Structural basis of lipid binding for the membrane-embedded tetraacyldisaccharide-1-phosphate 4′-kinase LpxK

Journal of Biological Chemistry

Volumn 289, Issue 35, 2014, Pages 24059-24068

  Emptage, Ryan P ^a   Tonthat, Nam K ^a   York, John D ^b   Schumacher, Maria A ^a   Zhou, Pei ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; MOLECULES; SUBSTRATES;

BIOSYNTHETIC PATHWAY; GRAM-NEGATIVE PATHOGENS; HYDROPHOBIC MEMBRANE; LIPID MODIFICATIONS; MEMBRANE-BOUND ENZYMES; SMALL MOLECULE INHIBITOR; STEADY-STATE KINETICS; STRUCTURAL TEMPLATES;

ENZYMES;

GLUCOSAMINE; LIPID A; PHOSPHATE; PHOSPHOTRANSFERASE; PROTEIN LPXK; TETRAACYLDISACCHARIDE 1 PHOSPHATE 4' KINASE; UNCLASSIFIED DRUG; LIPID; MEMBRANE PROTEIN; PROTEIN BINDING; TETRAACYLDISACCHARIDE 4'-KINASE;

AMINO TERMINAL SEQUENCE; AQUIFEX AEOLICUS; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM MUTANT; BINDING AND RELATED PHENOMENA; BINDING KINETICS; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CRYSTAL STRUCTURE; ENZYME BINDING; ESCHERICHIA COLI; LIPID BINDING; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; STEADY STATE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; GENE SILENCING; GENETIC COMPLEMENTATION; GENETICS; KINETICS; METABOLISM; POINT MUTATION; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; GENE KNOCKDOWN TECHNIQUES; GENETIC COMPLEMENTATION TEST; KINETICS; LIPIDS; MEMBRANE PROTEINS; MODELS, MOLECULAR; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); POINT MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 84906857850     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.589986     Document Type: Article

References (37)

