Localization and characterization of prolipoprotein diacylglyceryl transferase (Lgt) critical in bacterial lipoprotein biosynthesis

Biochimie

Volumn 90, Issue 11-12, 2008, Pages 1647-1655

  Selvan, Anthonymuthu Tamil ^a   Sankaran, Krishnan ^a  

^a ANNA UNIVERSITY   (India)

Author keywords

Bacterial lipoprotein; Enzyme assay; Localization; Peptide substrate; Prolipoprotein diacylglyceryl transferase

Indexed keywords

LIPOPROTEIN; PROLIPOPROTEIN DIACYLGLYCERYLTRANSFERASE; SYNTHETIC PEPTIDE; TRANSFERASE; UNCLASSIFIED DRUG;

ARTICLE; ENZYME ANALYSIS; ENZYME KINETICS; ENZYME STABILITY; HYDROPHOBICITY; IONIC STRENGTH; NONHUMAN; PROTEIN MODIFICATION; PROTEIN SYNTHESIS; SOLUBILIZATION;

AMINO ACID SEQUENCE; BACTERIAL OUTER MEMBRANE PROTEINS; LIPOPROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN SORTING SIGNALS; STAPHYLOCOCCUS AUREUS; TRANSFERASES;

BACTERIA (MICROORGANISMS);

EID: 55349122529     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2008.06.005     Document Type: Article

References (49)

