CGDEase, a Pseudomonas fluorescens protein of the PLC/APase superfamily with CDP-ethanolamine and (dihexanoyl)glycerophosphoethanolamine hydrolase activity induced by osmoprotectants under phosphate-deficient conditions

Molecular Microbiology

Volumn 78, Issue 6, 2010, Pages 1556-1576

  Costas, María Jesús ^a   Pinto, Rosa María ^a   Cordero, Paloma Martín ^b   Cabezas, Alicia ^a   Alves Pereira, Isabel ^c   Cameselle, José Carlos ^a   Ribeiro, João Meireles ^a  

^a UNIVERSITY OF EXTREMADURA   (Spain)

^b Badajoz Servicio de Urgencias Complejo Universitario Hospitalario de Badajoz Badajoz Espana   (Spain)

^c UNIVERSITY OF ÉVORA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE; CHOLINE DERIVATIVE; CYTIDINE DIPHOSPHATE ETHANOLAMINE PYROPHOSPHATASE DIHEXANOYL GLYCEROPHOSPHOETHANOLAMINE PHOSPHODIESTERASE; GLYCEROL; HYDROLASE; PEPTIDE; PHOSPHATE; PHOSPHOETHANOLAMINE; PHOSPHOLIPASE C; PHOSPHOLIPID DERIVATIVE; PHOSPHORYLCHOLINE; PROTEIN CGDEASE; PROTEIN NDP X; UNCLASSIFIED DRUG;

ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME LOCALIZATION; ENZYME STRUCTURE; GENETIC CONSERVATION; MOLECULAR CLONING; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; OSMOTIC STRESS; PEPTIDE ANALYSIS; PHOSPHATE DEFICIENCY; POPULATION DENSITY; PRIORITY JOURNAL; PROTEIN FAMILY; PSEUDOMONAS FLUORESCENS; QUORUM SENSING; SITE DIRECTED MUTAGENESIS;

CATALYTIC DOMAIN; CYTIDINE DIPHOSPHATE; ETHANOLAMINES; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHOSPHATES; PHOSPHORIC DIESTER HYDROLASES; PSEUDOMONAS FLUORESCENS; PYROPHOSPHATASES; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS); PSEUDOMONAS FLUORESCENS;

EID: 78650010952     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07425.x     Document Type: Article

References (75)

