- -

A functional Rim101 complex is required for proper accumulation of the Ena1 Na+-ATPase protein in response to salt stress in Saccharomyces cerevisiae

RiuNet: Repositorio Institucional de la Universidad Politécnica de Valencia

Compartir/Enviar a

Citas

Estadísticas

  • Estadisticas de Uso

A functional Rim101 complex is required for proper accumulation of the Ena1 Na+-ATPase protein in response to salt stress in Saccharomyces cerevisiae

Mostrar el registro sencillo del ítem

Ficheros en el ítem

Thumbnail
Nombre: pdf.pdf
Tamaño: 1.810Mb
Formato: PDF
Descripción: Versión del Autor.
Abrir
[Cerrado]
Nombre: MARI CARMEN MARQU ...
Tamaño: 9.220Mb
Formato: PDF
Descripción: Versión editorial
Solicitar una copia al autor
dc.contributor.author Marqués, M. Carmen es_ES
dc.contributor.author Zamarbide-Forés, Sara es_ES
dc.contributor.author Pedelini, Leda es_ES
dc.contributor.author Llopis Torregrosa, Vicent es_ES
dc.contributor.author Yenush, Lynne es_ES
dc.date.accessioned 2017-04-18T07:09:04Z
dc.date.available 2017-04-18T07:09:04Z
dc.date.issued 2015-06
dc.identifier.issn 1567-1356
dc.identifier.uri http://hdl.handle.net/10251/79711
dc.description.abstract [EN] The maintenance of ionic homeostasis is essential for cell viability, thus the activity of plasma membrane ion transporters must be tightly controlled. Previous studies in Saccharomyces cerevisiae revealed that the proper trafficking of several nutrient permeases requires the E3 ubiquitin ligase Rsp5 and, in many cases, the presence of specific adaptor proteins needed for Rsp5 substrate recognition. Among these adaptor proteins are nine members of the arrestin-related trafficking adaptor (ART) family. We studied the possible role of the ART family in the regulation of monovalent cation transporters. We show here that the salt sensitivity phenotype of the rim8/art9 mutant is due to severe defects in Ena1 protein accumulation, which is not attributable to transcriptional defects. Many components of the Rim pathway are required for correct Ena1 accumulation, but not for the accumulation of other nutrient permeases. Moreover, we observe that strains lacking components of the endosomal sorting complexes required for transport (ESCRT) pathway previously described to play a role in Rim complex formation present similar defects in Ena1 accumulation. Our results show that, in response to salt stress, a functional Rim complex via specific ESCRT interactions is required for the proper accumulation of the Ena1 protein, but not induction of the ENA1 gene. es_ES
dc.description.sponsorship This work was supported by grants BFU2011-30197-C03-03 from the Spanish Ministry of Science and Innovation (Madrid, Spain) and EUI2009-04147 [Systems Biology of Microorganisms (SysMo2) European Research Area-Network (ERA-NET)]. V. L-T. was supported by a pre-doctoral fellowship from the Polytechnic University of Valencia. en_EN
dc.language Inglés es_ES
dc.publisher Oxford University Press (OUP) es_ES
dc.relation.ispartof FEMS Yeast Research es_ES
dc.rights Reserva de todos los derechos es_ES
dc.subject Ion transport es_ES
dc.subject Rim101 pathway es_ES
dc.subject ESCRT pathway es_ES
dc.subject ENA1 es_ES
dc.subject Protein trafficking es_ES
dc.subject Salt stress es_ES
dc.subject.classification BIOQUIMICA Y BIOLOGIA MOLECULAR es_ES
dc.title A functional Rim101 complex is required for proper accumulation of the Ena1 Na+-ATPase protein in response to salt stress in Saccharomyces cerevisiae es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1093/femsyr/fov017
dc.relation.projectID info:eu-repo/grantAgreement/MICINN//BFU2011-30197-C03-03/ES/PAPEL DEL TRAFICO DE PROTEINAS EN LA HOMEOSTASIS DE IONES Y NUTRIENTES EN LEVADURA Y PLANTAS/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MICINN//EUI2009-04147/ES/MODELADO DE REDES GENICAS Y DE PROTEINAS RELEVANTES EN LA HOMEOSTASIS DE CATIONES EN LEVADURA/ es_ES
