View Item 

Show simple item record

Identification and characterization of pilG , a highly conserved pilus-assembly gene in pathogenic Neisseria
dc.contributor.authorTønjum, Toneen_US
dc.contributor.authorFreitag, Nancy E.en_US
dc.contributor.authorNamork, Ellenen_US
dc.contributor.authorKoomey, Michaelen_US
dc.date.accessioned2010-06-01T19:53:50Z
dc.date.available2010-06-01T19:53:50Z
dc.date.issued1995-05en_US
dc.identifier.citationTØnjum, Tone; Freitag, Nancy E.; Namork, Ellen; Koomey, Michael (1995). "Identification and characterization of pilG , a highly conserved pilus-assembly gene in pathogenic Neisseria." Molecular Microbiology 16(3): 451-464. <http://hdl.handle.net/2027.42/73027>en_US
dc.identifier.issn0950-382Xen_US
dc.identifier.issn1365-2958en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/73027
dc.identifier.urihttp://www.ncbi.nlm.nih.gov/sites/entrez?cmd=retrieve&db=pubmed&list_uids=7565106&dopt=citationen_US
dc.description.abstractExpression of type IV pili appears to be a requisite determinant of infectivity for the strict human pathogens Neisseria gonorrhoeae and Neisseria meningitidis. The assembly of these colonization factors is a complex process. This report describes a new pilus-assembly gene, pilG , that immediately precedes the gonococcal ( Gc) pilD gene encoding the pre-pilin leader peptidase. The nucleotide sequence of this region revealed a single complete open reading frame whose derived polypeptide displayed significant identities to the pilus-assembty protein PilC of Pseudomonas aeruginosa and other polytopic integral cytoplasmic membrane constituents involved in protein export and competence. A unique polypeptide of M r 38kDa corresponding to the gene product was identified. A highly related gene and flanking sequences were cloned from a group E polysaccharide-producing strain of N. meningitidis (Mc). The results indicate that the pilG genes and genetic organization at these loci in Gc and Me are extremely conserved. Hybridization studies strongly suggest that pilG -related genes exist in commensal Neisseria species and other species known to express type IV pili. Defined genetic lesions were created by using insertional and transposon mutagenesis and moved into the Gc and Me chromosomes by allelic replacement. Chromosomal pilG insertion mutants were devoid of pili and displayed dramatically reduced competence for transformation. These findings could not be ascribed to pilin-gene alterations or to polarity exerted on pilD expression. The results indicated that PilG exerts its own independent role in neisserial pilus biogenesis.en_US
dc.format.extent5329258 bytes
dc.format.extent3109 bytes
dc.format.mimetypeapplication/pdf
dc.format.mimetypetext/plain
dc.publisherBlackwell Publishing Ltden_US
dc.rights1995 Blackwell Publishingen_US
dc.titleIdentification and characterization of pilG , a highly conserved pilus-assembly gene in pathogenic Neisseriaen_US
dc.typeArticleen_US
dc.subject.hlbsecondlevelMicrobiology and Immunologyen_US
dc.subject.hlbtoplevelScienceen_US
dc.description.peerreviewedPeer Revieweden_US
dc.contributor.affiliationumDepartment of Microbiology and Immunology. University of Michigan Medical School, Ann Arbor, Michigan 48109-0620, USA.en_US
dc.contributor.affiliationotherKaptein W. Wilhelmsen og Frues Bakteriologiske Instituit Rikshospitalet (National Hospital), University of Oslo, N-0Q27 Oslo 1 Norway.en_US
dc.contributor.affiliationotherElectron Microscopy Unit, National Institute of Public Health, 0462 Oslo, Norway.en_US
dc.identifier.pmid7565106en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/73027/1/j.1365-2958.1995.tb02410.x.pdf
dc.identifier.doi10.1111/j.1365-2958.1995.tb02410.xen_US
dc.identifier.sourceMolecular Microbiologyen_US
dc.identifier.citedreferenceAho, E.L., and Cannon, J.G. ( 1988 ) Characterization of a silent pilin gene locus from Neisseria meningitidis strain FAM18. Microb Pathogenesis 5: 391 – 398.en_US