1. Alves-Pereira, I., Canales, J., Cabezas, A., Cordero, P.M., Costas, M.J., and Cameselle, J.C. (2008) CDP-alcohol hydrolase, a very efficient activity of the 5'-nucleotidase/UDP-sugar hydrolase encoded by the ushA gene of Yersinia intermedia and Escherichia coli. J Bacteriol 190: 6153-6161.
2. Amtmann, E. (1996) The antiviral, antitumoural xanthate D609 is a competitive inhibitor of phosphatidylcholine-specific phospholipase C. Drugs Exp Clin Res 22: 287-294.
3. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201.
4. Bessman, M.J., Frick, D.N., and O'Handley, S.F. (1996) The MutT proteins or 'Nudix' hydrolases, a family of versatile, widely distributed, 'housecleaning' enzymes. J Biol Chem 271: 25059-25062.
5. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
6. Burns, D.M., and Beacham, I.R. (1986) Nucleotide sequence and transcriptional analysis of the E. coli ushA gene, encoding periplasmic UDP-sugar hydrolase (5'-nucleotidase): regulation of the ushA gene, and the signal sequence of its encoded protein product. Nucleic Acids Res 14: 4325-4342.
7. 2+-dependent ADP-ribose/CDP-alcohol pyrophosphatase: a novel metallophosphoesterase family preferentially expressed in rodent immune cells. Biochem J 413: 103-113.
8. Chapalain, A., Rossignol, G., Lesouhaitier, O., Merieau, A., Gruffaz, C., Guerillon, J., et al. (2008) Comparative study of 7 fluorescent pseudomonad clinical isolates. Can J Microbiol 54: 19-27.
9. Child, R., Wehrly, T.D., Rockx-Brouwer, D., Dorward, D.W., and Celli, J. (2010) Acid phosphatases do not contribute to the pathogenesis of type A Francisella tularensis. Infect Immun 78: 59-67.
10. Corda, D., Kudo, T., Zizza, P., Iurisci, C., Kawai, E., Kato, N., et al. (2009) The developmentally regulated osteoblast phosphodiesterase GDE3 is glycerophosphoinositol-specific and modulates cell growth. J Biol Chem 284: 24848-24856.
11. Cornish-Bowden, A. (1995) Fundamentals of Enzyme Kinetics. London: Portland Press.
12. Crevel, I., Sally, U., Carne, A., and Katan, M. (1994) Purification and properties of zinc-metallophospholipase C from Pseudomonas fluorescens. Eur J Biochem 224: 845-852.
13. De Buck, E., Lammertyn, E., and Anne, J. (2008) The importance of the twin-arginine translocation pathway for bacterial virulence. Trends Microbiol 16: 442-453.
14. Dehal, P.S., Joachimiak, M.P., Price, M.N., Bates, J.T., Baumohl, J.K., Chivian, D., et al. (2010) MicrobesOnline: an integrated portal for comparative and functional genomics. Nucleic Acids Res 38: D396-D400.
15. Doi, O., and Nojima, S. (1971) Phospholipase C from Pseudomonas fluorescens. Biochim Biophys Acta 248: 234-244.
16. El-Sayed, M.Y., DeBose, C.D., Coury, L.A., and Roberts, M.F. (1985) Sensitivity of phospholipase C (Bacillus cereus) activity to phosphatidylcholine structural modifications. Biochim Biophys Acta 837: 325-335.
17. Felts, R.L., Reilly, T.J., and Tanner, J.J. (2006) Structure of Francisella tularensis AcpA: prototype of a unique superfamily of acid phosphatases and phospholipases C. J Biol Chem 281: 30289-30298.
18. Flores-Díaz, M., Thelestam, M., Clark, G.C., Titball, R.W., and Alape-Giron, A. (2004) Effects of Clostridium perfringens phospholipase C in mammalian cells. Anaerobe 10: 115-123.
19. Gallazzini, M., Ferraris, J.D., and Burg, M.B. (2008) GDPD5 is a glycerophosphocholine phosphodiesterase that osmotically regulates the osmoprotective organic osmolyte GPC. Proc Natl Acad Sci USA 105: 11026-11031.
20. Galperin, M.Y., Moroz, O.V., Wilson, K.S., and Murzin, A.G. (2006) House cleaning, a part of good housekeeping. Mol Microbiol 59: 5-19.
