A novel FK-506-binding-like protein that lacks peptidyl-prolyl isomerase activity is involved in intracellular infection and in vivo virulence of Burkholderia pseudomallei

Microbiology

Volumn 157, Issue 9, 2011, Pages 2629-2638

  Norville, Isobel H ^a   Breitbach, Katrin ^b   Eske Pogodda, Kristin ^b   Harmer, Nicholas J ^c   Sarkar Tyson, Mitali ^a   Titball, Richard W ^c   Steinmetz, Ivo ^b  

^a DEFENCE SCIENCE AND TECHNOLOGY LABORATORY   (United Kingdom)

^b UNIVERSITY OF GREIFSWALD   (Germany)

^c UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; CHLORAMPHENICOL; FK 506 BINDING PROTEIN; GENOMIC DNA; IMIPENEM; KANAMYCIN; PEPTIDYLPROLYL ISOMERASE; RECOMBINANT PROTEIN; STREPTOMYCIN; TETRACYCLINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL INFECTION; BACTERIAL VIRULENCE; BACTERIUM CULTURE; BACTERIUM MUTANT; BURKHOLDERIA PSEUDOMALLEI; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; ESCHERICHIA COLI; GENE EXPRESSION; HELA CELL; HUMAN; HUMAN CELL; MACROPHAGE; MELIOIDOSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN FAMILY; PSEUDOMONAS INFECTION;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BETA-LACTAMS; BURKHOLDERIA PSEUDOMALLEI; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; FEMALE; HELA CELLS; HUMANS; MELIOIDOSIS; MICE; MICE, INBRED BALB C; MICROBIAL SENSITIVITY TESTS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PEPTIDYLPROLYL ISOMERASE; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; TACROLIMUS BINDING PROTEINS; VIRULENCE;

BACTERIA (MICROORGANISMS); BURKHOLDERIA PSEUDOMALLEI; MURINAE;

EID: 80052381917     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.049163-0     Document Type: Article

References (54)

