Crystal structure of phosphatidylglycerophosphatase (PGPase), a putative membrane-bound lipid phosphatase, reveals a novel binuclear metal binding site and two "proton wires"

Proteins: Structure, Function and Genetics

Volumn 64, Issue 4, 2006, Pages 851-862

  Kumaran, Desigan ^a   Bonanno, Jeffrey B ^b   Burley, Stephen K ^b   Swaminathan, Subramanyam ^a  

^a BROOKHAVEN NATIONAL LABORATORY   (United States)

^b SGX Pharmaceuticals Inc   (United States)

Author keywords

Binuclear metal site; Lipid metabolism; PGPase; Phosphatase; Proton wires

Indexed keywords

CALCIUM ION; LIPID PHOSPHATASE; MAGNESIUM ION; METAL ION; PHOSPHATASE; PHOSPHATIDYLGLYCEROPHOSPHATASE; PROTON; UNCLASSIFIED DRUG; CALCIUM; MAGNESIUM;

ARTICLE; BINDING SITE; CATALYSIS; CHANNEL GATING; CRYSTAL STRUCTURE; LIPID METABOLISM; LISTERIA MONOCYTOGENES; MEMBRANE BINDING; METAL BINDING; OLIGOMERIZATION; PRIORITY JOURNAL; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; CRYSTALLIZATION; ENZYMOLOGY; HYDROGEN BOND; MOLECULAR GENETICS; PROTEIN QUATERNARY STRUCTURE; SEQUENCE ALIGNMENT; X RAY CRYSTALLOGRAPHY;

LISTERIA MONOCYTOGENES;

AMINO ACID SEQUENCE; BINDING SITES; CALCIUM; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; HYDROGEN BONDING; LISTERIA MONOCYTOGENES; MAGNESIUM; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHORIC MONOESTER HYDROLASES; PROTEIN STRUCTURE, QUATERNARY; PROTONS; SEQUENCE ALIGNMENT;

EID: 33748442330     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.21039     Document Type: Article

References (58)

