Tartrate-resistant acid phosphatase: A target for anti-osteoporotic chemotherapeutics

Current Enzyme Inhibition

Volumn 6, Issue 3, 2010, Pages 118-129

  Vella, Peter ^a   McGeary, Ross P ^a   Gahan, Lawrence R ^a   Schenk, Gerhard ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Bone metabolism; Drug design and development; Osteoporosis; Purple acid phosphatase; Reaction mechanism; Tartrate resistant acid phosphatase

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; ENZYME INHIBITOR; FLUORIDE; METAL DERIVATIVE; MOLYBDIC ACID; PHOSPHATE; SULFATE; TARTRATE RESISTANT ACID PHOSPHATASE INHIBITOR; TUNGSTIC ACID; UNCLASSIFIED DRUG; VANADIC ACID;

AMINO ACID SEQUENCE; BINDING AFFINITY; CATALYSIS; CRYSTAL STRUCTURE; DRUG BINDING; DRUG DESIGN; DRUG SYNTHESIS; ENZYME ACTIVITY; ENZYME BINDING; ENZYME STRUCTURE; HUMAN; IC 50; IRON TRANSPORT; METAL BINDING; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOLYSIS; OSTEOPOROSIS; REVIEW; STRUCTURE ACTIVITY RELATION;

ANIMALIA;

EID: 79953872639     PISSN: 15734080     EISSN: None     Source Type: Journal    
DOI: 10.2174/157340810793384133     Document Type: Review

References (82)

1. Mitić, N.; Smith, S.J.; Neves, A.; Guddat, L.W.; Gahan, L.R.; Schenk, G. The catalytic mechanisms of binuclear metallohydrolases. Chem. Rev., 2006, 106, 3338-3363.
2. Bull, H.; Murray, P.G.; Thomas, D.; Fraser, A.M.; Nelson, P.N. Acid phosphatases. Mol. Pathol., 2002, 55, 65-72.
3. Antanaitis, B.C.; Aisen, P.; Lilienthal, H.R. Physical characterization of two-iron uteroferrin. Evidence for a spincoupled binuclear iron cluster. J. Biol. Chem., 1983, 258, 3166-3172.
4. Yang, Y.S.; McCormick, J.M.; Solomon, E.I. Circular dichroism and magnetic circular dichroism studies of the mixed-valence binuclear non-heme iron active site in uteroferrin and its anion complexes. J. Am. Chem. Soc., 1997, 119, 11832-11842.
5. Oddie, G.W.; Schenk, G.; Angel, N.Z.; Walsh, N.; Guddat, L.W.; de Jersey, J.; Cassady, A.I.; Hamilton, S.E.; Hume, D.A. Structure, function, and regulation of tartrate-resistant acid phosphatase. Bone, 2000, 27, 575-584.
6. Bernhardt, P.V.; Schenk, G.; Wilson, G.J. Direct electrochemistry of porcine purple acid phosphatase (uteroferrin). Biochemistry, 2004, 43, 10387-10392.
7. Wang, D.L.; Holz, R.C.; David, S.S.; Que, L.; Stankovich, M.T. Electrochemical properties of the diiron core of uteroferrin and its anion complexes. Biochemistry, 1991, 30, 8187-8194.
8. Beck, J.L.; McConachie, L.A.; Summors, A.C.; Arnold, W.N.; de Jersey, J.; Zerner, B. Properties of a purple phosphatase from red kidney bean a zinc-iron metalloenzyme. Biochim. Biophys. Acta, 1986, 869, 61-68.
9. Durmus, A.; Eicken, C.; Sift, B.H.; Kratel, A.; Kappl, R.; Huttermann, J.; Krebs, B. The active site of purple acid phosphatase from sweet potatoes (Ipomoea batatas) Metal content and spectroscopic characterization. Eur. J. Biochem., 1999, 260, 709-716.
10. Schenk, G.; Ge, Y.B.; Carrington, L.E.; Wynne, C.J.; Searle, I.R.; Carroll, B.J.; Hamilton, S.; de Jersey, J. Binuclear metal centers in plant purple acid phosphatases: Fe-Mn in sweet potato and Fe-Zn in soybean. Arch. Biochem. Biophys., 1999, 370, 183-189.
