Substrate recognition of a structure motif for phosphorylcholine post-translational modification in Neisseria meningitidis

Biochemical and Biophysical Research Communications

Volumn 431, Issue 4, 2013, Pages 808-814

  Jen, Freda E C ^a   Jones, Christopher E ^b   Wilson, Jennifer C ^a   Schulz, Benjamin L ^c   Jennings, Michael P ^a  

^a GRIFFITH UNIVERSITY   (Australia)

^b UNIVERSITY OF WESTERN SYDNEY   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Bacteria; Neisseria; Phosphorylcholine; Pili

Indexed keywords

CHOLINE PHOSPHATE CYTIDYLYLTRANSFERASE; GLYCAN; PILIN;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL COLONIZATION; CHEMICAL MODIFICATION; CONTROLLED STUDY; DISULFIDE BOND; ENZYME STRUCTURE; NEISSERIA MENINGITIDIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; SEQUENCE ANALYSIS;

AMINO ACID MOTIFS; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; CYSTEINE; FIMBRIAE PROTEINS; MOLECULAR SEQUENCE DATA; NEISSERIA MENINGITIDIS; PEPTIDE FRAGMENTS; PHOSPHORYLCHOLINE; PROTEIN CONFORMATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SUBSTRATE SPECIFICITY; TRANSFERASES (OTHER SUBSTITUTED PHOSPHATE GROUPS);

BACTERIA (MICROORGANISMS); NEISSERIA; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS;

EID: 84875267980     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.12.088     Document Type: Article

References (35)

