The UDP-diacylglucosamine pyrophosphohydrolase LpxH In lipid a biosynthesis utilizes Mn2+ cluster for catalysis

Journal of Biological Chemistry

Volumn 288, Issue 38, 2013, Pages 26987-27001

  Young, Hayley E ^a   Donohue, Matthew P ^b   Smirnova, Tatyana I ^b   Smirnov, Alex I ^b   Zhou, Pei ^a  

^a DUKE UNIVERSITY   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONSERVED RESIDUES; HAEMOPHILUS INFLUENZAE; HYDROLASE ACTIVITIES; METAL-BINDING MOTIF; NOVEL ANTIBIOTICS; PHOSPHOESTER BONDS; STRUCTURAL INVESTIGATION; SURFACE-DILUTION KINETICS;

BIOCHEMISTRY; BIOSYNTHESIS; ENZYMES; ESCHERICHIA COLI; MANGANESE;

MANGANESE COMPOUNDS;

INORGANIC PYROPHOSPHATASE; LIPID A; MANGANESE; PYROPHOSPHOHYDROLASE LPXH; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME KINETICS; ESCHERICHIA COLI; GENE AMPLIFICATION; GENE OVEREXPRESSION; HAEMOPHILUS INFLUENZAE; LIPOGENESIS; MOLECULAR CLONING; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION;

ELECTRON PARAMAGNETIC RESONANCE (EPR); ENZYMES; LIPIDS; LIPOPOLYSACCHARIDE (LPS); METALLOENZYMES;

BACTERIAL PROTEINS; CATALYSIS; CLONING, MOLECULAR; GENE EXPRESSION; HAEMOPHILUS INFLUENZAE; LIPID A; MANGANESE; PYROPHOSPHATASES;

EID: 84884550173     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.497636     Document Type: Article

References (47)