11. Schenk, G.; Guddat, L. W.; Ge, Y.; Carrington, L.E.; Hume, D.A.; Hamilton, S.; de Jersey, J. Identification of mammalian-like purple acid phosphatases in a wide range of plants. Gene, 2000, 250, 117-125.
12. Schenk, G.; Korsinczky, M. L. J.; Hume, D. A.; Hamilton, S.; de Jersey, J., Purple acid phosphatases from bacteria: similarities to mammalian and plant enzymes. Gene 2000, 255, 419-424.
13. Flanagan, J.U.; Cassady, A.I.; Schenk, G.; Guddat, L.W.; Hume, D.A. Identification and molecular modeling of a novel, plant-like, human purple acid phosphatase. Gene, 2006, 377, 12-20.
14. Sibille, J.C.; Doi, K.; Aisen, P. Hydroxyl radical formation and iron-binding proteins. Stimulation by the purple acid phosphatases. J. Biol. Chem., 1987, 262, 59-62.
15. Nuttleman, P.R.; Roberts, R.M. Transfer of iron from uteroferrin (purple acid phosphatase) to transferrin related to acid phosphatase activity. J. Biol. Chem., 1990, 265, 12192-12199.
16. Räisänen, S.R.; Alatalo, S.L.; Ylipahkala, H.; Halleen, J.M.; Cassady, A.I.; Hume, D.A.;Väänänen, H.K. Macrophages overexpressing tartrate-resistant acid phosphatase show altered profile of free radical production and enhanced capacity of bacterial killing. Biochem. Biophys. Res. Commun., 2005, 331, 120-126.
17. Moss, D.W.; Raymond, F.D.; Wile, D.B.; Rej, R. Clinical and Biological Aspects of Acid Phosphatase. Crit. Rev. Clin. Lab. Sci., 1995, 32, 431-467.
18. Angel, N.Z.; Walsh, N.; Forwood, M.R.; Ostrowski, M.C.; Cassady, A.I.; Hume, D.A. Transgenic mice overexpressing tartrate-resistant acid phosphatase exhibit an increased rate of bone turnover. J. Bone Miner. Res., 2000, 15, 103-110.
19. Hayman, A.R.; Jones, S.J.; Boyde, A.; Foster, D.; Colledge, W.H.; Carlton, M.B.; Evans, M.J.; Cox, T.M. Mice lacking tartrateresistant acid phosphatase (Acp 5) have disrupted endochondral ossification and mild osteopetrosis. Development, 1996, 122, 3151-3162.
20. Ek-Rylander, B.; Flores, M.; Wendel, M.; Heinegard, D.; Andersson, G. Dephosphorylation of osteopontin and bone sialoprotein by osteoclastic tartrate-resistant acid phosphatase. Modulation of osteoclast adhesion in vitro. J. Biol. Chem., 1994, 269, 14853-14856.
21. Valizadeh, M.; Schenk, G.; Nash, K.; Oddie, G.W.; Guddat, L.W.; Hume, D.A.; de Jersey, J.; Burke, T.R.; Hamilton, S. Phosphotyrosyl peptides and analogues as substrates and inhibitors of purple acid phosphatases. Arch. Biochem. Biophys., 2004, 424, 154-162.
22. McGeary, R.P.; Vella, P.; Mak, J.Y.W.; Guddat, L.W.; Schenk, G. Inhibition of purple acid phosphatase with [alpha]-alkoxynaphthylmethylphosphonic acids. Bioorg. Med. Chem. Lett., 2009, 19, 163-166.
23. Hayman, A.R.; Dryden, A.J.; Chambers, T.J.; Warburton, M.J. Tartrate-resistant acid phosphatase from human osteoclastomas is translated as a single polypeptide. Biochem. J., 1991, 277, 631-634.
24. Janckila, A.J.; Parthasarathy, R.N.; Parthasarathy, L.K.; Seelan, R.S.; Yam, L.T. Stable expression of human tartrate-resistant acid phosphatase isoforms by CHO cells. Clin. Chim. Acta, 2002, 326, 113-122.
