Crystal structures of a purple acid phosphatase, representing different steps of this enzyme's catalytic cycle

BMC Structural Biology

Volumn 8, Issue , 2008, Pages

  Schenk, Gerhard ^a   Elliott, Tristan W ^a   Leung, Eleanor ^a   Carrington, Lyle E ^a   Mitić, Nataša ^a   Gahan, Lawrence R ^a   Guddat, Luke W ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; FERRIC ION; FLUORIDE; HYDROXIDE; METAL; METAL ION; SULFATE; ZINC; ACID PHOSPHATASE; GLYCOPROTEIN; LIGAND; VEGETABLE PROTEIN;

ARTICLE; BEAN; COORDINATION; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME DEGRADATION; ENZYME MECHANISM; ENZYME METABOLISM; ENZYME STRUCTURE; HYDROGEN BOND; HYDROLYSIS; KINETICS; NONHUMAN; SPECTROSCOPY; BINDING SITE; CATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; METABOLISM; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

ANIMALIA; BACTERIA (MICROORGANISMS); PHASEOLUS VULGARIS;

ACID PHOSPHATASE; BINDING SITES; CATALYSIS; CRYSTALLOGRAPHY, X-RAY; FLUORIDES; GLYCOPROTEINS; KINETICS; LIGANDS; MODELS, MOLECULAR; PHASEOLUS; PLANT PROTEINS; PROTEIN CONFORMATION; SULFATES;

EID: 40849135696     PISSN: None     EISSN: 14726807     Source Type: Journal    
DOI: 10.1186/1472-6807-8-6     Document Type: Article

References (67)