1. Raetz, C. R., and Whitfield, C. (2002) Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71, 635-700
2. Raetz, C. R., Reynolds, C. M., Trent, M. S., and Bishop, R. E. (2007) Lipid A modification systems in Gram-negative bacteria. Annu. Rev. Biochem. 76, 295-329
3. Park, B. S., Song, D. H., Kim, H. M., Choi, B. S., Lee, H., and Lee, J. O. (2009) The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458, 1191-1195
4. Rietschel, E. T., Kirikae, T., Schade, F. U., Mamat, U., Schmidt, G., Loppnow, H., Ulmer, A. J., Zähringer, U., Seydel, U., and Di Padova, F. (1994) Bacterial endotoxin: molecular relationships of structure to activity and function. FASEB J. 8, 217-225
5. Russell, J. A. (2006) Management of sepsis. N. Engl. J. Med. 355, 1699-1713
6. Barb, A. W., and Zhou, P. (2008) Mechanism and inhibition of LpxC: an essential zinc-dependent deacetylase of bacterial lipid A synthesis. Curr. Pharm. Biotechnol. 9, 9-15
7. Opiyo, S. O., Pardy, R. L., Moriyama, H., and Moriyama, E. N. (2010) Evolution of the Kdo2-lipidAbiosynthesis in bacteria. BMCE vol. Biol. 10, 362
8. Babinski, K. J., Ribeiro, A. A., and Raetz, C. R. (2002) The Escherichia coli gene encoding the UDP-2, 3-diacylglucosamine pyrophosphatase of lipid A biosynthesis. J. Biol. Chem. 277, 25937-25946
9. Babinski, K. J., Kanjilal, S. J., and Raetz, C. R. (2002) Accumulation of the lipid A precursor UDP-2, 3-diacylglucosamine in an Escherichia coli mutant lacking the lpxH gene. J. Biol. Chem. 277, 25947-25956
10. Metzger, L. E., 4th, and Raetz, C. R. (2010) An alternative route for UDPdiacylglucosamine hydrolysis in bacterial lipid A biosynthesis. Biochemistry 49, 6715-6726
11. Mitić, N., Smith, S. J., Neves, A., Guddat, L. W., Gahan, L. R., and Schenk, G. (2006) The catalytic mechanisms of binuclear metallohydrolases. Chem. Rev. 106, 3338-3363
12. Cleland, W. W., and Hengge, A. C. (2006) Enzymatic mechanisms of phosphate and sulfate transfer. Chem. Rev. 106, 3252-3278
13. 2+-binding site of bacteriophage phosphoprotein phosphatase: effects of metal ligand mutations on electron paramagnetic resonance spectra and phosphatase activities. Biochemistry 40, 8918-8929
14. Zhuo, S., Clemens, J. C., Stone, R. L., and Dixon, J. E. (1994) Mutational analysis of a Ser/Thr phosphatase. Identification of residues important in phosphoesterase substrate binding and catalysis. J. Biol. Chem. 269, 26234-26238
15. Battistuzzi, G., Dietrich, M., Löcke, R., and Witzel, H. (1997) Evidence for a conserved binding motif of the dinuclear metal site in mammalian and plant purple acid phosphatases: 1H NMR studies of the di-iron derivative of the Fe (III) Zn (II) enzyme from kidney bean. Biochem. J. 323, 593-596
16. Ago, H., Oda, M., Takahashi, M., Tsuge, H., Ochi, S., Katunuma, N., Miyano, M., and Sakurai, J. (2006) Structural basis of the sphingomyelin phosphodiesterase activity in neutral sphingomyelinase from Bacillus cereus. J. Biol. Chem. 281, 16157-16167
17. Koonin, E. V. (1994) Conserved sequence pattern in a wide variety of phosphoesterases. Protein Sci. 3, 356-358
18. Lucast, L. J., Batey, R. T., and Doudna, J. A. (2001) Large-scale purification of a stable form of recombinant tobacco etch virus protease. BioTechniques 30, 544-546
19. Bligh, E. G., and Dyer, W. J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917
20. Radika, K., and Raetz, C. R. (1988) Purification and properties of lipid A disaccharide synthase of Escherichia coli. J. Biol. Chem. 263, 14859-14867
21. Belford, A. I., and Belford, R. L. (1995) Rapid quantitation from inhomogeneously broadened EPR spectra by a fast convolution algorithm. J. Magn. Reson. A 113, 65-73
22. Rusnak, F., Yu, L., Todorovic, S., and Mertz, P. (1999) Interaction of bacteriophage protein phosphatase with Mn (II): evidence for the formation of a [Mn (II)]2 cluster. Biochemistry 38, 6943-6952
23. Hayden, J. A., and Hendrich, M. P. (2010) EPR spectroscopy and catalase activity of manganese-bound DNA-binding protein from nutrient starved cells. J. Biol. Inorg. Chem. 15, 729-736
24. +: determination of the exchange constant and of the spin parameters for the S 1, 2, and 3 spin states. Chemistry 9, 4260-4268
25. Howard, T., Telser, J., and DeRose, V. J. (2000) An electron paramagnetic resonance study of Mn2 (H2O) (OAc) 4 (tmeda) 2 (tmeda N, N, N', N'-tetramethylethylenediamine): a model for dinuclear manganese enzyme active sites. Inorg. Chem. 39, 3379-3385
