Skip to main content
SpringerLink
Log in

Modeling of three-dimensional structure of the H+-dependent phosphate transporter of cytoplasmic membrane from the yeast Yarrowia lipolytica

  • Articles
  • Published:
Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology Aims and scope

Abstract

Information concerning phosphate transport systems in yeasts (specifically in Saccharomyces cerevisiae), their regulation on transcriptional and post-translational levels has been summarized. There are proofs that S. cerevisiae growing only at low pH levels cannot serve a model organism for research studies of Na+-dependent phosphate transport systems that exhibit maximum activity in alkaline media. We propose the Yarrowia lipolytica yeast as an alternative organism for such studies as it can grow at high pH values (up to 9.7) in the presence of 12% NaCl, which suggests the existence of unique systems for maintaining cell homeostasis. As far as the Y. lipolytica genome has been recently sequenced, it became possible to analyze these systems through bioinformatics approaches. A sequence of H+-dependent phosphate transporter with the same function as that of the PHO84 gene product in S. cerevisiae genome was found. Based on the sequence homology with glycerol-3-phosphate transporter from E. coli, the model of three-dimensional structure of H+-dependent phosphate transporter from Y. lipolytica (from 38 to 545 residue) was constructed, analyzed, optimized, and compared with the known models. The quality of the constructed model is better than the accepted models of the H+-dependent phosphate transporter of cytoplasmic membrane from yeast Y. lipolytica.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Persson B.L., Lagerstedt J.O., Pratt J.R., Pattison-Granberg J., Lundh K., Shokrollahzadeh S., Lundh F. 2003. Regulation of phosphate acquisition in Saccharomyces cerevisiae. Curr. Genet. 43, 225–244.

    Article  PubMed  CAS  Google Scholar 

  2. Zvyagilskaya R.A., Persson B.L. 2004. A novel alkalitolerant Yarrowia lipolytica strain is a perspective model forstudy of properties and regulation of yeast Na+-dependent phosphate transporters. Biochimiya (Rus.). 69, 1613–1621.

    Google Scholar 

  3. Zvyagilskaya R.A., Persson B.L. 2005. A novel alkalitolerant Yarrowia lipolytica strain for dissecting Na+-coupled phosphate transport systems (Mini-review). Cell Biol. Intern. 29, 87–94.

    Article  CAS  Google Scholar 

  4. Zvyagilskaya R.A., Lundh F.L., Samyn D., Pattison-Granberg J., Mouillon J.-M., Popova Y., Thevelein J.M., Persson B.L. 2008. Characterization of the Pho89 phosphate transporter by functional hyperexpression in Saccharomyces cerevisiae. FEMS Yeast Res. 8, 685–696.

    Article  PubMed  CAS  Google Scholar 

  5. Lundh F., Mouillon J.M., Samyn D., Stadler K., Popova Y., Lagerstedt J.O., Thevelein J.M., Persson B.L. 2009. Molecular mechanisms controlling phosphate-induced downregulation of the yeast Pho84 phosphate transporter. Biochemistry. 48, 4497–4505.

    Article  PubMed  CAS  Google Scholar 

  6. Mouillon J.M., Persson B.L. 2006. New aspects on phosphate sensing and signalling in Saccharomyces cerevisiae. FEMS Yeast Res. 6, 171–176.

    Article  PubMed  CAS  Google Scholar 

  7. Giots F., Donaton M.C., Thevelein J.M. 2003. Inorganic phosphate is sensed by specific phosphate carriers and acts in concert with glucose as a nutrient signal for activation of the protein kinase A pathway in the yeast Saccharomyces cerevisiae. Mol. Microbiol. 47, 1163–1181.

    Article  PubMed  CAS  Google Scholar 

  8. Holsbeeks I., Lagatie O., Van Nuland A., Van de Velde S., Thevelein J.M. 2004. The eukaryotic plasma membrane as a nutrient-sensing device. Trends Biochem. Sci. 29, 556–564.

    Article  PubMed  CAS  Google Scholar 

  9. Thevelein J.M., Gelad R., Holsbeeks I., Lagatie O., Popova Y., Rolland F., Stolz F., Van de Velde S., Van Dijck P., Vandormael P., Van Nuland A., Van Roey K., Van Zeebroeck G., Yan B. 2005. Nutrient sensing systems for rapid activation of the protein kinase A pathway in yeast. Biochem. Soc. Trans. 33, 253–256.