1. SJ Lippard JM Berg, Principles of Bioinorganic Chemistry, University Science Books, Mill Valley, CA 1994
2. Binuclear metallohydrolases. DE Wilcox, Chem Rev 1996 96 2435 2458 10.1021/cr950043b 11848832
3. Manganese enzymes with binuclear active sites. GC Dismukes, Chem Rev 1996 96 2909 2926 10.1021/cr950053c 11848845
4. The structure and mechanism of protein phosphatases: Insights into catalysis and regulation. D Barford AK Das MP Egloff, Annu Rev Biophys Biomol Struct 1998 27 133 164 10.1146/annurev.biophys.27.1.133 9646865
5. Molecular reactions of protein phosphatases - Insights from structure and chemistry. MD Jackson JM Denu, Chem Rev 2001 101 2313 2340 10.1021/cr000247e 11749375
6. Structure and function of the methionine aminopeptidases. WT Lowther BW Matthews, Biochimica Et Biophysica Acta-Protein Structure and Molecular Enzymology 2000 1477 157 167 10.1016/S0167-4838(99)00271-X
7. Geometric and electronic structure/function correlations in non-heme iron enzymes. EI Solomon TC Brunold MI Davis JN Kemsley SK Lee N Lehnert F Neese AJ Skulan YS Yang J Zhou, Chem Rev 2000 100 235 349 10.1021/cr9900275 11749238
8. The catalytic mechanisms of binuclear metallohydrolases. N Mitic SJ Smith A Neves LW Guddat LR Gahan G Schenk, Chem Rev 2006 106 3338 3363 10.1021/cr050318f 16895331
9. Two-metal ion catalysis in enzymatic acyl- and phosphoryl-transfer reactions. N Sträter WN Lipscomb T Klabunde B Krebs, Angewandte Chemie-International Edition in English 1996 35 2024 2055 10.1002/anie.199620241
10. Purple Acid-Phosphatase - a Diiron Enzyme That Catalyzes a Direct Phospho Group Transfer to Water. EG Mueller MW Crowder BA Averill JR Knowles, J Am Chem Soc 1993 115 2974 2975 10.1021/ja00060a055
11. Studies on the Catalytic Mechanism of Pig Purple Acid-Phosphatase. CJ Wynne SE Hamilton DA Dionysius JL Beck J Dejersey, Arch Biochem Biophys 1995 319 133 141 10.1006/abbi.1995.1275 7771777
12. 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. M Merkx MWH Pinkse BA Averill, Biochemistry 1999 38 9914 9925 10.1021/bi9904454 10433698
13. Alkaline phosphatase revisited: Hydrolysis of alkyl phosphates. PJ O'Brien D Herschlag, Biochemistry 2002 41 3207 3225 10.1021/bi012166y 11863460
14. Mechanism of the Reaction of Different Phosphates with the Iron(Ii)Iron(Iii) Form of Purple Acid-Phosphatase from Porcine Uteri (Uteroferrin). MAS Aquino JS Lim AG Sykes, Journal of the Chemical Society-Dalton Transactions 1994 429 436 10.1039/dt9940000429
15. Spectroscopic characterization of a ternary phosphatase-substrate- fluoride complex. Mechanistic implications for dinuclear hydrolases. XD Wang RYN Ho AK Whiting L Que, J Am Chem Soc 1999 121 9235 9236 10.1021/ja990732v
16. Reactivity of M-II metal-substituted derivatives of pig purple acid phosphatase (Uteroferrin) with phosphate. MB Twitchett G Schenk MAS Aquino DTY Yiu TC Lau AG Sykes, Inorg Chem 2002 41 5787 5794 10.1021/ic020037f 12401084
17. Electron-nuclear double resonance spectroscopic evidence for a hydroxo-bridge nucleophile involved in catalysis by a dinuclear hydrolase. SK Smoukov L Quaroni XD Wang PE Doan BM Hoffman L Que, J Am Chem Soc 2002 124 2595 2603 10.1021/ja003169l 11890810
18. Phosphate forms an unusual tripodal complex with the Fe-Mn center of sweet potato purple acid phosphatase. G Schenk LR Gahan LE Carrington N Mitić M Valizadeh SE Hamilton J de Jersey LW Guddat, Proc Natl Acad Sci USA 2005 102 273 278 15625111 10.1073/pnas.0407239102
19. Structurally distinct active sites in the copper(II)-substituted aminopeptidases from Aeromonas proteolytica and Escherichia coli. B Bennett WE Antholine VM D'Souza GJ Chen L Ustinyuk RC Holz, J Am Chem Soc 2002 124 13025 13034 10.1021/ja026341p 12405829