dc.identifier.citedreferenceAlbano, M., Breitling, R., and Dubnau, D.A. ( 1989 ) Nucleotide sequence and genetic organization of the Bacillus subtilis comG operon. J Bacteriol 171; 5386 – 5404.en_US
dc.identifier.citedreferenceBally, M., Ball, G., Badere, A., and Lazdunski, A. ( 1991a ) Protein secretion in Pseudomonas aeruginosa. The xcpA gene encodes an integral inner membrane protein homologous to Klebsiella pneumoniae secretion function protein PulO. J Bactarioil 73; 479 – 486.en_US
dc.identifier.citedreferenceBally, M., Filloux, A., Akrim, M., Ball, G., Lazdunski, A., and Tommassen, J. ( 1991b ) Protein secretion in Pseudomonas aeruginosa: characterization of seven xcp genes and processing of secretory apparatus components by pre-pilin peptidase Mol Microbiol 6: 1121 – 1131.en_US
dc.identifier.citedreferenceBlake, M.S., MacDonald, C., and Klugmann, K.P. ( 1989 ) Colony morphology of piliated Neisseria meningitidis. J Exp Med 170: 1727 – 1736.en_US
dc.identifier.citedreferenceDempsey, J.E., and Cannon, J.G. ( 1994 ) Locations of genetic markers on the physical map of the chromosome of Neisseria gonorrhoeae FA1090. J Bacteriol 176: 2055 – 2060.en_US
dc.identifier.citedreferenceDevereux, J., Haeberli, P., and Smithies, O. ( 1984 ) A comprehensive set of sequence analysis programs for the VAX. Nucl Acids Res 12: 387 – 395.en_US
dc.identifier.citedreferenceDubnau, D. ( 1991 ) Genetic competence in Bacillus subtilis. Microbiol Rev 55: 395 – 424.en_US
dc.identifier.citedreferenceDums, F., Dow, J.M., and Daniels, M.J. ( 1991 ) Structural characterization of protein secretion genes of the bacterial phytopathogen Xanthomonas campestris pathovar campestris: relatedness to secretion systems of other Gram-negative bacteria. Mol Gen Genet 229: 357 – 364.en_US
dc.identifier.citedreferenceDupuy, B., and Pugsley, A.P. ( 1994 ) Type IV pre-pilin peptidase gene of Neisseria gononhoeae MS 11: presence of a related gene in other piliated and non-piliated Neisseria strains. J Bacteriol 176: 1323 – 1331.en_US
dc.identifier.citedreferenceFreitag, N., Seifert, H.S., and Koomey, M. ( 1995 ) Characterization of the pilF-pilD pilus assembly locus of Nesseria gonorrhoeae. Mol Microbiol, in press.en_US
dc.identifier.citedreferenceFrischauf, A.M., Lehrach, H., Poustka, A., and Murray, N. ( 1983 ) Lambda replacement vectors carrying polylinker sequences. J Mol Biol 170: 827 – 842.en_US
dc.identifier.citedreferenceFrØholm, L.O., Jyssum, K., and BØvre, K. ( 1973 ) Electron microscopical and cultural features of Neisseria meningitidis competence variants. Acta Path Microbiol Scand 81: 525 – 537.en_US
dc.identifier.citedreferenceGibbs, C.P., Reimann B.Y., Schultz, E., Kaufmann, A., Haas, R., and Meyer, T.F. ( 1989 ) Reassortment of pilin genes in Neisseria gonorrhoeae occurs by two distinct mechanisms. Nature 338: 651 – 652.en_US
dc.identifier.citedreferenceGiron, J.A., Ho, A.S.Y., and Schoolnik, G.K. ( 1991 ) An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science 254: 710 – 714.en_US
dc.identifier.citedreferencede Groot, A., Heijnen, I., de Cock, H., Filloux, A., and Tommassen, J. ( 1994 ) Characterization of Type IV pilus genes in plant growth-promoting Pseudomonas putida WCS358. J Bacteriol 176; 642 – 650.en_US
dc.identifier.citedreferenceHaas, R., and Meyer, T.E. ( 1986 ) The repertoire of silent pilus genes in Neisseria gonorrhoeae: evidence for gene conversion. Cell 44: 107 – 115.en_US
dc.identifier.citedreferenceHaas, R., Schwarz, H., and Meyer, T.E. ( 1987 ) Release of soluble pilin antigen coupled with gene conversion in Neisseria gonorrhoeae. Proc Natl Acad Sci USA 84: 9079 – 9083.en_US
dc.identifier.citedreferenceHe, S.Y., Lindeberg, M., Chatterjee, A.K., and Collmer, A. ( 1991 ) Cloned Erwinia chrysanthemi out genes enable Escherichia coli to selectively secrete a diverse family of heterologous proteins into its milieu. Proc Natl Acad Sci USA 88: 1079 – 1083.en_US
