Identification and Characterization of pptA: A Gene Involved in the Phase-Variable Expression of Phosphorylcholine on Pili of Neisseria meningitidis

Infection and Immunity

Volumn 71, Issue 12, 2003, Pages 6892-6898

  Warren, Matthew J ^a   Jennings, Michael P ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MONOCLONAL ANTIBODY; PHOSPHORYLCHOLINE; PILIN;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM PILUS; BIOSYNTHESIS; CONTROLLED STUDY; GENE CONSTRUCT; GENE EXPRESSION; GENE SWITCHING; GENETIC IDENTIFICATION; GENETIC TRAIT; GENETIC VARIABILITY; NEISSERIA MENINGITIDIS; NONHUMAN; OPEN READING FRAME; PHOSPHORYLATION; PPTA GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; WESTERN BLOTTING;

BACTERIAL PROTEINS; BASE SEQUENCE; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MENINGOCOCCAL INFECTIONS; MOLECULAR SEQUENCE DATA; NEISSERIA MENINGITIDIS; PHOSPHORYLCHOLINE; TRANSFERASES; TRANSFERASES (OTHER SUBSTITUTED PHOSPHATE GROUPS); VIRULENCE;

EID: 0345714747     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.71.12.6892-6898.2003     Document Type: Article

References (49)