25. Ljusberg, J.; Ek-Rylander, B.; Andersson, G. Tartrate-resistant purple acid phosphatase is synthesized as a latent proenzyme and activated by cysteine proteinases. Biochem. J., 1999, 343, 63-69.
26. Mitć, N.; Valizadeh, M.; Leung, E.W.W.; de Jersey, J.; Hamilton, S.; Hume, D.A.; Cassady, A.I.; Schenk, G. Human tartrate-resistant acid phosphatase becomes an effective ATPase upon proteolytic activation. Arch. Biochem. Biophys., 2005, 439, 154-164.
27. Ljusberg, J.; Wang, Y.; Lang, P.; Norgard, M.; Dodds, R.; Hultenby, K.; Ek-Rylander, B.; Andersson, G. Proteolytic excision of a repressive loop domain in tartrate-resistant acid phosphatase by cathepsin K in osteoclasts. J. Biol. Chem., 2005, 280, 28370-28381.
28. Kaija, H.; Alatalo, S.L.; Halleen, J.M.; Lindqvist, Y.; Schneider, G.; Kalervo Väänänen, H.; Vihko, P. Phosphatase and oxygen radical-generating activities of mammalian purple acid phosphatase are functionally independent. Biochem. Biophys. Res. Commun., 2002, 292, 128-132.
29. Halleen, J.M.; Räisänen, S.R.; Salo, J.J.; Reddy, S.V.; Roodman, G.D.; Hentunen, T.A.; Lehenkari, P.P.; Kaija, H.; Vihko, P.; Vaananen, H.K. Intracellular fragmentation of bone resorption fragments by ROS generated by osteoclastic TRAP. J. Biol. Chem., 1999, 274, 22907-22910.
30. Vääräniemi, J.; Halleen, J.M.; Kaarlonen, K.; Ylipahkala, H.; Alatalo, S.L.; Andersson, G.R.; Kaija, H.; Vihko, P.; Väänänen, H.K. Intracellular machinery for matrix degradation in boneresorbing osteoclasts. J. Bone Miner. Res., 2004, 19, 1432-1440.
31. Räisänen, S.R.; Halleen, J.; Parikka, V.; Väänänen, H.K. Tartrateresistant acid phosphatase facilitates hydroxyl radical formation and colocalizes with phagocytosed Staphylococcus aureus in alveolar macrophages. Biochem. Biophys. Res. Commun., 2001, 288, 142-150.
32. Bune, A.J.; Hayman, A.R.; Evans, M.J.; Cox, T.M. Mice lacking tartrate-resistant acid phosphatase (Acp 5) have disordered macrophage inflammatory responses and reduced clearance of the pathogen, Staphylococcus aureus. Immunology, 2001, 102, 103-113.
33. Cashikar, A.G.; Kumaresan, R.; Rao, N.M. Biochemical characterization and subcellular localization of the red kidney bean purple acid phosphatase. Plant Physiol., 1997, 114, 907-915.
34. Leung, E.; Teixeira, M.; Guddat, L.W.; Mitic, N.; Schenk, G. Structure, function and diversity of purple acid phosphatases. Curr. Topics Plant Biol., 2007, 8, 21-31.
35. Li, D.; Zhu, H.; Liu, K.; Liu, X.; Leggewie, G.; Udvardi, M.; Wang, D. Purple acid phosphatases of Arabidopsis thaliana: comparative analysis and differential regulation by phosphate deprivation. J. Biol. Chem., 2002, 277, 27772-27781.
36. Zimmermann, P.; Regierer, B.; Kossmann, J.; Frossard, E.; Amrhein, N.; Bucher, M. Differential expression of three purple acid phosphatases from potato potato. Plant Biol., 2004, 5, 519-518.
37. Bozzo, G.G.; Raghothama, K.G.; Plaxton, W.C. Structural and kinetic properties of a novel purple acid phosphatase from phosphate-starved tomato (Lycopersicon esculentum) cell cultures. Biochem. J., 2004, 377, 419-428.
38. Bozzo, G.G.; Raghothama, K.G.; Plaxton, W.C. Purification and characterization of two secreted purple acid phosphatase isozymes from phosphate-starved tomato (Lycopersicon esculentum) cell cultures. Eur. J. Biochem., 2002, 269, 6278-6286.
