Polyphosphatase PPX1 of Saccharomyces cerevisiae as a Tool for Polyphosphate Assay

Lidiya Lichko, Tatiana Kulakovskaya

Skryabin Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences, Pushchino, Russia.

DOI: 10.4236/aer.2015.34010                

Abstract

The recombinant exopolyphosphatase PPX1 with a specific activity of ~300 U/mg protein was purified from the strain of Saccharomyces cerevisiae with the inactivated PPN1 gene transformed by the expression vector carrying the yeast PPX1 gene. The recombinant PPX1 was similar to the PPX1 of wild strains in its substrate specificity and requirement for cations. PPX1 had the high substrate specificity to polyphosphates. The preparation was suitable for polyphosphate assay in the presence of orthophosphate and nucleoside phosphates not hydrolyzed by PPX1. The yield of the enzyme preparation was 250 assays per 1 g of the biomass. The recombinant PPX1 was successfully used in polyphosphate assay in different yeast species and some foodstuffs.

Keywords

Saccharomyces cerevisiae, PPX1, Polyphosphate, Polyphosphatase, Assay, Food

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Kornberg, A., Rao, N.N. and Ault-Riché, D. (1999) Inorganic Polyphosphate: A Molecule with Many Functions. Annual Review of Biochemistry, 68, 89-125. http://dx.doi.org/10.1146/annurev.biochem.68.1.89
[2]	Kulaev, I.S., Vagabov, V.M. and Kulakovskaya, T.V. (2004) The Biochemistry of Inorganic Polyphosphates. John Wiley and Sons Ltd., Chichester. http://dx.doi.org/10.1002/0470858192
[3]	Rao, N.N., Gómez-García, M.R. and Kornberg, A. (2009) Inorganic Polyphosphate: Essential for Growth and Survival. Annual Review of Biochemistry, 78, 605-647. http://dx.doi.org/10.1146/annurev.biochem.77.083007.093039
[4]	Leyhausen, G., Lorenz, B., Zhu, H., Geurtsen, W., Bohnensack, R., Müller, W.E.G. and Schrüder, H.C. (1998) Inorganic Poly-Phosphate in Human Osteoblast-Like Cells. Journal of Bone and Mineral Metabolism, 13, 803-812. http://dx.doi.org/10.1359/jbmr.1998.13.5.803
[5]	Morimoto, D., Tomita, T., Kuroda, S., Higuchi, C., Rato, S., Shiba, T., Nakagami, H., Morishita, R. and Yoshikawa, H. (2010) In-Organic Polyphosphate Differentiates Human Mesenchymal Stem Cells into Osteoblastic Cells. Journal of Bone and Mineral Metabolism, 28, 418-423. http://dx.doi.org/10.1007/s00774-010-0157-4
[6]	Müller, W.E., Wang, X., Diehl-Seifert, B., Kropf, K., Schloβmacher, U., Lieberwirth, I., Glasser, G., Wiens, M. and Schröder, H.C. (2011) Inorganic Polymeric Phosphate/Polyphosphate as an Inducer of Alkaline Phosphatase and a Modulator of Intracellular Ca(2+) Level in Osteoblasts (SaOS-2 Cells) in Vitro. Acta Biomaterialia, 7, 2661-2671. http://dx.doi.org/10.1016/j.actbio.2011.03.007
[7]	Omelon, S., Georgiou, J., Henneman, Z.J., Wise, L.M., Sukhu, B., Hant, T., Wynnyckyj, S., Holmyard, D., Bielecki, R. and Grynpas, M.D. (2009) Control of Vertebrate Skeletal Mineralization by Polyphosphates. PLoS ONE, 4, e5634 http://dx.doi.org/10.1371/journal.pone.0005634
[8]	Smith, S.A. and Morrissey, J.H. (2008) Polyphosphate as a General Procoagulant Agent. Journal of Thrombosis and Haemostasis, 6, 1750-1756.http://dx.doi.org/10.1111/j.1538-7836.2008.03104.x
[9]	Travers, R.J., Smith, S.A. and Morrissey, J.H. (2015) Polyphosphate, Platelets, and Coagulation. International Journal of Laboratory Hematology, 37, 31-35. http://dx.doi.org/10.1111/ijlh.12349