dc.rights.accessRights Abierto es_ES
dc.contributor.affiliation Universitat Politècnica de València. Instituto Universitario Mixto de Biología Molecular y Celular de Plantas - Institut Universitari Mixt de Biologia Molecular i Cel·lular de Plantes es_ES
dc.contributor.affiliation Universitat Politècnica de València. Escuela Técnica Superior de Ingeniería Agronómica y del Medio Natural - Escola Tècnica Superior d'Enginyeria Agronòmica i del Medi Natural es_ES
dc.description.bibliographicCitation Marqués, MC.; Zamarbide-Forés, S.; Pedelini, L.; Llopis Torregrosa, V.; Yenush, L. (2015). A functional Rim101 complex is required for proper accumulation of the Ena1 Na+-ATPase protein in response to salt stress in Saccharomyces cerevisiae. FEMS Yeast Research. 15(4):1-12. https://doi.org/10.1093/femsyr/fov017 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion http://dx.doi.org/10.1093/femsyr/fov017 es_ES
dc.description.upvformatpinicio 1 es_ES
dc.description.upvformatpfin 12 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 15 es_ES
dc.description.issue 4 es_ES
dc.relation.senia 290609 es_ES
dc.identifier.eissn 1567-1364
dc.identifier.pmid 25934176
dc.description.references Abriel, H., Loffing, J., Rebhun, J. F., Pratt, J. H., Schild, L., Horisberger, J.-D., … Staub, O. (1999). Defective regulation of the epithelial Na+ channel by Nedd4 in Liddle’s syndrome. Journal of Clinical Investigation, 103(5), 667-673. doi:10.1172/jci5713 es_ES
dc.description.references Alepuz, P. M., Cunningham, K. W., & Estruch, F. (1997). Glucose repression affects ion homeostasis in yeast through the regulation of the stress‐activated ENA1 gene. Molecular Microbiology, 26(1), 91-98. doi:10.1046/j.1365-2958.1997.5531917.x es_ES
dc.description.references Arino, J., Ramos, J., & Sychrova, H. (2010). Alkali Metal Cation Transport and Homeostasis in Yeasts. Microbiology and Molecular Biology Reviews, 74(1), 95-120. doi:10.1128/mmbr.00042-09 es_ES
dc.description.references Bagnat, M., Chang, A., & Simons, K. (2001). Plasma Membrane Proton ATPase Pma1p Requires Raft Association for Surface Delivery in Yeast. Molecular Biology of the Cell, 12(12), 4129-4138. doi:10.1091/mbc.12.12.4129 es_ES
dc.description.references Boysen, J. H., & Mitchell, A. P. (2006). Control of Bro1-Domain Protein Rim20 Localization by External pH, ESCRT Machinery, and the Saccharomyces cerevisiae Rim101 Pathway. Molecular Biology of the Cell, 17(3), 1344-1353. doi:10.1091/mbc.e05-10-0949 es_ES
dc.description.references Calcagno-Pizarelli, A. M., Hervas-Aguilar, A., Galindo, A., Abenza, J. F., Penalva, M. A., & Arst, H. N. (2011). Rescue of Aspergillus nidulans severely debilitating null mutations in ESCRT-0, I, II and III genes by inactivation of a salt-tolerance pathway allows examination of ESCRT gene roles in pH signalling. Journal of Cell Science, 124(23), 4064-4076. doi:10.1242/jcs.088344 es_ES
dc.description.references Crespo, J. L., Daicho, K., Ushimaru, T., & Hall, M. N. (2001). The GATA Transcription Factors GLN3 and GAT1 Link TOR to Salt Stress inSaccharomyces cerevisiae. Journal of Biological Chemistry, 276(37), 34441-34444. doi:10.1074/jbc.m103601200 es_ES
dc.description.references Galindo, A., Calcagno-Pizarelli, A. M., Arst, H. N., & Penalva, M. A. (2012). An ordered pathway for the assembly of fungal ESCRT-containing ambient pH signalling complexes at the plasma membrane. Journal of Cell Science, 125(7), 1784-1795. doi:10.1242/jcs.098897 es_ES