dc.identifier.citedreferenceHeckels, J.E. ( 1989 ) Structure and function of pill of pathogenic Neisseria species. Clin Microbiol Rev 2: S66 – S73.en_US
dc.identifier.citedreferenceHobbs, M., and Mattick, J.S. ( 1993 ) Common components in the assembly of type IV fimbriae, DNA transfer systems, the filamentous phage and protein-secretion apparatus: a general system for the formation of surface-associated protein complexes. Mol Microbiol 10: 233 – 243.en_US
dc.identifier.citedreferenceHolten, E. ( 1979 ) Serotypes of Neisseria meningitidis isolated from patients in Norway during the first six months of 1978. J Clin Microbiol 9: 186 – 187.en_US
dc.identifier.citedreferenceHultgren, S., and Normark, S. ( 1991 ) Biogenesis of the bacterial pilus. Curr Opin Gen Develop 1: 313 – 318.en_US
dc.identifier.citedreferenceJaeger, J.A., Turner, D.H., and Zuker, M. ( 1989 ) Predicting optimal and suboptimal secondary structure of RNA. Meth Enzymol 183: 281 – 306.en_US
dc.identifier.citedreferenceJiang, B., and Howard, S.P. ( 1992 ) The Aermonas hydrophila exeE gene, required both for protein secretion and normal outer membrane biogenesis, is a member of a general secretion pathway. Mol Microbiol 6: 1351 – 1361.en_US
dc.identifier.citedreferenceJonsson, A.B., Nyberg, G., and Normark, S. ( 1991 ) Phase variation of gonococcal pili by a frameshift mutation in pilC, a novel gene for pilus-assembly. EMBO J 10: 477 – 488.en_US
dc.identifier.citedreferenceJonsson, A.B., Pfeiffer, J., and Normark, S. ( 1992 ) Neisseria gonorrhoeae PilC expression provides a selective mechanism for structural diversity of pili. Proc Natl Acad Sci USA 89: 3204 – 3208.en_US
dc.identifier.citedreferenceJonsson, A.B., Liver, D., Falk, P., Pepose, J., and Normark, S. ( 1994 ) Sequence changes in the pilus subunit lead to tropism variation of Neisseria gonorrhoeae to human tissue, Mol Microbiol 13; 403 – 416.en_US
dc.identifier.citedreferenceJyssum, K., and Lie, S. ( 1965 ) Genetic factors determining competence in transformation of Neisseria meningitidis. Acta Path Microbiol Scand 63: 306 – 316.en_US
dc.identifier.citedreferenceKaufmann, M.R., Shaw, C.E., Jones, L.D., and Taylor, R.K. ( 1993 ) Biogenesis and regulation of the Vibrio cholerae toxin-coregulated pilus: analogies to other virulence factor secretory systems. Gene 126: 43 – 49.en_US
dc.identifier.citedreferenceKellogg, D.S., Cohen, I.R., Norins, L.C, Schroeter, A.L., and Reising, G. ( 1968 ) Neisseria gonorrhoeae II. Colonial variation and pathogenicity during 35 months in vitro. J Bacteriol 96; 596 – 605.en_US
dc.identifier.citedreferenceKoga, T., Ishimoto, K., and Lory, S. ( 1993 ) Genetic and functional characterization of the gene cluster specifying expression of Pseudomonas aeruginosa pili, Infect Immun 61; 1371 – 1377.en_US
dc.identifier.citedreferenceKoomey, J.M., Gotschlich, E.C, Robbins, K., Bergstrom, S., and Swanson, J. ( 1987 ) Effects of recA mutations on pilus antigenic variation and phase transitions in Neisseria gonorrhoeae. Genetics 117: 391 – 398.en_US
dc.identifier.citedreferenceKoomey, J.M., BergstrØm, S., Blake, M., and Swanson, J. ( 1991 ) Pilin expression and processing in pilus mutants of Neisseria gonorrhoeae: critical role of Gly-1 in assembly, Mol Microbiol 5; 279 – 287.en_US
dc.identifier.citedreferenceLauer, P., Albertson, N.H., and Koomey, M. ( 1993 ) Conservation of genes encoding components of a type IV pilusassembly/two-step protein export pathway in Neisseria gonorrhoeae. Mol Microbiol 8: 357 – 368.en_US
dc.identifier.citedreferenceMeyer, T.F., Billyard, E., Haas, R, Storzbach, S., and So, M. ( 1984 ) Pilus genes of Neisseria gonorrhoeae chromosomal organization and DNA sequence, Proc Natl Acad Sci USA 81: 6110 – 6114.en_US
dc.identifier.citedreferenceMeyer, T.F., Gibbs, C., and Haas, R. ( 1990 ) Variation and control of protein expression In Neisseria. Annu Rev Microbiol 44: 451 – 477.en_US
