The Rickettsia prowazekii ExoU homologue possesses phospholipase A 1 (PLA 1), PLA 2, and Lyso-PLA 2 activities and can function in the absence of any eukaryotic cofactors in vitro

Journal of Bacteriology

Volumn 193, Issue 18, 2011, Pages 4634-4642

  Housley, Nicole A ^a   Winkler, Herbert H ^a   Audia, Jonathon P ^a  

^a UNIVERSITY OF SOUTH ALABAMA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CELL EXTRACT; CYTOTOXIN; EXOU PROTEIN; LYSOPHOSPHOLIPASE; MICROORGANISM PROTEIN; PHOSPHATIDYLCHOLINE; PHOSPHOLIPASE A1; RECOMBINANT PROTEIN; RP534 PROTEIN; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIUM CULTURE; CYTOLYSIS; ENZYME ACTIVITY; ESCHERICHIA COLI; EUKARYOTE; IMMUNOPRECIPITATION; IN VITRO STUDY; MUTAGENESIS; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; RICKETTSIA PROWAZEKII;

HYDROLYSIS; LYSOPHOSPHOLIPASE; PHOSPHATIDYLCHOLINES; PHOSPHOLIPASES A1; PHOSPHOLIPASES A2; RECOMBINANT PROTEINS; RICKETTSIA PROWAZEKII; SUPEROXIDE DISMUTASE;

BOVINAE; EUKARYOTA; PSEUDOMONAS AERUGINOSA; RICKETTSIA PROWAZEKII; RICKETTSIACEAE;

EID: 80052551902     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00141-11     Document Type: Article

References (57)

