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Gene Review

ENA1  -  Na(+)/Li(+)-exporting P-type ATPase ENA1

Saccharomyces cerevisiae S288c

Synonyms: HOR6, PMR2, PMR2A, Sodium transport ATPase 1, YD6888.02C, ...
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Disease relevance of ENA1

  • As expected, the disruption of the PPZ genes did not complement the characteristic hypersensitivity for Na+ and Li+ of a ena1 delta strain [1].

High impact information on ENA1

  • The genes for two new P-type ATPases, PMR1 and PMR2, have been identified in yeast [2].
  • In yeast, a transcription repressor, Sko1, mediates regulation of the sodium-pump ENA1 gene by the Hog1 MAP kinase [3].
  • In addition, we found that the calcineurin-dependent transcriptional regulation of PMR2 and PMC1 required CRZ1 [4].
  • However, transcription of PMR2 and PMC1 was activated by only a subset of the treatments that activated FKS2 transcription [4].
  • Interestingly, RPD3 deacetylates the ENA1 coding region, and both deacetylases contribute to ENA1 repression [5].

Biological context of ENA1


Anatomical context of ENA1

  • This can be explained by the fact that expression of the ENA1 gene, which encodes the major component of the efflux system for these cations, is strongly increased in ppz1 delta ppz2 delta cells [1].
  • Na+ tolerance in S. cerevisiae is mediated primarily by transcriptional induction of ENA1, which encodes the plasma membrane sodium pump, and by conversion of the potassium uptake system to a higher affinity form that discriminates more efficiently against Na+ [10].
  • The role of the intracellular membranes structures produced with the overexpression of ENA1 in Na+ and Li+ tolerances and the existence of a beta-subunit of the ENA1 ATPase are discussed [11].

Associations of ENA1 with chemical compounds

  • One important mechanism of ENA1 transcriptional regulation is based on repression under normal growth conditions, which is relieved by either osmotic induction or glucose starvation [12].
  • A glutathione S-transferase-Sko1 fusion protein binds specifically to the URSCRE-ENA1 element [12].
  • Here we show that transcription of ENA1, a gene encoding a lithium and sodium ion transporter essential for salt tolerance in yeast, is controlled by the TOR signaling pathway [13].
  • Overexpression of the GPD1 gene encoding glycerol-3-phosphate dehydrogenase, ENA1 encoding sodium ion efflux protein, and CUP1 encoding copper metallothionein conferred high salt stress tolerance to yeast cells, and our selection of candidate genes for the creation of stress-tolerant yeast strains based on the transcriptome data was validated [14].
  • NaCl-induced ENA1 expression was inhibited by EGTA, cch1Delta mutation, and FK506, indicating that the [Ca(2+)](cyt) transient activates calcineurin signaling to mediate ion homeostasis and salt tolerance [15].

Regulatory relationships of ENA1

  • Furthermore, a hog1 mitogen-activated protein kinase deletion strain could not counteract repression on URSCRE-ENA1 during osmotic shock [12].
  • We have investigated the molecular mechanisms involved in ENA1 induction by the calcium-calcineurin-activated transcription factor Crzl/Tcn1 [16].
  • These results indicate that Ptc1p modulates the function of Ena1p by regulating the Hal3/Ppz1,2 pathway [17].
  • Itis suggested that ISC1-dependent hydrolysis of an unidentified yeast inositol phosphosphingolipid represents an early event in one of the salt-induced signalling pathways of ENA1 transcriptional activation [9].
  • Finally, we show that the Na+ tolerance mediated through these pumps is regulated by calmodulin via a calcineurin-independent mechanism which activates the Pmr2 ion pumps post-transcriptionally [18].

Other interactions of ENA1

  • Repressors and upstream repressing sequences of the stress-regulated ENA1 gene in Saccharomyces cerevisiae: bZIP protein Sko1p confers HOG-dependent osmotic regulation [12].
  • Analysis of the ENA1 promoter revealed a Mig1p-binding motif (-533 to -544) which was characterized as an upstream repressing sequence (URSMIG-ENA1) regulated by carbon source [12].
  • Fourth, TOR1, similar to ENA1, is required for growth under saline stress conditions [13].
  • These results show that SIT4 acts in a parallel pathway not involving induction of transcription of ENA1 and suggest a novel function for SIT4 in response to salt stress [19].
  • Second, the absence of the TOR-controlled GATA transcription factors GLN3 and GAT1 results in reduced basal and salt-induced expression of ENA1 [13].

