Topology of the outer-membrane secretin PilQ from Neisseria meningitidis

Microbiology

Volumn 152, Issue 12, 2006, Pages 3751-3764

  Frye, Stephan A ^a   Assalkhou, Reza ^a   Collins, Richard F ^b   Ford, Robert C ^b   Petersson, Christoffer ^c   Derrick, Jeremy P ^b   Tønjum, Tone ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c LINKÖPING UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

POLYHISTIDINE; PROTEIN PILQ; SECRETIN; UNCLASSIFIED DRUG; VANCOMYCIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL MEMBRANE; BACTERIUM PILUS; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; DRUG PENETRATION; ELECTRON MICROSCOPY; GENE INSERTION; GENE MUTATION; IN VIVO STUDY; NEISSERIA MENINGITIDIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE;

BACTERIAL OUTER MEMBRANE PROTEINS; CELL MEMBRANE; FIMBRIAE PROTEINS; FREEZE FRACTURING; IMMUNOHISTOCHEMISTRY; MICROSCOPY, IMMUNOELECTRON; MODELS, MOLECULAR; MUTAGENESIS, INSERTIONAL; MUTATION; NEISSERIA MENINGITIDIS; PERIPLASM; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINATION, GENETIC; SUBCELLULAR FRACTIONS;

NEISSERIA MENINGITIDIS;

EID: 33846018001     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.2006/000315-0     Document Type: Article

References (63)

