Biol., 11, pp. 113-127
  • Kato, K., Yamamoto, Y., Izawa, S., Severe ethanol stress induces assembly of stress granules in Saccharomyces cerevisiae (2011) Yeast, 28, pp. 339-347
  • Kedersha, N., Stoecklin, G., Ayodele, M., Yacono, P., Lykke-Andersen, J., Fritzler, M.J., Scheuner, D., Anderson, P., Stress granules and processing bodies are dynamically linked sites of mRNP remodeling (2005) J. Cell Biol., 169, pp. 871-884
  • Kraakman, L., Lemaire, K., Ma, P., Teunissen, A.W., Donaton, M.C., Van Dijck, P., Winderickx, J., Thevelein, J.M., A Saccharomyces cerevisiae G-protein coupled receptor, Gpr1, is specifically required for glucose activation of the cAMP pathway during the transition to growth on glucose (1999) Mol. Microbiol., 32, pp. 1002-1012
  • Lui, J., Campbell, S.G., Ashe, M.P., Inhibition of translation initiation followingglucose depletion in yeast facilitates a rationalization of mRNA content (2010) Biochem. Soc. Trans., 38, pp. 1131-1136
  • McAlister, L., Holland, M.J., Targeted deletion of a yeast enolase structural gene. Identification and isolation of yeast enolase isozymes (1982) J. Biol. Chem., 257, pp. 7181-7188
  • Narayanaswamy, R., Levy, M., Tsechansky, M., Stovall, G.M., O'Connell, J.D., Mirrielees, J., Ellington, A.D., Marcotte, E.M., Widespread reorganization of metabolic enzymes into reversible assemblies upon nutrient starvation (2009) Proc. Natl. Acad. Sci., 106, pp. 10147-10152. , USA
  • Nielsen, K.H., Szamecz, B., Valásek, L., Jivotovskaya, A., Shin, B.S., Hinnebusch, A.G., Functions of eIF3 downstream of 48S assembly impact AUG recognition and GCN4 translational control (2004) EMBO J., 23, pp. 1166-1177
  • Ocampo, J., Fernandez Nuñez, L., Silva, F., Pereyra, E., Moreno, S., Garre, V., Rossi, S., A subunit of protein kinase a regulates growth and differentiation in the fungus Mucor circinelloides (2009) Eukaryot. Cell, 8, pp. 933-944
  • Oshima, T., Takano, I., Mutants Showing Heterothallism from a Homothallic Strain of SACCHAROMYCES CEREVISIAE (1980) Genetics, 94, pp. 841-857
  • Parker, R., Sheth, U., P bodies and the control of mRNA translation and degradation (2007) Mol. Cell, 25, pp. 635-646
  • Pestova, T.V., Lorsch, J.R., Hellen, C.U.T., Mechanisms of translation initiation in eukaryotes (2007) Translational Control in Biology and Medicine, pp. 87-128. , (ed. M. B. Mathews, N. Sonenberg and J. W. B. Hershey),Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press
  • Portela, P., Howell, S., Moreno, S., Rossi, S.K., In vivo and in vitro phosphorylation of two isoforms of yeast pyruvate kinase by protein kinase A (2002) J. Biol. Chem., 277, pp. 30477-30487
  • Ramachandran, V., Shah, K.H., Herman, P.K., The cAMP-dependent protein kinase signaling pathway is a key regulator of P body foci formation (2011) Mol. Cell, 43, pp. 973-981
  • Reijns, M.A., Alexander, R.D., Spiller, M.P., Beggs, J.D., A role for Q/N-rich aggregation-prone regions in P-body localization (2008) J. Cell Sci., 121, pp. 2463-2472
  • Rolland, F., De Winde, J.H., Lemaire, K., Boles, E., Thevelein, J.M., Winderickx, J., Glucose-induced cAMP signalling in yeast requires both a G-protein coupled receptor system for extracellular glucose detection and a separable hexose kinase-dependent sensing process (2000) Mol. Microbiol., 38, pp. 348-358