26. Mathur, P., Crowder, M., and Dismukes, G. C. (1987) Dimanganese (II) complexes of a septadentate ligand. Functional analogs of the manganese pseudocatalase. J. Am. Chem. Soc. 109, 5227-5233
27. +. Determination of the spin parameters for the S 1 and S 2 spin states. Inorg. Chem. 42, 4568-4578
28. Chakraborty, P., and Chandra, S. K. (1994) Synthesis, structure, EPR, and electrochemical studies of a μ2-phenoxo bridged manganese (II) dimer afforded by a binucleating macrocyclic ligand. Polyhedron 13, 683-687
29. Kessissoglou, D. P., Li, X., Butler, W. M., and Pecoraro, V. L. (1987) Mononuclear manganese (IV) complexes of hydroxyl-rich Schiff base ligands. Inorg. Chem. 26, 2487-2492
30. Mabad, B., Cassoux, P., Tuchagues, J. P., and Hendrickson, D. N. (1986) Manganese (II) complexes of polydentate Schiff bases. 1. Synthesis, characterization, magnetic properties, and molecular structure. Inorg. Chem. 25, 1420-1431
31. Mathur, P., and Dismukes, G. C. (1983) Models for the photosynthetic water oxidizing enzyme. 2. Electronic, magnetic, and EPR characterization of a binuclear manganese (II) semiquinone complex. J. Am. Chem. Soc. 105, 7093-7098
32. Gelasco, A., Kirk, M. L., Kampf, J. W., and Pecoraro, V. L. (1997) The [Mn (2) (2-OHsalpn) (2)] (2-, -, 0, +) system: Synthesis, structure, spectroscopy, and magnetism of the first structurally characterized dinuclear manganese series containing four distinct oxidation states. Inorg. Chem. 36, 1829-1837
33. Tzima, T. D., Ferentinos, E., Maganas, D., Melissas, V. S., Sanakis, Y., and Kyritsis, P. (2013) Electronic and magnetic properties of the binuclear [Mn2{(OPPh2) 2N}4] complex, as revealed by magnetometry, EPR and density functional broken-symmetry studies. Polyhedron 52, 706-712
34. Golombek, A. P., and Hendrich, M. P. (2003) Quantitative analysis of dinuclear manganese (II) EPR spectra. J. Magn. Reson. 165, 33-48
35. Epel, B., Schäfer, K. O., Quentmeier, A., Friedrich, C., and Lubitz, W. (2005) Multifrequency EPR analysis of the dimanganese cluster of the putative sulfate thiohydrolase SoxB of Paracoccus pantotrophus. J. Biol. Inorg. Chem. 10, 636-642
36. Aravind, L., and Koonin, E. V. (1998) Phosphoesterase domains associated with DNA polymerases of diverse origins. Nucleic Acids Res. 26, 3746-3752
37. Sharples, G. J., and Leach, D. R. (1995) Structural and functional similarities between the SbcCD proteins of Escherichia coli and the RAD50 and MRE11 (RAD32) recombination and repair proteins of yeast. Mol. Microbiol. 17, 1215-1217
38. Outten, C. E., and O'Halloran, T. V. (2001) Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292, 2488-2492
39. Dismukes, G. C. (1996) Manganese enzymes with binuclear active sites. Chem. Rev. 96, 2909-2926
40. Wehenkel, A., Bellinzoni, M., Schaeffer, F., Villarino, A., and Alzari, P. M. (2007) Structural and binding studies of the three-metal center in two mycobacterial PPM Ser/Thr protein phosphatases. J. Mol. Biol. 374, 890-898
41. Su, J., Schlicker, C., and Forchhammer, K. (2011) A third metal is required for catalytic activity of the signal-transducing protein phosphatase M tPphA. J. Biol. Chem. 286, 13481-13488
42. Rantanen, M. K., Lehtiö, L., Rajagopal, L., Rubens, C. E., and Goldman, A. (2007) Structure of Streptococcus agalactiae serine/threonine phosphatase. The subdomain conformation is coupled to the binding of a third metal ion. FEBS J. 274, 3128-3137
43. Mildvan, A. S., Xia, Z., Azurmendi, H. F., Saraswat, V., Legler, P. M., Massiah, M. A., Gabelli, S. B., Bianchet, M. A., Kang, L. W., and Amzel, L. M. (2005) Structures and mechanisms of Nudix hydrolases. Arch. Biochem. Biophys. 433, 129-143
44. Goldberg, J., Huang, H. B., Kwon, Y. G., Greengard, P., Nairn, A. C., and Kuriyan, J. (1995) Three-dimensional structure of the catalytic subunit of protein serine/threonine phosphatase-1. Nature 376, 745-753
45. Voegtli, W. C., White, D. J., Reiter, N. J., Rusnak, F., and Rosenzweig, A. C. (2000) Structure of the bacteriophage Ser/Thr protein phosphatase with sulfate ion bound in two coordination modes. Biochemistry 39, 15365-15374
46. Schenk, G., Carrington, L. E., Hamilton, S. E., De Jersey, J., and Guddat, L. W. (1999) Crystallization and preliminary x-ray diffraction data for a purple acid phosphatase from sweet potato. Acta Crystallogr. DBiol. Crystallogr. 55, 2051-2052
47. Hopfner, K. P., Karcher, A., Craig, L., Woo, T. T., Carney, J. P., and Tainer, J. A. (2001) Structural biochemistry and interaction architecture of the DNAdouble-strand break repair Mre11 nuclease and Rad50-ATPase. Cell 105, 473-485