20. Substrate-activated zinc binding of metallo-beta-lactamases - Physiological importance of the mononuclear enzymes. S Wommer S Rival U Heinz M Galleni JM Frere N Franceschini G Amicosante B Rasmussen R Bauer HW Adolph, J Biol Chem 2002 277 24142 24147 10.1074/jbc.M202467200 11967267
21. Properties of a Purple Phosphatase from Red Kidney Bean - a Zinc-Iron Metalloenzyme. JL Beck LA McConachie AC Summors WN Arnold J de Jersey B Zerner, Biochim Biophys Acta 1986 869 61 68
22. Binuclear metal centers in plant purple acid phosphatases: Fe-Mn in sweet potato and Fe-Zn in soybean. G Schenk YB Ge LE Carrington CJ Wynne IR Searle BJ Carroll S Hamilton J de Jersey, Arch Biochem Biophys 1999 370 183 189 10.1006/abbi.1999.1407 10510276
23. The active site of purple acid phosphatase from sweet potatoes (Ipomoea batatas) - Metal content and spectroscopic characterization. A Durmus C Eicken BH Sift A Kratel R Kappl J Huttermann B Krebs, Eur J Biochem 1999 260 709 716 10.1046/j.1432-1327.1999.00230.x 10102999
24. Iron-Containing Acid-Phosphatases - Comparison of Enzymes from Beef Spleen and Pig Allantoic Fluid. HD Campbell DA Dionysius DT Keough BE Wilson J de Jersey B Zerner, Biochem Biophys Res Commun 1978 82 615 620 10.1016/0006-291X(78)90919-1 666864
25. The Type-5, Acid-Phosphatase from Spleen of Humans with Hairy-Cell Leukemia - Purification, Properties, Immunological Characterization, and Comparison with Porcine Uteroferrin. CM Ketcham GA Baumbach FW Bazer RM Roberts, J Biol Chem 1985 260 5768 5776 3988771
26. Spectroscopic and Magnetic Studies of the Purple Acid-Phosphatase from Bovine Spleen. BA Averill JC Davis S Burman T Zirino J Sandersloehr TM Loehr JT Sage PG Debrunner, J Am Chem Soc 1987 109 3760 3767 10.1021/ja00246a039
27. Cloning, Sequence, and Developmental Expression of a Type-5, Tartrate-Resistant, Acid-Phosphatase of Rat Bone. B Ek-Rylander P Bill M Norgard S Nilsson G Andersson, J Biol Chem 1991 266 24684 24689 1722212
28. The highly exposed loop region in mammalian purple acid phosphatase controls the catalytic activity. EG Funhoff CHW Klaassen B Samyn J Van Beeumen BA Averill, Chem Bio Chem 2001 2 355 363 11828464
29. Purple acid phosphatases from bacteria: similarities to mammalian and plant enzymes. G Schenk MLJ Korsinczky DA Hume S Hamilton J de Jersey, Gene 2000 255 419 424 10.1016/S0378-1119(00)00305-X 11024303
30. Electrochemical Properties of the Diiron Core of Uteroferrin and Its Anion Complexes. DL Wang RC Holz SS David L Que MT Stankovich, Biochemistry 1991 30 8187 8194 10.1021/bi00247a014 1868093
31. Direct electrochemistry of porcine purple acid phosphatase (uteroferrin). PV Bernhardt G Schenk GJ Wilson, Biochemistry 2004 43 10387 10392 10.1021/bi0490338 15301537
32. Structure, function, and regulation of tartrate-resistant acid phosphatase. GW Oddie G Schenk NZ Angel N Walsh LW Guddat J de Jersey AI Cassady SE Hamilton DA Hume, Bone 2000 27 575 584 10.1016/S8756-3282(00)00368-9 11062342
33. Phosphotyrosyl peptides and analogues as substrates and inhibitors of purple acid phosphatases. M Valizadeh G Schenk K Nash GW Oddie LW Guddat DA Hume J de Jersey TR Burke S Hamilton, Arch Biochem Biophys 2004 424 154 162 10.1016/j.abb.2004.01.008 15047187
34. Properties of the Fe(Ii)-Fe(Iii) Derivative of Red Kidney Bean Purple Phosphatase - Evidence for a Binuclear Zn-Fe Center in the Native Enzyme. JL Beck J de Jersey B Zerner MP Hendrich PG Debrunner, J Am Chem Soc 1988 110 3317 3318 10.1021/ja00218a061
