Glycosylation is required for outer membrane localization of the lectin LecB in Pseudomonas aeruginosa

Journal of Bacteriology

Volumn 193, Issue 5, 2011, Pages 1107-1113

  Bartels, Kai Malte ^a   Funken, Horst ^a   Knapp, Andreas ^a   Brocker, Melanie ^b   Bott, Michael ^b   Wilhelm, Susanne ^a   Jaeger, Karl Erich ^a   Rosenau, Frank ^a,c  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

^c UNIVERSITY OF ULM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LECTIN; LECTIN B; MANNOSE; OUTER MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CYTOPLASM; ENZYME ASSAY; GLYCOSYLATION; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; PSEUDOMONAS AERUGINOSA; SITE DIRECTED MUTAGENESIS;

CELL MEMBRANE; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GLYCOSYLATION; LECTINS; MOLECULAR WEIGHT; MUTAGENESIS, SITE-DIRECTED; PERIPLASM; PROTEIN TRANSPORT; PSEUDOMONAS AERUGINOSA;

PSEUDOMONAS AERUGINOSA;

EID: 79951634140     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01507-10     Document Type: Article

References (63)

1. Abu-Qarn, M., J. Eichler, and N. Sharon. 2008. Not just for Eukarya anymore: protein glycosylation in Bacteria and Archaea. Curr. Opin. Struct. Biol. 18:544-550.
2. Adam, E. C., B. S. Mitchell, D. U. Schumacher, G. Grant, and U. Schumacher. 1997. P. aeruginosa PA-II lectin stops human ciliary beating: therapeutic implications of fucose. Am. J. Respir. Crit. Care Med. 155:2102-2104.
3. Adam, E. C., D. U. Schumacher, and U. Schumacher. 1997. Cilia from a cystic fibrosis patient react to cilitoxic Pseudomonas aeruginosa II lectin in a similar manner to normal control cilia - a case report. J. Laryngol. Otol. 111:760-762.
4. Beachey, E. H. 1980. Bacterial adherence. Chapman and Hall, London, England.
5. Beuth, J., B. Stoffel, H. L. Ko, J. Jeljaszewicz, and G. Pulverer. 1995. Mistellektin-1: neue therapeutische Perspektiven in der Onkologie. Onkologie 18:36-40.
6. Burrows, L. L. 2005. Weapons of mass retraction. Mol. Microbiol. 57:878-888.
7. Castric, P., F. J. Cassels, and R. W. Carlson. 2001. Structural characterization of the Pseudomonas aeruginosa 1244 pilin glycan. J. Biol. Chem. 276: 26479-26485.
8. de Smet, M. J., J. Kingma, and B. Witholt. 1978. The effect of toluene on the structure and permeability of the outer and cytoplasmic membranes of Escherichia coli. Biochim. Biophys. Acta 506:64-80. (Pubitemid 8237845)
9. Gabius, H. J., S. Andre, H. Kaltner, and H. C. Siebert. 2002. The sugar code: functional lectinomics. Biochim. Biophys. Acta 1572:165-177.
10. Garber, N. C., U. Guempel, N. Gilboa-Garber, and R. J. Doyle. 1987. Specificity of the fucose-binding lectin of Pseudomonas aeruginosa. FEMS Microbiol. Lett. 48:331-334.
11. Gilboa-Garber, N. 1982. Pseudomonas aeruginosa lectins. Methods Enzymol. 83:378-385.
12. Gilboa-Garber, N., and N. Garber. 1992. Microbial lectins, p. 541-591. In H. J. Allen and E. C. Kisailus (ed.), Glycoconjugates: composition, structure and function. M. Dekker, Inc., New York, NY.
13. Gilboa-Garber, N., D. J. Katcoff, and N. C. Garber. 2000. Identification and characterization of Pseudomonas aeruginosa PA-IIL lectin gene and protein compared to PA-IL. FEMS Immunol. Med. Microbiol. 29:53-57.
14. Glick, J., and N. Garber. 1983. The intracellular localization of Pseudomonas aeruginosa lectins. J. Gen. Microbiol. 129:3085-3090.
15. Hardie, K. R., S. Pommier, and S. Wilhelm. 2009. The secreted proteins of Pseudomonas aeruginosa: their export machineries, and how they contribute to pathogenesis, p. 451-458. In K. Wooldridge (ed.), Bacterial secreted proteins: secretory mechanisms and role in pathogenesis. Caister Academic Press, Norwich, United Kingdom.
16. Hauber, H. P., et al. 2008. Inhalation with fucose and galactose for treatment of Pseudomonas aeruginosa in cystic fibrosis patients. Int. J. Med. Sci. 5:371-376.