1. Alexander, H. E. 1965. The Haemophilus group, p. 724-741. In J. Dabos and J. G. Hirsch (ed.), Bacterial and mycotic infections of man. Pitman Medical Publishing Co., Ltd., London, England.
2. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein, database search programs. Nucleic Acids Res. 25:3389-3402.
3. Andresen, P. A., I. Kaasen, O. B. Styrvold, G. Boulnois, and A. R. Strom. 1988. Molecular cloning, physical mapping and expression of the bet genes governing the osmoregulatory choline-glycine betaine pathway of Escherichia coli. J. Gen. Microbiol. 134:1737-1746.
4. Arondel, V., C. Benning, and C. R. Somerville. 1993. Isolation and functional expression in Escherichia coli of a gene encoding phosphatidylethanolamine methyltransferase (EC 2.1.1.17) from Rhodobacter sphaeroides. J. Biol. Chem. 268:16002-16008.
5. Behr, T., W. Fischer, J. Peter-Katalinic, and H. Egge. 1992. The structure of pneumococcal lipoteichoic acid. Improved preparation, chemical and mass spectrometric studies. Eur. J. Biochem. 207:1063-1075.
6. Berrington, A. W., Y.-C. Tan, Y. Srikhanta, B. Kuipers, P. van der Ley, I. R. A. Peak, and M. P. Jennings. 2002. Phase variation in meningococcal lipooligosaccharide biosynthesis genes. FEMS Immunol. Med. Microbiol. 34:267-275.
7. Cundell, D. R., N. P. Gerard, C. Gerard, I. Idanpaan-Heikkila, and E. I. Tuomanen. 1995. Streptococcus pneumoniae anchor to activated human cells by the receptor for platelet-activating factor. Nature 377:435-438.
8. de Rudder, K. E., I. M. Lopez-Lara, and O. Geiger. 2000. Inactivation of the gene for phospholipid N-methyltransferase in Sinorhizobium meliloti: phosphatidylcholine is required for normal growth. Mol. Microbiol. 37:763-772.
9. Dybvig, K. 1993. DNA rearrangements and phenotypic switching in prokaryotes. Mol. Microbiol. 10:465-471.
10. Fischer, W., T. Behr, R. Hartmann, J. Peter-Katalinic, and H. Egge. 1993. Teichoic acid and lipoteichoic acid of Streptococcus pneumoniae possess identical chain structures. A reinvestigation of teichoid acid (C polysaccharide). Eur. J. Biochem. 215:851-857.
11. Gillespie, S. H., S. Ainscough, A. Dickens, and J. Lewin. 1996. Phosphorylcholine-containing antigens in bacteria from the mouth and respiratory tract. J. Med. Microbiol. 44:35-40.
12. Gould, J. M., and J. N. Weiser. 2002. The inhibitory effect of C-reactive protein on bacterial phosphorylcholine platelet-activating factor receptor-mediated adherence is blocked by surfactant. J. Infect. Dis. 186:361-371.
13. Jennings, M. P., M. Virji, D. Evans, V. Foster, Y. N. Srikhanta, L. Steeghs, P. van der Ley, and E. R. Moxon. 1998. Identification of a novel gene involved in pilin glycosylation in Neisseria meningitidis. Mol. Microbiol. 29: 975-984.
14. Kolberg, J., E. A. Holby, and E. Jantzen. 1997. Detection of the phosphorylcholine epitope in streptococci, Haemophilus and pathogenic Neisseriae by immunoblotting. Microb. Pathog. 22:321-329.
15. Koomey, M. 1994. Mechanisms of pilus antigenic variation in Neisseria gonorrhoeae, p. 113-126. In V. L. Miller, J. B. Kaper, D. A. Kaper, and R. R. Isberg (ed.), Molecular genetics of bacterial pathogenesis. American Society for Microbiology, Washington, D.C.
16. Mackinnon, F. G., A. D. Cox, J. S. Plested, C. M. Tang, K. Makepeace, P. A. Coull, J. C. Wright, R. Chalmers, D. W. Hood, J. C. Richards, and E. R. Moxon. 2002. Identification of a gene (lpt-3) required for the addition of phosphoethanolamine to the lipopolysaccharide inner core of Neisseria meningitidis and its role in mediating susceptibility to bactericidal killing and opsonophagocytosis. Mol. Microbiol. 43:931-943.
17. Merz, A. J., C. A. Enns, and M. So. 1999. Type IV pili of pathogenic Neisseriae elicit cortical plaque formation in epithelial cells. Mol. Microbiol. 32:1316-1332.
18. Meyer, T. F., and J. P. van Putten. 1989. Genetic mechanisms and biological implications of phase variation in pathogenic neisseriae. Clin. Microbiol. Rev. 2(Suppl.):S139-S145.
19. Minder, A. C., K. E. de Rudder, F. Narberhaus, H. M. Fischer, H. Hennecke, and O. Geiger. 2001, Phosphatidyleholine levels in Bradyrhizobium japonicum membranes are critical for an efficient symbiosis with the soybean host plant. Mol. Microbiol. 39:1186-1198.
20. Mosser, J. L., and A. Tomasz. 1970. 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. 245:287-298.
21. Moxon, E. R., P. B. Rainey, M. A. Nowak, and R. E. Lenski. 1994. Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr. Biol. 4:24-33.
22. Parge, H. E., K. T. Forest, M. J. Hickey, D. A. Christensen, E. D. Getzoff, and J. A. Tainer. 1995. Structure of the fibre-forming protein pilin at 2.2 Å resolution. Nature 378:32-38.
23. Perrin, A., X. Nassif, and C. Tinsley. 1999. Identification of regions of the chromosome of Neisseria meningitidis and Neisseria gonorrhoeae which are specific to the pathogenic Neisseria species. Infect. Immun. 67:6119-6129.
24. Power, P. M., L. F. Roddam, M. Dieckelmann, Y. N. Srikhanta, Y. C. Tan, A. W. Berrington, and M. P. Jennings. 2000. Genetic characterisation of pilin glycosylation in Neisseria meningitidis. Microbiology 146:967-979.
25. a. Power, P. M., L. F. Roddam, K. Rutter, S. Z. Fitzpatrick, Y. N. Srikhanta, and M. P. Jennings. 2003. Genetic characterization of pilin glycosylation and phase variation in Neisseria meningitidis Mol. Microbiol. 49:833-847.