1. Allewelt, M., F. T. Coleman, M. Grout, G. P. Priebe, and G. B. Pier. 2000. Acquisition of expression of the Pseudomonas aeruginosa ExoU cytotoxin leads to increased bacterial virulence in a murine model of acute pneumonia and systemic spread. Infect. Immun. 68:3998-4004.
2. 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.
3. Altschul, S. F., et al. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
4. Anderson, B., H. Friedman, and M. Bendinelli. 1997. Rickettsial infection and immunity. Plenum Press, New York, NY.
5. Andersson, J. O., and S. G. E. Andersson. 2000. A century of typhus, lice and Rickettsia. Res. Microbiol. 151:143-150.
6. Andersson, S. G. E., et al. 1998. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396:133-140.
7. Andrews, D. L., B. Beames, M. D. Summers, and W. D. Park. 1988. Characterization of the lipid acyl hydrolase activity of the major potato (Solanum tuberosum) tuber protein, patatin, by cloning and abundant expression in a baculovirus vector. Biochem. J. 252:199-206.
8. Audia, J. P., and J. W. Foster. 2003. Acid shock accumulation of sigma S in Salmonella enterica involves increased translation, not regulated degradation. J. Mol. Microbiol. Biotechnol. 5:17-28.
9. Benson, M. A., K. M. Schmalzer, and D. W. Frank. 2010. A sensitive fluorescence-based assay for the detection of ExoU-mediated PLA(2) activity. Clin. Chim. Acta 411:190-197.
10. 2 active sites. Ann. N. Y. Acad. Sci. 1063:83-86.
11. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911-917.
12. Chao, C. C., D. Chelius, T. Zhang, L. Daggle, and W. M. Ching. 2004. Proteome analysis of Madrid E strain of Rickettsia prowazekii. Proteomics 4:1280-1292.
13. Clarke, D. H., and J. P. Fox. 1948. The phenomenon of in vitro hemolysis produced by the rickettsiae of typhus fever, with a note on the mechanism of rickettsial toxicity in mice. J. Exp. Med. 88:25-41.
14. Finck-Barbancon, V., and D. W. Frank. 2001. Multiple domains are required for the toxic activity of Pseudomonas aeruginosa ExoU. J. Bacteriol. 183: 4330-4344.
15. Finck-Barbancon, V., et al. 1997. ExoU expression by Pseudomonas aeruginosa correlates with acute cytotoxicity and epithelial injury. Mol. Microbiol. 25:547-557.
16. Fine, J. B., and H. Sprecher. 1982. Unidimensional thin-layer chromatography of phospholipids on boric acid-impregnated plates. J. Lipid Res. 23:660-663.
17. Frank, D. W. 1997. The exoenzyme S regulon of Pseudomonas aeruginosa. Mol. Microbiol. 26:621-629.
18. Frohlich, K. M., R. A. Roberts, N. A. Housley, and J. P. Audia. 2010. Rickettsia prowazekii uses an sn-glycerol-3-phosphate dehydrogenase and a novel dihydroxyacetone phosphate transport system to supply triose phosphate for phospholipid biosynthesis. J. Bacteriol. 192:4281-4288.
19. 2 family. Prog. Lipid. Res. 45:487-510.
20. Hackstadt, T. 1996. The biology of Rickettsiae. Infect. Agents Dis. 5:127-143.
21. Hirschberg, H. J., J. W. Simons, N. Dekker, and M. R. Egmond. 2001. Cloning, expression, purification and characterization of patatin, a novel phospholipase A. Eur. J. Biochem. 268:5037-5044.
22. Kolarovic, L., and N. C. Fournier. 1986. A comparison of extraction methods for the isolation of phospholipids from biological sources. Anal. Biochem. 156:244.
23. Kulasekara, B. R., et al. 2006. Acquisition and evolution of the exoU locus in Pseudomonas aeruginosa. J. Bacteriol. 188:4037-4050.
24. Miroux, B., and J. E. Walker. 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.
25. Netesov, S. V., and J. L. Conrad. 2001. Emerging infectious diseases in Russia, 1990-1999. Emerg. Infect. Dis. 7:1-5.
26. Ojcius, D. M., M. Thibon, C. Mounier, and A. Dautry-Varsat. 1995. pH and calcium dependence of hemolysis due to Rickettsia prowazekii: comparison with phospholipase activity. Infect. Immun. 63:3069-3072.
27. Phillips, R. M., D. A. Six, E. A. Dennis, and P. Ghosh. 2003. In vivo phospholipase activity of the Pseudomonas aeruginosa cytotoxin ExoU and protection of mammalian cells with phospholipase A2 inhibitors. J. Biol. Chem. 278:41326-41332.
28. Rabin, S. D., and A. R. Hauser. 2003. Pseudomonas aeruginosa ExoU, a toxin transported by the type III secretion system, kills Saccharomyces cerevisiae. Infect. Immun. 71:4144-4150.
29. Rahman, M. S., N. C. Ammerman, K. T. Sears, S. M. Ceraul, and A. F. Azad. 2010. Functional characterization of a phospholipase A(2) homolog from Rickettsia typhi. J. Bacteriol. 192:3294-3303.