1. Chang YY, Kennedy EP. Phosphatidyl glycerophosphate phosphatase. J Lipid Res 1967;8:456-462.
2. Dowhan W, Funk CR. Phosphatidylglycerophosphate phosphatase from Escherichia coli. Methods Enzymol 1992;209:224-230.
3. Hagio M, Sakurai I, Sato S, Kato T, Tabata S, Wada H. Phosphatidylglycerol is essential for the development of thylakoid membranes in Arabidopsis thaliana. Plant Cell Physiol 2002;43:1456-1464.
4. Hirschberg CB, Kennedy EP. Mechanism of the enzymatic synthesis of cardiolipin in Escherichia coli. Proc Natl Acad Sci USA 1972;69:648-651.
5. Chattopadhyay PK, Lai JS, Wu HC. Incorporation of phosphatidylglycerol into murein lipoprotein in intact cells of Salmonella typhimurium by phospholipid vesicle fusion. J Bacteriol 1979;137:309-312.
6. Schulman H, Kennedy EP. Relation of turnover of membrane phospholipids to synthesis of membrane-derived oligosaccharides of Escherichia coli. J Biol Chem 1977;252:4250-4255.
7. Kusters R, Breukink E, Gallusser A, Kuhn A, de Kruijff B. A dual role for phosphatidylglycerol in protein translocation across the Escherichia coli inner membrane. J Biol Chem 1994;269:1560-1563.
8. Lill R, Dowhan W, Wickner W. The ATPase activity of SecA is regulated by acidic phospholipids, SecY, and the leader and mature domains of precursor proteins. Cell 1990;60:271-280.
9. Raetz CR, Dowhan W. Biosynthesis and function of phospholipids in Escherichia coli. J Biol Chem 1990;265:1235-1238.
10. Kanfer J, Kennedy EP. Metabolism and function of bacterial lipids. I. Metabolism of phospholipids in Escherichia coli B. J Biol Chem 1963;238:2919-2922.
11. Kanfer J, Kennedy EP. Metabolism and function of bacterial lipids. Ii. Biosynthesis of phospholipids in Escherichia coli. J Biol Chem 1964;239:1720-1726.
12. Icho T, Raetz CR. Multiple genes for membrane-bound phosphatases in Escherichia coli and their action on phospholipid precursors. J Bacteriol 1983;153:722-730.
13. Funk CR, Zimniak L, Dowhan W. The pgpA and pgpB genes of Escherichia coli are not essential: evidence for a third phosphatidylglycerophosphate phosphatase. J Bacteriol 1992;174:205-213.
14. Icho T. Membrane-bound phosphatases in Escherichia coli: sequence of the pgpB gene and dual subcellular localization of the pgpB product. J Bacteriol 1988;170:5117-5124.
15. Terwilliger TC, Berendzen J. Automated structure solution for MIR and MAD. Acta Crystallogr D Biol Crystallogr 1997;55:849-861.
16. Bricogne G, Vonrhein C, Flensburg C, Schiltz M, Paciorek W. Generation, representation and flow of phase information in structure determination: Recent developments in and around SHARP 2.0. Acta Crystallogr D Biol Crystallogr 2003;59:2023-2030.
17. De La Fortelle E, Bricogne G. Maximum-likelihood heavy atom parameter refinement in the MIR and MAD methods. Methods Enzymol 1997;276:472-493.
18. Perrakis A, Morris R, Lamzin VS. Automated protein model building combined with iterative structure refinement. Nat Struct Biol 1999;6:458-463.
19. Jones TA. A graphics model building and refinement system for macromolecules. J Appl Crystallogr 1978;11:268-272.
20. Jones TA, Zou J, Cowtan S, Kjeldgaard M. Improved methods in building protein models in electron density map and the location of errors in these models. Acta Crystallogr A 1991;47:110-119.
21. Brunger AT, Adams PD, Clore GM, Delano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 1998;54:905-921.
22. Sander C, Schneider R. Database of homology-derived protein structures and the structural meaning of sequence alignment. Proteins 1991;9:56-68.
23. Harding MM. Geometry of metal-ligand interactions in proteins. Acta Crystallogr D Biol Crystallogr 2001;57:401-411.
24. Harding MM. The geometry of metal-ligand interactions relevant to proteins. Acta Crystallogr D Biol Crystallogr 1999;55:1432-1443.
25. Heikinheimo P, Tuominen V, Ahonen A-K, Teplyakov A, Cooperman BS, Baykov AA, Lahti R, et al. Toward a quantum-mechanical description of metal-assisted phophoryl transfer in pyrophosphatase. Proc Natl Acad Sci, USA 2001;98:3121-26.
26. Guddat LW, McAlpine AS, Hume D, Hamilton S, de Jersey J, Martin JL. Crystal structure of mammalian purple acid phosphatase. Structure Fold Des 1999;7:757-767.
27. 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.
28. Lindqvist Y, Johansson E, Kaija H, Vihko P, Schneider G. Three-dimensional structure of a mammalian purple acid phosphatase at 2.2 Å resolution with a mu-(hydr)oxo bridged di-iron center. J Mol Biol 1999;291:135-147.
29. Schenk G, Gahan LR, Carrington LE, Mitic N, Valizadeh M, Hamilton SE, de Jersey J, et al. 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.