39. Sträter, N.; Klabunde, T.; Tucker, P.; Witzel, H.; Krebs, B. Crystalstructure of a purple acid-phosphatase containing a dinuclear Fe(III)-Zn(II) active-site. Science, 1995, 268, 1489-1492.
40. Klabunde, T.; Strater, N.; Frohlich, R.; Witzel, H.; Krebs, B., Mechanism of Fe(III)-Zn(II) purple acid phosphatase based on crystal structures. J. Mol. Biol., 1996, 259, 737-748.
41. Guddat, L.W.; McAlpine, A.S.; Hume, D.; Hamilton, S.; de Jersey, J.; Martin, J.L. Crystal structure of mammalian purple acid phosphatase. Structure, 1999, 7, 757-767.
42. Lindqvist, Y.; Johansson, E.; Kaija, H.; Vihko, P.; Schneider, G. Three-dimensional structure of a mammalian purple acid phosphatase at 2.2 angstrom resolution with a mu-(hydr)oxo bridged di-iron center. J. Mol. Biol., 1999, 291, 135-147.
43. Uppenberg, J.; Lindqvist, F.; Svensson, C.; Ek-Rylander, B.; Andersson, G. Crystal structure of a mammalian purple acid phosphatase. J. Mol. Biol., 1999, 290, 201-211.
44. Sträter, N.; Jasper, B.; Scholte, M.; Krebs, B.; Duff, A.P.; Langley, D.B.; Han, R.L.; Averill, B.A.; Freeman, H.C.; Guss, J.M. Crystal structures of recombinant human purple acid phosphatase with and without an inhibitory conformation of the repression loop. J. Mol. Biol., 2005, 351, 233-246.
45. Schenk, G.; Gahan, L.R.; Carrington, L.E.; Mitic, N.; Valizadeh, M.; Hamilton, S.E.; de Jersey, J.; Guddat, L.W. Phosphate forms an unusual tripodal complex with the Fe-Mn center of sweet potato purple acid phosphatase. Proc. Natl. Acad. Sci. USA, 2005, 102, 273-278.
46. Schenk, G.; Elliott, T.; Leung, E.; Carrington, L.; Mitic, N.; Gahan, L.; Guddat, L. Crystal structures of a purple acid phosphatase, representing different steps of this enzyme's catalytic cycle. BMC Struct. Biol., 2008, 8, 6.
47. Schenk, G.; Boutchard, C.L.; Carrington, L.E.; Noble, C.J.; Moubaraki, B.; Murray, K.S.; de Jersey, J.; Hanson, G.R.; Hamilton, S. A purple acid phosphatase from sweet potato contains an antiferromagnetically coupled binuclear Fe-Mn center. J. Biol. Chem., 2001, 276, 19084-19088.
48. Mitić, N.; Noble, C.J.; Gahan, L.R.; Hanson, G.R.; Schenk, G. Metal-ion mutagenesis: conversion of a purple acid phosphatase from sweet potato to a neutral phosphatase with the formation of an unprecedented catalytically competent Mn(II)Mn(II) active site. J. Am. Chem. Soc., 2009, 131, 8173-8179.
49. Smith, S.; Hadler, K.S.; Hanson, G.R.; Schenk, G.; Mitić N. Binuclear Mn-dependant enzymes. In Biological Magnetic Resonance: High Resolution EPR: Applications to Metalloenzymes and Metals in Medicine, Hanson, G.R.; Berliner, L.J., Eds. Springer: New York, 2010, Vol. 29, 273-343.
50. Martin, B.L.; Graves, D.J. Isotope effects on the mechanism of calcineurin catalysis: kinetic solvent isotope and isotope exchange studies. Biochim. Biophys. Acta, 1994, 1206, 136-142.
51. Mueller, E.G.; Crowder, M.W.; Averill, B.A.; Knowles, J.R. Purple acid-phosphatase a diiron enzyme that catalyzes a direct phospho group transfer to water. J. Am. Chem. Soc., 1993, 115, 2974-2975.