1. Behrens, S., Maier, R., de Cock, H., Schmid, F. X. & Gross, C. A. (2001). The SurA periplasmic PPIase lacking its parvulin domains functions in vivo and has chaperone activity. EMBO J 20, 285-294.
2. Brandts, J. F., Halvorson, H. R. & Brennan, M. (1975). Consideration of the possibility that the slow step in protein denaturation reactions is due to cis-trans isomerism of proline residues. Biochemistry 14, 4953-4963.
3. Burtnick, M. N. & Woods, D. E. (1999). Isolation of polymyxin B-susceptible mutants of Burkholderia pseudomallei and molecular characterization of genetic loci involved in polymyxin B resistance. Antimicrob Agents Chemother 43, 2648-2656.
4. Ceymann, A., Horstmann, M., Ehses, P., Schweimer, K., Paschke, A. K., Steinert, M. & Faber, C. (2008). Solution structure of the Legionella pneumophila Mip-rapamycin complex. BMC Struct Biol 8, 17.
5. Choi, K. H., Mima, T., Casart, Y., Rholl, D., Kumar, A., Beacham, I. R. & Schweizer, H. P. (2008). Genetic tools for select-agent-compliant manipulation of Burkholderia pseudomallei. Appl Environ Microbiol 74, 1064-1075.
6. Cianciotto, N. P., Eisenstein, B. I., Mody, C. H., Toews, G. B. & Engleberg, N. C. (1989). A Legionella pneumophila gene encoding a species-specific surface protein potentiates initiation of intracellular infection. Infect Immun 57, 1255-1262.
7. Cunningham, F. X., Jr, Lafond, T. P. & Gantt, E. (2000). Evidence of a role for LytB in the nonmevalonate pathway of isoprenoid biosynthesis. J Bacteriol 182, 5841-5848.
8. Currie, B. J. & Jacups, S. P. (2003). Intensity of rainfall and severity of melioidosis, Australia. Emerg Infect Dis 9, 1538-1542.
9. Eske, K., Breitbach, K., Köhler, J., Wongprompitak, P. & Steinmetz, I. (2009). Generation of murine bone marrow derived macrophages in a standardised serum-free cell culture system. J Immunol Methods 342, 13-19.
10. Eswar, N., Webb, B., Marti-Renom, M. A., Madhusudhan, M. S., Eramian, D., Shen, M. Y., Pieper, U. & Sali, A. (2006). Comparative protein structure modeling using Modeller. Curr Protoc Bioinformatics Chapter 5, Unit 5.6.
11. Fischer, G. & Aumüller, T. (2003). Regulation of peptide bond cis/ trans isomerization by enzyme catalysis and its implication in physiological processes. Rev Physiol Biochem Pharmacol 148, 105-150.
12. Fischer, G., Bang, H. & Mech, C. (1984). [Determination of enzymatic catalysis for the cis-trans-isomerization of peptide binding in prolinecontaining peptides]. Biomed Biochim Acta 43, 1101-1111 (in German).
13. Fischer, G., Bang, H., Ludwig, B., Mann, K. & Hacker, J. (1992). Mip protein of Legionella pneumophila exhibits peptidyl-prolyl-cis/trans isomerase (PPlase) activity. Mol Microbiol 6, 1375-1383.
14. Gough, J., Karplus, K., Hughey, R. & Chothia, C. (2001). Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J Mol Biol 313, 903-919.
15. Gustafson, C. E., Kaul, S. & Ishiguro, E. E. (1993). Identification of the Escherichia coli lytB gene, which is involved in penicillin tolerance and control of the stringent response. J Bacteriol 175, 1203-1205.
16. Harding, M. W., Galat, A., Uehling, D. E. & Schreiber, S. L. (1989). A receptor for the immunosuppressant FK506 is a cis-trans peptidylprolyl isomerase. Nature 341, 758-760.
17. Helbig, J. H., König, B., Knospe, H., Bubert, B., Yu, C., Lück, C. P., Riboldi-Tunnicliffe, A., Hilgenfeld, R., Jacobs, E. & other authors (2003). The PPIase active site of Legionella pneumophila Mip protein is involved in the infection of eukaryotic host cells. Biol Chem 384, 125-137.
18. Holden, M. T., Titball, R. W., Peacock, S. J., Cerdeño-Tárraga, A. M., Atkins, T., Crossman, L. C., Pitt, T., Churcher, C., Mungall, K. & other authors (2004). Genomic plasticity of the causative agent of melioidosis, Burkholderia pseudomallei. Proc Natl Acad Sci U S A 101, 14240-14245.