17. Hegge, F. T., et al. 2004. Unique modifications with phosphocholine and phosphoethanolamine define alternate antigenic forms of Neisseria gonorrhoeae type IV pili. Proc. Natl. Acad. Sci. U. S. A. 101:10798-10803. (Pubitemid 38955822)
18. Hitchen, P. G., and A. Dell. 2006. Bacterial glycoproteomics. Microbiology 152:1575-1580.
19. Holloway, B. W., V. Krishnapillai, and A. F. Morgan. 1979. Chromosomal genetics of Pseudomonas. Microbiol. Rev. 43:73-102.
20. Hung, C. S., et al. 2002. Structural basis of tropism of Escherichia coli to the bladder during urinary tract infection. Mol. Microbiol. 44:903-915.
21. Imberty, A., E. P. Mitchell, and M. Wimmerová. 2005. Structural basis of high-affinity glycan recognition by bacterial and fungal lectins. Curr. Opin. Struct. Biol. 15:525-534.
22. Johansson, E. M., et al. 2008. Inhibition and dispersion of Pseudomonas aeruginosa biofilms by glycopeptide dendrimers targeting the fucose-specific lectin LecB. Chem. Biol. 15:1249-1257.
23. Kolomiets, E., et al. 2009. Glycopeptide dendrimers with high affinity for the fucose-binding lectin LecB from Pseudomonas aeruginosa. Chem. Med. Chem. 4:562-569.
24. Kovach, M. E., R. W. Phillips, P. H. Elzer, R. M. Roop II, and K. M. Peterson. 1994. pBBR1MCS: a broad-host-range cloning vector. Biotechniques 16:800-802.
25. Kowarik, M., et al. 2006. Definition of the bacterial N-glycosylation site consensus sequence. EMBO J. 25:1957-1966.
26. Lengeler, K. B., D. Tielker, and J. F. Ernst. 2008. Protein-O- mannosyltransferases in virulence and development. Cell Mol. Life Sci. 65:528-544.
27. Lindhout, T., P. C. Lau, D. Brewer, and J. S. Lam. 2009. Truncation in the core oligosaccharide of lipopolysaccharide affects flagella-mediated motility in Pseudomonas aeruginosa PAO1 via modulation of cell surface attachment. Microbiology 155:3449-3460.
28. Loris, R., D. Tielker, K.-E.Jaeger, and L. Wyns. 2003. Structural basis of carbohydrate recognition by the lectin LecB from Pseudomonas aeruginosa. J. Mol. Biol. 331:861-870. (Pubitemid 36945440)
29. Lyczak, J. B., C. L. Cannon, and G. B. Pier. 2002. Lung infections associated with cystic fibrosis. Clin. Microbiol. Rev. 15:194-222.
30. Ma, Q., et al. 2003. Protein secretion systems of Pseudomonas aeruginosa and P. fluorescens. Biochim. Biophys. Acta 1611:223-233. (Pubitemid 36351451)
31. Mewe, M., et al. 2005. Pseudomonas aeruginosa lectins I and II and their interaction with human airway cilia. J. Laryngol. Otol. 119:595-599.
32. Mitchell, E., et al. 2002. Structural basis for oligosaccharide-mediated adhesion of Pseudomonas aeruginosa in the lungs of cystic fibrosis patients. Nat. Struct. Biol. 9:918-921.
33. Mitchell, E. P., et al. 2005. High affinity fucose binding of Pseudomonas aeruginosa lectin PA-IIL: 1.0 Å resolution crystal structure of the complex combined with thermodynamics and computational chemistry approaches. Proteins 58:735-746.
34. Nilsson, C. L. 2007. Lectins: analytical tools from nature, p. 1-13. In C. L. Nilsson (ed.), Lectins: analytical technologies. Elsevier, Oxford, United Kingdom.
35. Ramphal, R., and S. K. Arora. 2001. Recognition of mucin components by Pseudomonas aeruginosa. Glycoconj. J. 18:709-713.
36. Rosenau, F., and K. Jaeger. 2000. Bacterial lipases from Pseudomonas: regulation of gene expression and mechanisms of secretion. Biochimie 82: 1023-1032.
37. Rudd, P. M., T. Elliott, P. Cresswell, I. A. Wilson, and R. A. Dwek. 2001. Glycosylation and the immune system. Science 291:2370-2376.
38. Scanlin, T. F., and M. C. Glick. 2001. Glycosylation and the cystic fibrosis transmembrane conductance regulator. Respir. Res. 2:276-279.
39. Schirm, M., et al. 2004. Structural, genetic, and functional characterization of the flagellin glycosylation process in Helicobacter pylori. J. Bacteriol. 186: 6721-6727.
40. Schirm, M., et al. 2004. Structural and genetic characterization of glycosylation of type a flagellin in Pseudomonas aeruginosa. J. Bacteriol. 186:2523-2531. (Pubitemid 38525904)