    Article  PubMed  CAS  Google Scholar 

  10. Toh-e A., Tanaka K., Uesono Y., Wickner R.B. 1988. PHO85, a negative regulator of the PHO system, is a homolog of the protein kinase gene, CDC28, of Saccharomyces cerevisiae. Mol. Gen. Genet. 214, 162–164.

    Article  PubMed  CAS  Google Scholar 

  11. Auesukaree C., Homma T., Kaneko Y., Harashima S. 2003. Transcriptional regulation of phosphate-responsive genes in low-affinity phosphate-transporter-defective mutants in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 306, 843–850.

    Article  PubMed  CAS  Google Scholar 

  12. Hürlimann H.C., Stadler-Waibel M., Werner T.P., Freimoser F.M. 2007. Pho91 is a vacuolar phosphate transporter that regulates phosphate and polyphosphate metabolism in Saccharomyces cerevisiae. Mol. Biol. Cell. 18, 4438–4445.

    Article  PubMed  Google Scholar 

  13. Wykoff D.D., Rizvi A.H., Raser J.M., Margolin B., O’shea E.K. 2007. Positive feedback regulates switching of phosphate transporters in S. cerevisiae. Mol. Cell. 27, 1005–1013.

    Article  PubMed  CAS  Google Scholar 

  14. Martinez P., Persson B.L. 1998. Identification, cloning and characterization of a derepressible Na+-coupled phosphate transporter in Saccharomyces cerevisiae. Mol. Gen. Genet. 258, 628–638.

    Article  PubMed  CAS  Google Scholar 

  15. Pattison-Granberg J., Persson B.L. 2000. Regulation of cation-coupled high-affinity phosphate uptake in the yeast Saccharomyces cerevisiae. J. Bacteriol. 182, 5017–5019.

    Article  PubMed  CAS  Google Scholar 

  16. Vogel K., Hörz W., Hinnen A. 1989. The two positively acting regulatory proteins PHO2 and PHO4 physically interact with PHO5 upstream activation regions. Mol. Cell. Biol. 99, 2050–2057.

    PubMed  CAS  Google Scholar 

  17. Kaffman A., Herskowitz I., Tjian R., O’shea E.K. 1994. Phosphorylation of the transcription factor PHO4 by a cyclin-CDK complex, PHO80-PHO85. Science. 263, 1153–1156.

    Article  PubMed  CAS  Google Scholar 

  18. Lau W.T., Howson R.W., Malkus P., Schekman R., O’shea E.K. 2000. Pho86p, an endoplasmic reticulum (ER) resident protein in Saccharomyces cerevisiae, is required for ER exit of the high-affinity phosphate transporter Pho84p. Proc. Natl. Acad. Sci. USA. 97, 1107–1112.

    Article  PubMed  CAS  Google Scholar 

  19. Lagerstedt J.O., Zvygilskaya R.A., Pratt J.R., Pattison-Granberg J., Kruckeberg A.L., Berden J.A., Persson B.L. 2002. Mutagenic and functional analysis of the C-terminus of the Saccharomyces cerevisiae Pho84 phosphate transporter. FEBS Lett. 526, 31–37.

    Article  PubMed  CAS  Google Scholar 

  20. Pratt J.R., Mouillon J.M., Lagerstedt J.O., Pattison-Granberg J., Lundh K.I., Persson B.L. 2004. Effects of methylphosphonate, a phosphate analogue, on the expression and degradation of the high-affinity phosphate transporter Pho84, in Saccharomyces cerevisiae. Biochemistry. 43, 14444–14453.

    Article  PubMed  CAS  Google Scholar 

  21. Petersson J., Pattison J., Kruckeberg A.L., Berden J.A., Persson B.L. 1999. Intracellular localization of an active green fluorescent protein-tagged Pho84 phosphate permease in Saccharomyces cerevisiae. FEBS Lett. 462, 37–42.

    Article  PubMed  CAS  Google Scholar 

  22. Lagerstedt J.O., Voss J.C., Wieslander A., Persson B.L. 2004. Structural modeling of dual-affinity purified Pho84 phosphate transporter. FEBS Lett. 578, 262–268.

    Article  PubMed  CAS  Google Scholar 

  23. Hicke L., Zanolari B., Riezman H. 1988. Cytoplasmic tail phosphorylation of the α-factor receptor is required for its ubiquitination and internalization. J. Cell Biol. 1141, 349–358.

    Article  Google Scholar 

  24. Estrella L.A., Krishnamurthy S., Timme C.R., Hamp-sey M. 2008. The Rsp5 E3 ligase mediates turnover of low affinity phosphate transporters in Saccharomyces cerevisiae. J. Biol. Chem. 283, 5327–5334.

