Artículo

Baccarini, L.; Martínez-Montañés, F.; Rossi, S.; Proft, M.; Portela, P. "PKA-chromatin association at stress responsive target genes from Saccharomyces cerevisiae" (2015) Biochimica et Biophysica Acta - Gene Regulatory Mechanisms. 1849(11):1329-1339
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Abstract:

Gene expression regulation by intracellular stimulus-activated protein kinases is essential for cell adaptation to environmental changes. There are three PKA catalytic subunits in Saccharomyces cerevisiae: Tpk1, Tpk2, and Tpk3 and one regulatory subunit: Bcy1. Previously, it has been demonstrated that Tpk1 and Tpk2 are associated with coding regions and promoters of target genes in a carbon source and oxidative stress dependent manner. Here we studied five genes, ALD6, SED1, HSP42, RPS29B, and RPL1B whose expression is regulated by saline stress. We found that PKA catalytic and regulatory subunits are associated with both coding regions and promoters of the analyzed genes in a stress dependent manner. Tpk1 and Tpk2 recruitment was completely abolished in catalytic inactive mutants. BCY1 deletion changed the binding kinetic to chromatin of each Tpk isoform and this strain displayed a deregulated gene expression in response to osmotic stress. In addition, yeast mutants with high PKA activity exhibit sustained association to target genes of chromatin-remodeling complexes such as Snf2-catalytic subunit of the SWI/SNF complex and Arp8-component of INO80 complex, leading to upregulation of gene expression during osmotic stress. Tpk1 accumulation in the nucleus was stimulated upon osmotic stress, while the nuclear localization of Tpk2 and Bcy1 showed no change. We found that each PKA subunit is transported into the nucleus by a different β-karyopherin pathway. Moreover, β-karyopherin mutant strains abolished the chromatin association of Tpk1 or Tpk2, suggesting that nuclear localization of PKA catalytic subunits is required for its association to target genes and properly gene expression. © 2015 Elsevier B.V.

Registro:

Documento: Artículo
Título:PKA-chromatin association at stress responsive target genes from Saccharomyces cerevisiae
Autor:Baccarini, L.; Martínez-Montañés, F.; Rossi, S.; Proft, M.; Portela, P.
Filiación:Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, IQUIBICEN-CONICET, Universidad de Buenos Aires, Buenos Aires, Argentina
Instituto de Biomedicina CSIC, Valencia, Spain
Department of Biology, University of Fribourg, Fribourg, Switzerland
Palabras clave:Chromatin; Osmotic stress; PKA; Saccharomyces cerevisiae; karyopherin beta; chromatin; cyclic AMP dependent protein kinase; Saccharomyces cerevisiae protein; ald6 gene; Article; cell survival; chromatin; chromatin assembly and disassembly; fungal gene; gene deletion; gene expression regulation; gene targeting; genetic analysis; hsp42 gene; nonhuman; osmotic stress; pKa; priority journal; promoter region; rps29b gene; Saccharomyces cerevisiae; sed1 gene; upregulation; biosynthesis; chromatin; enzymology; genetics; metabolism; physiological stress; physiology; Saccharomyces cerevisiae; Chromatin; Cyclic AMP-Dependent Protein Kinases; Gene Expression Regulation, Fungal; Saccharomyces cerevisiae; Saccharomyces cerevisiae Proteins; Stress, Physiological
Año:2015
Volumen:1849
Número:11
Página de inicio:1329
Página de fin:1339
DOI: http://dx.doi.org/10.1016/j.bbagrm.2015.09.007
Título revista:Biochimica et Biophysica Acta - Gene Regulatory Mechanisms
Título revista abreviado:Biochim. Biophys. Acta Gene Regul. Mech.
