Biosynthesis of the glycolipid anchor in lipoteichoic acid of Staphylococcus aureus RN4220: Role of YpfP, the diglucosyldiacylglycerol synthase

Journal of Bacteriology

Volumn 183, Issue 11, 2001, Pages 3506-3514

  Kiriukhin, Michael Y ^a,c   Debabov, Dmitri V ^a,d   Shinabarger, Dean L ^b   Neuhaus, Francis C ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b PFIZER INC   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^d Advanced Medicine Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; BACTERIAL ENZYME; CHLORAMPHENICOL; DIACYLGLYCEROL; DIGLUCOSYLDIACYLGLYCEROL SYNTHASE; GLUCOSE; GLYCINE; GLYCOLIPID; LIPOTEICHOIC ACID; PHOSPHATE; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GROWTH; ESCHERICHIA COLI; GENE EXPRESSION; LIPOGENESIS; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS;

ANIMALS; BACTERIAL PROTEINS; ESCHERICHIA COLI; GLUCOSE; GLUCOSYLTRANSFERASES; GLYCOLIPIDS; GLYCOSYLTRANSFERASES; LIPOPOLYSACCHARIDES; MICE; MICROSCOPY, ELECTRON, SCANNING; MUTATION; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; TEICHOIC ACIDS; VIRULENCE;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; FELIS CATUS; LURIA; POSIBACTERIA; STAPHYLOCOCCUS AUREUS;

EID: 0035026895     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.183.11.3506-3514.2001     Document Type: Article