52. Mertz, P.; Yu, L.; Sikkink, R.; Rusnak, F. Kinetic and spectroscopic analyses of mutants of a conserved histidine in the metallophosphatases calcineurin and lambda protein phosphatase. J. Biol. Chem., 1997, 272, 21296-21302.
53. Twitchett, M.B.; Sykes, A.G. Structure, properties and reactivity of the (FeFeIII)-Fe-II and (ZnFeIII)-Fe-II purple acid phosphatases. Eur. J. Inorg. Chem., 1999, 2105-2115.
54. Twitchett, M.B.; Schenk, G.; Aquino, M.A.S.; Yiu, D.T.Y.; Lau, T.C.; Sykes, A.G. Reactivity of M-II metal-substituted derivatives of pig purple acid phosphatase (Uteroferrin) with phosphate. Inorg. Chem., 2002, 41, 5787-5794.
55. Aquino, M.A.S.; Sykes, A.G. Redox reactivity of the binuclear iron active-site of porcine purple acid-phosphatase (uteroferrin). J. Chem. Soc. Dalton Trans., 1994, 683-687.
56. Aquino, M.A.S.; Lim, J.S.; Sykes, A.G. Mechanism of the reaction of different phosphates with the iron(II)iron(III) form of purple acid-phosphatase from porcine uteri (uteroferrin). J. Chem. Soc. Dalton Trans., 1994, 429-436.
57. Merkx, M.; Pinkse, M.W.H.; Averill, B.A. Evidence for nonbridged coordination of p-nitrophenyl phosphate to the dinuclear Fe(III)-M(II) center in bovine spleen purple acid phosphatase during enzymatic turnover. Biochemistry, 1999, 38, 9914-9925.
58. Smith, S.J.; Casellato, A.; Hadler, K.S.; Mitic, N.; Riley, M.J.; Bortoluzzi, A.J.; Szpoganicsz, B.; Schenk, G.; Neves, A.; Gahan, L.R. The reaction mechanism of the Ga(III)Zn(II) derivative of uteroferrin and corresponding biomimetics. J. Biol. Inorg. Chem., 2007, 12, 1207-1220.
59. Cox, R.S.; Schenk, G.; Mitic, N.; Gahan, L.R.; Hengge, A.C. Diesterase activity and substrate binding in purple acid phosphatases. J. Am. Chem. Soc., 2007, 129, 9550-9551.
60. Wang, X.D.; Ho, R.Y.N.; Whiting, A.K.; Que, L. Spectroscopic characterization of a ternary phosphatase-substrate-fluoride complex. Mechanistic implications for dinuclear hydrolases. J. Am. Chem. Soc., 1999, 121, 9235-9236.
61. Merkx, M.; Averill, B.A. Ga3+ as a functional substitute for Fe3+: Preparation and characterization of the Ga3+Fe2+ and Ga3+Zn2+ forms of bovine spleen purple acid phosphatase. Biochemistry 1998, 37, 8490-8497.
62. Merkx, M.; Averill, B. A., Probing the role of the trivalent metal in phosphate ester hydrolysis: Preparation and characterization of purple acid phosphatases containing AlIIIZnII and InIIIZnII active sites, including the first example of an active aluminium enzyme. J. Am. Chem. Soc., 1999, 121, 6683-6689.
63. Schenk, G.; Peralta, R.A.; Batista, S.C.; Bortoluzzi, A.J.; Szpoganics, B.; Dick, A.K.; Herrald, P.; Hanson, G.R.; Szilagyi, R.K.; Riley, M.J.; Gahan, L.R.; Neves, A. Probing role of the divalent metal ion in uteroferrin using metal ion replacement and a comparison to isostructural biomimetics. J. Biol. Inorg. Chem., 2008, 13, 139-155.
64. Smoukov, S.K.; Quaroni, L.; Wang, X.; Doan, P.E.; Hoffman, B.M.; Que, L., Jr. Electron-nuclear double resonance spectroscopic evidence for a hydroxo-bridge nucleophile involved in catalysis by a dinuclear hydrolase. J. Am. Chem. Soc., 2002, 124, 2595-2603.
65. Williams, A. Effective charge and transition-state structure in solution. Adv. Phys. Org. Chem., 1992, 27, 1-55.
66. Hengge, A.C. Isotope effects in the study of phosphoryl and sulfuryl transfer reactions. Acc. Chem. Res., 2002, 35, 105-112.