dc.description.references Garí, E., Piedrafita, L., Aldea, M., & Herrero, E. (1997). A Set of Vectors with a Tetracycline-Regulatable Promoter System for Modulated Gene Expression inSaccharomyces cerevisiae. Yeast, 13(9), 837-848. doi:10.1002/(sici)1097-0061(199707)13:9<837::aid-yea145>3.0.co;2-t es_ES
dc.description.references Gaxiola, R., de Larrinoa, I. F., Villalba, J. M., & Serrano, R. (1992). A novel and conserved salt-induced protein is an important determinant of salt tolerance in yeast. The EMBO Journal, 11(9), 3157-3164. doi:10.1002/j.1460-2075.1992.tb05392.x es_ES
dc.description.references Giaever, G., Chu, A. M., Ni, L., Connelly, C., Riles, L., Véronneau, S., … André, B. (2002). Functional profiling of the Saccharomyces cerevisiae genome. Nature, 418(6896), 387-391. doi:10.1038/nature00935 es_ES
dc.description.references Hayashi, M., Fukuzawa, T., Sorimachi, H., & Maeda, T. (2005). Constitutive Activation of the pH-Responsive Rim101 Pathway in Yeast Mutants Defective in Late Steps of the MVB/ESCRT Pathway. Molecular and Cellular Biology, 25(21), 9478-9490. doi:10.1128/mcb.25.21.9478-9490.2005 es_ES
dc.description.references Herrador, A., Herranz, S., Lara, D., & Vincent, O. (2009). Recruitment of the ESCRT Machinery to a Putative Seven-Transmembrane-Domain Receptor Is Mediated by an Arrestin-Related Protein. Molecular and Cellular Biology, 30(4), 897-907. doi:10.1128/mcb.00132-09 es_ES
dc.description.references Herranz, S., Rodriguez, J. M., Bussink, H.-J., Sanchez-Ferrero, J. C., Arst, H. N., Penalva, M. A., & Vincent, O. (2005). Arrestin-related proteins mediate pH signaling in fungi. Proceedings of the National Academy of Sciences, 102(34), 12141-12146. doi:10.1073/pnas.0504776102 es_ES
dc.description.references Horák, J. (2003). The role of ubiquitin in down-regulation and intracellular sorting of membrane proteins: insights from yeast. Biochimica et Biophysica Acta (BBA) - Biomembranes, 1614(2), 139-155. doi:10.1016/s0005-2736(03)00195-0 es_ES
dc.description.references Ito, T., Chiba, T., Ozawa, R., Yoshida, M., Hattori, M., & Sakaki, Y. (2001). A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proceedings of the National Academy of Sciences, 98(8), 4569-4574. doi:10.1073/pnas.061034498 es_ES
dc.description.references Lamb, T. M., & Mitchell, A. P. (2003). The Transcription Factor Rim101p Governs Ion Tolerance and Cell Differentiation by Direct Repression of the Regulatory Genes NRG1 and SMP1 in Saccharomyces cerevisiae. Molecular and Cellular Biology, 23(2), 677-686. doi:10.1128/mcb.23.2.677-686.2003 es_ES
dc.description.references Lamb, T. M., Xu, W., Diamond, A., & Mitchell, A. P. (2000). Alkaline Response Genes ofSaccharomyces cerevisiaeand Their Relationship to theRIM101Pathway. Journal of Biological Chemistry, 276(3), 1850-1856. doi:10.1074/jbc.m008381200 es_ES
dc.description.references Lauwers, E., Erpapazoglou, Z., Haguenauer-Tsapis, R., & André, B. (2010). The ubiquitin code of yeast permease trafficking. Trends in Cell Biology, 20(4), 196-204. doi:10.1016/j.tcb.2010.01.004 es_ES
dc.description.references Léon, S., & Haguenauer-Tsapis, R. (2009). Ubiquitin ligase adaptors: Regulators of ubiquitylation and endocytosis of plasma membrane proteins. Experimental Cell Research, 315(9), 1574-1583. doi:10.1016/j.yexcr.2008.11.014 es_ES
dc.description.references Liu, Y. (2006). Quality control of a mutant plasma membrane ATPase: ubiquitylation prevents cell-surface stability. Journal of Cell Science, 119(2), 360-369. doi:10.1242/jcs.02749 es_ES
dc.description.references Longtine, M. S., Mckenzie III, A., Demarini, D. J., Shah, N. G., Wach, A., Brachat, A., … Pringle, J. R. (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast, 14(10), 953-961. doi:10.1002/(sici)1097-0061(199807)14:10<953::aid-yea293>3.0.co;2-u es_ES