1. Beveridge, T. J., Popkin, T. J. & Cole, R. M. (1994). Electron microscopy. In Methods for General and Molecular Microbiology, pp. 44-70. Edited by P. Gerhardt, R. G. E. Murray, W. A. Woods & N. R. Krieg. Washington, DC: American Society for Microbiology.
2. Bille, E., Zahar, J. R., Perrin, A. & 7 other authors (2005). A chromosomally integrated bacteriophage in invasive meningococci. J Exp Med 201, 1905-1913.
3. Bitter, W., Koster, M., Latijnhouwers, M., de Cock H. & Tommassen, J. (1998). Formation of oligomeric rings by XcpQ and PilQ, which are involved in protein transport across the outer membrane of Pseudomonas aeruginosa. Mol Microbiol 27, 209-219.
4. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
5. Brinton, C. C., Bryan, J., Dillon, J.-A. & other authors (1978). Uses of pili in gonorrhoea control: role of bacterial pili in disease, purification and properties of gonococcal pili, and progress in the development of a gonococcal pilus vaccine for gonorrhoeae. In Immunobiology of Neisseria gonorrhoeae, pp. 155-178. Edited by G. E. Brooks, E. C. Gotschlich, K. H. Homes, W. D. Sawyer & F. E. Young. Washington, DC: American Society for Microbiology.
6. Carbonnelle, E., Helaine, S., Prouvensier, L., Nassif, X. & Pelicic, V. (2005). Type IV pilus biogenesis in Neisseria meningitidis. PilW is involved in a step occurring after pilus assembly, essential for fibre stability and function. Mol Microbiol 55, 54-64.
7. Chen, C. J., Tobiason, D. M., Thomas, C. E., Shafer, W. M., Seifert, H. S. & Sparling, P. F. (2004). A mutant form of the Neisseria gonorrhoeae pilus secretin protein PilQ allows increased entry of heme and antimicrobial compounds. J Bacteriol 186, 730-739.
8. Chirica, L. C., Petersson, C., Hurtig, M., Jonsson, B. H., Boren, T. & Lindskog, S. (2002). Expression and localization of alpha- and beta-carbonic anhydrase in Helicobacter pylori. Biochim Biophys Acta 1601, 192-199.
9. Collins, R. F., Davidsen, L., Derrick J. P., Ford, R. C. & Tønjum, T. (2001). Analysis of the PilQ secretin from Neisseria meningitidis by transmission electron microscopy reveals a dodecameric quaternary structure. J Bacteriol 183, 3825-3832.
10. Collins, R. F., Ford, R. C., Kitmitto, A., Olsen, R. O., Tønjum, T. & Derrick J. P. (2003). Three-dimensional structure of the Neisseria meningitidis secretin PilQ determined from negative-stain transmission electron microscopy. J Bacteriol 185, 2611-2617.
11. Collins, R. F., Frye, S. A., Kitmitto, A, Ford, R. C., Tønjum, T. & Derrick, J. P. (2004). Structure of the Neisseria meningitidis outer membrane PilQ secretin complex at 12 Å resolution. J Biol Chem 279, 39750-39756.
12. Collins, R. F., Frye, S. A., Balasingham, S., Ford, R. C., Tønjum, T. & Derrick, J. P. (2005). Interaction with type IV pili induces structural changes in the bacterial outer membrane secretin PilQ. J Biol Chem 280, 18923-18930.
13. Collins, R. F., Beis, K, Clarke, B. R., Ford, R. C., Hulley, M., Naismith, J. H. & Whitfield, C. (2006). Periplasmic protein-protein contacts in the inner membrane protein Wzc form a tetrameric complex required for the assembly of Escherichia coli group 1 capsules. J Biol Chem 281, 2144-2150.
14. Corbett, M. J., Black, J. R. & Wilde, C. E., 3rd (1988). Antibodies to outer-membrane protein-macromolecular complex (OMP-MC) are bactericidal for serum-resistant gonococci. In Gonococci and Meningococci, pp. 685-691. Edited by J. T. Poolmann, H. C. Zanen, T. F. Meyer, J. E. Heckel, P. R. H. Makela, H. Smith & E. C. Beuvery. Dordrecht, The Netherlands: Kluwer.
15. Cuff, J. A., Clamp, M. E., Siddiqui, A. S., Finlay, M. & Barton, G. J. (1998). JPred: a consensus secondary structure prediction server. Bioinformatics 14, 892-893.
16. Daefler, S., Russel, M. & Model, P. (1997). Module swaps between related translocator proteins pIV(f1), pIV(IKe) and PulD: identification of a specificity domain. J Mol Biol 266, 978-992.
17. Devoe, I. W. & Gilchrist, J. E. (1974). Ultrastructure of pili and annular structures on the cell wall surface of Neisseria meningitidis. Infect Immun 10, 872-876.
18. Drake, S. L. & Koomey, M. (1995). The product of the pilQ gene is essential for the biogenesis of type IV pili in Neisseria gonorrhoeae. Mol Microbiol 18, 975-986.
