The peptide chain release factor methyltransferase PrmC is essential for pathogenicity and environmental adaptation of Pseudomonas aeruginosa PA14

Environmental Microbiology

Volumn 15, Issue 2, 2013, Pages 597-609

  Pustelny, Christian ^a,b   Brouwer, Stephan ^a,b   Müsken, Mathias ^a,b   Bielecka, Agata ^a,b   Dötsch, Andreas ^a,b   Nimtz, Manfred ^a   Häussler, Susanne ^a,b  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^b INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; METHYLTRANSFERASE; VIRULENCE FACTOR;

ADAPTATION; ANIMAL; ARTICLE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; METABOLISM; MICROBIOLOGY; MOTH; MUTATION; PATHOGENICITY; PROTEOMICS; PSEUDOMONAS AERUGINOSA; QUORUM SENSING;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; LARVA; METHYLTRANSFERASES; MOTHS; MUTATION; PROTEOMICS; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; VIRULENCE FACTORS;

ESCHERICHIA COLI; GALLERIA MELLONELLA; PSEUDOMONAS AERUGINOSA;

EID: 84873115953     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12040     Document Type: Article

References (67)

1. Aendekerk, S., Diggle, S.P., Song, Z., Hoiby, N., Cornelis, P., Williams, P., and Camara, M. (2005) The MexGHI-OpmD multidrug efflux pump controls growth, antibiotic susceptibility and virulence in Pseudomonas aeruginosa via 4-quinolone-dependent cell-to-cell communication. Microbiology 151: 1113-1125.
2. Ankenbauer, R.G., and Quan, H.N. (1994) FptA, the Fe(III)-pyochelin receptor of Pseudomonas aeruginosa: a phenolate siderophore receptor homologous to hydroxamate siderophore receptors. J Bacteriol 176: 307-319.
3. Aperis, G., Fuchs, B.B., Anderson, C.A., Warner, J.E., Calderwood, S.B., and Mylonakis, E. (2007) Galleria mellonella as a model host to study infection by the Francisella tularensis live vaccine strain. Microbes Infect 9: 729-734.
4. Arai, H., Mizutani, M., and Igarashi, Y. (2003) Transcriptional regulation of the nos genes for nitrous oxide reductase in Pseudomonas aeruginosa. Microbiology 149: 29-36.
5. Armstrong, S., Yates, S.P., and Merrill, A.R. (2002) Insight into the catalytic mechanism of Pseudomonas aeruginosa exotoxin A. Studies of toxin interaction with eukaryotic elongation factor-2. J Biol Chem 277: 46669-46675.
6. Bergin, D., Murphy, L., Keenan, J., Clynes, M., and Kavanagh, K. (2006) Pre-exposure to yeast protects larvae of Galleria mellonella from a subsequent lethal infection by Candida albicans and is mediated by the increased expression of antimicrobial peptides. Microbes Infect 8: 2105-2112.
7. Blackwood, L.L., Stone, R.M., Iglewski, B.H., and Pennington, J.E. (1983) Evaluation of Pseudomonas aeruginosa exotoxin A and elastase as virulence factors in acute lung infection. Infect Immun 39: 198-201.
8. Bodey, G.P., Bolivar, R., Fainstein, V., and Jadeja, L. (1983) Infections caused by Pseudomonas aeruginosa. Rev Infect Dis 5: 279-313.
9. Braun, V. (2001) Iron uptake mechanisms and their regulation in pathogenic bacteria. Int J Med Microbiol 291: 67-79.
10. Bredenbruch, F., Nimtz, M., Wray, V., Morr, M., Muller, R., and Haussler, S. (2005) Biosynthetic pathway of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines. J Bacteriol 187: 3630-3635.
11. Caiazza, N.C., Shanks, R.M., and O'Toole, G.A. (2005) Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J Bacteriol 187: 7351-7361.
12. Champion, O.L., Cooper, I.A., James, S.L., Ford, D., Karlyshev, A., Wren, B.W., etal. (2009) Galleria mellonella as an alternative infection model for Yersinia pseudotuberculosis. Microbiology 155: 1516-1522.
13. Chastre, J., and Fagon, J.Y. (2002) Ventilator-associated pneumonia. Am J Respir Crit Care Med 165: 867-903.