ISSN:18749399
CAS:cyclic AMP dependent protein kinase; Chromatin; Cyclic AMP-Dependent Protein Kinases; Saccharomyces cerevisiae Proteins
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_18749399_v1849_n11_p1329_Baccarini

Referencias:

  • Kyriakis, J.M., Avruch, J., Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation (2001) Physiol. Rev., 81, pp. 807-869
  • Proft, M., Struhl, K., Hog1 kinase converts the Sko1-Cyc8-Tup1 repressor complex into an activator that recruits SAGA and SWI/SNF in response to osmotic stress (2002) Mol. Cell, 9, pp. 1307-1317
  • De, N.E., Zapater, M., Alepuz, P.M., Sumoy, L., Mas, G., Posas, F., The MAPK Hog1 recruits Rpd3 histone deacetylase to activate osmoresponsive genes (2004) Nature, 427, pp. 370-374
  • Li, H., Tsang, C.K., Watkins, M., Bertram, P.G., Zheng, X.F., Nutrient regulates Tor1 nuclear localization and association with rDNA promoter (2006) Nature, 442, pp. 1058-1061
  • Pascual-Ahuir, A., Proft, M., The Sch9 kinase is a chromatin-associated transcriptional activator of osmostress-responsive genes (2007) EMBO J., 26, pp. 3098-3108
  • Pokholok, D.K., Zeitlinger, J., Hannett, N.M., Reynolds, D.B., Young, R.A., Activated signal transduction kinases frequently occupy target genes (2006) Science, 313, pp. 533-536
  • Schaekel, A., Desai, P.R., Ernst, J.F., Morphogenesis-regulated localization of protein kinase A to genomic sites in Candida albicans (2013) BMC Genomics, 14, p. 842
  • Reiter, W., Watt, S., Dawson, K., Lawrence, C.L., Bahler, J., Jones, N., Wilkinson, C.R., Fission yeast MAP kinase Sty1 is recruited to stress-induced genes (2008) J. Biol. Chem., 283, pp. 9945-9956
  • Thevelein, J.M., de Winde, J.H., Novel sensing mechanisms and targets for the cAMP-protein kinase A pathway in the yeast Saccharomyces cerevisiae (1999) Mol. Microbiol., 33, pp. 904-918
  • 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
  • Toda, T., Cameron, S., Sass, P., Zoller, M., Wigler, M., Three different genes in S. cerevisiae encode the catalytic subunits of the cAMP-dependent protein kinase (1987) Cell, 50, pp. 277-287
  • Pedruzzi, I., Burckert, N., Egger, P., De Virgilio, C., Saccharomyces cerevisiaeRas/cAMP pathway controls post-diauxic shift element-dependent transcription through the zinc finger protein Gis1 (2000) EMBO J., 19, pp. 2569-2579
  • Martinez-Pastor, M.T., Marchler, G., Schuller, C., Marchler-Bauer, A., Ruis, H., Estruch, F., The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE) (1996) EMBO J., 15, pp. 2227-2235
  • Gorner, W., Durchschlag, E., Martinez-Pastor, M.T., Estruch, F., Ammerer, G., Hamilton, B., Ruis, H., Schuller, C., Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity (1998) Genes Dev., 12, pp. 586-597
  • Chang, Y.W., Howard, S.C., Herman, P.K., The Ras/PKA signaling pathway directly targets the Srb9 protein, a component of the general RNA polymerase II transcription apparatus (2004) Mol. Cell, 15, pp. 107-116
  • Pelechano, V., Jimeno-Gonzalez, S., Rodriguez-Gil, A., Garcia-Martinez, J., Perez-Ortin, J.E., Chavez, S., Regulon-specific control of transcription elongation across the yeast genome (2009) PLoS Genet., 5, p. e1000614