19. Horne, S. M., Kottom, T. J., Nolan, L. K. & Young, K. D. (1997). Decreased intracellular survival of an fkpA mutant of Salmonella typhimurium Copenhagen. Infect Immun 65, 806-810.
20. Hottenrott, S., Schumann, T., Plückthun, A., Fischer, G. & Rahfeld, J. U. (1997). The Escherichia coli SlyD is a metal ion-regulated peptidyl-prolyl cis/trans-isomerase. J Biol Chem 272, 15697-15701.
21. Ikura, T. & Ito, N. (2007). Requirements for peptidyl-prolyl isomerization activity: a comprehensive mutational analysis of the substrate-binding cavity of FK506-binding protein 12. Protein Sci 16, 2618-2625.
22. Inglis, T. J. & Sagripanti, J. L. (2006). Environmental factors that affect the survival and persistence of Burkholderia pseudomallei. Appl Environ Microbiol 72, 6865-6875.
23. Janowski, B., Wöllner, S., Schutkowski, M. & Fischer, G. (1997). A protease-free assay for peptidyl prolyl cis/trans isomerases using standard peptide substrates. Anal Biochem 252, 299-307.
24. Justice, S. S., Hunstad, D. A., Harper, J. R., Duguay, A. R., Pinkner, J. S., Bann, J., Frieden, C., Silhavy, T. J. & Hultgren, S. J. (2005). Periplasmic peptidyl prolyl cis-trans isomerases are not essential for viability, but SurA is required for pilus biogenesis in Escherichia coli. J Bacteriol 187, 7680-7686.
25. Justice, S. S., Lauer, S. R., Hultgren, S. J. & Hunstad, D. A. (2006). Maturation of intracellular Escherichia coli communities requires SurA. Infect Immun 74, 4793-4800.
26. Knappe, T. A., Eckert, B., Schaarschmidt, P., Scholz, C. & Schmid, F. X. (2007). Insertion of a chaperone domain converts FKBP12 into a powerful catalyst of protein folding. J Mol Biol 368, 1458-1468.
27. Kofron, J. L., Kuzmic, P., Kishore, V., Colón-Bonilla, E. & Rich, D. H. (1991). Determination of kinetic constants for peptidyl prolyl cis-trans isomerases by an improved spectrophotometric assay. Biochemistry 30, 6127-6134.
28. Köhler, R., Fanghänel, J., König, B., Lüneberg, E., Frosch, M., Rahfeld, J. U., Hilgenfeld, R., Fischer, G., Hacker, J. & Steinert, M. (2003). Biochemical and functional analyses of the Mip protein: influence of the N-terminal half and of peptidylprolyl isomerase activity on the virulence of Legionella pneumophila. Infect Immun 71, 4389-4397.
29. Lazar, S. W. & Kolter, R. (1996). SurA assists the folding of Escherichia coli outer membrane proteins. J Bacteriol 178, 1770-1773.
30. Leuzzi, R., Serino, L., Scarselli, M., Savino, S., Fontana, M. R., Monaci, E., Taddei, A., Fischer, G., Rappuoli, R. & Pizza, M. (2005). Ng-MIP, a surface-exposed lipoprotein of Neisseria gonorrhoeae, has a peptidyl-prolyl cis/trans isomerase (PPIase) activity and is involved in persistence in macrophages. Mol Microbiol 58, 669-681.
31. Lovell, S. C., Davis, I. W., Arendall, W. B., III, de Bakker, P. I., Word, J. M., Prisant, M. G., Richardson, J. S. & Richardson, D. C. (2003). Structure validation by Ca geometry: w, y and Cb deviation. Proteins 50, 437-450.
32. Löw, C., Neumann, P., Tidow, H., Weininger, U., Haupt, C., Friedrich-Epler, B., Scholz, C., Stubbs, M. T. & Balbach, J. (2010). Crystal structure determination and functional characterization of the metallochaperone SlyD from Thermus thermophilus. J Mol Biol 398, 375-390.
33. Lundemose, A. G., Kay, J. E. & Pearce, J. H. (1993). Chlamydia trachomatis Mip-like protein has peptidyl-prolyl cis/trans isomerase activity that is inhibited by FK506 and rapamycin and is implicated in initiation of chlamydial infection. Mol Microbiol 7, 777-783.
34. Lupyan, D., Leo-Macias, A. & Ortiz, A. R. (2005). A new progressiveiterative algorithm for multiple structure alignment. Bioinformatics 21, 3255-3263.
35. Malik, K. M. (1997). Chemometric and Quantum Mechanical Methods to Analyse CD Data. London: University of London.