    Article  PubMed  CAS  Google Scholar 

  25. Saier M.H.,Jr. 2000. A functional-phylogenetic classification system for transmembrane solute transporters. Microbiol. Mol. Biol. Rev. 64, 354–411.

    Article  PubMed  CAS  Google Scholar 

  26. Werner A., Kinne R.K.H. 2001. Evolution of the Na-Pi cotransport systems. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280, 301–312.

    Google Scholar 

  27. Collins J.F., Bai L., Ghishan F.K. 2004. The SLC20 family of proteins: dual functions as sodium-phosphate cotransporters and viral receptors. Pflugers Arch. 447, 647–652.

    Article  PubMed  CAS  Google Scholar 

  28. Bottger P., Pedersen L. 2002. Two highly conserved glutamate residues critical for type III sodium-dependent phosphate transport revealed by uncoupling transport function from retroviral receptor function. J. Biol. Chem. 277, 42741–42747.

    Article  PubMed  CAS  Google Scholar 

  29. Bottger P., Hede S.E., Grunnert M., Hoyer B., Klaerke D.A., Pedersen L. 2006. Characterization of transport mechanisms and determinants critical for Na+-dependent Pi symport of the PiT family paralogs human PiT1 and PiT2. Am. J. Physiol. Cell Physiol. 291, 1377–1387.

    Article  Google Scholar 

  30. Garcia R., Bermejo C., Grau C., Perez R., Rodriguez-Pena J.M., Francois J., Nombela C., Arroyo J. 2004. The global transcriptional response to transient cell wall damage in Saccharomyces cerevisiae and its regulation by the cell integrity signaling pathway. J. Biol. Chem. 279, 15183–15195.

    Article  PubMed  CAS  Google Scholar 

  31. Viladevall L., Serrano R., Ruiz A., Domenech G., Giraldo J., Barcelo A., Arino J. 2004. Characterization of the calcium-mediated response to alkaline stress in Saccharomyces cerevisiae. J. Biol. Chem. 279, 43614–43624.

    Article  PubMed  CAS  Google Scholar 

  32. Wiesenberger G., Steinleitner K., Malli R., Graier W.F., Vormann J., Schweyen R. J., Stadler J.A. 2007. Mg2+ deprivation elicits rapid Ca2+ uptake and activates Ca2+/calcineurin signaling in Saccharomyces cerevisiae. Eukaryot. Cell. 6, 592–599.

    Article  PubMed  CAS  Google Scholar 

  33. Serrano R., Ruiz A., Bernal D., Chambers J.R., Arino J. 2002. The transcriptional response to alkaline pH in Saccharomyces cerevisiae: Evidence for calcium-mediated signaling. Mol. Microbiol. 46, 1319–1333.

    Article  PubMed  CAS  Google Scholar 

  34. Yoshimoto H., Saltsman K., Gasch A.P., Li H.X., Ogawa N., Botstein D., Brown P. O., Cyert M.S. 2002. Genome-wide analysis of gene expression regulated by the calcineurin/Crz1p signaling pathway in Saccharomyces cerevisiae. J. Biol. Chem. 277, 31079–31088.

    Article  PubMed  CAS  Google Scholar 

  35. Andreicheva E.N., Isakova E.P., Sidorov N.N., Abramova N.B., Ushakova N.A., Soares M.I.M., Zvyagilskaya R.A. 1999. Adaptation to salt stress in a salttolerantstrain of the yeast Yarrowia lipolytica. Biochimiya (Rus.). 64, 109–116.

    Google Scholar 

  36. Zvyagilskaya R.A., Andreishcheva E., Soares I.M.I., Khozin I., Berhe A., Persson B.L. 2001. Isolation and characterization of a novel leaf-inhabiting osmo-, salt, and alkali-tolerant Yarrowia lipolytica strain. J. Basic Microbiol. 41, 283–303.

    Article  Google Scholar 

  37. Kerscher S., Kashani-Poor N., Zwicker K., Zicker-mann V., Brandt U. 2001. Exploring the catalytic core of complex I by Yarrowia lipolytica yeast genetics. J. Bioenerg. Biomembr. 33, 187–196.

    Article  PubMed  CAS  Google Scholar 

  38. Zvyagilskaya R.A., Parchomenko O.A., Persson B.L. 2000. Two systems for phosphate uptake in Yarrowia lipolytica cells grown under alkaline conditions. IUBMB Life. 50, 151–155.

    PubMed  CAS  Google Scholar 

  39. Zvyagilskaya R.A., Allard P., Persson B.L. 2000. Two systems for phosphate uptake in Yarrowia lipolytica cells grown at acidic conditions. IUBMB Life. 49, 143–147.