dc.description.references MacGurn, J. A., Hsu, P.-C., & Emr, S. D. (2012). Ubiquitin and Membrane Protein Turnover: From Cradle to Grave. Annual Review of Biochemistry, 81(1), 231-259. doi:10.1146/annurev-biochem-060210-093619 es_ES
dc.description.references Maeda, T. (2012). The signaling mechanism of ambient pH sensing and adaptation in yeast and fungi. FEBS Journal, 279(8), 1407-1413. doi:10.1111/j.1742-4658.2012.08548.x es_ES
dc.description.references Märquez, J., & Serrano, R. (1996). Multiple transduction pathways regulate the sodium-extrusion gene PMR2/ENA1 during salt stress in yeast. FEBS Letters, 382(1-2), 89-92. doi:10.1016/0014-5793(96)00157-3 es_ES
dc.description.references Mulet, J. M., Leube, M. P., Kron, S. J., Rios, G., Fink, G. R., & Serrano, R. (1999). A Novel Mechanism of Ion Homeostasis and Salt Tolerance in Yeast: the Hal4 and Hal5 Protein Kinases Modulate the Trk1-Trk2 Potassium Transporter. Molecular and Cellular Biology, 19(5), 3328-3337. doi:10.1128/mcb.19.5.3328 es_ES
dc.description.references Mulet, J. M., Llopis-Torregrosa, V., Primo, C., Marqués, M. C., & Yenush, L. (2013). Endocytic regulation of alkali metal transport proteins in mammals, yeast and plants. Current Genetics, 59(4), 207-230. doi:10.1007/s00294-013-0401-2 es_ES
dc.description.references Obara, K., & Kihara, A. (2014). Signaling Events of the Rim101 Pathway Occur at the Plasma Membrane in a Ubiquitination-Dependent Manner. Molecular and Cellular Biology, 34(18), 3525-3534. doi:10.1128/mcb.00408-14 es_ES
dc.description.references Perez-Valle, J., Jenkins, H., Merchan, S., Montiel, V., Ramos, J., Sharma, S., … Yenush, L. (2007). Key Role for Intracellular K+ and Protein Kinases Sat4/Hal4 and Hal5 in the Plasma Membrane Stabilization of Yeast Nutrient Transporters. Molecular and Cellular Biology, 27(16), 5725-5736. doi:10.1128/mcb.01375-06 es_ES
dc.description.references Pérez-Valle, J., Rothe, J., Primo, C., Martínez Pastor, M., Ariño, J., Pascual-Ahuir, A., … Yenush, L. (2010). Hal4 and Hal5 Protein Kinases Are Required for General Control of Carbon and Nitrogen Uptake and Metabolism. Eukaryotic Cell, 9(12), 1881-1890. doi:10.1128/ec.00184-10 es_ES
dc.description.references Platara, M., Ruiz, A., Serrano, R., Palomino, A., Moreno, F., & Ariño, J. (2006). The Transcriptional Response of the Yeast Na+-ATPaseENA1Gene to Alkaline Stress Involves Three Main Signaling Pathways. Journal of Biological Chemistry, 281(48), 36632-36642. doi:10.1074/jbc.m606483200 es_ES
dc.description.references Proft, M., & Serrano, R. (1999). Repressors and Upstream Repressing Sequences of the Stress-RegulatedENA1Gene inSaccharomyces cerevisiae: bZIP Protein Sko1p Confers HOG-Dependent Osmotic Regulation. Molecular and Cellular Biology, 19(1), 537-546. doi:10.1128/mcb.19.1.537 es_ES
dc.description.references Rienzo, A., Pascual-Ahuir, A., & Proft, M. (2012). The use of a real-time luciferase assay to quantify gene expression dynamics in the living yeast cell. Yeast, 29(6), 219-231. doi:10.1002/yea.2905 es_ES
dc.description.references Rotin, D., & Staub, O. (2010). Role of the ubiquitin system in regulating ion transport. Pflügers Archiv - European Journal of Physiology, 461(1), 1-21. doi:10.1007/s00424-010-0893-2 es_ES
dc.description.references Ruiz, A., & Ariño, J. (2007). Function and Regulation of theSaccharomyces cerevisiae ENASodium ATPase System. Eukaryotic Cell, 6(12), 2175-2183. doi:10.1128/ec.00337-07 es_ES
dc.description.references Schild, L., Lu, Y., Gautschi, I., Schneeberger, E., Lifton, R. P., & Rossier, B. C. (1996). Identification of a PY motif in the epithelial Na channel subunits as a target sequence for mutations causing channel activation found in Liddle syndrome. The EMBO Journal, 15(10), 2381-2387. doi:10.1002/j.1460-2075.1996.tb00594.x es_ES
