Inorganic polyphosphate in industry, agriculture and medicine: Modern state and outlook

Abstract Inorganic polyphosphates (PolyP) are linear polymers containing a few to several hundred orthophosphate residues linked by energy-rich phosphoanhydride bonds. PolyPs are widely used as reagents in water treatment, fertilizers, flame retardants and food additives due to its unique properties, inexpensiveness, nontoxicity and biodegradability. The practice of enhanced biological phosphorus removal (EBPR), based on PolyP accumulation by sludge bacteria, is an accepted and low-cost strategy for controlling eutrophication. PolyPs are present in the cells of all living organisms, from bacteria to mammals. They perform numerous functions in the cells: phosphate and energy storage, sequestration and storage of cations, formation of membrane channels, cell envelope formation and function, gene activity control, regulation of enzyme activities, stress response and stationary phase adaptation. PolyPs participate in bone tissue development and in the blood coagulation cascade and are promising candidates in therapy for bone and blood diseases. They may also have application in creating novel bone substitute materials, serving as carriers for prolonged action drugs, and acting as a phosphodonor in enzymatic synthesis of biologically active compounds. The importance of polyphosphate kinases in the virulence of pathogens forms a basis for the development of new antibiotics. Further study of PolyP biochemistry and cell biology can be applied to medicine, environmental protection and agriculture.

[1]  W. L. Davis,et al.  Evaluation of new high-performance calcium polyphosphate bioceramics as bone graft materials. , 1993, Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons.

[2]  L. Shelef,et al.  Factors affecting sensitivity of Staphylococcus aureus 196E to polyphosphates , 1986, Applied and environmental microbiology.

[3]  M. Gómez-García,et al.  Inorganic Polyphosphate and Energy Metabolism in Mammalian Cells* , 2010, The Journal of Biological Chemistry.

[4]  T. Kowalczyk,et al.  Glucose determination using immobilized polyphosphate glucokinase. , 1991, Analytical biochemistry.

[5]  A. Kornberg Inorganic polyphosphate: a molecule of many functions. , 2003, Annual review of biochemistry.

[6]  R. Kandel,et al.  Porous calcium polyphosphate scaffolds for bone substitute applications -- in vitro characterization. , 2001, Biomaterials.

[7]  T Noguchi,et al.  Use of Escherichia coli polyphosphate kinase for oligosaccharide synthesis. , 1998, Bioscience, biotechnology, and biochemistry.

[8]  Van Wazer,et al.  Phosphorus and its compounds , 1958 .

[9]  I. Kulaev Biochemistry of inorganic polyphosphates. , 1975, Reviews of physiology, biochemistry and pharmacology.

[10]  R. Morishita,et al.  Inorganic polyphosphate differentiates human mesenchymal stem cells into osteoblastic cells , 2010, Journal of Bone and Mineral Metabolism.

[11]  T. Graham Researches on the Arseniates, Phosphates, and Modifications of Phosphoric Acid. [Abstract] , 2009 .

[12]  J. Heemskerk,et al.  Polyphosphates: a link between platelet activation, intrinsic coagulation and inflammation? , 2010, Expert review of hematology.

[13]  Arthur Kornberg,et al.  Inorganic polyphosphate: essential for growth and survival. , 2009, Annual review of biochemistry.

[14]  R. Reusch,et al.  Putative structure and functions of a poly-beta-hydroxybutyrate/calcium polyphosphate channel in bacterial plasma membranes. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[15]  E. W. V. van Niel,et al.  Recent developments in the biochemistry and ecology of enhanced biological phosphorus removal. , 2000, Biochemistry. Biokhimiia.

[16]  A. Kornberg,et al.  Novel Assay Reveals Multiple Pathways Regulating Stress-Induced Accumulations of Inorganic Polyphosphate in Escherichia coli , 1998, Journal of bacteriology.

[17]  T. Uchihashi,et al.  Inorganic Polyphosphate Induces Osteoblastic Differentiation , 2010, Journal of dental research.

[18]  J. Keasling,et al.  Genetic manipulation of polyphosphate metabolism affects cadmium tolerance in Escherichia coli , 1996, Applied and environmental microbiology.

[19]  J. McGrath,et al.  Microbial phosphate removal and polyphosphate production from wastewaters. , 2003, Advances in applied microbiology.

[20]  M. Loessner,et al.  Long-Chain Polyphosphate Causes Cell Lysis and Inhibits Bacillus cereus Septum Formation, Which Is Dependent on Divalent Cations , 1999, Applied and Environmental Microbiology.