  • Roy, A., Shin, Y.J., Cho, K.H., Kim, J.H., Mth1 regulates the interaction between the Rgt1 repressor and the Ssn6-Tup1 corepressor complex by modulating PKA-dependent phosphorylation of Rgt1 (2013) Mol. Biol. Cell, 24, pp. 1493-1503
  • Robertson, L.S., Fink, G.R., The three yeast a kinases have specific signaling functions in pseudohyphal growth (1998) Proc. Natl. Acad. Sci. U. S. A., 95, pp. 13783-13787
  • Pan, X., Heitman, J., Cyclic AMP-dependent protein kinase regulates pseudohyphal differentiation in Saccharomyces cerevisiae (1999) Mol. Cell. Biol., 19, pp. 4874-4887
  • Malcher, M., Schladebeck, S., Mosch, H.U., The Yak1 protein kinase lies at the center of a regulatory cascade affecting adhesive growth and stress resistance in Saccharomyces cerevisiae (2011) Genetics, 187, pp. 717-730
  • 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
  • Griffioen, G., Anghileri, P., Imre, E., Baroni, M.D., Ruis, H., Nutritional control of nucleocytoplasmic localization of cAMP-dependent protein kinase catalytic and regulatory subunits in Saccharomyces cerevisiae (2000) J. Biol. Chem., 275, pp. 1449-1456
  • 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) J. Cell Sci., 125, pp. 5221-5232
  • Leslie, D.M., Zhang, W., Timney, B.L., Chait, B.T., Rout, M.P., Wozniak, R.W., Aitchison, J.D., Characterization of karyopherin cargoes reveals unique mechanisms of Kap121p-mediated nuclear import (2004) Mol. Cell. Biol., 24, pp. 8487-8503
  • Bakhrat, A., Baranes, K., Krichevsky, O., Rom, I., Schlenstedt, G., Pietrokovski, S., Raveh, D., Nuclear import of ho endonuclease utilizes two nuclear localization signals and four importins of the ribosomal import system (2006) J. Biol. Chem., 281, pp. 12218-12226
  • Caesar, S., Greiner, M., Schlenstedt, G., Kap120 functions as a nuclear import receptor for ribosome assembly factor Rpf1 in yeast (2006) Mol. Cell. Biol., 26, pp. 3170-3180
  • Mosammaparast, N., Guo, Y., Shabanowitz, J., Hunt, D.F., Pemberton, L.F., Pathways mediating the nuclear import of histones H3 and H4 in yeast (2002) J. Biol. Chem., 277, pp. 862-868
  • Greiner, M., Caesar, S., Schlenstedt, G., The histones H2A/H2B and H3/H4 are imported into the yeast nucleus by different mechanisms (2004) Eur. J. Cell Biol., 83, pp. 511-520
  • Quan, X., Yu, J., Bussey, H., Stochaj, U., The localization of nuclear exporters of the importin-beta family is regulated by Snf1 kinase, nutrient supply and stress (2007) Biochim. Biophys. Acta, 1773, pp. 1052-1061
  • Stochaj, U., Rassadi, R., Chiu, J., Stress-mediated inhibition of the classical nuclear protein import pathway and nuclear accumulation of the small GTPase Gsp1p (2000) FASEB J., 14, pp. 2130-2132
  • Demlow, C.M., Fox, T.D., Activity of mitochondrially synthesized reporter proteins is lower than that of imported proteins and is increased by lowering cAMP in glucose-grown Saccharomyces cerevisiae cells (2003) Genetics, 165, pp. 961-974
  • Ito, H., Fukuda, Y., Murata, K., Kimura, A., Transformation of intact yeast cells treated with alkali cations (1983) J. Bacteriol., 153, pp. 163-168
  • 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
  • Shulga, N., Mosammaparast, N., Wozniak, R., Goldfarb, D.S., Yeast nucleoporins involved in passive nuclear envelope permeability (2000) J. Cell Biol., 149, pp. 1027-1038