36. Mizuguchi, K., Deane, C. M., Blundell, T. L., Johnson, M. S. & Overington, J. P. (1998). JOY: protein sequence-structure representation and analysis. Bioinformatics 14, 617-623.
37. Moro, A., Ruiz-Cabello, F., Fernández-Cano, A., Stock, R. P. & González, A. (1995). Secretion by Trypanosoma cruzi of a peptidylprolyl cis-trans isomerase involved in cell infection. EMBO J 14, 2483-2490.
38. Ngauy, V., Lemeshev, Y., Sadkowski, L. & Crawford, G. (2005). Cutaneous melioidosis in a man who was taken as a prisoner of war by the Japanese during WorldWar II. J ClinMicrobiol 43, 970-972.
39. Pilatz, S., Breitbach, K., Hein, N., Fehlhaber, B., Schulze, J., Brenneke, B., Eberl, L. & Steinmetz, I. (2006). Identification of Burkholderia pseudomallei genes required for the intracellular life cycle and in vivo virulence. Infect Immun 74, 3576-3586.
40. Rotz, L. D., Khan, A. S., Lillibridge, S. R., Ostroff, S. M. & Hughes, J. M. (2002). Public health assessment of potential biological terrorism agents. Emerg Infect Dis 8, 225-230.
41. Rouvière, P. E. & Gross, C. A. (1996). SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins. Genes Dev 10, 3170-3182.
42. Schreiber, S. L. (1991). Chemistry and biology of the immunophilins and their immunosuppressive ligands. Science 251, 283-287.
43. Shi, J., Blundell, T. L. & Mizuguchi, K. (2001). FUGUE: sequencestructure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J Mol Biol 310, 243-257.
44. Suzuki, R., Nagata, K., Yumoto, F., Kawakami, M., Nemoto, N., Furutani, M., Adachi, K., Maruyama, T. & Tanokura, M. (2003). Threedimensional solution structure of an archaeal FKBP with a dual function of peptidyl prolyl cis-trans isomerase and chaperone-like activities. J Mol Biol 328, 1149-1160.
45. Sydenham, M., Douce, G., Bowe, F., Ahmed, S., Chatfield, S. & Dougan, G. (2000). Salmonella enterica serovar typhimurium surA mutants are attenuated and effective live oral vaccines. Infect Immun 68, 1109-1115.
46. Tormo, A., Almirón, M. & Kolter, R. (1990). surA, an Escherichia coli gene essential for survival in stationary phase. J Bacteriol 172, 4339-4347.
47. Wagner, C., Khan, A. S., Kamphausen, T., Schmausser, B., Unal, C., Lorenz, U., Fischer, G., Hacker, J. & Steinert, M. (2007). Collagen binding protein Mip enables Legionella pneumophila to transmigrate through a barrier of NCI-H292 lung epithelial cells and extracellular matrix. Cell Microbiol 9, 450-462.
48. Watts, K. M. & Hunstad, D. A. (2008). Components of SurA required for outer membrane biogenesis in uropathogenic Escherichia coli. PLoS ONE 3, e3359.
49. Weininger, U., Haupt, C., Schweimer, K., Graubner, W., Kovermann, M., Brüser, T., Scholz, C., Schaarschmidt, P., Zoldak, G. & Schmid, F. X. (2009). NMR solution structure of SlyD from Escherichia coli: spatial separation of prolyl isomerase and chaperone function. J Mol Biol 387, 295-305.
50. White, N. J. (2003). Melioidosis. Lancet 361, 1715-1722.
51. Wintermeyer, E., Ludwig, B., Steinert, M., Schmidt, B., Fischer, G. & Hacker, J. (1995). Influence of site specifically altered Mip proteins on intracellular survival of Legionella pneumophila in eukaryotic cells. Infect Immun 63, 4576-4583.
52. Wülfing, C., Lombardero, J. & Plückthun, A. (1994). An Escherichia coli protein consisting of a domain homologous to FK506-binding proteins (FKBP) and a new metal binding motif. J Biol Chem 269, 2895-2901.
53. Wuthiekanun, V., Smith, M. D., Dance, D. A., Walsh, A. L., Pitt, T. L. & White, N. J. (1996). Biochemical characteristics of clinical and environmental isolates of Burkholderia pseudomallei. J Med Microbiol 45, 408-412.
54. Zhang, J. W., Leach, M. R. & Zamble, D. B. (2007). The peptidyl-prolyl isomerase activity of SlyD is not required for maturation of Escherichia coli hydrogenase. J Bacteriol 189, 7942-7944.