[21]  A. Gruber,et al.  Platelet polyphosphate: an endogenous activator of coagulation factor XII , 2010, Journal of thrombosis and haemostasis : JTH.

[22]  K. Morita,et al.  Enhanced initial bone regeneration with inorganic polyphosphate-adsorbed hydroxyapatite. , 2010, Acta biomaterialia.

[23]  M. Grynpas,et al.  Relationships between polyphosphate chemistry, biochemistry and apatite biomineralization. , 2008, Chemical reviews.

[24]  E. Oldfield,et al.  Human Platelet Dense Granules Contain Polyphosphate and Are Similar to Acidocalcisomes of Bacteria and Unicellular Eukaryotes* , 2004, Journal of Biological Chemistry.

[25]  T. Jensen,et al.  Nickel sequestering by polyphosphate bodies in Staphylococcus aureus. , 1998, Microbios.

[26]  Hisao Ohtake,et al.  Bacterial phosphate metabolism and its application to phosphorus recovery and industrial bioprocesses. , 2010, Journal of bioscience and bioengineering.

[27]  T. Kohgo,et al.  Induction of Calcification in MC3T3-E1 Cells by Inorganic Polyphosphate , 2004, Journal of dental research.

[28]  A. Kornberg,et al.  An exopolyphosphatase of Escherichia coli. The enzyme and its ppx gene in a polyphosphate operon. , 1993, The Journal of biological chemistry.

[29]  R. Kandel,et al.  Osteochondral defect repair using a novel tissue engineering approach: sheep model study. , 2007, Technology and health care : official journal of the European Society for Engineering and Medicine.

[30]  R. Bohnensack,et al.  Inorganic Polyphosphate in Human Osteoblast‐like Cells , 1998, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[31]  H. Ohtake,et al.  A simple method to release polyphosphate from activated sludge for phosphorus reuse and recycling. , 2002, Biotechnology and bioengineering.

[32]  M. Calvo,et al.  Changing phosphorus content of the US diet: potential for adverse effects on bone. J Nutr 126:1168S-1180S , 1996 .

[33]  T. Kulakovskaya,et al.  Effect of a carbon source on polyphosphate accumulation in Saccharomyces cerevisiae. , 2008, FEMS yeast research.

[34]  H. W. Veen,et al.  Biology of polyphosphate-accumulating bacteria involved in enhanced biological phosphorus removal. , 1994, FEMS microbiology reviews.

[35]  Richard K. Brow,et al.  Review: the structure of simple phosphate glasses , 2000 .

[36]  M. Matera,et al.  Analysis of polyphosphates in fish and shrimps tissues by two different ion chromatography methods: Implications on false-negative and -positive findings , 2005, Food additives and contaminants.

[37]  G. Glasser,et al.  Inorganic polymeric phosphate/polyphosphate as an inducer of alkaline phosphatase and a modulator of intracellular Ca2+ level in osteoblasts (SaOS-2 cells) in vitro. , 2011, Acta biomaterialia.

[38]  M. Kiyono,et al.  Accumulation of mercury in transgenic tobacco expressing bacterial polyphosphate. , 2006, Biological & pharmaceutical bulletin.

[39]  David Jenkins,et al.  Polyphosphate Kinase from Activated Sludge Performing Enhanced Biological Phosphorus Removal , 2002, Applied and Environmental Microbiology.

[40]  M. Uehara,et al.  Greater Effect of Dietary Potassium Tripolyphoshate than of Potassium Dihydrogenphosphate on the Nephrocalcinosis and Proximal Tubular Function in Female Rats from the Intake of a High-phosphorus Diet , 2001, Bioscience, biotechnology, and biochemistry.

[41]  A. Yamamoto,et al.  Analysis of condensed phosphates in food products by ion chromatography with an on-line hydroxide eluent generator. , 2000, Journal of chromatography. A.

[42]  M. Duchen,et al.  Targeted polyphosphatase expression alters mitochondrial metabolism and inhibits calcium-dependent cell death , 2007, Proceedings of the National Academy of Sciences.

[43]  Linda L. Blackall,et al.  A review and update of the microbiology of enhanced biological phosphorus removal in wastewater treatment plants , 2004, Antonie van Leeuwenhoek.

[44]  H. Ohtake,et al.  Use of an Escherichia coli Recombinant Producing Thermostable Polyphosphate Kinase as an ATP Regenerator To Produce Fructose 1,6-Diphosphate , 2007, Applied and Environmental Microbiology.