26. Risberg, A., E. K. Schweda, and P. E. Jansson. 1997. Structural studies of the cell-envelope oligosaccharide from the lipopolysaccharide of Haemophilus influenzae strain RM.118-28. Eur. J. Biochem. 243:701-707.
27. Robertson, B. D., and T. F. Meyer. 1992. Genetic variation in pathogenic bacteria. Trends Genet. 8:422-427.
28. Rudel, T., J. P. van Putten, C. P. Gibbs, R. Haas, and T. F. Meyer. 1992. Interaction of two variable proteins (PilE and PilC) required for pilus-mediated adherence of Neisseria gonorrhoeae to human epithelial cells. Mol. Microbiol. 6:3439-3450.
29. Saiki, R. K., D. H. Gelfand, S. Stoffel, S. J. Scharf, R. Higuchi, G. T. Horn, K. B. Mullis, and H. A. Erlich. 1988. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239:487-491.
30. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
31. Saunders, N. J., A. C. Jeffries, J. F. Peden, D. W. Hood, H. Tettelin, R. Rappuoli, and E. R. Moxon. 2000. Repeat-associated phase variable genes in the complete genome sequence of Neisseria meningitidis strain MC58. Mol. Microbiol. 37:207-215.
32. Seifert, H. S. 1996. Questions about gonococcal pilus phase- and antigenic-variation. Mol. Microbiol. 21:433-440.
33. Serino, L., and M. Virji. 2002. Genetic and functional analysis of the phosphorylcholine moiety of commensal Neisseria lipopolysaccharide. Mol. Microbiol. 43:437-448.
34. Serino, L., and M. Virji. 2000. Phosphorylcholine decoration of lipopolysaccharide differentiates commensal Neisseriae from pathogenic strains: identification of licA-type genes in commensal Neisseriae. Mol. Microbiol. 35:1550-1559.
35. Snyder, L. A., N. J. Saunders, and W. M. Shafer. 2001. A putatively phase variable gene (dca) required for natural competence in Neisseria gonorrhoeae but not Neisseria meningitidis is located within the division cell wall (dcw) gene cluster. J. Bacteriol. 183:1233-1241.
36. Swords, W. E., B. A. Buscher, K. Ver Steeg Ii, A. Preston, W. A. Nichols, J. N. Weiser, B. W. Gibson, and M. A. Apicella. 2000. Non-typeable Haemophilus influenzae adhere to and invade human bronchial epithelial cells via an interaction of lipooligosaccharide with the PAF receptor. Mol. Microbiol. 37:13-27.
37. Szalai, A. J., D. E. Briles, and J. E. Volanakis. 1995. Human C-reactive protein is protective against fatal Streptococcus pneumoniae infection in transgenic mice. J. Immunol. 155:2557-2563.
38. Tettelin, H., N. J. Saunders, J. Heidelberg, A. C. Jeffries, K. E. Nelson, J. A. Eisen, K. A. Ketchum, D. W. Hood, J. F. Peden, R. J. Dodson, W. C. Nelson, M. L. Gwinn, R. DeBoy, J. D. Peterson, E. K. Hickey, D. H. Haft, S. L. Salzberg, O. White, R. D. Fleischmann, B. A. Dougherty, T. Mason, A. Ciecko, D. S. Parksey, E. Blair, H. Cittone, E. B. Clark, M. D. Cotton, T. R. Utterback, H. Khouri, H. Qin, J. Vamathevan, J. Gill, V. Scarlato, V. Masignani, M. Pizza, G. Grandi, L. Sun, H. O. Smith, C. M. Fraser, E. R. Moxon, R. Rappuoli, and J. C. Venter. 2000. Complete genome sequence of Neisseria meningitidis serogroup B strain MC58. Science 287:1809-1815.
39. Tong, H. H., L. E. Blue, M. A. James, Y. P. Chen, and T. F. DeMaria. 2000. Evaluation of phase variation of nontypeable Haemophilus influenzae lipooligosaccharide during nasopharyngeal colonization and development of otitis media in the chinchilla model. Infect. Immun. 68:4593-4597.
40. Tonjum, T., and M. Koomey. 1997. The pilus colonization factor of pathogenic neisserial species: organelle biogenesis and structure/function relationships - a review. Gene 192:155-163.
41. Virji, M., H. Kathty, D. J. P. Ferguson, C. Alexandrescu, J. E. Heckels, and E. R. Moxon. 1991. The role of pili in the interactions of pathogenic Neisseria with cultured human endothelial cells. Mol. Microbiol. 5:1831-1841.
42. Virji, M., J. R. Saunders, G. Sims, K. Makepeace, D. Maskell, and D. J. Ferguson. 1993. 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 of pilin. Mol Microbiol. 10:1013-1028.
43. Weiser, J. N., J. B. Goldberg, N. Pan, L. Wilson, and M. Virji. 1998. 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. 66:4263-4267.
44. Weiser, J. N., A. A. Lindberg, E. J. Manning, E. J. Hansen, and E. R. Moxon. 1989. Identification of a chromosomal locus for expression of lipopolysaccharide epitopes in Haemophilus influenzae. Infect. Immun. 57:3045-3052.
45. Weiser, J. N., Z. Markiewicz, E. I. Tuomanen, and J. H. Wani. 1996. Relationship between phase variation in colony morphology, intrastrain variation in cell wall physiology, and nasopharyngeal colonization by Streptococcus pneumoniae. Infect. Immun. 64:2240-2245.
46. Weiser, J. N., N. Pan, K. L. McGowan, D. Musher, A. Martin, and J. Richards. 1998. 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. 187:631-640.
47. Weiser, J. N., M. Shchepetov, and S. T. H. Chong. 1997. Decoration of lipopolysaccharide with phosphorylcholine: a phase-variable characteristic of Haemophilus influenzae. Infect. Immun. 65:943-950.
48. Wilderman, P. J., A. I. Vasil, W. E. Martin, R. C. Murphy, and M. L. Vasil. 2002. Pseudomonas aeruginosa synthesizes phosphatidylcholine by use of the phosphatidylcholine synthase pathway. J. Bacteriol. 184:4792-4799.
49. Zhang, J. R., I. Idanpaan-Heikkila, W. Fischer, and E. I. Tuomanen. 1999. Pneumococcal licD2 gene is involved in phosphorylcholine metabolism. Mol. Microbiol. 31:1477-1488.