    Article  PubMed  CAS  Google Scholar 

  40. Zvyagilskaya R.A., Parchomenko O., Abramova N., Allard P., Panaretakis T., Pattison-Granberg J., Persson B.L. 2001. Proton- and sodium-coupled phosphate transport systems and energy status of Yarrowia lipolytica cells grown at acidic and alkaline growth conditions. J. Membr. Biol. 183, 39–50.

    Article  PubMed  CAS  Google Scholar 

  41. Zvyagilskaya R., Persson B.L. 2003. Dual regulation of proton- and sodium-coupled phosphate transport systems in the Yarrowia lipolytica yeast by extracellular phosphate and pH. IUBMB Life. 55, 151–154.

    Article  PubMed  CAS  Google Scholar 

  42. Kosinsky U.A., Pyrkov T.V., Lutsenko S.V., Efremov R.G. 2006. The protein-ligand complex structure prediction: from computer model to biological function. Ros. khim. zhurnal (Rus.). 50, 36–44.

    Google Scholar 

  43. Chugunov A.O., Efremov R.G. 2009. Protein spatial structure prediction: accent on membrane targets. Bioorganich. khimiya (Rus.). 35, 744–760.

    CAS  Google Scholar 

  44. Liu S., Zhang C., Liang S., Zhou Y. 2007. Fold recognition by concurrent use of solvent accessibility and residue depth. Proteins. 68, 636–645.

    Article  PubMed  CAS  Google Scholar 

  45. Yunfang R., Hong Q., Jiannan F., Song L., Beifen S. 2000. Active regions’ setting of the extracellular ligandbinding domain of human interleukin-6 receptor. Chinese Sci. Bulletin. 45, 1182–1187.

    Article  Google Scholar 

  46. Klyshko E.V., Il’ina A.P., Lichatskaya G.N., Isaeva M.P., Guzev K.V., Monastyrnaya M.M., Kozlovskaya E.P., Lipkin A.V., Barsova E.I., Kryzgko I.B., Trifonov E.V., Nurminsky E.A. 2004. Actinoporins: structure and function. Vestnik DVO RAN (Rus.). 3, 45–53.

    Google Scholar 

  47. Kelley L.A., Sternberg M. 2009. Protein structure prediction on the Web: A case study using the Phyre server. Nat. Protocols. 4, 363–371.

    Article  CAS  Google Scholar 

  48. van der Spoel D., Lindahl E., Hess B., van Buuren A.R., Apol E., Meulenhoff P.J., Tieleman D.P., Sijbers A.L.T.M., Feenstra K.A., van Drunen R., Berendsen H.J.C. 2005. Gromacs User Manual, Version 3.3. http://www.gromacs. org.

  49. Stern A., Doron-Faigenboim A., Erez E., Martz E., Bacharach E., Pupko T. 2007. Selection 2007: Advanced models for detecting positive and purifying selection using a Bayesian inference approach. Nucl. Acids Res. 35, 506–511.

    Article  Google Scholar 

  50. Laskoswki R.A., MacArthur M.W., Moss D.S., Thorton J.M. 1993. PROCHECK: A program to check the stereochemical quality of protein structures. J. Appl. Cryst. 26, 283–291.

    Article  Google Scholar 

  51. Luthy R., Bowie J.U., Eisenberg D. 1992. Assessment of protein models with three-dimensional profiles. Nature. 356, 83–85.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Bach Institute of Biochemistry, Russian Academy of Sciences, Leninsky prosp., 33, Moscow, 119071, Russia

    A. G. Rogov, L. I. Uralsky, L. A. Uralskaya & R. A. Zvyagilskaya

Authors
  1. A. G. Rogov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. I. Uralsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. L. A. Uralskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. A. Zvyagilskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. G. Rogov.

Additional information

Original Russian Text © A.G. Rogov, L.I. Uralsky, L.A. Uralskaya, R.A. Zvyagilskaya, 2011, published in Biologicheskie Membrany, 2011, Vol. 28, No. 5, pp. 354–364.

The article was translated by the authors.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rogov, A.G., Uralsky, L.I., Uralskaya, L.A. et al. Modeling of three-dimensional structure of the H+-dependent phosphate transporter of cytoplasmic membrane from the yeast Yarrowia lipolytica . Biochem. Moscow Suppl. Ser. A 5, 324–334 (2011). https://doi.org/10.1134/S1990747811050114

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1990747811050114

Keywords

Search

Navigation