References (55)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Archibald, A. R., J. Baddiley, and S. Heptinstall. 1973. The alanine ester content and magnesium binding capacity of walls of Staphylococcus aureus H grown at different pH values. Biochim. Biophys. Acta 291:629-634.
3. Baird-Parker, A. C. 1962. An improved diagnostic and selective medium for isolating coagulase positive staphylococci. J. Appl. Bacteriol. 25:12-19.
4. Bierbaum, G., and H.-G. Sahl. 1991. Induction of autolysis of Staphylucoccus simulans 22 by Pep5 and nisin and influence of the catioric peptides on the activity of the autolytic enzymes, p 386-396. In G. Jung and H.-G. Sahl (ed.), Nisin and novel lantibiotics. ESCOM, Leiden, The Netherlands.
5. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911-917.
6. Boaretti, M., P. Canepari, M. M. Lleò, and G. Satta. 1993. The activity of daptomycin on Enterococcux faecium protoplasts: indirect evidence supporting a novel mode of action on lipoteichoic acid synthesis. J. Antimicrob. Chemother. 31:227-235.
7. Boyd, D. A., D. G. Cvitkovitch, A. S. Bleiweis, M. Y. Kiriukhin, D. V. Debabov, F. C. Neuhaus, and I. R. Hamilton. 2000. Defects in D-alanyl-lipoteichoic acid synthesis in Streptococcus mutans results in acid sensitivity. J. Bacteriol. 182:6055-6065.
8. Brautigan, V. M., W. C. Childs III, and F. C. Neuhaus. 1981. Biosynthesis of D-alanyl-lipoteichoic acid in Lactobacillus casei: D-alanyl-lipophilic compounds as intermediates. J. Bacteriol. 146:239-250.
9. Button, D., and N. L. Hemmings. 1976. Teichoic acids and lipids associated with the membrane of a Bacillus licheniformis mutant and the membrane lipids of the parental strain. J. Bacteriol. 128:149-156.
10. Childs, W. C., III, and F. C. Neuhaus. 1980. Biosynthesis of D-alanyl-lipoteichoic acid: characterization of ester-linked D-alanine in the in vitro-synthesized product. J. Bacteriol. 143:293-301.
11. Chiu, T.-H., H. Morimoto, and J. J. Baker. 1993. Biosynthesis and characterization of phosphatidylglycerophosphoglycerol, a possible intermediate in lipoteichoic acid biosynthesis in Streptococcus sanguis. Biochim. Biophys. Acta 1166:222-228.
12. Debabov, D. V., M. Y. Kiriukhin, and F. C. Neuhaus. 2000. Biosynthesis of lipoteichoic acid in Lactobacillus rhamnosus: role of DltD in D-alanylation. J. Bacteriol. 182:2855-2864.
13. Devereux, J., P. Haeberli, and O. Smithies. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12:387-395.
14. Duwat, P., A. Cochu, S. D. Ehrlich, and A. Gruss. 1997. Characterization of Lactococcus lactis UV-sensitive mutants obtained by ISS-1 transposition. J. Bacteriol. 179:4473-4479.
15. Fischer, W., P. Rosel, and H. U. Koch. 1981. Effect of alanine ester substitution and other structural features of lipoteichoic acids on their inhibitory activity against autolysins of Staphylococcus aureus. J. Bacteriol. 146:467-475.
16. Fischer, W., H. U. Koch, and R. Haas. 1983. Improved preparation of lipoteichoic acids. Eur. J. Biochem. 133:523-530.
17. Fischer, W. 1988. Physiology of lipoteichoic acids in bacteria. Adv. Microb. Physiol. 29:233-302.
18. Fischer, W. P. 1994. Lipoleichoic acid and lipids in the membrane of Staphylococcus aureus. Med. Microbiol. Immunol. 183:61-76.
19. Gustafson, J. E., B. Berger-Bächi, A. Strässle, and B. J. Wilkinson. 1992. Autolysis of methicillin-resistant and -susceptible Staphylococcus aureus. Antimicrob. Agents Chemother. 36:566-572.
20. Hanahan, D. 1983. Studies on transformation of Escherichia coli with plasmids J. Mol. Biol. 166:557-580.
21. Heaton, M. P., R. B. Johnston, and T. L. Thompson. 1988. Controlled lysis of bacterial cells utilizing mutants with defective synthesis of D-alanine. Can. J. Microbiol. 34:256-261.
22. Heptinstall, S., A. R. Archibald, and J. Baddiley. 1970. Teichoic acids and membrane function in bacteria. Nature 225:519-521.
23. Holo, H., and I. F. Nes. 1989. High frequency transformation, by electroporation, of Lactococcus lactis subsp. cremoris grown with glycine in osmotically stabilized media. Appl. Environ. Microbiol. 55:3119-3123.
24. Hughes, A. H., I. C. Hancock, and J. Baddiley. 1973. The function of teichoic acids in cation control in bacterial membranes. Biochem. J. 132:83-93.
25. Iwasaki, H., A. Shimada, and E. Ito. 1986. Comparative studies of lipoteichoic acids from several Bacillus strains. J. Bacteriol. 167:508-516.
26. Jorasch, P., D. C. Warnecke, B. Lindner, U. Zähringer, and E. Heinz. 2000. Novel processive and nonprocessive glycosyltransferases from Staphylococcus aureus and Arabidopsis thaliana synthesize glycoglycerolipids, glycophospholipids, glycosphingolipids and glycosylsterols. Eur. J. Biochem. 267:3770-3783.
27. Jorasch, P., F. P. Wolter, U. Zähringer, and E. Heinz. 1998. A UDP-glucosyltransferase from Bacillus subtilis successively transfers up to four glucose residues to 1,2-diacylglycerol: expression of ypfP in Escherichia coli and structural analysis of its reaction products. Mol. Microbiol. 29:419-430.
28. Jorasch, P., F. P. Wolter, U. Zähringer, and E. Heinz. 1998. Complete loss of glycolipids in a glucosyltransferase knock-out mutant of Bacillus subtilis, p. 243-246. In J. Sánchez, E. Cerdá-Olmedo, and E. Martínez-Force (ed.), Advances in plant lipid research - 1998. Secretariado de Publicaciones de la Universidad de Sevilla, Seville, Spain.