67. Funhoff, E.G.; Wang, Y.; Andersson, G.; Averill, B.A. Substrate positioning by His92 is important in catalysis by purple acid phosphatase. FEBS J., 2005, 272, 2968-2977.
68. Truong, N.T.; Naseri, J.I.; Vogel, A.; Rompel, A.; Krebs, B. Structure-function relationships of purple acid phosphatase from red kidney beans based on heterologously expressed mutants. Arch. Biochem. Biophys., 2005, 440, 38-45.
69. Crans, D.C.; Ehde, P.M.; Shin, P.K.; Pettersson, L. Structural and kinetic characterization of simple complexes as models for vanadate-protein interactions. J. Am. Chem. Soc., 1991, 113, 3728-3736.
70. Pinkse, M.W.H.; Merkx, M.; Averill, B.A. Fluoride inhibition of bovine spleen purple acid phosphatase: Characterization of a ternary enzyme-phosphate-fluoride complex as a model for the active enzyme-substrate-hydroxide complex. Biochemistry, 1999, 38, 9926-9936.
71. Elliott, T.E.; Mitic, N.; Gahan, L.R.; Guddat, L.W.; Schenk, G. Inhibition studies of purple acid phosphatases: implications for the catalytic mechanism. J. Braz. Chem. Soc., 2006, 17, 1558-1565.
72. Voegtli, W. C.; White, D. J.; Reiter, N. J.; Rusnak, F.; Rosenzweig, A. C., Structure of the bacteriophage lambda Ser/Thr protein phosphatase with sulfate ion bound in two coordination modes. Biochemistry 2000, 39, 15365-15374.
73. Dikiy, A.; Funhoff, E.G.; Averill, B.A.; Ciurli, S. New Insights into the mechanism of purple acid phosphatase through 1H NMR spectroscopy of the recombinant human enzyme. J. Am. Chem. Soc., 2002, 124, 13974-13975.
74. Cama, E.; Pethe, S.; Boucher, J.L.; Han, S.F.; Emig, F.A.; Ash, D.E.; Viola, R.E.; Mansuy, D.; Christianson, D.W. Inhibitor coordination interactions in the binuclear manganese cluster of arginase. Biochemistry, 2004, 43, 8987-8999.
75. Neri, F.; Kok, D.; Miller, M.A.; Smulevich, G. Fluoride binding in hemoproteins: the importance of the distal cavity structure. Biochemistry, 1997, 36, 8947-8953.
76. Meier, B.; Scherk, C.; Schmidt, M.; Parak, F. pH-dependent inhibition by azide and fluoride of the iron superoxide dismutase from Propionibacterium shermanii. Biochem. J., 1998, 331, 403-407.
77. Lahiri, S.D.; Zhang, G.; Dunaway-Mariano, D.; Allen, K.N. The pentacovalent phosphorus intermediate of a phosphoryl transfer reaction. Science, 2003, 299, 2067-2071.
78. Davies, D.R.; Hol, W.G.J. The power of vanadate in crystallographic investigations of phosphoryl transfer enzymes. FEBS Lett., 2004, 577, 315-321.
79. Crans, D.C.; Simone, C.M.; Holz, R.C.; Que, L. Interaction of porcine uterine fluid purple acid phosphatase with vanadate and vanadyl cation. Biochemistry, 1992, 31, 11731-11739.
80. Holtz, K.M.; Stec, B.; Kantrowitz, E.R. A model of the transition state in the alkaline phosphatase reaction. J. Biol. Chem., 1999, 274, 8351-8354.
81. Schwender, C.F.; Beers, S.A.; Malloy, E.; Demarest, K.; Minor, L.; Lau, K.H.W. 1-napthylmethylphosphonic acid derivatives as osteoclastic acid phosphatase inhibitors. Bioorg. Med. Chem. Lett., 1995, 5, 1801-1806.
82. Myers, J.K.; Antonelli, S.M.; Widlanski, T.S. Motifs for metallophosphatase inhibition. J. Am. Chem. Soc., 1997, 119, 3163-3164.