  • Rothstein, R., Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast (1991) Methods Enzymol., 194, pp. 281-301
  • Santangelo, G.M., Glucose signaling in Saccharomyces cerevisiae (2006) Microbiol. Mol. Biol. Rev., 70, pp. 253-282
  • Sheth, U., Parker, R., Decapping and decay of messenger RNA occur in cytoplasmic processing bodies (2003) Science, 300, pp. 805-808
  • Teixeira, D., Sheth, U., Valencia-Sanchez, M.A., Brengues, M., Parker, R., Processing bodies require RNA for assembly and contain nontranslating mRNAs (2005) RNA, 11, pp. 371-382
  • Toda, T., Cameron, S., Sass, P., Zoller, M., Scott, J.D., McMullen, B., Hurwitz, M., Wigler, M., Cloning and characterization of BCY1, a locus encoding a regulatory subunit of the cyclic AMP-dependent protein kinase in Saccharomyces cerevisiae (1987) Mol. Cell. Biol., 7, pp. 1371-1377
  • Tudisca, V., Recouvreux, V., Moreno, S., Boy-Marcotte, E., Jacquet, M., Portela, P., Differential localization to cytoplasm, nucleus or P-bodies of yeast PKA subunits under different growth conditions (2010) Eur. J. Cell Biol., 89, pp. 339-348
  • Wells, S.E., Hillner, P.E., Vale, R.D., Sachs, A.B., Circularization of mRNA by eukaryotic translation initiation factors (1998) Mol. Cell, 2, pp. 135-140
  • Werner-Washburne, M., Becker, J., Kosic-Smithers, J., Craig, E.A., Yeast Hsp70 RNA levels vary in response to the physiological status of the cell (1989) J. Bacteriol., 171, pp. 2680-2688
  • Werner-Washburne, M., Braun, E., Johnston, G.C., Singer, R.A., Stationary phase in the yeast Saccharomyces cerevisiae (1993) Microbiol. Rev., 57, pp. 383-401
  • Werner-Washburne, M., Braun, E.L., Crawford, M.E., Peck, V.M., Stationary phase in Saccharomyces cerevisiae (1996) Mol. Microbiol., 19, pp. 1159-1166
  • Wilczynska, A., Aigueperse, C., Kress, M., Dautry, F., Weil, D., The translational regulator CPEB1 provides a link between dcp1 bodies and stress granules (2005) J. Cell Sci., 118, pp. 981-992
  • Zakrajšek, T., Raspor, P., Jamnik, P., Saccharomyces cerevisiae in the stationary phase as a model organism-characterization at cellular and proteome level (2011) J. Proteomics, 74, pp. 2837-2845

Citas:

---------- APA ----------
Tudisca, V., Simpson, C., Castelli, L., Lui, J., Hoyle, N., Moreno, S., Ashe, M.,..., Portela, P. (2012) . PKA isoforms coordinate mRNA fate during nutrient starvation. Journal of Cell Science, 125(21), 5221-5232.
http://dx.doi.org/10.1242/jcs.111534
---------- CHICAGO ----------
Tudisca, V., Simpson, C., Castelli, L., Lui, J., Hoyle, N., Moreno, S., et al. "PKA isoforms coordinate mRNA fate during nutrient starvation" . Journal of Cell Science 125, no. 21 (2012) : 5221-5232.
http://dx.doi.org/10.1242/jcs.111534
---------- MLA ----------
Tudisca, V., Simpson, C., Castelli, L., Lui, J., Hoyle, N., Moreno, S., et al. "PKA isoforms coordinate mRNA fate during nutrient starvation" . Journal of Cell Science, vol. 125, no. 21, 2012, pp. 5221-5232.
http://dx.doi.org/10.1242/jcs.111534
---------- VANCOUVER ----------
Tudisca, V., Simpson, C., Castelli, L., Lui, J., Hoyle, N., Moreno, S., et al. PKA isoforms coordinate mRNA fate during nutrient starvation. J. Cell Sci. 2012;125(21):5221-5232.
http://dx.doi.org/10.1242/jcs.111534