35. A purple acid phosphatase from sweet potato contains an antiferromagnetically coupled binuclear Fe-Mn center. G Schenk CL Boutchard LE Carrington CJ Noble B Moubaraki KS Murray J de Jersey GR Hanson S Hamilton, J Biol Chem 2001 276 19084 19088 10.1074/jbc.M009778200 11278566
36. Recombinant purple acid phosphatase isoform 3 from sweet potato is an enzyme with a diiron metal center. T Waratrujiwong B Krebs F Spener P Visoottiviseth, FEBS J 2006 273 1649 1659 10.1111/j.1742-4658.2006.05179.x 16623702
37. Structure, function and diversity of purple acid phosphatases. E Leung M Teixeira LW Guddat N Mitić G Schenk, Curr Topics Plant Biol 2007 8 21 31
38. Physical Characterization of 2-Iron Uteroferrin - Evidence for a Spin-Coupled Binuclear Iron Cluster. BC Antanaitis P Aisen HR Lilienthal, J Biol Chem 1983 258 3166 3172 6298226
39. Circular dichroism and magnetic circular dichroism studies of the mixed-valence binuclear non-heme iron active site in uteroferrin and its anion complexes. YS Yang JM McCormick EI Solomon, J Am Chem Soc 1997 119 11832 11842 10.1021/ja971896j
40. Crystal-Structure of a Purple Acid-Phosphatase Containing a Dinuclear Fe(Iii)-Zn(Ii) Active-Site. N Sträter T Klabunde P Tucker H Witzel B Krebs, Science 1995 268 1489 1492 10.1126/science.7770774 7770774
41. Mechanism of Fe(III)-Zn(II) purple acid phosphatase based on crystal structures. T Klabunde N Strater R Fröhlich H Witzel B Krebs, J Mol Biol 1996 259 737 748 10.1006/jmbi.1996.0354 8683579
42. Crystal structure of mammalian purple acid phosphatase. LW Guddat AS McAlpine D Hume S Hamilton J de Jersey JL Martin, Structure 1999 7 757 767 10.1016/S0969-2126(99)80100-2 10425678
43. Three-dimensional structure of a mammalian purple acid phosphatase at 2.2 angstrom resolution with a mu-(hydr)oxo bridged di-iron center. Y Lindqvist E Johansson H Kaija P Vihko G Schneider, J Mol Biol 1999 291 135 147 10.1006/jmbi.1999.2962 10438611
44. Crystal structure of a mammalian purple acid phosphatase. J Uppenberg F Lindqvist C Svensson B Ek-Rylander G Andersson, J Mol Biol 1999 290 201 211 10.1006/jmbi.1999.2896 10388567
45. Crystal structures of recombinant human purple acid phosphatase with and without an inhibitory conformation of the repression loop. N Sträter B Jasper M Scholte B Krebs AP Duff DB Langley RL Han BA Averill HC Freeman JM Guss, J Mol Biol 2005 351 233 246 10.1016/j.jmb.2005.04.014 15993892
46. Identification of mammalian-like purple acid phosphatases in a wide range of plants. G Schenk LT Guddat Y Ge LE Carrington DA Hume S Hamilton J de Jersey, Gene 2000 250 117 125 10.1016/S0378-1119(00)00186-4 10854785
47. Identification and molecular modeling of a novel, plant-like, human purple acid phosphatase. JU Flanagan AI Cassady G Schenk LW Guddat DA Hume, Gene 2006 377 12 20 10.1016/j.gene.2006.02.031 16793224
48. Magnetic susceptibility studies on the diiron forms of the metalloprotein purple acid phosphatase from bovine spleen and kidney bean. S Gehring P Fleischhauer M Behlendorf M Huber J Lorösch W Haase M Dietrich H Witzel R Locke B Krebs, Inorg Chim Acta 1996 252 13 17 10.1016/S0020-1693(96)05292-9
49. New insights into the mechanism of purple acid phosphatase through H-1 NMR spectroscopy of the recombinant human enzyme. A Dikiy EG Funhoff BA Averill S Ciurli, J Am Chem Soc 2002 124 13974 13975 10.1021/ja027195q 12440878
50. Inhibition studies of purple acid phosphatases: implications for the catalytic mechanism. TE Elliott N Mitić LR Gahan LW Guddat G Schenk, J Braz Chem Soc 2006 17 1558 1565 10.1590/S0103-50532006000800011
51. Inhibitor coordination interactions in the binuclear manganese cluster of arginase. E Cama S Pethe JL Boucher SF Han FA Emig DE Ash RE Viola D Mansuy DW Christianson, Biochemistry 2004 43 8987 8999 10.1021/bi0491705 15248756