30. Ramm, L. E., and H. H. Winkler. 1976. Identification of cholesterol in the receptor site for rickettsiae on sheep erythrocyte membranes. Infect. Immun. 13:120-126.
31. Ramm, L. E., and H. H. Winkler. 1973. Rickettsial hemolysis: adsorption of rickettsiae to erythrocytes. Infect. Immun. 7:93-99.
32. Ramm, L. E., and H. H. Winkler. 1973. Rickettsial hemolysis: effect of metabolic inhibitors upon hemolysis and adsorption. Infect. Immun. 7:550-555.
33. Raoult, D., et al. 1998. Outbreak of epidemic typhus associated with trench fever in Burundi. Lancet 352:353-358.
34. Rydel, T. J., et al. 2003. The crystal structure, mutagenesis, and activity studies reveal that patatin is a lipid acyl hydrolase with a Ser-Asp catalytic dyad. Biochemistry 42:6696-6708.
35. Sato, H., J. B. Feix, and D. W. Frank. 2006. Identification of superoxide dismutase as a cofactor for the pseudomonas type III toxin, ExoU. Biochemistry 45:10368-10375.
36. Sato, H., and D. W. Frank. 2004. ExoU is a potent intracellular phospholipase. Mol. Microbiol. 53:1279-1290.
37. Sato, H., et al. 2003. The mechanism of action of the Pseudomonas aeruginosa-encoded type III cytotoxin, ExoU. EMBO J. 22:2959-2969.
38. Schulert, G. S., et al. 2003. Secretion of the toxin ExoU is a marker for highly virulent Pseudomonas aeruginosa isolates obtained from patients with hospital-acquired pneumonia. J. Infect. Dis. 188:1695-1706.
39. Silverman, D. J., L. A. Santucci, N. Meyers, and Z. Sekeyova. 1992. Penetration of host cells by Rickettsia rickettsii appears to be mediated by a phospholipase of rickettsial origin. Infect. Immun. 60:2733-2740.
40. Snyder, J. C., M. R. Bovarnick, J. C. Miller, and S.-M. Chang. 1954. Observations on the hemolytic properties of typhus rickettsiae. J. Bacteriol. 67:724-730.
41. Strickland, J. A., G. L. Orr, and T. A. Walsh. 1995. Inhibition of Diabrotica larval growth by patatin, the lipid acyl hydrolase from potato tubers. Plant Physiol. 109:667-674.
42. Tamura, M., et al. 2004. Lysophospholipase A activity of Pseudomonas aeruginosa type III secretory toxin ExoU. Biochem. Biophys. Res. Commun. 316:323-331.
43. Tucker, A. M., L. K. Pannell, and D. O. Wood. 2005. Dissecting the Rickettsia prowazekii genome: genetic and proteomic approaches. Ann. N. Y. Acad. Sci. 1063:35-46.
44. Vallis, A. J., V. Finck-Barbancon, T. L. Yahr, and D. W. Frank. 1999. Biological effects of Pseudomonas aeruginosa type III-secreted proteins on CHO cells. Infect. Immun. 67:2040-2044.
45. Walker, D. H. (ed.). 1988. Biology of rickettsial diseases, vol. II. CRC Press, Boca Raton, FL.
46. 2 as a pathogenic mechanism in a model of cell injury by typhus and spotted fever group rickettsiae. Am. J. Trop. Med. Hyg. 65:936-942.
47. Weiss, E. 1982. The biology of rickettsiae. Annu. Rev. Microbiol. 36:345-370.
48. Winkler, H. H. 1974. Inhibitory and restorative effects of adenine nucleotides on rickettsial adsorption and hemolysis. Infect. Immun. 9:119-126.
49. Winkler, H. H. 1990. Rickettsia species (as organisms). Annu. Rev. Microbiol. 44:131-153.
50. Winkler, H. H. 1977. Rickettsial hemolysis: adsorption, desorption, readsorption, and hemagglutination. Infect. Immun. 17:607-612.
51. Winkler, H. H., and R. M. Daugherty. 1989. Phospholipase A activity associated with the growth of Rickettsia prowazekii in L929 cells. Infect. Immun. 57:36-40.
52. Winkler, H. H., L. C. Day, and R. M. Daugherty. 1994. Analysis of the hydrolytic products from choline labeled host cell phospholipids during the growth of Rickettsia prowazekii. Infect. Immun. 62:1457-1459.
53. Winkler, H. H., L. C. Day, R. M. Daugherty, and J. Turco. 1993. Effect of gamma interferon on phospholipid hydrolysis and fatty acid incorporation in L929 cells infected with Rickettsia prowazekii. Infect. Immun. 61:3412-3415.
54. Winkler, H. H., and E. T. Miller. 1981. Immediate cytotoxicity and phospholipase A: the role of phospholipase A in the interaction of R. prowazekii and L-cells, p. 327-333. In W. Burgdorfer and R. Anacker (ed.), Rickettsiae and rickettsial diseases. Academic Press, Inc., New York, NY.
55. Winkler, H. H., and E. T. Miller. 1980. Phospholipase A activity in the hemolysis of sheep and human erythrocytes by Rickettsia prowazeki. Infect. Immun. 29:316-321.
56. Winkler, H. H., and E. T. Miller. 1982. Phospholipase A and the interaction of Rickettsia prowazekii and mouse fibroblasts (L-929 cells). Infect. Immun. 38:109-113.
57. Winkler, H. H., and L. E. Ramm. 1975. Adsorption of typhus rickettsiae to ghosts of sheep erythrocytes. Infect. Immun. 11:1244-1251.