19. Drake, S. L., Sandstedt, S. A. & Koomey, M. (1997). PilP, a pilus biogenesis lipoprotein in Neisseria gonorrhoeae, affects expression of PilQ as a high-molecular-mass multimer. Mol Microbiol 23, 657-668.
20. Frasch, C. E. & Chapman, S. S. (1972). Classification of Neisseria meningitidis group B into distinct serotypes. I. Serological typing by a microbactericidal method. Infect Immun 5, 98-102.
21. Frøholm, L. O., Jyssum, K. & Bøvre, K. (1973). Electron microscopical and cultural features of Neisseria meningitidis competence variants. Acta Pathol Microbiol Scand [B] 81, 525-537.
22. Frosch, M., Schultz E., Glenn-Calvo, E. & Meyer, T. F. (1990). Generation of capsule-deficient Neisseria meningitidis strains by homologous recombination. Mol Microbiol 4, 1215-1218.
23. Fujimoto, K. (1995). Freeze-fracture replica electron microscopy combined with SDS digestion for cytochemical labeling of integral membrane proteins. Application to the immunogold labeling of intercellular junctional complexes. J Cell Sci 108, 3443-3449.
24. Genin, S. & Boucher, C. A. (1994). A superfamily of proteins involved in different secretion pathways in Gram-negative bacteria: modular structure and specificity of the N-terminal domain. Mol Gen Genet 243, 112-118.
25. Gromiha, M. M., Majumdar, R. & Ponnuswamy, P. K. (1997). Identification of membrane spanning beta strands in bacterial porins. Protein Eng 10, 497-500.
26. Guilvout, I., Hardie, K. R., Sauvonnet, N. & Pugsley, A. P. (1999). Genetic dissection of the outer membrane secretin PulD: are there distinct domains for multimerization and secretion specificity? J Bacteriol 181, 7212-7220.
27. Hansen, M. V. & Wilde, C. E., 3rd (1984). Conservation of peptide structure of outer membrane protein-macromolecular complex from Neisseria gonorrhoeae. Infect Immun 43, 839-845.
28. Hardie, K. R., Seydal, A., Guilvout, I. & Pugsley, A. P. (1996). The secretin-specific, chaperone-like protein of the general secretory pathway: separation of proteolytic protection and piloting functions. Mol Microbiol 22, 967-976.
29. Harris, J. R. (1997). Negative Staining and Cryoelectron Microscopy. Oxford: BIOS Scientific.
30. Hegge, F. T., Hitchen, P. G., Aas, F. E. & 10 other authors (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.
31. Henrichsen, J., Froholm, L. O. & Bovre, K. (1972). Studies on bacterial surface translocation. 2. Correlation of twitching motility and fimbriation in colony variants of Moraxella nonliquefaciens, M. bovis, and M. kingii. Acta Pathol Microbiol Scand [B] 80, 445-452.
32. Horton, R. M., Cal, Z. L., Ho, S. N. & Pease, L. R. (1990). Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques 8, 528-535.
33. Jönsson, A. B., Ilver, D., Falk P., Pepose, J. & Normark S. (1994). Sequence changes in the pilus subunit lead to tropism variation of Neisseria gonorrhoeae to human tissue. Mol Microbiol 13, 403-416.
34. Linderoth, N. A., Model, P. & Russel, M. (1996). Essential role of a sodium dodecyl sulfate-resistant protein IV multimer in assembly-export of filamentous phage. J Bacteriol 178, 1962-1970.
35. Mathis, L. S. & Scocca, J. J. (1984). On the role of pill in transformation of Neisseria gonorrhoeae. J Gen Microbiol 130, 3165-3173.
36. Merz, A. J., So, M. & Sheetz, M. P. (2000). Pilus retraction powers bacterial twitching motility. Nature 407, 98-102.
37. Nunn, D. (1999). Bacterial type II protein export and pilus biogenesis: more than just homologies? Trends Cell Biol 9, 402-408.
38. Nunn, D. N. & Lory, S. (1991). Product of the Pseudomonas aeruginosa gene pilD is a prepilin leader peptidase. Proc Natl Acad Sci U S A 88, 3281-3285.
39. Opalka, N., Beckmann, R., Boisset N., Simon, M. N., Russel, M. & Darst, S. A. (2003). Structure of the filamentous phage pIV multimer by cryo-electron microscopy. J Mol Biol 325, 461-470.
40. Peabody, C. R., Chung, Y. J., Yen, M. R., Vidal-Ingigliardi, D., Pugsley, A. P. & Saier, M. H., Jr (2003). Type II protein secretion and its relationship to bacterial type IV pill and archaeal flagella. Microbiology 149, 3051-3072.
41. Petersson, C., Larsson, B., Mahdavi, J., Boren, T. & Magnusson, K. E. (2000). A new method to visualize the Helicobacter pylori-associated Lewis(b)-binding adhesin utilizing SDS-digested freeze-fracture replica labeling. J Histochem Cytochem 48, 877-883.