[45]  J. Keasling,et al.  Guanosine pentaphosphate phosphohydrolase of Escherichia coli is a long-chain exopolyphosphatase. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[46]  T. E. Cloete,et al.  Enhanced Biological Phosphorus Removal in Activated Sludge Systems , 1990 .

[47]  E. Lombi,et al.  Polyphosphate-fertilizer solution stability with time, temperature, and pH , 2007 .

[48]  James H Morrissey,et al.  Polyphosphate exerts differential effects on blood clotting, depending on polymer size. , 2010, Blood.

[49]  D. J. White,et al.  Hexametaphosphate effects on tooth surface conditioning film chemistry--in vitro and in vivo studies. , 2002, The Journal of clinical dentistry.

[50]  Qingyu Wu,et al.  Hageman factor, platelets and polyphosphates: early history and recent connection , 2010, Journal of thrombosis and haemostasis : JTH.

[51]  H. Philippou,et al.  Polyphosphate modifies the fibrin network and down-regulates fibrinolysis by attenuating binding of tPA and plasminogen to fibrin. , 2010, Blood.

[52]  T. Mino,et al.  Microbial selection of polyphosphate-accumulating bacteria in activated sludge wastewater treatment processes for enhanced biological phosphate removal. , 2000, Biochemistry. Biokhimiia.

[53]  H. Ohtake,et al.  A sensitive method for detecting AMP by utilizing polyphosphate-dependent ATP regeneration and bioluminescence reactions , 2001 .

[54]  D. Kohn,et al.  Development and characterization of a biodegradable polyphosphate. , 1997, Journal of biomedical materials research.

[55]  C. D. Boswell,et al.  Phosphate uptake and release by Acinetobacter johnsonii in continuous culture and coupling of phosphate release to heavy metal accumulation , 2001, Journal of Industrial Microbiology and Biotechnology.

[56]  J. Tanner,et al.  Aptamer-mediated inhibition of Mycobacterium tuberculosis polyphosphate kinase 2. , 2011, Biochemistry.

[57]  T. Renné,et al.  Platelet polyphosphates: The nexus of primary and secondary hemostasis , 2011, Scandinavian journal of clinical and laboratory investigation.

[58]  A. Orell,et al.  Copper tolerance of the thermoacidophilic archaeon Sulfolobus metallicus: possible role of polyphosphate metabolism. , 2006, Microbiology.

[59]  J. Keasling,et al.  Engineering polyphosphate metabolism in Escherichia coli: implications for bioremediation of inorganic contaminants. , 1998, Biotechnology and bioengineering.

[60]  H. Schröder,et al.  Anti-HIV-1 activity of inorganic polyphosphates. , 1997, Journal of acquired immune deficiency syndromes and human retrovirology : official publication of the International Retrovirology Association.

[61]  E. Toyserkani,et al.  Solid freeform fabrication and characterization of porous calcium polyphosphate structures for tissue engineering purposes. , 2010, Journal of biomedical materials research. Part B, Applied biomaterials.

[62]  T. Renné,et al.  Platelet Polyphosphates Are Proinflammatory and Procoagulant Mediators In Vivo , 2009, Cell.

[63]  J. Keasling,et al.  Intracellular polyphosphate content and cadmium tolerance in Anacystis nidulans R2 , 1996 .

[64]  C. Bladen,et al.  A large, voltage-dependent channel, isolated from mitochondria by water-free chloroform extraction. , 2005, Biophysical journal.

[65]  T. Mino,et al.  Location of Phosphorus in Activated Sludge and Function of Intracellular Polyphosphates in Biological Phosphorus Removal Process , 1985 .

[66]  Ruiping Huang,et al.  Poly-3-hydroxybutyrate/polyphosphate complexes form voltage-activated Ca2+ channels in the plasma membranes of Escherichia coli. , 1995, Biophysical journal.

[67]  A. Kornberg,et al.  Inorganic polyphosphate stimulates mammalian TOR, a kinase involved in the proliferation of mammary cancer cells , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[68]  A. Labigne,et al.  Polyphosphate kinase: a new colonization factor of Helicobacter pylori. , 2005, FEMS microbiology letters.

[69]  R. Reusch,et al.  Transmembrane ion transport by polyphosphate/poly-(R)-3-hydroxybutyrate complexes. , 2000, Biochemistry. Biokhimiia.

[70]  R. Reusch,et al.  Poly-β-hydroxybutyrate/Calcium Polyphosphate Complexes in Eukaryotic Membranes , 1989 .

[71]  J. Morrissey,et al.  Polyphosphate as a general procoagulant agent , 2008, Journal of thrombosis and haemostasis : JTH.