21. Gennari, M., and Dragotto, F. (1992) A study of the incidence of different fluorescent Pseudomonas species and biovars in the microflora of fresh and spoiled meat and fish, raw milk, cheese, soil and water. J Appl Bacteriol 72: 281-288.
22. Gershman, M.D., Kennedy, D.J., Noble-Wang, J., Kim, C., Gullion, J., Kacica, M., et al. (2008) Multistate outbreak of Pseudomonas fluorescens bloodstream infection after exposure to contaminated heparinized saline flush prepared by a compounding pharmacy. Clin Infect Dis 47: 1372-1379.
23. Gonzalez, C., Gutierrez, C., and Grande, T. (1987) Bacterial flora in bottled uncarbonated mineral drinking water. Can J Microbiol 33: 1120-1125.
24. Gründling, A., Gonzalez, M.D., and Higgins, D.E. (2003) Requirement of the Listeria monocytogenes broad-range phospholipase PC-PLC during infection of human epithelial cells. J Bacteriol 185: 6295-6307.
25. Hergenrother, P.J., and Martin, S.F. (1997) Determination of the kinetic parameters for phospholipase C (Bacillus cereus) on different phospholipid substrates using a chromogenic assay based on the quantitation of inorganic phosphate. Anal Biochem 251: 45-49.
26. Hernychová, L., Stulík, J., Halada, P., Macela, A., Kroca, M., Johansson, T., and Malina, M. (2001) Construction of a Francisella tularensis two-dimensional electrophoresis protein database. Proteomics 1: 508-515.
27. Hsueh, P.R., Teng, L.J., Pan, H.J., Chen, Y.C., Sun, C.C., Ho, S.W., and Luh, K.T. (1998) Outbreak of Pseudomonas fluorescens bacteremia among oncology patients. J Clin Microbiol 36: 2914-2917.
28. Hyatt, D., Chen, G.L., Locascio, P.F., Land, M.L., Larimer, F.W., and Hauser, L.J. (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11: 119.
29. Kewitz, H., and Pleul, O. (1976) Synthesis of choline from ethanolamine in rat brain. Proc Natl Acad Sci USA 73: 2181-2185.
30. Khabbaz, R.F., Arnow, P.M., Highsmith, A.K., Herwaldt, L.A., Chou, T., Jarvis, W.R., et al. (1984) Pseudomonas fluorescens bacteremia from blood transfusion. Am J Med 76: 62-68.
31. Korbsrisate, S., Tomaras, A.P., Damnin, S., Ckumdee, J., Srinon, V., Lengwehasatit, I., et al. (2007) Characterization of two distinct phospholipase C enzymes from Burkholderia pseudomallei. Microbiology 153: 1907-1915.
32. Lamarche, M.G., Wanner, B.L., Crepin, S., and Harel, J. (2008) The phosphate regulon and bacterial virulence: a regulatory network connecting phosphate homeostasis and pathogenesis. FEMS Microbiol Rev 32: 461-473.
33. Larson, T.J., and Van Loo-Bhattacharya, A.T. (1988) Purification and characterization of glpQ-encoded glycerophosphodiester phosphodiesterase from Escherichia coli K-12. Arch Biochem Biophys 260: 577-584.
34. Larson, T.J., Ehrmann, M., and Boos, W. (1983) Periplasmic glycerophosphodiester phosphodiesterase of Escherichia coli, a new enzyme of the glp regulon. J Biol Chem 258: 5428-5432.
35. Liffourrena, A.S., Massimelli, M.J., Forrellad, M.A., Lisa, A.T., Domenech, C.E., and Lucchesi, G.I. (2007) Tetradecyltrimethylammonium inhibits Pseudomonas aeruginosa hemolytic phospholipase C induced by choline. Curr Microbiol 55: 530-536.
36. Lisa, T.A., Casale, C.H., and Domenech, C.E. (1994) Cholinesterase, acid phosphatase, and phospholipase C of Pseudomonas aeruginosa and hyperosmotic conditions in a high-phosphate medium. Curr Microbiol 28: 71-76.
37. Liu, M., Wang, H., and Griffiths, M.W. (2007) Regulation of alkaline metalloprotease promoter by N-acyl homoserine lactone quorum sensing in Pseudomonas fluorescens. J Appl Microbiol 103: 2174-2184.