1. Foley T.L., Burkart M.D. Site-specific protein modification: advances and applications. Curr. Opin. Chem. Biol. 2007, 11:12-19.
2. Vik A., Aas F.E., Anonsen J.H., Bilsborough S., Schneider A., Egge-Jacobsen W., Koomey M. Broad spectrum O-linked protein glycosylation in the human pathogen Neisseria gonorrhoeae. Proc. Natl. Acad. Sci. USA 2009, 106:4447-4452.
3. Gillespie S.H., Ainscough S., Dickens A., Lewin J. Phosphorylcholine-containing antigens in bacteria from the mouth and respiratory tract. J. Med. Microbiol. 1996, 44:35-40.
4. Weiser J.N., Shchepetov M., Chong S.T. Decoration of lipopolysaccharide with phosphorylcholine: a phase-variable characteristic of Haemophilus influenzae. Infect. Immun. 1997, 65:943-950.
5. Serino L., Virji M. Genetic and functional analysis of the phosphorylcholine moiety of commensal Neisseria lipopolysaccharide. Mol. Microbiol. 2002, 43:437-448.
6. Fischer W., Behr T., Hartmann R., Peter-Katalinic J., Egge H. Teichoic acid and lipoteichoic acid of Streptococcus pneumoniae possess identical chain structures. A reinvestigation of teichoid acid (C polysaccharide). Eur. J. Biochem. 1993, 215:851-857.
7. Weiser J.N., Goldberg J.B., Pan N., Wilson L., Virji M. The phosphorylcholine epitope undergoes phase variation on a 43-kilodalton protein in Pseudomonas aeruginosa and on pili of Neisseria meningitidis and Neisseria gonorrhoeae. Infect. Immun. 1998, 66:4263-4267.
8. Barbier M., Oliver A., Rao J., Hanna S.L., Goldberg J.B., Alberti S. Novel phosphorylcholine-containing protein of Pseudomonas aeruginosa chronic infection isolates interacts with airway epithelial cells. J. Infect. Dis. 2008, 197:465-473.
9. Warren M.J., Jennings M.P. Identification and characterisation of pptA: a gene involved in the phase-variable expression of phosphorylcholine on pili of Neisseria meningitidis. Infect. Immun. 2003, 71:6892-6898.
10. Virji M., Saunders J.R., Sims G., Makepeace K., Maskell D., Ferguson D.J. Pilus-facilitated adherence of Neisseria meningitidis to human epithelial and endothelial cells: modulation of adherence phenotype occurs concurrently with changes in primary amino acid sequence and the glycosylation status ofpilin. Mol.Microbiol. 1993, 10:1013-1028.
11. Alexander H.E. The Haemophilus group. Bacterial and Mycotic Infections of Man 1965, Pitman Medical Publishing Co, London.
12. Sambrook J., Russell D.W. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 3rd ed.
13. Erster O., Liscovitch M. A modified inverse PCR procedure for insertion, deletion, or replacement of a DNA fragment in a target sequence and its application in the ligand interaction scan method for generation of ligand-regulated proteins. Methods Mol. Biol. 2010, 634:157-174.
14. Power P.M., Roddam L.F., Dieckelmann M., Srikhanta Y.N., Tan Y.C., Berrington A.W., Jennings M.P. Genetic characterisation of pilin glycosylation in Neisseria meningitidis. Microbiology 2000, 146(Pt 4):967-979.
15. Ku S.C., Schulz B.L., Power P.M., Jennings M.P. The pilin O-glycosylation pathway of pathogenic Neisseria is a general system that glycosylates AniA, an outer membrane nitrite reductase. Biochem. Biophys. Res. Commun. 2009, 378:84-89.
16. Cardinale J.A., Clark V.L. Expression of AniA, the major anaerobically induced outer membrane protein of Neisseria gonorrhoeae, provides protection against killing by normal human sera. Infect. Immun. 2000, 68:4368-4369.
17. Liu M. Improved WATERGATE pulse sequences for solvent suppression in NMR spectroscopy. J. Magn. Reson. 1998, 132:125-129.
18. Mosser J.L., Tomasz A. Choline-containing teichoic acid as a structural component of pneumococcal cell wall and its role in sensitivity to lysis by an autolytic enzyme. J. Biol. chem. 1970, 245:287-298.
19. Fan X., Pericone C.D., Lysenko E., Goldfine H., Weiser J.N. Multiple mechanisms for choline transport and utilization in Haemophilus influenzae. Mol. Microbiol. 2003, 50:537-548.
20. Serino L., Virji M. Phosphorylcholine decoration of lipopolysaccharide differentiates commensal Neisseriae from pathogenic strains: identification of licA-type genes in commensal Neisseriae. Mol. Microbiol. 2000, 35:1550-1559.
21. Martinez-Morales F., Schobert M., Lopez-Lara I.M., Geiger O. Pathways for phosphatidylcholine biosynthesis in bacteria. Microbiology 2003, 149:3461-3471.
22. Morse S.A., Bartenstein L. Purine metabolism in Neisseria gonorrhoeae: the requirement for hypoxanthine. Can. J. Microbiol. 1980, 26:13-20.
23. Naessan C.L., Egge-Jacobsen W., Heiniger R.W., Wolfgang M.C., Aas F.E., Rohr A., Winther-Larsen H.C., Koomey M. Genetic and functional analyses of PptA, a phospho-form transferase targeting type IV pili in Neisseria gonorrhoeae. J. Bacteriol. 2008, 190:387-400.
24. Craig L., Volkmann N., Arvai A.S., Pique M.E., Yeager M., Egelman E.H., Tainer J.A. Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions. Mol. Cell 2006, 23:651-662.
25. Harvey H., Habash M., Aidoo F., Burrows L.L. Single-residue changes in the C-terminal disulphide-bonded loop of the Pseudomonas aeruginosa type IV pilin influence pilus assembly and twitching motility. J. Bacteriol. 2009, 191:6513-6524.
26. Duddy W.J., Nissink J.W., Allen F.H., Milner-White E.J. Mimicry by asx- and ST-turns of the four main types of beta-turn in proteins. Protein Sci. 2004, 13:3051-3055.
27. Song B., Kibler P., Malde A., Kodukula K., Galande A.K. Design of short linear peptides that show hydrogen bonding constraints in water. J. Am. Chem. Soc. 2010, 132:4508-4509.
28. Jennings M.P., Virji M., Evans D., Foster V., Srikhanta Y.N., Steeghs L., van der Ley P., Moxon E.R. Identification of a novel gene involved in pilin glycosylation in Neisseria meningitidis. Mol. Microbiol. 1998, 29:975-984.
29. Power P.M., Jennings M.P. The genetics of glycosylation in Gram-negative bacteria. FEMS Microbiol. Lett. 2003, 218:211-222.
30. Power P.M., Seib K.L., Jennings M.P. Pilin glycosylation in Neisseria meningitidis occurs by a similar pathway to wzy-dependent O-antigen biosynthesis in Escherichia coli. Biochem. Biophys. Res. Commun. 2006, 347:904-908.
31. Cundell D.R., Gerard N.P., Gerard C., Idanpaan-Heikkila I., Tuomanen E.I. Streptococcus pneumoniae anchor to activated human cells by the receptor for platelet-activating factor. Nature 1995, 377:435-438.
32. Swords W.E., Buscher B.A., Ver SteegIi K., Preston A., Nichols W.A., Weiser J.N., Gibson B.W., Apicella M.A. Non-typeable Haemophilus influenzae adhere to and invade human bronchial epithelial cells via an interaction of lipooligosaccharide with the PAF receptor. Mol.Microbiol. 2000, 37:13-27.
33. Szalai A.J., Briles D.E., Volanakis J.E. Role of complement in C-reactive-protein-mediated protection of mice from Streptococcus pneumoniae. Infect. Immun. 1996, 64:4850-4853.
34. Weiser J.N., Pan N., McGowan K.L., Musher D., Martin A., Richards J. Phosphorylcholine on the lipopolysaccharide of Haemophilus influenzae contributes to persistence in the respiratory tract and sensitivity to serum killing mediated by C-reactive protein. J. Exp. Med. 1998, 187:631-640.
35. Casey R., Newcombe J., McFadden J., Bodman-Smith K.B. The acute-phase reactant C-reactive protein binds to phosphorylcholine-expressing Neisseria meningitidis and increases uptake by human phagocytes. Infect. Immun. 2008, 76:1298-1304.