1. Raetz, C. R., Guan, Z., Ingram, B. O., Six, D. A., Song, F., Wang, X., and Zhao, J. (2009) Discovery of new biosynthetic pathways: the lipid A story. J. Lipid Res. 50, S103-S108
2. Raetz, C. R., and Whitfield, C. (2002) Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71, 635-700 (Pubitemid 34800232)
3. 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
4. Ray, B. L., and Raetz, C. R. (1987) The biosynthesis of gram-negative endotoxin. A novel kinase in Escherichia coli membranes that incorporates the 4′-phosphate of lipid A. J. Biol. Chem. 262, 1122-1128 (Pubitemid 17028423)
5. Garrett, T. A., Kadrmas, J. L., and Raetz, C. R. (1997) Identification of the gene encoding the Escherichia coli lipid A 4′-kinase: facile phosphorylation of endotoxin analogs with recombinant LpxK. J. Biol. Chem. 272, 21855-21864 (Pubitemid 27382802)
6. Emptage, R. P., Daughtry, K. D., Pemble, C. W., 4th, and Raetz, C. R. (2012) Crystal structure of LpxK, the 4′-kinase of lipid A biosynthesis and atypical P-loop kinase functioning at the membrane interface. Proc. Natl. Acad. Sci. U.S.A. 109, 12956-12961
7. Emptage, R. P., Pemble, C. W., 4th, York, J. D., Raetz, C. R., and Zhou, P. (2013) Mechanistic characterization of the tetraacyldisaccharide-1-phosphate 4′-kinase LpxK involved in lipid A biosynthesis. Biochemistry 52, 2280-2290
8. Punta, M., Coggill, P. C., Eberhardt, R. Y., Mistry, J., Tate, J., Boursnell, C., Pang, N., Forslund, K., Ceric, G., Clements, J., Heger, A., Holm, L., Sonnhammer, E. L., Eddy, S. R., Bateman, A., and Finn, R. D. (2012) The Pfam protein families database. Nucleic Acids Res. 40, D290-D301
9. Cheek, S., Zhang, H., and Grishin, N. V. (2002) Sequence and structure classification of kinases. J. Mol. Biol. 320, 855-881 (Pubitemid 34729411)
10. Leipe, D. D., Koonin, E. V., and Aravind, L. (2003) Evolution and classification of P-loop kinases and related proteins. J. Mol. Biol. 333, 781-815 (Pubitemid 37268019)
11. Plötz, B. M., Lindner, B., Stetter, K. O., and Holst, O. (2000) Characterization of a novel lipid A containing D-galacturonic acid that replaces phosphate residues. The structure of the lipid a of the lipopolysaccharide from the hyperthermophilic bacterium Aquifex pyrophilus. J. Biol. Chem. 275, 11222-11228 (Pubitemid 30212767)
12. Mamat, U., Schmidt, H., Munoz, E., Lindner, B., Fukase, K., Hanuszkiewicz, A., Wu, J., Meredith, T. C., Woodard, R. W., Hilgenfeld, R., Mesters, J. R., and Holst, O. (2009) WaaA of the hyperthermophilic bacterium Aquifex aeolicus is a monofunctional 3-deoxy-D-manno-oct-2-ulosonic acid transferase involved in lipopolysaccharide biosynthesis. J. Biol. Chem. 284, 22248-22262
13. Sambrook, J. G., and Russell, D. W. (2001). Molecular Cloning: A Laboratory Manual, 3rd Ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
14. Inoue, H., Nojima, H., and Okayama, H. (1990) High efficiency transformation of Escherichia coli with plasmids. Gene 96, 23-28
15. Guzman, L. M., Belin, D., Carson, M. J., and Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177, 4121-4130
16. Garrett, T. A., Que, N. L., and Raetz, C. R. (1998) Accumulation of a lipid A precursor lacking the 4′-phosphate following inactivation of the Escherichia coli lpxK gene. J. Biol. Chem. 273, 12457-12465 (Pubitemid 28240619)
17. Hamilton, C. M., Aldea, M., Washburn, B. K., Babitzke, P., and Kushner, S. R. (1989) New method for generating deletions and gene replacements in Escherichia coli. J. Bacteriol. 171, 4617-4622 (Pubitemid 19209055)
18. Bachmann, B. J. (1972) Pedigrees of some mutant strains of Escherichia coli K-12. Bacteriol. Rev. 36, 525-557
19. Miroux, B., and Walker, J. E. (1996) Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260, 289-298 (Pubitemid 26254109)
20. Chung, H. S., and Raetz, C. R. (2010) Interchangeable domains in the Kdo transferases of Escherichia coli and Haemophilus influenzae. Biochemistry 49, 4126-4137
21. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
22. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc-Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221
23. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12-21
24. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921
25. Ohto, U., Fukase, K., Miyake, K., and Satow, Y. (2007) Crystal structures of human MD-2 and its complex with antiendotoxic lipid IVa. Science 316, 1632-1634
26. Yoon, S. I., Hong, M., Han, G. W., and Wilson, I. A. (2010) Crystal structure of soluble MD-1 and its interaction with lipid IVa. Proc. Natl. Acad. Sci. U.S.A. 107, 10990-10995
27. 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
28. Ohto, U., Fukase, K., Miyake, K., and Shimizu, T. (2012) Structural basis of species-specific endotoxin sensing by innate immune receptor TLR4/ MD-2. Proc. Natl. Acad. Sci. U.S.A. 109, 7421-7426
29. Metzger, L. E., 4th, Lee, J. K., Finer-Moore, J. S., Raetz, C. R., and Stroud, R. M. (2012) LpxI structures reveal how a lipid A precursor is synthesized. Nat. Struct. Mol. Biol. 19, 1132-1138
30. Wang, Z., Min, X., Xiao, S. H., Johnstone, S., Romanow, W., Meininger, D., Xu, H., Liu, J., Dai, J., An, S., Thibault, S., and Walker, N. (2013) Molecular basis of sphingosine kinase 1 substrate recognition and catalysis. Structure 21, 798-809
31. Lemmon, M. A. (2008) Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell Biol. 9, 99-111
32. Stahelin, R. V. (2009) Lipid binding domains: more than simple lipid effectors. J. Lipid Res. 50, S299-S304
33. Moravcevic, K., Oxley, C. L., and Lemmon, M. A. (2012) Conditional peripheral membrane proteins: facing up to limited specificity. Structure 20, 15-27
34. Trésaugues, L., Silvander, C., Flodin, S., Welin, M., Nyman, T., Gräslund, S., Hammarström, M., Berglund, H., and Nordlund, P. (2014) Structural basis for phosphoinositide substrate recognition, catalysis, and membrane interactions in human inositol polyphosphate 5-phosphatases. Structure 22, 744-755
35. Huang, C. Y., Shih, H. W., Lin, L. Y., Tien, Y. W., Cheng, T. J., Cheng, W. C., Wong, C. H., and Ma, C. (2012) Crystal structure of Staphylococcus aureus transglycosylase in complex with a lipid II analog and elucidation of peptidoglycan synthesis mechanism. Proc. Natl. Acad. Sci. U.S.A. 109, 6496-6501
36. Lavogina, D., Enkvist, E., and Uri, A. (2010) Bisubstrate inhibitors of protein kinases: from principle to practical applications. ChemMedChem 5, 23-34
37. Lienhard, G. E., and Secemski, I. I. (1973) P1, P5-Di(adenosine-5′) pentaphosphate, a potent multisubstrate inhibitor of adenylate kinase. J. Biol. Chem. 248, 1121-1123