30. Strater N, Klabunde T, Tucker P, Witzel H, Krebs B. Crystal structure of a purple acid phosphatase containing a dinuclear Fe(III)-Zn(II) active site. Science 1995;268:1489-1492.
31. 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.
32. York JD, Ponder JW, Chen ZW, Mathews FS, Majerus PW. Crystal structure of inositol polyphosphate 1-phosphatase at 2.3-Å resolution. Biochemistry 1994;33:13164-13171.
33. Swingle MR, Honkanen RE, Ciszak EM. Structural basis for the catalytic activity of human serine/threonine protein phosphatase-5. J Biol Chem 2004;279:33992-33999.
34. III purple acid phosphatases. Eur J Inorg Chem 1999;1999:2105-2115.
35. Koonin EV. Conserved sequence pattern in a wide variety of phosphoesterases. Protein Sci 1994;3:356-358.
36. Zhuo S, Clemens JC, Stone RL, Dixon JE. Mutational analysis of a Ser/Thr phosphatase. Identification of residues important in phosphoesterase substrate binding and catalysis. J Biol Chem 1994;269:26234-2638.
37. Knofel T, Strater N. Mechanism of hydrolysis of phosphate esters by the dimetal center of 5′-nucleotidase based on crystal structures. J Mol Biol 2001;309:239-254.
38. Knofel T, Strater N. X-ray structure of the Escherichia coli periplasmic 5′-nucleotidase containing a dimetal catalytic site. Nat Struct Biol 1999;6:448-453.
39. Agre P, Kozono D. Aquaporin water channels: molecular mechanisms for human diseases. FEBS Lett 2003;555:72-78.
40. de Groot BL, Grubmuller H. The dynamics and energetics of water permeation and proton exclusion in aquaporins. Curr Opin Struct Biol 2005;15:176-183.
41. Pomes R, Roux B. Structure and dynamics of a proton wire: a theoretical study of H+ translocation along the single-file water chain in the gramicidin A channel. Biophys J 1996;71:19-39.
42. Baciou L, Michel H. Interruption of the water chain in the reaction center from Rhodobacter sphaeroides reduces the rates of the proton uptake and of the second electron transfer to QB. Biochemistry 1995;34:7967-7972.
43. Ermler U, Fritzsch G, Buchanan SK, Michel H. Structure of the photosynthetic reaction centre from Rhodobacter sphaeroides at 2.65 Å resolution: cofactors and protein-cofactor interactions. Structure 1994;2:925-936.
44. Kandt C, Gerwert K, Schlitter J. Water dynamics simulation as a tool for probing proton transfer pathways in a heptahelical membrane protein. Proteins 2005;58:528-537.
45. Lanyi JK, Luecke H. Bacteriorhodopsin. Curr Opin Struct Biol 2001;11:415-419.
46. Luecke H, Richter HT, Lanyi JK. Proton transfer pathways in bacteriorhodopsin at 2.3 Å resolution. Science 1998;280:1934-1937.
47. Martinez SE, Huang D, Ponomarev M, Cramer WA, Smith JL. The heme redox center of chloroplast cytochrome f is linked to a buried five-water chain. Protein Sci 1996;5:1081-1092.
48. Martinez SE, Huang D, Szczepaniak A, Cramer WA, Smith JL. Crystal structure of chloroplast cytochrome f reveals a novel cytochrome fold and unexpected heme ligation. Structure 1994;2:95-105.
49. Ponamarev MV, Cramer WA. Perturbation of the internal water chain in cytochrome f of oxygenic photosynthesis: loss of the concerted reduction of cytochromes f and b6. Biochemistry 1998;37:17199-17208.
50. Iwata S, Ostermeier C, Ludwig B, Michel H. Structure at 2.8 resolution of cytochrome c oxidase from denitrificans. Nature 1995;376:660-669.
51. Seibold SA, Mills DA, Ferguson-Miller S, Cukier RI. Water chain formation and possible proton pumping routes in Rhodobacter sphaeroides cytochrome c oxidase: a molecular dynamics comparison of the wild type and R481K mutant. Biochemistry 2005;44:10475-10485.
52. Wilkstrom M, Verkhovsky MI, Hummer G. Water-gated mechanism of proton translocation by cytochrome c oxidase. Biochim Biophys Acta 2003;1604:61-65.
53. Pomes R, Roux B. Molecular mechanism of H+ conduction in the single-file water chain of the gramicidin channel. Biophys J 2002;82:2304-23016.
54. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994;22:4673-4680.
55. Esnouf RM. Further additions to MolScript version 1.4, including reading and contouring of electron-density maps. Acta Crystallogr D Biol Crystallogr 1999;55:938-940.
56. Kraulis PJ. MOLSCRIPT: a program to produce both detailed and schematic plots of proteins. J Appl Crystallogr 1991;24:946-950.
57. Merritt EA. Raster3D Version 2.0. A program for photorealistic molecular graphics. Acta Crystallogr D Biol Crystallogr 1994;50:869-873.
58. Nicholls A, Sharp KA, Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 1991;11:281-296.