  • Roberts, P.M., Goldfarb, D.S., In vivo nuclear transport kinetics in Saccharomyces cerevisiae (1998) Methods Cell Biol., 53, pp. 545-557
  • Kuras, L., Struhl, K., Binding of TBP to promoters in vivo is stimulated by activators and requires Pol II holoenzyme (1999) Nature, 399, pp. 609-613
  • Proft, M., Pascual-Ahuir, A., de Nadal, E., Arino, J., Serrano, R., Posas, F., Regulation of the Sko1 transcriptional repressor by the Hog1 MAP kinase in response to osmotic stress (2001) EMBO J., 20, pp. 1123-1133
  • Martinez-Bono, B., Quilis, I., Zalve, E., Igual, J.C., Yeast karyopherins Kap123 and Kap95 are related to the function of the cell integrity pathway (2010) FEMS Yeast Res., 10, pp. 28-37
  • Berry, D.B., Gasch, A.P., Stress-activated genomic expression changes serve a preparative role for impending stress in yeast (2008) Mol. Biol. Cell, 19, pp. 4580-4587
  • Causton, H.C., Ren, B., Koh, S.S., Harbison, C.T., Kanin, E., Jennings, E.G., Lee, T.I., Young, R.A., Remodeling of yeast genome expression in response to environmental changes (2001) Mol. Biol. Cell, 12, pp. 323-337
  • Norbeck, J., Blomberg, A., The level of cAMP-dependent protein kinase A activity strongly affects osmotolerance and osmo-instigated gene expression changes in Saccharomyces cerevisiae (2000) Yeast, 16, pp. 121-137
  • Saha, A., Wittmeyer, J., Cairns, B.R., Chromatin remodeling by RSC involves ATP-dependent DNA translocation (2002) Genes Dev., 16, pp. 2120-2134
  • Ford, J., Odeyale, O., Shen, C.H., Activator-dependent recruitment of SWI/SNF and INO80 during INO1 activation (2008) Biochem. Biophys. Res. Commun., 373, pp. 602-606
  • Klopf, E., Paskova, L., Sole, C., Mas, G., Petryshyn, A., Posas, F., Wintersberger, U., Schuller, C., Cooperation between the INO80 complex and histone chaperones determines adaptation of stress gene transcription in the yeast Saccharomyces cerevisiae (2009) Mol. Cell. Biol., 29, pp. 4994-5007
  • Posas, F., Chambers, J.R., Heyman, J.A., Hoeffler, J.P., de Nadal, E., Arino, J., The transcriptional response of yeast to saline stress (2000) J. Biol. Chem., 275, pp. 17249-17255
  • Marquez, J.A., Serrano, R., Multiple transduction pathways regulate the sodium-extrusion gene PMR2/ENA1 during salt stress in yeast (1996) FEBS Lett., 382, pp. 89-92
  • Pascual-Ahuir, A., Posas, F., Serrano, R., Proft, M., Multiple levels of control regulate the yeast cAMP-response element-binding protein repressor Sko1p in response to stress (2001) J. Biol. Chem., 276, pp. 37373-37378
  • Yaakov, G., Bell, M., Hohmann, S., Engelberg, D., Combination of two activating mutations in one HOG1 gene forms hyperactive enzymes that induce growth arrest (2003) Mol. Cell. Biol., 23, pp. 4826-4840
  • Vendrell, A., Martinez-Pastor, M., Gonzalez-Novo, A., Pascual-Ahuir, A., Sinclair, D.A., Proft, M., Posas, F., Sir2 histone deacetylase prevents programmed cell death caused by sustained activation of the Hog1 stress-activated protein kinase (2011) EMBO Rep., 12, pp. 1062-1068
  • Dolado, I., Nebreda, A.R., AKT and oxidative stress team up to kill cancer cells (2008) Cancer Cell, 14, pp. 427-429
  • de, N.E., Posas, F., Osmostress-induced gene expression - a model to understand how stress-activated protein kinases (SAPKs) regulate transcription (2015) FEBS J.