14. Chugani, S., and Greenberg, E.P. (2007) The influence of human respiratory epithelia on Pseudomonas aeruginosa gene expression. Microb Pathog 42: 29-35.
15. Colson, C. (1977) Genetics of ribosomal protein methylation in Escherichia coli. I. A mutant deficient in methylation of protein L11. Mol Gen Genet 154: 167-173.
16. Cox, C.D. (1980) Iron uptake with ferripyochelin and ferric citrate by Pseudomonas aeruginosa. J Bacteriol 142: 581-587.
17. Deziel, E., Lepine, F., Milot, S., He, J., Mindrinos, M.N., Tompkins, R.G., and Rahme, L.G. (2004) Analysis of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines (HAQs) reveals a role for 4-hydroxy-2-heptylquinoline in cell-to-cell communication. Proc Natl Acad Sci USA 101: 1339-1344.
18. Diggle, S.P., Winzer, K., Chhabra, S.R., Worrall, K.E., Camara, M., and Williams, P. (2003) The Pseudomonas aeruginosa quinolone signal molecule overcomes the cell density-dependency of the quorum sensing hierarchy, regulates rhl-dependent genes at the onset of stationary phase and can be produced in the absence of LasR. Mol Microbiol 50: 29-43.
19. Diggle, S.P., Matthijs, S., Wright, V.J., Fletcher, M.P., Chhabra, S.R., Lamont, I.L., etal. (2007) The Pseudomonas aeruginosa 4-quinolone signal molecules HHQ and PQS play multifunctional roles in quorum sensing and iron entrapment. Chem Biol 14: 87-96.
20. Dötsch, A., Eckweiler, D., Schniederjans, M., Zimmermann, A., Jensen, V., Scharfe, M., etal. (2012) The Pseudomonas aeruginosa transcriptome in planktonic cultures and static biofilms using RNA sequencing. PLoS ONE 7: e31092.
21. Elsheikh, L.E., Kronevi, T., Wretlind, B., Abaas, S., and Iglewski, B.H. (1987) Assessment of elastase as a Pseudomonas aeruginosa virulence factor in experimental lung infection in mink. Vet Microbiol 13: 281-289.
22. Engel, J., and Balachandran, P. (2009) Role of Pseudomonas aeruginosa type III effectors in disease. Curr Opin Microbiol 12: 61-66.
23. Farrow, J.M., 3rd, Sund, Z.M., Ellison, M.L., Wade, D.S., Coleman, J.P., and Pesci, E.C. (2008) PqsE functions independently of PqsR-Pseudomonas quinolone signal and enhances the rhl quorum-sensing system. J Bacteriol 190: 7043-7051.
24. Fedhila, S., Daou, N., Lereclus, D., and Nielsen-LeRoux, C. (2006) Identification of Bacillus cereus internalin and other candidate virulence genes specifically induced during oral infection in insects. Mol Microbiol 62: 339-355.
25. Figaro, S., Scrima, N., Buckingham, R.H., and Heurgue-Hamard, V. (2008) HemK2 protein, encoded on human chromosome 21, methylates translation termination factor eRF1. FEBS Lett 582: 2352-2356.
26. Folders, J., Algra, J., Roelofs, M.S., van Loon, L.C., Tommassen, J., and Bitter, W. (2001) Characterization of Pseudomonas aeruginosa chitinase, a gradually secreted protein. J Bacteriol 183: 7044-7052.
27. Gallagher, L.A., McKnight, S.L., Kuznetsova, M.S., Pesci, E.C., and Manoil, C. (2002) Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J Bacteriol 184: 6472-6480.
28. Garbom, S., Olofsson, M., Bjornfot, A.C., Srivastava, M.K., Robinson, V.L., Oyston, P.C., etal. (2007) Phenotypic characterization of a virulence-associated protein, VagH, of Yersinia pseudotuberculosis reveals a tight link between VagH and the type III secretion system. Microbiology 153: 1464-1473.
29. Garcia-Lara, J., Needham, A.J., and Foster, S.J. (2005) Invertebrates as animal models for Staphylococcus aureus pathogenesis: a window into host-pathogen interaction. FEMS Immunol Med Microbiol 43: 311-323.
30. Gething, M.J., and Sambrook, J. (1992) Protein folding in the cell. Nature 355: 33-45.
31. Glessner, A., Smith, R.S., Iglewski, B.H., and Robinson, J.B. (1999) Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of twitching motility. J Bacteriol 181: 1623-1629.