52. Structure, properties and reactivity of the (FeFeIII)-Fe-II and (ZnFeIII)-Fe-II purple acid phosphatases. MB Twitchett AG Sykes, Eur J Inorg Chem 1999 2105 2115 10.1002/(SICI)1099-0682(199912)1999:12<2105::AID- EJIC2105>3.0.CO;2-2
53. Diesterase Activity and Substrate Binding in Purple Acid Phosphatases. RS Cox G Schenk N Mitić LR Gahan AC Hengge, J Am Chem Soc 2007 129 9550 9551 10.1021/ja072647q 17636903
54. The reaction mechanism of the Ga(III)Zn(II) derivative of uteroferrin and corresponding biomimetics. SJ Smith A Casellato KS Hadler N Mitić MJ Riley AJ Bortoluzzi B Szpoganicsz G Schenk A Neves LR Gahan, J Biol Inorg Chem 2007 12 1207 1220 10.1007/s00775-007-0286-y 17701232
55. Probing role of the divalent metal ion in uteroferrin using metal ion replacement and a comparison to isostructural biomimetics. G Schenk RA Peralta SC Batista AJ Bortoluzzi B Szpoganics AK Dick P Herrald GR Hanson RK Szilagyi MJ Riley LR Gahan A Neves, J Biol Inorg Chem 2008 13 139 155 10.1007/s00775-007- 0305-z 17938975
56. Redox Reactivity of the Binuclear Iron Active-Site of Porcine Purple Acid-Phosphatase (Uteroferrin). MAS Aquino AG Sykes, J Chemical Soc Dalton Trans 1994 683 687 10.1039/dt9940000683
57. Structure of the bacteriophage lambda Ser/Thr protein phosphatase with sulfate ion bound in two coordination modes. WC Voegtli DJ White NJ Reiter F Rusnak AC Rosenzweig, Biochemistry 2000 39 15365 15374 10.1021/bi0021030 11112522
58. 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. MWH Pinkse M Merkx BA Averill, Biochemistry 1999 38 9926 9936 10.1021/bi990446w 10433699
59. Direct observation of multiple protonation states in recombinant human purple acid phosphatase. EG Funhoff TE de Jongh BA Averill, J Biol Inorg Chem 2005 10 550 563 10.1007/s00775-005-0001-9 16096803
60. Spectroscopic characterization of soybean lipoxygenase-1 mutants: the role of second coordination sphere residues in the regulation of enzyme activity. G Schenk ML Neidig J Zhou TR Holman EI Solomon, Biochemistry 2003 42 7294 7302 10.1021/bi027380g 12809485
61. Structure-based rationalization of urease inhibition by phosphate: novel insights into the enzyme mechanism. S Benini WR Rypniewski KS Wilson S Ciurli S Mangani, J Biol Inorg Chem 2001 6 778 790 10.1007/s007750100254 11713685
62. An Unprecedented FeIII(-OH)ZnII Complex that Mimics the Structural and Functional Properties of Purple Acid Phosphatases. A Neves M Lanznaster AJ Bortoluzzi RA Peralta A Casellato EE Castellano P Herrald MJ Riley G Schenk, J Am Chem Soc 2007 129 7486 7487 10.1021/ja071184l 17518469
63. The finer things in X-ray diffraction data collection. JW Pflugrath, Acta Crystallogr D Biol Crystallogr 1999 55 1718 1725 10531521 10531521 10.1107/S090744499900935X
64. Rapid automated molecular replacement by evolutionary search. CR Kissinger DK Gehlhaar DB Fogel, Acta Crystallogr D Biol Crystallogr. 1999 55 484 491 10089360 10089360 10.1107/S0907444998012517
65. Crystallography & NMR system: A new software suite for macromolecular structure determination. AT Brünger PD Adams GM Clore WL DeLano P Gros RW Grosse-Kunstleve JS Jiang J Kuszewski M Nilges NS Pannu RJ Read LM Rice T Simonson GL Warren, Acta Crystallogr D Biol Crystallogr 1998 54 905 921 9757107 9757107 10.1107/S0907444998003254
66. Improved Methods for Building Protein Models in Electron-Density Maps and the Location of Errors in These Models. TA Jones JY Zou SW Cowan M Kjeldgaard, Acta Crystallogr A 1991 47 110 119 2025413 2025413 10.1107/S0108767390010224
67. WL DeLano, The PyMOL Molecular Graphics System DeLano Scientific, San Carlos, CA, USA 2002