dc.description.references Serrano, R., Ruiz, A., Bernal, D., Chambers, J. R., & Ariño, J. (2002). The transcriptional response to alkaline pH in Saccharomyces cerevisiae: evidence for calcium-mediated signalling. Molecular Microbiology, 46(5), 1319-1333. doi:10.1046/j.1365-2958.2002.03246.x es_ES
dc.description.references Staub, O., Dho, S., Henry, P., Correa, J., Ishikawa, T., McGlade, J., & Rotin, D. (1996). WW domains of Nedd4 bind to the proline-rich PY motifs in the epithelial Na+ channel deleted in Liddle’s syndrome. The EMBO Journal, 15(10), 2371-2380. doi:10.1002/j.1460-2075.1996.tb00593.x es_ES
dc.description.references Subramanian, S., Woolford, C. A., Desai, J. V., Lanni, F., & Mitchell, A. P. (2012). cis - and trans -Acting Localization Determinants of pH Response Regulator Rim13 in Saccharomyces cerevisiae. Eukaryotic Cell, 11(10), 1201-1209. doi:10.1128/ec.00158-12 es_ES
dc.description.references Tréton, B., Blanchin-Roland, S., Lambert, M., Lépingle, A., & Gaillardin, C. (2000). Ambient pH signalling in ascomycetous yeasts involves homologues of the Aspergillus nidulans genes palF and palH. Molecular and General Genetics MGG, 263(3), 505-513. doi:10.1007/s004380051195 es_ES
dc.description.references Vidan, S., & Mitchell, A. P. (1997). Stimulation of yeast meiotic gene expression by the glucose-repressible protein kinase Rim15p. Molecular and Cellular Biology, 17(5), 2688-2697. doi:10.1128/mcb.17.5.2688 es_ES
dc.description.references Wadskog, I., Forsmark, A., Rossi, G., Konopka, C., Öyen, M., Goksör, M., … Adler, L. (2006). The Yeast Tumor Suppressor Homologue Sro7p Is Required for Targeting of the Sodium Pumping ATPase to the Cell Surface. Molecular Biology of the Cell, 17(12), 4988-5003. doi:10.1091/mbc.e05-08-0798 es_ES
dc.description.references Wang, G., Yang, J., & Huibregtse, J. M. (1999). Functional Domains of the Rsp5 Ubiquitin-Protein Ligase. Molecular and Cellular Biology, 19(1), 342-352. doi:10.1128/mcb.19.1.342 es_ES
dc.description.references Xu, W., & Mitchell, A. P. (2001). Yeast PalA/AIP1/Alix Homolog Rim20p Associates with a PEST-Like Region and Is Required for Its Proteolytic Cleavage. Journal of Bacteriology, 183(23), 6917-6923. doi:10.1128/jb.183.23.6917-6923.2001 es_ES
dc.description.references Xu, W., Smith, F. J., Subaran, R., & Mitchell, A. P. (2004). Multivesicular Body-ESCRT Components Function in pH Response Regulation in Saccharomyces cerevisiae and Candida albicans. Molecular Biology of the Cell, 15(12), 5528-5537. doi:10.1091/mbc.e04-08-0666 es_ES
dc.description.references Yang, B., & Kumar, S. (2009). Nedd4 and Nedd4-2: closely related ubiquitin-protein ligases with distinct physiological functions. Cell Death & Differentiation, 17(1), 68-77. doi:10.1038/cdd.2009.84 es_ES
dc.description.references Yoshikawa, K., Tanaka, T., Furusawa, C., Nagahisa, K., Hirasawa, T., & Shimizu, H. (2009). Comprehensive phenotypic analysis for identification of genes affecting growth under ethanol stress inSaccharomyces cerevisiae. FEMS Yeast Research, 9(1), 32-44. doi:10.1111/j.1567-1364.2008.00456.x es_ES
dc.description.references Zahrádka, J., & Sychrová, H. (2012). Plasma-membrane hyperpolarization diminishes the cation efflux via Nha1 antiporter and Ena ATPase under potassium-limiting conditions. FEMS Yeast Research, 12(4), 439-446. doi:10.1111/j.1567-1364.2012.00793.x es_ES
dc.description.references Zhao, J., Lin, W., Ma, X., Lu, Q., Ma, X., Bian, G., & Jiang, L. (2010). The protein kinase Hal5p is the high-copy suppressor of lithium-sensitive mutations of genes involved in the sporulation and meiosis as well as the ergosterol biosynthesis in Saccharomyces cerevisiae. Genomics, 95(5), 290-298. doi:10.1016/j.ygeno.2010.02.010 es_ES


Este ítem aparece en la(s) siguiente(s) colección(ones)

Mostrar el registro sencillo del ítem