29. Koch, H. U., R. Haas, and W. Fischer. 1984. The role of lipoteichoic acid biosynthesis in membrane lipid metabolism of growing Staphylucoccus aureus. Eur. J. Biochem. 138:357-363.
30. Koo, S.-P., M. R. Yeaman, C. C. Nast, and A. S. Bayer. 1997. The cytoplasmic membrane is a primary target for the staphylocidal action of thrombin-induced platelet microbicidal protein. Infect. Immun. 65:4795-4800.
31. Kreiswirth, B. N., S. Lofdahl, M. J. Betley, M. O'Reilly, P. M. Schlievert, M. S. Bergdoll, and R. P. Novick. 1983. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305:709-712
32. Kuipers, O. P., M. M. Beerthuyzen, R. J. Siezen, and W. M. de Vos. 1993. Characterization of the nisin gene cluster nisABTCIPR of Lactococcus lactis: requirement of expression of the nisA and nisI genes for development of immunity. Eur. J. Biochem. 216:281-291.
33. Kullik, I., and P. Giachino. 1997. The alternative sigma factor sigma B in Staphylococcus aureus: regulation of the sigB operon in response to growth phase and heat shock. Arch. Microbiol. 167:151-159.
34. Lambert, P. A., I. C. Hancock, and J. Baddiley. 1975. Influence of alanyl ester residues on the binding of magnesium ions to teichoic acid. Biochem. J. 151:671-676.
35. Lingyi, D., and J. S. Anderson. 1997. Biosynthesis of teichuronic acid in the bacterial cell wall. Purification and characterization of the glucosyltransferase of Micrococcus luteus. J. Biol. Chem. 272:479-485.
36. Ludovice, A. M., S. W. Wu, and H. de Lancastre. 1998. Molecular cloning and DNA sequencing of the Staphylococcus aureus UDP-N-acetylmuramyl tripeptidc synthetase (murE) gene, essential for the optimal expression of methicillin resistance. Microb. Drug Resist. 4:85-90.
37. Maguin, E., P. Duwat, T. Hege, D. Ehrlich, and A. Gruss. 1992. New thermosensitive plasmid for gram-positive bacteria. J. Bacteriol. 174:5633-5638.
38. Neuhaus, F. C., M. P. Heaton, D. V. Debabov, and Q. Zhang. 1996. The dlt operon in the biosynthesis of D-alanyl-lipoteichoic acid in Lactobacillus casei. Microb. Drug Resist. 2:77-84.
39. Ntamere, A. S., D. J. Taron, and F. C. Neuhaus. 1987. Assembly of D-alanyl-lipoteichoic acid in Lactobacillus casai: mutants deficient in the D-alanyl ester content of this amphiphile. J. Bacteriol. 169:1702-1711.
40. O'Sullivan, D. J., and T. R. Klaenhammer. 1993. Rapid mini-prep isolation of high-quality plasmid DNA from Lactococcus and Lactobacillus spp. Appl. Environ. Microbiol. 59:2730-2733.
41. Ou, L.-T., and R. E. Marquis. 1970. Electromechanical interactions in cell walls of gram-positive cocci. J. Bacteriol. 101:92-101.
42. Perego, M., P. Glaser, A. Minutello, M. A. Strauch, K. Leopold, and W. Fischer. 1995. Incorporation of D-alanine into lipoteichoic acid and wall teichoic acid in Bacillus subtilis: identification of genes and regulation. J. Biol. Chem. 270:15595-15606.
43. Peschel, A., M. Otto, R. W. Jack, H. Kalbacher, G. Jung, and F. Götz. 1999. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J. Biol. Chem. 274: 8405-8410.
44. Pollack, J. H., A. S. Ntamere, and F. C. Neuhaus. 1992. D-Alanyl-lipoteichoic acid in Lactobacillus casei: secretion of vesicles in response to benzylpenicillin. J. Gen. Microbiol. 138:849-859.
45. Pollack, J. H., and F. C. Neuhaus. 1994. Changes in wall teichoic acid during the rod-sphere transition of Bacillus subtilis 168. J. Bacteriol. 176:7252-7259.
46. Price, K. D., S. Roels, and R. Losick. 1997. A Bacillus subtilis gene encoding a protein similar to nucleotide sugar transferases influences cell shape and viability. J. Bacteriol. 179:4959-4961.
47. Roethlisberger, P., N. Iida-Tanaka, K. Hollemeyer, E. Heinzle, I. Ishizuka, and W. Fischer. 2000. Unique poly(glycerophosphate) lipoteichoic acid and the glycolipids of Streptococcus sp. closely related to Streptococcus pneumoniae. Eur. J. Biochem. 267:5520-5530.
48. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
49. Shimojima, M., H. Ohta, A. Iwamatsu, T. Masuda, Y. Shioi, and K. Takamiya. 1997. Cloning of the gene for monogalactosyl diacylglycerol synthase and its evolutionary origin. Proc. Natl. Acad. Sci. USA 94:333-337.
50. Spatafora, G., A. M. Sheets, R. June, D. Luylmbezi, K. Howard, R. Holbert, D. Barnard, M. El Janne, and M. C. Hudson. 1999. Regulated expression of the Streptococcus mutans dlt genes correlate with intracellular polysaccharide accumulation. J. Bacteriol. 181:2363-2372.
51. Studier, F. W., A. H. Rosenberg, J. J. Dunn, and J. W. Dubendorff. 1990. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185:60-89
52. Sutcliffe, I. C., and N. Shaw. 1991. Atypical lipoteichoic acids of gram-positive bacteria. J. Bacteriol. 173:7065-7069.
53. Taron, D. J., W. C. Childs III, and F. C. Neuhaus. 1983. Biosynthesis of D-alanyl-lipoteichoic acid: role of diglyceride kinase in the synthesis of phosphatidylglycerol for chain elongation. J. Bacteriol. 154:1110-1116.
54. Vikström, S., L. Li, and Å. Wieslander. 2000. The nonbilayer/bilayer lipid balance in membranes: regulatory enzyme in Acholeplasma laidlawii is stimulated by metabolic phosphates, activator phospholipids, and double-stranded DNA. J. Biol. Chem. 275:9296-9302.
55. Wecke, J., M. Perego, and W. Fischer. 1997. D-Alanine deprivation of Bacillus subtilis teichoic acids is without effect on cell growth and morphology but affects autolytic activity. Microb. Drug Resist. 2:2953-2960.