[72]  H. Ohtake,et al.  Molecular analysis of polyphosphate accumulation in bacteria. , 2000, Biochemistry. Biokhimiia.

[73]  A. Kornberg,et al.  Polyphosphate kinase is highly conserved in many bacterial pathogens , 1998, Molecular microbiology.

[74]  H. Wurst,et al.  The gene for a major exopolyphosphatase of Saccharomyces cerevisiae , 1995, Journal of bacteriology.

[75]  S. R. Kornberg Adenosine triphosphate synthesis from polyphosphate by an enzyme from Escherichia coli. , 1957, Biochimica et biophysica acta.

[76]  M. Cho,et al.  High dietary inorganic phosphate increases lung tumorigenesis and alters Akt signaling. , 2009, American journal of respiratory and critical care medicine.

[77]  Robert J. Seviour,et al.  The Microbiology of Activated Sludge , 1999, Springer Netherlands.

[78]  K. Ishige,et al.  Inorganic polyphosphate and polyphosphate kinase: their novel biological functions and applications. , 2000, Biochemistry. Biokhimiia.

[79]  H. Schröder,et al.  Polyphosphate in bone. , 2000, Biochemistry. Biokhimiia.

[80]  J. Keasling,et al.  Application of polyphosphate metabolism to environmental and biotechnological problems. , 2000, Biochemistry. Biokhimiia.

[81]  Lin Zhao,et al.  [Feasibility of calcium polyphosphate fiber as scaffold materials for tendon tissue engineering in vitro]. , 2002, Zhongguo xiu fu chong jian wai ke za zhi = Zhongguo xiufu chongjian waike zazhi = Chinese journal of reparative and reconstructive surgery.

[82]  M. Grynpas,et al.  Control of Vertebrate Skeletal Mineralization by Polyphosphates , 2009, PloS one.

[83]  James H Morrissey,et al.  Polyphosphate modulates blood coagulation and fibrinolysis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[84]  I. Kulaev,et al.  Polyphosphate metabolism in micro-organisms. , 1983, Advances in microbial physiology.

[85]  Y. Kawazoe,et al.  Modulation of Mitogenic Activity of Fibroblast Growth Factors by Inorganic Polyphosphate* , 2003, Journal of Biological Chemistry.

[86]  C. M. Hooijmans,et al.  Biological phosphate removal processes , 1997, Applied Microbiology and Biotechnology.

[87]  T. Kulakovskaya,et al.  High molecular mass exopolyphosphatase from the cytosol of the yeast Saccharomyces cerevisiae is encoded by the PPN1 gene , 2006, Biochemistry (Moscow).

[88]  V. Gowariker,et al.  The Fertilizer Encyclopedia , 2009 .

[89]  L. Leung,et al.  Polyphosphate binds with high affinity to exosite II of thrombin , 2010, Journal of thrombosis and haemostasis : JTH.

[90]  R. Reusch Streptomyces lividans potassium channel contains poly-(R)-3-hydroxybutyrate and inorganic polyphosphate. , 1999, Biochemistry.

[91]  N. Andreeva,et al.  Purification and characterization of highly active and stable polyphosphatase from Saccharomyces cerevisiae cell envelope , 1993, Yeast.

[92]  J. Keasling,et al.  Polyphosphate kinase genes from full-scale activated sludge plants , 2007, Applied Microbiology and Biotechnology.

[93]  P. Gong,et al.  Effect of combined application of bFGF and inorganic polyphosphate on bioactivities of osteoblasts and initial bone regeneration. , 2009, Acta biomaterialia.

[94]  A. Negoda,et al.  Importance of oligo-R-3-hydroxybutyrates to S. lividans KcsA channel structure and function. , 2010, Molecular bioSystems.

[95]  J. Gilbert,et al.  Novel Analysis of Oceanic Surface Water Metagenomes Suggests Importance of Polyphosphate Metabolism in Oligotrophic Environments , 2011, PloS one.

[96]  A. Beeton,et al.  Environmental Phosphorus Handbook. , 1973 .

[97]  B. Lorenz,et al.  Mammalian intestinal alkaline phosphatase acts as highly active exopolyphosphatase. , 2001, Biochimica et biophysica acta.

[98]  R. Reusch Biological complexes of poly-β-hydroxybutyrate , 1992 .

[99]  D. J. Oosthuizen,et al.  The role of extracellular exopolymers in the removal of phosphorus from activated sludge. , 2001, Water research.

[100]  R. Kandel,et al.  Porous calcium polyphosphate scaffolds for bone substitute applications in vivo studies. , 2002, Biomaterials.