38. McLennan, A.G. (2006) The Nudix hydrolase superfamily. Cell Mol Life Sci 63: 123-143.
39. Mao, F., Dam, P., Chou, J., Olman, V., and Xu, Y. (2009) DOOR: a database for prokaryotic operons. Nucleic Acids Res 37: D459-D463.
40. Martin, R.G., and Ames, B.N. (1961) A method for determining the sedimentation behavior of enzymes: application to protein mixtures. J Biol Chem 236: 1372-1379.
41. Mavrodi, D.V., Paulsen, I.T., Ren, Q., and Loper, J.E. (2007) Genomics of Pseudomonas fluorescens Pf-5. In Pseudomonas, Vol. 5. Ramos, J.-L., and Filloux, A. (eds). Springer, pp. 3-30.
42. Mildvan, A.S., Xia, Z., Azurmendi, H.F., Saraswat, V., Legler, P.M., Massiah, M.A., et al. (2005) Structures and mechanisms of Nudix hydrolases. Arch Biochem Biophys 433: 129-143.
43. Namnyak, S., Hussain, S., Davalle, J., Roker, K., and Strickland, M. (1999) Contaminated lithium heparin bottles as a source of pseudobacteraemia due to Pseudomonas fluorescens. J Hosp Infect 41: 23-28.
44. Natale, P., Bruser, T., and Driessen, A.J. (2008) Sec- and Tat-mediated protein secretion across the bacterial cytoplasmic membrane - distinct translocases and mechanisms. Biochim Biophys Acta 1778: 1735-1756.
45. Nyyssola, A., and Leisola, M. (2001) Actinopolyspora halophila has two separate pathways for betaine synthesis. Arch Microbiol 176: 294-300.
46. Ostroff, R.M., Wretlind, B., and Vasil, M.L. (1989) Mutations in the hemolytic-phospholipase C operon result in decreased virulence of Pseudomonas aeruginosa PAO1 grown under phosphate-limiting conditions. Infect Immun 57: 1369-1373.
47. Ostroff, R.M., Vasil, A.I., and Vasil, M.L. (1990) Molecular comparison of a nonhemolytic and a hemolytic phospholipase C from Pseudomonas aeruginosa. J Bacteriol 172: 5915-5923.
48. Preuss, I., Kaiser, I., and Gehring, U. (2001) Molecular characterization of a phosphatidylcholine-hydrolyzing phospholipase C. Eur J Biochem 268: 5081-5091.
49. Raynaud, C., Guilhot, C., Rauzier, J., Bordat, Y., Pelicic, V., Manganelli, R., et al. (2002) Phospholipases C are involved in the virulence of Mycobacterium tuberculosis. Mol Microbiol 45: 203-217.
50. Ribeiro, J.M., Carloto, A., Costas, M.J., and Cameselle, J.C. (2001) Human placenta hydrolases active on free ADP-ribose: an ADP-sugar pyrophosphatase and a specific ADP-ribose pyrophosphatase. Biochim Biophys Acta 1526: 86-94.
51. Rittmann, D., Sorger-Herrmann, U., and Wendisch, V.F. (2005) Phosphate starvation-inducible gene ushA encodes a 5' nucleotidase required for growth of Corynebacterium glutamicum on media with nucleotides as the phosphorus source. Appl Environ Microbiol 71: 4339-4344.
52. Rohman, M., and Harrison-Lavoie, K.J. (2000) Separation of copurifying GroEL from glutathione-S-transferase fusion proteins. Protein Expr Purif 20: 45-47.
53. Rossignol, G., Merieau, A., Guerillon, J., Veron, W., Lesouhaitier, O., Feuilloley, M.G., and Orange, N. (2008) Involvement of a phospholipase C in the hemolytic activity of a clinical strain of Pseudomonas fluorescens. BMC Microbiol 8: 189.
54. Sage, A.E., Vasil, A.I., and Vasil, M.L. (1997) Molecular characterization of mutants affected in the osmoprotectant-dependent induction of phospholipase C in Pseudomonas aeruginosa PAO1. Mol Microbiol 23: 43-56.
55. Shortridge, V.D., Lazdunski, A., and Vasil, M.L. (1992) Osmoprotectants and phosphate regulate expression of phospholipase C in Pseudomonas aeruginosa. Mol Microbiol 6: 863-871.
56. Smith, G.A., Marquis, H., Jones, S., Johnston, N.C., Portnoy, D.A., and Goldfine, H. (1995) The two distinct phospholipases C of Listeria monocytogenes have overlapping roles in escape from a vacuole and cell-to-cell spread. Infect Immun 63: 4231-4237.