32. Hauser, A.R. (2009) The type III secretion system of Pseudomonas aeruginosa: infection by injection. Nat Rev Microbiol 7: 654-665.
33. Hazan, R., He, J., Xiao, G., Dekimpe, V., Apidianakis, Y., Lesic, B., etal. (2010) Homeostatic interplay between bacterial cell-cell signaling and iron in virulence. PLoS Pathog 6: e1000810.
34. Heurgue-Hamard, V., Champ, S., Engstrom, A., Ehrenberg, M., and Buckingham, R.H. (2002) The hemK gene in Escherichia coli encodes the N(5)-glutamine methyltransferase that modifies peptide release factors. EMBO J 21: 769-778.
35. Heurgue-Hamard, V., Champ, S., Mora, L., Merkulova-Rainon, T., Kisselev, L.L., and Buckingham, R.H. (2005) The glutamine residue of the conserved GGQ motif in Saccharomyces cerevisiae release factor eRF1 is methylated by the product of the YDR140w gene. J Biol Chem 280: 2439-2445.
36. Hong, Y.Q., and Ghebrehiwet, B. (1992) Effect of Pseudomonas aeruginosa elastase and alkaline protease on serum complement and isolated components C1q and C3. Clin Immunol Immunopathol 62: 133-138.
37. Hornef, M.W., Roggenkamp, A., Geiger, A.M., Hogardt, M., Jacobi, C.A., and Heesemann, J. (2000) Triggering the ExoS regulon of Pseudomonas aeruginosa: a GFP-reporter analysis of exoenzyme (Exo) S, ExoT and ExoU synthesis. Microb Pathog 29: 329-343.
38. Hutchison, M.L., and Govan, J.R. (1999) Pathogenicity of microbes associated with cystic fibrosis. Microbes Infect 1: 1005-1014.
39. Jander, G., Rahme, L.G., and Ausubel, F.M. (2000) Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J Bacteriol 182: 3843-3845.
40. John, M., Kudva, I.T., Griffin, R.W., Dodson, A.W., McManus, B., Krastins, B., etal. (2005) Use of in vivo-induced antigen technology for identification of Escherichia coli O157:H7 proteins expressed during human infection. Infect Immun 73: 2665-2679.
41. Kessler, E., Safrin, M., Olson, J.C., and Ohman, D.E. (1993) Secreted LasA of Pseudomonas aeruginosa is a staphylolytic protease. J Biol Chem 268: 7503-7508.
42. Konig, B., Jaeger, K.E., Sage, A.E., Vasil, M.L., and Konig, W. (1996) Role of Pseudomonas aeruginosa lipase in inflammatory mediator release from human inflammatory effector cells (platelets, granulocytes, and monocytes). Infect Immun 64: 3252-3258.
43. Latifi, A., Foglino, M., Tanaka, K., Williams, P., and Lazdunski, A. (1996) A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol Microbiol 21: 1137-1146.
44. Liberati, N.T., Urbach, J.M., Miyata, S., Lee, D.G., Drenkard, E., Wu, G., etal. (2006) An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc Natl Acad Sci USA 103: 2833-2838.
45. Lyczak, J.B., Cannon, C.L., and Pier, G.B. (2000) Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect 2: 1051-1060.
46. Lyczak, J.B., Cannon, C.L., and Pier, G.B. (2002) Lung infections associated with cystic fibrosis. Clin Microbiol Rev 15: 194-222.
47. McGrath, S., Wade, D.S., and Pesci, E.C. (2004) Dueling quorum sensing systems in Pseudomonas aeruginosa control the production of the Pseudomonas quinolone signal (PQS). FEMS Microbiol Lett 230: 27-34.
48. Mavrodi, D.V., Bonsall, R.F., Delaney, S.M., Soule, M.J., Phillips, G., and Thomashow, L.S. (2001) Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa PAO1. J Bacteriol 183: 6454-6465.
49. Miyata, S., Casey, M., Frank, D.W., Ausubel, F.M., and Drenkard, E. (2003) Use of the Galleria mellonella caterpillar as a model host to study the role of the type III secretion system in Pseudomonas aeruginosa pathogenesis. Infect Immun 71: 2404-2413.