1. Babu M.M., Priya M.L., Selvan A.T., Madera M., Gough J., Aravind L., and Sankaran K. A database of bacterial lipoproteins (DOLOP) with functional assignments to predicted lipoproteins. J. Bacteriol. 188 (2006) 2761-2773
2. Sutcliffe I.C., and Russell R.R. Lipoproteins of gram-positive bacteria. J. Bacteriol. 177 (1995) 1123-1128
3. Hantke K., and Braun V. Covalent binding of lipid to protein. Diglyceride and amide-linked fatty acid at the N-terminal end of the murein-lipoprotein of the Escherichia coli outer membrane. Eur. J. Biochem. 34 (1973) 284-296
4. Kamalakkannan S., Murugan V., Jagannadham M.V., Nagaraj R., and Sankaran K. Bacterial lipid modification of proteins for novel protein engineering applications. Protein Eng. Des. Sel. 17 (2004) 721-729
5. Kamalakkannan S., Murugan V., and Sankaran K. Bacterial lipid modification of proteins and its potential applications. BIOforum Europe. 3 (2005) 44-47
6. Inukai M., Takeuchi M., Shimizu K., and Arai M. Mechanism of action of globomycin. J. Antibiot. (Tokyo) 31 (1978) 1203-1205
7. Dev I.K., and Ray P.H. Rapid assay and purification of a unique signal peptidase that processes the prolipoprotein from Escherichia coli B. J. Biol. Chem. 259 (1984) 11114-11120
8. BenMohamed L., Wechsler S.L., and Nesburn A.B. Lipopeptide vaccines - yesterday, today, and tomorrow, Lancet Infect. Dis. 2 (2002) 425-431
9. Radolf J.D., Arndt L.L., Akins D.R., Curetty L.L., Levi M.E., Shen Y., Davis L.S., and Norgard M.V. Treponema pallidum and Borrelia burgdorferi lipoproteins and synthetic lipopeptides activate monocytes/macrophages. J. Immunol. 154 (1995) 2866-2877
10. Erdile L.F., Brandt M.A., Warakomski D.J., Westrack G.J., Sadziene A., Barbour A.G., and Mays J.P. Role of attached lipid in immunogenicity of Borrelia burgdorferi OspA. Infect. Immun. 61 (1993) 81-90
11. Fariselli P., Finocchiaro G., and Casadio R. SPEPlip: the detection of signal peptide and lipoprotein cleavage sites. Bioinformatics 19 (2003) 2498-2499
12. Gonnet P., Rudd K.E., and Lisacek F. Fine-tuning the prediction of sequences cleaved by signal peptidase II: a curated set of proven and predicted lipoproteins of Escherichia coli K-12. Proteomics 4 (2004) 1597-1613
13. Juncker A.S., Willenbrock H., Von Heijne G., Brunak S., Nielsen H., and Krogh A. Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci. 12 (2003) 1652-1662
14. Sutcliffe I.C., and Harrington D.J. Pattern searches for the identification of putative lipoprotein genes in Gram-positive bacterial genomes. Microbiology 148 (2002) 2065-2077
15. Sankaran K., and Wu H.C. Lipid modification of bacterial prolipoprotein. Transfer of diacylglyceryl moiety from phosphatidylglycerol. J. Biol. Chem. 269 (1994) 19701-19706
16. Sankaran K., Gupta S.D., and Wu H.C. Modification of bacterial lipoproteins. Methods Enzymol. 250 (1995) 683-697
17. Sankaran K., Gan K., Rash B., Qi H., Wu H.C., and Rick P.D. Roles of Histidine-103 and Tyrosine-235 in the function of the prolipoprotein diacylglyceryl transferase of Escherichia coli. J. Bacteriol. 179 (1997) 2944-2948
18. Hussain M., Ichihara S., and Mizushima S. Accumulation of glyceride-containing precursor of the outer membrane lipoprotein in the cytoplasmic membrane of Escherichia coli treated with globomycin. J. Biol. Chem. 255 (1980) 3707-3712
19. Tokunaga H., and Wu H.C. Studies on the modification and processing of prolipoprotein in Escherichia coli. Effects of structural alterations in prolipoprotein on its maturation in wild type and lpp mutants. J. Biol. Chem. 259 (1984) 6098-6104
20. Sankaran K., and Wu H.C. Bacterial prolipoprotein signal peptidase. Methods Enzymol. 248 (1995) 169-180
21. Munoa F.J., Miller K.W., Beers R., Graham M., and Wu H.C. Membrane topology of Escherichia coli prolipoprotein signal peptidase (signal peptidase II). J. Biol. Chem. 266 (1991) 17667-17672
22. Gupta S.D., and Wu H.C. Identification and subcellular localization of apolipoprotein N-acyltransferase in Escherichia coli. FEMS Microbiol. Lett. 62 (1991) 37-41
23. Gupta S.D., Dowhan W., and Wu H.C. Phosphatidylethanolamine is not essential for the N-acylation of apolipoprotein in Escherichia coli. J. Biol. Chem. 266 (1991) 9983-9986
24. Tjalsma H., Kontinen V.P., Pragai Z., Wu H.C., Meima R., Venema G., Bron S., Sarvas M., and Van Dijl J.M. The role of lipoprotein processing by signal peptidase II in the Gram-positive eubacterium Bacillus subtilis. Signal peptidase II is required for the efficient secretion of alpha-amylase, a non-lipoprotein. J. Biol. Chem. 274 (1999) 1698-1707