57. Songer, J.G. (1997) Bacterial phospholipases and their role in virulence. Trends Microbiol 5: 156-161.
58. Stefan, C., Jansen, S., and Bollen, M. (2005) NPP-type ectophosphodiesterases: unity in diversity. Trends Biochem Sci 30: 542-550.
59. Stonehouse, M.J., Cota-Gomez, A., Parker, S.K., Martin, W.E., Hankin, J.A., Murphy, R.C., et al. (2002) A novel class of microbial phosphocholine-specific phospholipases C. Mol Microbiol 46: 661-676.
60. Summers, P.S., and Weretilnyk, E.A. (1993) Choline synthesis in spinach in relation to salt stress. Plant Physiol 103: 1269-1276.
61. Thain, A., Gaston, K., Jenkins, O., and Clarke, A.R. (1996) A method for the separation of GST fusion proteins from co-purifying GroEL. Trends Genet 12: 209-210.
62. Tirrell, I.M., Wall, J.L., Daley, C.J., Denial, S.J., Tennis, F.G., Galens, K.G., and O'Handley, S.F. (2006) YZGD from Paenibacillus thiaminolyticus, a pyridoxal phosphatase of the HAD (haloacid dehalogenase) superfamily and a versatile member of the Nudix (nucleoside diphosphate x) hydrolase superfamily. Biochem J 394: 665-674.
63. Titball, R.W. (1993) Bacterial phospholipases C. Microbiol Rev 57: 347-366.
64. Tommassen, J., Eiglmeier, K., Cole, S.T., Overduin, P., Larson, T.J., and Boos, W. (1991) Characterization of two genes, glpQ and ugpQ, encoding glycerophosphoryl diester phosphodiesterases of Escherichia coli. Mol Gen Genet 226: 321-327.
65. Urbina, P., Flores-Diaz, M., Alape-Giron, A., Alonso, A., and Goñi, F.M. (2009) Phospholipase C and sphingomyelinase activities of the Clostridium perfringens alpha-toxin. Chem Phys Lipids 159: 51-57.
66. Vasil, M.L. (2006) Pseudomonas aeruginosa phospholipases and phospholipids. In Pseudomonas, Vol. 4. Ramos, J.L., and Levesque, R.C. (eds). Springer, pp. 69-97.
67. Vasil, M.L., Stonehouse, M.J., Vasil, A.I., Wadsworth, S.J., Goldfine, H., Bolcome, R.E., 3rd, and Chan, J. (2009) A complex extracellular sphingomyelinase of Pseudomonas aeruginosa inhibits angiogenesis by selective cytotoxicity to endothelial cells. PLoS Pathog 5: e1000420.
68. Voulhoux, R., Ball, G., Ize, B., Vasil, M.L., Lazdunski, A., Wu, L.F., and Filloux, A. (2001) Involvement of the twin-arginine translocation system in protein secretion via the type II pathway. EMBO J 20: 6735-6741.
69. Wargo, M.J., Ho, T.C., Gross, M.J., Whittaker, L.A., and Hogan, D.A. (2009) GbdR regulates Pseudomonas aeruginosa plcH and pchP transcription in response to choline catabolites. Infect Immun 77: 1103-1111.
70. Williams, P., Winzer, K., Chan, W.C., and Camara, M. (2007) Look who's talking: communication and quorum sensing in the bacterial world. Philos Trans R Soc Lond B Biol Sci 362: 1119-1134.
71. Xu, W., Dunn, C.A., Jones, C.R., D'Souza, G., and Bessman, M.J. (2004) The 26 Nudix hydrolases of Bacillus cereus, a close relative of Bacillus anthracis. J Biol Chem 279: 24861-24865.
72. Yagil, E., and Beacham, I.R. (1975) Uptake of adenosine 5'-monophosphate by Escherichia coli. J Bacteriol 121: 401-405.
73. Yanaka, N. (2007) Mammalian glycerophosphodiester phosphodiesterases. Biosci Biotechnol Biochem 71: 1811-1818.
74. Yuelling, L.M., and Fuss, B. (2008) Autotaxin (ATX): a multi-functional and multi-modular protein possessing enzymatic lysoPLD activity and matricellular properties. Biochim Biophys Acta 1781: 525-530.
75. Zablocki, K., Miller, S.P., Garcia-Perez, A., and Burg, M.B. (1991) Accumulation of glycerophosphocholine (GPC) by renal cells: osmotic regulation of GPC: choline phosphodiesterase. Proc Natl Acad Sci USA 88: 7820-7824.