41. Shevchenko, A., M. Wilm, O. Vorm, and M. Mann. 1996. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 68:850-858.
42. Simon, R., M. O'Connell, M. Labes, and A. Puhler. 1986. Plasmid vectors for the genetic analysis and manipulation of Rhizobia and other gram-negative bacteria. Methods Enzymol. 118:640-659.
43. Skropeta, D. 2009. The effect of individual N-glycans on enzyme activity. Bioorg. Med. Chem. 17:2645-2653.
44. Sonawane, A., J. Jyot, and R. Ramphal. 2006. Pseudomonas aeruginosa LecB is involved in pilus biogenesis and protease IV activity but not in adhesion to respiratory mucins. Infect. Immun. 74:7035-7039.
45. Steinberger, R. E., A. R. Allen, H. G. Hansa, and P. A. Holden. 2002. Elongation correlates with nutrient deprivation in Pseudomonas aeruginosaunsaturates biofilms. Microb. Ecol. 43:416-423.
46. Steuer, M. K., et al. 1993. Hemmung der bakteriellen Adhäsion durch Lektinblockade bei durch Pseudomonas aeruginosa induzierter Otitis externa im Vergleich zur lokalen Therapie mit Antibiotika. Otorhinolaryngol. Nova 3:19-25.
47. Swanson, A. F., and C. C. Kuo. 1991. Evidence that the major outer membrane protein of Chlamydia trachomatis is glycosylated. Infect. Immun. 59: 2120-2125.
48. Szymanski, C. M., and B. W. Wren. 2005. Protein glycosylation in bacterial mucosal pathogens. Nat. Rev. Microbiol. 3:225-237.
49. Tarentino, A. L., C. M. Gómez, and T. H. Plummer, Jr. 1985. Deglycosylation of asparagine-linked glycans by peptide: N-glycosidase F. Biochemistry 24:4665-4671.
50. Tielker, D., et al. 2005. Pseudomonas aeruginosa lectin LecB is located in the outer membrane and is involved in biofilm formation. Microbiology 151: 1313-1323.
51. Tielker, D., F. Rosenau, K.-M. Bartels, T. Rosenbaum, and K.-E. Jaeger. 2006. Lectin-based affinity tag for one-step protein purification. Biotechniques 41:327-332. (Pubitemid 46534896)
52. Tommassen, J., A. Filloux, M. Bally, M. Murgier, and A. Lazdunski. 1992. Protein secretion in Pseudomonas aeruginosa. FEMS Microbiol. Rev. 9:73-90.
53. Totten, P. A., and S. Lory. 1990. Characterization of the type a flagellin gene from Pseudomonas aeruginosa PAK. J. Bacteriol. 172:7188-7199.
54. Ungar, D. 2009. Golgi linked protein glycosylation and associated diseases. Semin. Cell Dev. Biol. 20:762-769.
55. Urban, A., M. Leipelt, T. Eggert, and K.-E. Jaeger. 2001. DsbA and DsbC affect extracellular enzyme formation in Pseudomonas aeruginosa. J. Bacteriol. 183:587-596. (Pubitemid 32048117)
56. von Bismarck, P., R. Schneppenheim, and U. Schumacher. 2001. Successful treatment of Pseudomonas aeruginosa respiratory tract infection with a sugar solution - a case report on a lectin based therapeutic principle. Klin. Padiatr. 213:285-287.
57. Weerepana, E., and B. Imperiali. 2006. Asparagine-linked protein glycosylation: from eukaryotic to prokaryotic systems. Glycobiology 16:91-101.
58. Wilhelm, S., J. Tommassen, and K.-E. Jaeger. 1999. A novel lipolytic enzyme located in the outer membrane of Pseudomonas aeruginosa. J. Bacteriol. 181:6977-6986. (Pubitemid 29536510)
59. Wilhelm, S., A. Gdynia, P. Tielen, F. Rosenau, and K.-E. Jaeger. 2007. The autotransporter esterase EstA of Pseudomonas aeruginosa is required for rhamnolipid production, cell motility, and biofilm formation. J. Bacteriol. 189:6977-6986.
60. Winzer, K., et al. 2000. The Pseudomonas aeruginosa lectins PA-IL and PA-IIL are controlled by quorum sensing and by RpoS. J. Bacteriol. 182: 6401-6411.
61. Woodcock, D. M., et al. 1989. Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res. 17:3469-3478.
62. Yasuda, Y., et al. 1999. Role of N-glycosylation in cathepsin E. A comparative study of cathepsin E with distinct N-linked oligosaccharides and its nonglycosylated mutant. Eur. J. Biochem. 266:383-391.
63. Young, N. M., et al. 2002. Structure of the N-linked glycan present on multiple glycoproteins in the Gram-negative bacterium, Campylobacter jejuni. J. Biol. Chem. 277:42530-42539. (Pubitemid 35285620)