  • Strom, A.C., Weis, K., Importin-beta-like nuclear transport receptors (2001) Genome Biol., 2. , (REVIEWS3008)
  • Weis, K., Nucleocytoplasmic transport: cargo trafficking across the border (2002) Curr. Opin. Cell Biol., 14, pp. 328-335
  • Griffioen, G., Swinnen, S., Thevelein, J.M., Feedback inhibition on cell wall integrity signaling by Zds1 involves Gsk3 phosphorylation of a cAMP-dependent protein kinase regulatory subunit (2003) J. Biol. Chem., 278, pp. 23460-23471
  • Solari, C.A., Tudisca, V., Pugliessi, M., Nadra, A.D., Moreno, S., Portela, P., Regulation of PKA activity by an autophosphorylation mechanism in Saccharomyces cerevisiae (2014) Biochem. J., 462, pp. 567-579
  • Haesendonckx, S., Tudisca, V., Voordeckers, K., Moreno, S., Thevelein, J.M., Portela, P., The activation loop of PKA catalytic isoforms is differentially phosphorylated by Pkh protein kinases in Saccharomyces cerevisiae (2012) Biochem. J., 448, pp. 307-320
  • Soulard, A., Cremonesi, A., Moes, S., Schutz, F., Jeno, P., Hall, M.N., The rapamycin-sensitive phosphoproteome reveals that TOR controls protein kinase A toward some but not all substrates (2010) Mol. Biol. Cell, 21, pp. 3475-3486
  • Kosugi, S., Hasebe, M., Tomita, M., Yanagawa, H., Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs (2009) Proc. Natl. Acad. Sci. U. S. A., 106, pp. 10171-10176
  • Chook, Y.M., Suel, K.E., Nuclear import by karyopherin-betas: recognition and inhibition (2011) Biochim. Biophys. Acta, 1813, pp. 1593-1606
  • Alepuz, P.M., Jovanovic, A., Reiser, V., Ammerer, G., Stress-induced map kinase Hog1 is part of transcription activation complexes (2001) Mol. Cell, 7, pp. 767-777
  • Nelson, J.D., LeBoeuf, R.C., Bomsztyk, K., Direct recruitment of insulin receptor and ERK signaling cascade to insulin-inducible gene loci (2011) Diabetes, 60, pp. 127-137
  • Lawrence, M.C., Shao, C., McGlynn, K., Naziruddin, B., Levy, M.F., Cobb, M.H., Multiple chromatin-bound protein kinases assemble factors that regulate insulin gene transcription (2009) Proc. Natl. Acad. Sci. U. S. A., 106, pp. 22181-22186

Citas:

---------- APA ----------
Baccarini, L., Martínez-Montañés, F., Rossi, S., Proft, M. & Portela, P. (2015) . PKA-chromatin association at stress responsive target genes from Saccharomyces cerevisiae. Biochimica et Biophysica Acta - Gene Regulatory Mechanisms, 1849(11), 1329-1339.
http://dx.doi.org/10.1016/j.bbagrm.2015.09.007
---------- CHICAGO ----------
Baccarini, L., Martínez-Montañés, F., Rossi, S., Proft, M., Portela, P. "PKA-chromatin association at stress responsive target genes from Saccharomyces cerevisiae" . Biochimica et Biophysica Acta - Gene Regulatory Mechanisms 1849, no. 11 (2015) : 1329-1339.
http://dx.doi.org/10.1016/j.bbagrm.2015.09.007
---------- MLA ----------
Baccarini, L., Martínez-Montañés, F., Rossi, S., Proft, M., Portela, P. "PKA-chromatin association at stress responsive target genes from Saccharomyces cerevisiae" . Biochimica et Biophysica Acta - Gene Regulatory Mechanisms, vol. 1849, no. 11, 2015, pp. 1329-1339.
http://dx.doi.org/10.1016/j.bbagrm.2015.09.007
---------- VANCOUVER ----------
Baccarini, L., Martínez-Montañés, F., Rossi, S., Proft, M., Portela, P. PKA-chromatin association at stress responsive target genes from Saccharomyces cerevisiae. Biochim. Biophys. Acta Gene Regul. Mech. 2015;1849(11):1329-1339.
http://dx.doi.org/10.1016/j.bbagrm.2015.09.007