[10]	Abramov, A.Y., Fraley, C., Diao, C.T., Winkfein, R., Colicos, M.A., Duchen, M.R., French, R.J. and Pavlov, E. (2007) Targeted Polyphosphatase Expression Alters Mitochondrial Metabolism and Inhibits Calcium-Dependent Cell Death. Proceedings of the National Academy of Sciences of the United States of America, 13, 18091-18096. http://dx.doi.org/10.1073/pnas.0708959104
[11]	Müller, W.E., Tolba, E., Feng, Q., Schröder, H.C., Markl, J.S., Kokkinopoulou, M. and Wang, X. (2015) Amorphous Ca2+ Poly-Phosphate Nanoparticles Regulate the ATP Level in Bone-Like SaOS-2 Cells. Journal of Cell Science, 128, 2202-2207. http://dx.doi.org/10.1242/jcs.170605
[12]	Ozeki, N., Hase, N., Yamaguchi, H., Hiyama, T., Kawai, R., Kondo, A., Nakata, K. and Mogi, M. (2015) Polyphosphate Induces Matrix Metalloproteinase-3-Mediated Proliferation of Odontoblast-Like Cells Derived from Induced Pluripotent Stem Cells. Experimental Cell Research, 333, 303-315. http://dx.doi.org/10.1016/j.yexcr.2015.01.007
[13]	Müller, W.E., Tolba, E., Schröder, H.C. and Wang, X. (2015) Polyphosphate: A Morphogenetically Active Implant Material Serving as Metabolic Fuel for Bone Regeneration. Macromolecular Bioscience, 15, 1182-1197. http://dx.doi.org/10.1002/mabi.201500100
[14]	Wu, A.T.H., Aoki, T., Sakoda, M., Ohta, S., Ichimura, S., Ito, T., Ushida, T. and Furukawa, K.S. (2015) Enhancing Osteogenic Differentiation of MC3T3-E1 Cells by Immobilizing Inorganic Polyphosphate onto Hyaluronic Acid Hydrogel. Biomacromolecules, 16, 166-173. http://dx.doi.org/10.1021/bm501356c
[15]	Müller, F. and Renné, T. (2011) Platelet Polyphosphates: The Nexus of Primary and Secondary Hemostasis. Scandinavian Journal of Clinical and Laboratory Investigation, 71, 82-86.
[16]	Travers, R.J., Smith, S.A. and Morrissey, J.H. (2015) Polyphosphate, Platelets, and Coagulation. International Journal of Laboratory Hematology, 37, 31-35. http://dx.doi.org/10.1111/ijlh.12349
[17]	Zhu, S., Travers, R.J., Morrissey, J.H. and Diamond, S.L. (2015) FXIa and Platelet Polyphosphate as Therapeutic Targets during Human Blood Clotting on Collagen/Tissue Factor Surfaces under Flow. Blood, 126, 1494-1502. http://dx.doi.org/10.1182/blood-2015-04-641472
[18]	Kulakovskaya, T.V., Vagabov, V.M. and Kulaev, I.S. (2012) Inorganic Polyphosphate in Industry, Agriculture and Medicine: Modern State and Outlook. Process Biochemistry, 47, 1-10. http://dx.doi.org/10.1016/j.procbio.2011.10.028
[19]	Smith, J. and Hong-Shum, L., Eds. (2003) Food Additives Data Book. Wiley-Blackwell, Oxford. http://dx.doi.org/10.1002/9780470995327
[20]	Gunther IV, N.W., Rajkowski, K.T. and Sommers, C. (2015) Survival after Cryogenic Freezing of Campylobacter Species in Ground Turkey Patties Treated with Polyphosphates. Journal of Food Protection, 78, 419-423. http://dx.doi.org/10.4315/0362-028X.JFP-14-301
[21]	Sekiguchi, Y., Matsunaga, A., Yamamoto, A. and Inoue, Y. (2000) Analysis of Condensed Phosphates in Food Products by Ion Chromatography with an Online Hydroxide Eluent Generator. Journal of Chromatography, 881, 639-644. http://dx.doi.org/10.1016/S0021-9673(99)01278-9
[22]	Kaufmann, M., Maden, K., Leisser, W., Matera, M. and Gude, T. (2005) Analysis of Polyphosphates in Fish and Shrimps Tissues by Two Different Chromatography Methods: Implication of False-Negative and -Positive Findings. Food Additives & Contaminants, 22, 1073-1082. http://dx.doi.org/10.1080/02652030500239565