25. Leskela S., Wahlstrom E., Kontinen V.P., and Sarvas M. Lipid modification of prelipoproteins is dispensable for growth but essential for efficient protein secretion in Bacillus subtilis: characterization of the Lgt gene. Mol. Microbiol. 31 (1999) 1075-1085
26. Beermann C., Lochnit G., Geyer R., Groscurth P., and Filgueira L. The lipid component of lipoproteins from Borrelia burgdorferi: structural analysis, antigenicity, and presentation via human dendritic cells. Biochem. Biophys. Res. Commun. 267 (2000) 897-905
27. Narita S., and Tokuda H. An ABC transporter mediating the membrane detachment of bacterial lipoproteins depending on their sorting signals. FEBS Lett. 580 (2006) 1164-1170
28. Yamaguchi K., Yu F., and Inouye M. A single amino acid determinant of the membrane localization of lipoproteins in E. coli. Cell 53 (1988) 423-432
29. Gan K., Sankaran K., Williams M., Aldea M., Rudd K., Kushner S., and Wu H.C. The umpA gene of Escherichia coli encodes phosphatidylglycerol:prolipoprotein diacylglyceryl transferase (lgt) and regulates thymidylate synthase levels through translational coupling. J. Bacteriol. 177 (1995) 1879-1882
30. Yamagata H., Daishima K., and Mizushima S. Cloning and expression of a gene coding for the prolipoprotein signal peptidase of Escherichia coli. FEBS Lett. 158 (1983) 301-304
31. Witke C., and Gotz F. Cloning and nucleotide sequence of the signal peptidase II (lsp)-gene from Staphylococcus carnosus. FEMS Microbiol. Lett. 126 (1995) 233-239
32. Vidal-Ingigliardi D., Lewenza S., and Buddelmeijer N. Identification of essential residues in apolipoprotein N-acyl transferase, a member of the CN hydrolase family. J. Bacteriol. 189 (2007) 4456-4464
33. Petit C.M., Brown J.R., Ingraham K., Bryant A.P., and Holmes D.J. Lipid modification of prelipoproteins is dispensable for growth in vitro but essential for virulence in Streptococcus pneumoniae. FEMS Microbiol. Lett 200 (2001) 229-233
34. Stoll H., Dengjel J., Nerz C., and Gotz F. Staphylococcus aureus deficient in lipidation of prelipoproteins is attenuated in growth and immune activation. Infect. Immun. 73 (2005) 2411-2423
35. Baumgartner M., Karst U., Gerstel B., Loessner M., Wehland J., and Jansch L. Inactivation of Lgt allows systematic characterization of lipoproteins from Listeria monocytogenes. J. Bacteriol. 189 (2007) 313-324
36. Daley D.O., Rapp M., Granseth E., Melén K., Drew D.G., and Heijne V. Global topology analysis of the Escherichia coli inner membrane proteome. Science 308 (2005) 1321-1323
37. Qi H., Sankaran K., Gan K., and Wu H.C. Structure-function relationship of bacterial prolipoprotein diacylglyceryl transferase: functionally significant conserved regions. J. Bacteriol. 177 (1995) 6820-6824
38. Babu M.M., and Sankaran K. DOLOP - database of bacterial lipoproteins. Bioinformatics 18 (2002) 641-643
39. Kyte J., and Doolittle R.F. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157 (1982) 105-132
40. Ellman G. Tissue sulfhydryl groups. Arch. Biochem. Biophys. 82 (1959) 70-77
41. Schägger H., and Jagow G.V. Tricine-sodium dodecyl sulfate polyacrylamide gel electrophoresis for the separation of proteins in the range from 1-100 kDa. Anal. Biochem. 166 (1987) 368-379
42. Short S.A., and White D.C. Metabolism of phosphatidylglycerol, lysylphosphatidylglycerol, and cardiolipin of Staphylococcus aureus. J. Bacteriol. 108 (1971) 219-226
43. Bligh E., and Dryer W. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37 (1959) 911-917
44. Ames B.N., and Dubin D.T. The role of polyamines in the neutralization of bacteriophage deoxyribonucleic acid. J. Biol. Chem. 235 (1960) 769-775
45. Kresze G.B., Steber L., Oesterhelt D., and Lynen F. Reaction of yeast fatty acid synthetase with iodoacetamide. Eur. J. Biochem. 79 (1977) 181-190
46. Stepka W. Identification of amino acids by paper chromatography. Methods Enzymol. 3 (1975) 504-528
47. Sims R.P.A., and Larose J.A.G. The use of iodine vapor as a general detecting agent in the thin layer chromatography of lipids. J. Am. Oil Chem. Soc. 39 (1962) 232
48. Tokunaga M., Loranger J.M., and Wu H.C. Prolipoprotein modification and processing enzymes in Escherichia coli. J. Biol. Chem. 259 (1984) 3825-3830
49. Hayashi S., and Wu H.C. In: Hooper N.M., and Turner A.J. (Eds). Lipid Modification of Proteins: A Practical Approach (1992), Oxford University Press, Eynsham, UK 261-285