42. Pugsley, A. P. (1993). The complete general secretory pathway in Gram-negative bacteria. Microbiol Rev 57, 50-108.
43. Rudel, T., Scheurerpflug, I. & Meyer, T. F. (1995). Neisseria PilC protein identified as type-4 pilus tip-located adhesin. Nature 373, 357-359.
44. Russel, M. (1994). Mutants at conserved positions in gene IV, a gene required for assembly and secretion of filamentous phages. Mol Microbiol 14, 357-369.
45. Russel, M., Linderoth, N. A. & Sali, A. (1997). Filamentous phage assembly: variation on a protein export theme. Gene 192, 23-32.
46. Sambrook J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
47. Schägger, H. & von Jagow, G. (1987). Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166, 368-379.
48. Schmidt, S. A., Bieber, D., Ramer, S. W., Hwang, J., Wu, C. Y. & Schoolnik, G. (2001). Structure-function analysis of BfpB, a secretin-like protein encoded by the bundle-forming-pilus operon of enteropathogenic Escherichia coli. J Bacteriol 183, 4848-4859.
49. Seifert, H. S., Ajioka, R. S., Paruchuri, D., Heffron, F. & So, M. (1990). Shuttle mutagenesis of Neisseria gonorrhoeae: pilin null mutations lower DNA transformation competence, J Bacteriol 172, 40-46.
50. Swanson, J., Kraus, S. J. & Gotschlich, E. C. (1971). Studies on gonococcus infection. I. Pili and zones of adhesion: their relation to gonococcal growth patterns. J Exp Med 134, 886-906.
51. Tonjum, T., Caugant, D. A., Dunham, S. A. & Koomey, M. (1998). Structure and function of repetitive sequence elements associated with a highly polymorphic domain of the Neisseria meningitidis PilQ protein. Mol Microbiol 29, 111-124.
52. Tønjum, T., Freitag, N. E., Namork E. & Koomey, M. (1995). Identification and characterization of pilG, a highly conserved pilus-assembly gene in pathogenic Neisseria. Mol Microbiol 16, 451-464.
53. Tønjum, T. & Koomey, M. (1997). The pilus colonization factor of pathogenic neisserial species: organelle biogenesis and structure/ function relationships - a review. Gene 192, 155-163.
54. Tønjum, T., Caugant, D. A., Dunham, S. A. & Koomey, M. (1998). Structure and function of repetitive sequence elements associated with a highly polymorphic domain of the Neisseria meningitidis PilQ protein. Mol Microbiol 29, 111-124.
55. Tsai, W. M., Larsen, S. H. & Wilde, C. E., 3rd (1989). Cloning and DNA sequence of the omc gene encoding the outer membrane protein-macromolecular complex from Neisseria gonorrhoeae. Infect Immun 57, 2653-2659.
56. Valu, J. A. (1976). Simple disk-plate method for the biochemical confirmation of pathogenic Neisseria. J Clin Microbiol 3, 172-174.
57. Virji, M. (1999). Glycans in meningococcal pathogenesis. Biochem Soc Trans 27, 498-507.
58. Voulhoux, R., Bos, M. P., Geurtsen, J., Mols, M. & Tommassen, J. (2003). Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299, 262-265.
59. Wall, D., Kolenbrander, P. E. & Kaiser, D. (1999). The Myxococcus xanthus pilQ (sglA) gene encodes a secretin homolog required for type IV pilus biogenesis, social motility, and development. J Bacteriol 181, 24-33.
60. Winther-Larsen, H. C., Hegge, F. T., Wolfgang, M., Hayes, S. F., van Putten, J. P. & Koorney, M. (2001). Neisseria gonorrhoeae PilV, a type IV pilus-associated protein essential to human epithelial cell adherence. Proc Natl Acad Sci U S A 98, 15276-15281.
61. Wolfgang, M., Lauer, P., Park, H. S., Brossay, L., Hebert, J. & Koomey, M. (1998). PilT mutations lead to simultaneous defects in competence for natural transformation and twitching motility in piliated Neisseria gonorrhoeae. Mol Microbiol 29, 321-330.
62. Wolfgang, M., van Putten, J. P., Hayes, S. F. & Koomey, M. (1999). The comP locus of Neisseria gonorrhoeae encodes a type IV prepilin that is dispensable for pilus biogenesis but essential for natural transformation. Mol Microbiol 31, 1345-1357.
63. Zhao, S., Tobiason, D. M., Hu, M., Seifert, H. S. & Nicholas, R. A. (2005). The penC mutation conferring antibiotic resistance in Neisseria gonorrhoeae arises from a mutation in the PilQ secretin that interferes with multimer stability. Mol Microbiol 57, 1238-1251.