[23]	Wang, L., Li, J. and Zhang, L. (2015) Determination of Polyphosphates in Fish and Shrimp Muscles by Capillary Electrophoresis with Indirect UV Detection after Phosphatase Inhibition Using High Pressure Pretreatment. Food Chemistry, 185, 349-354. http://dx.doi.org/10.1016/j.foodchem.2015.04.008
[24]	Andreeva, N.A. and Okorokov, L.A. (1993) Purification and Characterization of Highly Active and Stable Polyphosphatase from Saccharomyces cerevisiae Cell Envelope. Yeast, 9, 127-139. http://dx.doi.org/10.1002/yea.320090204
[25]	Wurst, H., Shiba, T. and Kornberg, A. (1995) The Gene for a Major Exopolyphosphatase of Saccharomyces cerevisiae. Journal of Bacteriology, 177, 898-906.
[26]	Andreeva, N.A., Kulakovskaya, T.V., Karpov, A.V., Sidorov, I.A. and Kulaev, I.S. (1998) Purification and Properties of Polyphosphatase from Saccharomyces cerevisiae Cytosol. Yeast, 14, 383-390. http://dx.doi.org/10.1002/(SICI)1097-0061(19980315)14:4<383::AID-YEA232>3.3.CO;2-J
[27]	Lichko, L.P., Eldarov, M.A., Dumina, M.V. and Kulakovskaya, T.V. (2014) PPX1 Gene Overexpression Has No Influence on Polyphosphates in Saccharomyces cerevisiae. Biochemistry, 79, 1211-1215. http://dx.doi.org/10.1134/S000629791411008X
[28]	Kulakovskaya, T.V., Andreeva, N.A., Karpov, A.V., Sidorov, I.A. and Kulaev, I.S. (1999) Hydrolysis of Tripolyphosphate by Purified Exopolyphosphatase of Saccharomyces cerevisiae Cytosol: Kinetic Model. Biochemistry (Moscow), 64, 990-993.
[29]	Kumble, K.D. and Kornberg, A. (1995) Inorganic Polyphosphate in Mammalian Cells and Tissues. Journal of Biological Chemistry, 270, 5818-5822. http://dx.doi.org/10.1074/jbc.270.11.5818
[30]	Vagabov, V.M., Trilisenko, L.V. and Kulaev, I.S. (2000) Dependence of Inorganic Polyphosphate Chain Length on the Orthophosphate Content in the Culture Medium of the Yeast Saccharomyces cerevisiae. Biochemistry (Moscow), 65, 349-355.
[31]	Andreeva, N.A., Kulakovskaya, T.V. and Kulaev, I.S. (1996) Purification and Characterization of Polyphosphatase from Saccharomyces cerevisiae Cytosol. Biochemistry (Moscow), 61, 1213-1220.
[32]	Lorenz, B., Müller, W.G.E., Kulaev, I.S. and Schröder, H.C.J. (1994) Purification and Characterization of an Exopolyphosphatase from Saccharomyces cerevisiae. Journal of Biological Chemistry, 269, 22198-22204.
[33]	Andreeva, N., Trilisenko, L., Eldarov, M. and Kulakovskaya, T. (2015) Polyphosphatase PPN1 of Saccharomyces cerevisiae: Switching of Exopolyphosphatase and Endopolyphosphatase Activities. PLoS ONE, 10, e0119594. http://dx.doi.org/10.1371/journal.pone.0119594
[34]	Kulaev, I.S. (1979) The Biochemistry of Inorganic Polyphosphates. Wiley, New York.
[35]	Wang, L., Li, J. and Zhang, L. (2015) Determination of Polyphosphates in Fish and Shrimp Muscles by Capillary Electro-Phoresis with Indirect UV Detection after Phosphatase Inhibition Using High Pressure Pretreatment. Food Chemistry, 185, 349-354. http://dx.doi.org/10.1016/j.foodchem.2015.04.008
[36]	Nagyová, G., Buňka, F., Salek, R.N., Cerníková, M., Mancík, P., Grûber, T. and Kuchar, D. (2014) Use of Sodium Polyphosphates with Different Linear Lengths in the Production of Spreadable Processed Cheese. Journal of Dairy Science, 97, 111-122. http://dx.doi.org/10.3168/jds.2013-7210