50. Mukherjee, K., Altincicek, B., Hain, T., Domann, E., Vilcinskas, A., and Chakraborty, T. (2010) Galleria mellonella as a model system for studying Listeria pathogenesis. Appl Environ Microbiol 76: 310-317.
51. Mylonakis, E., Moreno, R., El Khoury, J.B., Idnurm, A., Heitman, J., Calderwood, S.B., etal. (2005) Galleria mellonella as a model system to study Cryptococcus neoformans pathogenesis. Infect Immun 73: 3842-3850.
52. Nakahigashi, K., Kubo, N., Narita, S., Shimaoka, T., Goto, S., Oshima, T., etal. (2002) HemK, a class of protein methyl transferase with similarity to DNA methyl transferases, methylates polypeptide chain release factors, and hemK knockout induces defects in translational termination. Proc Natl Acad Sci USA 99: 1473-1478.
53. Ochsner, U.A., Koch, A.K., Fiechter, A., and Reiser, J. (1994) Isolation and characterization of a regulatory gene affecting rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. J Bacteriol 176: 2044-2054.
54. Ochsner, U.A., Reiser, J., Fiechter, A., and Witholt, B. (1995) Production of Pseudomonas aeruginosa rhamnolipid biosurfactants in heterologous hosts. Appl Environ Microbiol 61: 3503-3506.
55. Pannekoek, Y., Heurgue-Hamard, V., Langerak, A.A., Speijer, D., Buckingham, R.H., and van der Ende, A. (2005) The N5-glutamine S-adenosyl-l-methionine-dependent methyltransferase PrmC/HemK in Chlamydia trachomatis methylates class 1 release factors. J Bacteriol 187: 507-511.
56. Park, S.Y., Kim, K.M., Lee, J.H., Seo, S.J., and Lee, I.H. (2007) Extracellular gelatinase of Enterococcus faecalis destroys a defense system in insect hemolymph and human serum. Infect Immun 75: 1861-1869.
57. Park, Y., Yilmaz, O., Jung, I.Y., and Lamont, R.J. (2004) Identification of Porphyromonas gingivalis genes specifically expressed in human gingival epithelial cells by using differential display reverse transcription-PCR. Infect Immun 72: 3752-3758.
58. Pesci, E.C., Milbank, J.B., Pearson, J.P., McKnight, S., Kende, A.S., Greenberg, E.P., and Iglewski, B.H. (1999) Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 96: 11229-11234.
59. Polevoda, B., Span, L., and Sherman, F. (2006) The yeast translation release factors Mrf1p and Sup45p (eRF1) are methylated, respectively, by the methyltransferases Mtq1p and Mtq2p. J Biol Chem 281: 2562-2571.
60. Rampioni, G., Pustelny, C., Fletcher, M.P., Wright, V.J., Bruce, M., Rumbaugh, K.P., etal. (2010) Transcriptomic analysis reveals a global alkyl-quinolone-independent regulatory role for PqsE in facilitating the environmental adaptation of Pseudomonas aeruginosa to plant and animal hosts. Environ Microbiol 12: 1659-1673.
61. Schuster, M., Lostroh, C.P., Ogi, T., and Greenberg, E.P. (2003) Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 185: 2066-2079.
62. Verstraeten, N., Braeken, K., Debkumari, B., Fauvart, M., Fransaer, J., Vermant, J., and Michiels, J. (2008) Living on a surface: swarming and biofilm formation. Trends Microbiol 16: 496-506.
63. Webb, J.S., Thompson, L.S., James, S., Charlton, T., Tolker-Nielsen, T., Koch, B., etal. (2003) Cell death in Pseudomonas aeruginosa biofilm development. J Bacteriol 185: 4585-4592.
64. Wilhelm, S., Gdynia, A., Tielen, P., Rosenau, F., and Jaeger, K.E. (2007) The autotransporter esterase EstA of Pseudomonas aeruginosa is required for rhamnolipid production, cell motility, and biofilm formation. J Bacteriol 189: 6695-6703.
65. Williams, P., and Camara, M. (2009) Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Curr Opin Microbiol 12: 182-191.
66. Xu, H., Lin, W., Xia, H., Xu, S., Li, Y., Yao, H., etal. (2005) Influence of ptsP gene on pyocyanin production in Pseudomonas aeruginosa. FEMS Microbiol Lett 253: 103-109.
67. 2O) to dinitrogen by Bacteria and Archaea. Adv Microbial Physiol 52: 107-227.