Analytical, diagnostic and therapeutic context of ENA1


  1. The PPZ protein phosphatases are important determinants of salt tolerance in yeast cells. Posas, F., Camps, M., Ariño, J. J. Biol. Chem. (1995) [Pubmed]
  2. The yeast secretory pathway is perturbed by mutations in PMR1, a member of a Ca2+ ATPase family. Rudolph, H.K., Antebi, A., Fink, G.R., Buckley, C.M., Dorman, T.E., LeVitre, J., Davidow, L.S., Mao, J.I., Moir, D.T. Cell (1989) [Pubmed]
  3. Ion homeostasis during salt stress in plants. Serrano, R., Rodriguez-Navarro, A. Curr. Opin. Cell Biol. (2001) [Pubmed]
  4. Calcineurin acts through the CRZ1/TCN1-encoded transcription factor to regulate gene expression in yeast. Stathopoulos, A.M., Cyert, M.S. Genes Dev. (1997) [Pubmed]
  5. TUP1 utilizes histone H3/H2B-specific HDA1 deacetylase to repress gene activity in yeast. Wu, J., Suka, N., Carlson, M., Grunstein, M. Mol. Cell (2001) [Pubmed]
  6. Glucose repression affects ion homeostasis in yeast through the regulation of the stress-activated ENA1 gene. Alepuz, P.M., Cunningham, K.W., Estruch, F. Mol. Microbiol. (1997) [Pubmed]
  7. Yeast putative transcription factors involved in salt tolerance. Mendizabal, I., Rios, G., Mulet, J.M., Serrano, R., de Larrinoa, I.F. FEBS Lett. (1998) [Pubmed]
  8. ARL1 participates with ATC1/LIC4 to regulate responses of yeast cells to ions. Munson, A.M., Love, S.L., Shu, J., Palanivel, V.R., Rosenwald, A.G. Biochem. Biophys. Res. Commun. (2004) [Pubmed]
  9. ISC1-encoded inositol phosphosphingolipid phospholipase C is involved in Na+/Li+ halotolerance of Saccharomyces cerevisiae. Betz, C., Zajonc, D., Moll, M., Schweizer, E. Eur. J. Biochem. (2002) [Pubmed]
  10. Transcriptional regulation of the S. cerevisiae ENA1 gene by casein kinase II. Tenney, K.A., Glover, C.V. Mol. Cell. Biochem. (1999) [Pubmed]
  11. Overexpression of the sodium ATPase of Saccharomyces cerevisiae: conditions for phosphorylation from ATP and Pi. Benito, B., Quintero, F.J., Rodríguez-Navarro, A. Biochim. Biophys. Acta (1997) [Pubmed]
  12. Repressors and upstream repressing sequences of the stress-regulated ENA1 gene in Saccharomyces cerevisiae: bZIP protein Sko1p confers HOG-dependent osmotic regulation. Proft, M., Serrano, R. Mol. Cell. Biol. (1999) [Pubmed]
  13. The GATA transcription factors GLN3 and GAT1 link TOR to salt stress in Saccharomyces cerevisiae. Crespo, J.L., Daicho, K., Ushimaru, T., Hall, M.N. J. Biol. Chem. (2001) [Pubmed]
  14. Comparative analysis of transcriptional responses to saline stress in the laboratory and brewing strains of Saccharomyces cerevisiae with DNA microarray. Hirasawa, T., Nakakura, Y., Yoshikawa, K., Ashitani, K., Nagahisa, K., Furusawa, C., Katakura, Y., Shimizu, H., Shioya, S. Appl. Microbiol. Biotechnol. (2006) [Pubmed]
  15. An osmotically induced cytosolic Ca2+ transient activates calcineurin signaling to mediate ion homeostasis and salt tolerance of Saccharomyces cerevisiae. Matsumoto, T.K., Ellsmore, A.J., Cessna, S.G., Low, P.S., Pardo, J.M., Bressan, R.A., Hasegawa, P.M. J. Biol. Chem. (2002) [Pubmed]
  16. Promoter sequences regulated by the calcineurin-activated transcription factor Crz1 in the yeast ENA1 gene. Mendizabal, I., Pascual-Ahuir, A., Serrano, R., de Larrinoa, I.F. Mol. Genet. Genomics (2001) [Pubmed]
  17. Role of protein phosphatases 2C on tolerance to lithium toxicity in the yeast Saccharomyces cerevisiae. Ruiz, A., González, A., García-Salcedo, R., Ramos, J., Ariño, J. Mol. Microbiol. (2006) [Pubmed]
  18. The PMR2 gene cluster encodes functionally distinct isoforms of a putative Na+ pump in the yeast plasma membrane. Wieland, J., Nitsche, A.M., Strayle, J., Steiner, H., Rudolph, H.K. EMBO J. (1995) [Pubmed]
  19. Regulation of monovalent ion homeostasis and pH by the Ser-Thr protein phosphatase SIT4 in Saccharomyces cerevisiae. Masuda, C.A., Ramírez, J., Peña, A., Montero-Lomelí, M. J. Biol. Chem. (2000) [Pubmed]
  20. Validation of a flour-free model dough system for throughput studies of baker's yeast. Panadero, J., Randez-Gil, F., Prieto, J.A. Appl. Environ. Microbiol. (2005) [Pubmed]
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