dc.identifier.citedreferenceNassif, X., Beretti, J.L., Lowy, J., Stenberg, P., O'Gaora, P., Pfeifer, J., Normark, S., and So, M. ( 1994 ) Roles of pilin and PilC in adhesion of Neisseria meningitidis to human epithelial and endothelial cells. Proc Natl Acad Sci USA 91: 3769 – 3773.en_US
dc.identifier.citedreferenceNunn, D.N, Bergman, S., and Lory, S. ( 1990 ) Products of three accessory genes, pilB, pilC, and pilD, are requited for biogenesis of Pseudomonas aeruginosa pili. J Bacteriol 172; 2911 – 2919.en_US
dc.identifier.citedreferencePasloske, B.L., Finlay, B.B., and Paranchych, W. ( 1985 ) Cloning and sequencing of the Pseudomonas aeruginosa PAK pilin gene. FEBS Lett 183: 408 – 412.en_US
dc.identifier.citedreferencePerry, A.C.F., Nicholson, I.J., and Saunders, J.R. ( 1988 ) Neisseria meningitidis strain C114 contains silent truncated pilin genes that are homologous to Neisseria gonorrhoeae pil sequences. J Bacteriol 170: 1691 – 1697.en_US
dc.identifier.citedreferencePotts, W.J., and Saunders, J.R. ( 1988 ) Nucleotide sequence of the structural gene for class I pilin from Neisseria meningitidis: homologies with the pile locus of Neisseria gonorrhoeae. Mol Microbiol 2; 647 – 653.en_US
dc.identifier.citedreferenceProjan, S.J., Monod, M., Narayanan, CS., and Dubnau, D. ( 1987 ) Replication properties of piM13, a naturally occurring plasmid found in Bacillus subtilis, and of its close relative pE5, a plasmid native to Staphylococcus aureus. J Bacteriol 169: 5131 – 5139.en_US
dc.identifier.citedreferencePugsley, A.P. ( 1993 ) The complete general secretory pathway in Gram-negative bacteria, Microbiol Rev 57: 50 – 108.en_US
dc.identifier.citedreferencePugsley, A.P., and Reyss, I. ( 1990 ) Five genes at the 3′ end of the Klebsiella pneumoniae pulC operon are required for pullulanase secretion. Mol Microbiol 4: 365 – 379.en_US
dc.identifier.citedreferenceRao, M.J.L., and Argos, P. ( 1986 ) A conformational preference parameter to predict helices in integral membrane proteins. Biochim Biophys Acta 869; 197 – 214.en_US
dc.identifier.citedreferenceRudel, T., van Putten, J.P.M., Gibbs, C.P., Haas, R., and Meyer, T.F. ( 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.en_US
dc.identifier.citedreferenceSambrook, J., Fritsch, E.F., and Maniatis, T. ( 1989 ) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.en_US
dc.identifier.citedreferenceSandkvist, M., Morales, V., and Bagdasarian, M. ( 1993 ) A soluble protein required for secretion of cholera toxin through the outer membrane of Vibrio cholerae. Gene 123: 81 – 86.en_US
dc.identifier.citedreferenceSanger, F., Nicklen, S., and Coulson, A.R. ( 1977 ) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74; 5463 – 5467.en_US
dc.identifier.citedreferenceSeifert, H.S., Ajioka, R.S., Parachuri, D., Heffron, F., and So, M. ( 1991 ) Shuttle mutagenesis of Neisseria gonorrhoeae: pilin null mutations lower DNA transformation competence. J Bacteriol 172: 40 – 46.en_US
dc.identifier.citedreferenceShaw, C.E., and Taylor, R.K. ( 1990 ) Vibrio cholerae 0395 tcpA pilin gene sequence and comparison of predicted protein structural features to those of type 4 pilins. Infect Immun 58: 3042 – 3049.en_US
dc.identifier.citedreferenceStephens, D.S., and McGee, Z.A. ( 1981 ) Attachment of Neisseria meningitidis to human mucosal surfaces: influence of pili and type of receptor cell. J Inf Dis 143; 525 – 532.en_US
dc.identifier.citedreferenceStrom, M.S., Nunn, D.N., and Lory, S. ( 1991 ) Multiple roles of the pilus biogenesis protein PilD: involvement of PilD in excretion of enzymes from Pseudomonas aeruginosa. J Bacteriol 173: 1175 – 1180.en_US
dc.identifier.citedreferenceStrom, M.S., Nunn, D.N., and Lory, S. ( 1993 ) A single bifunctional enzyme, PilD, catalyzes cleavage and N-methylation of proteins belonging to the type IV pilin family. Proc Natl Acad Sci USA 90: 2404 – 2408.en_US
dc.identifier.citedreferenceSwanson, J. ( 1973 ) Studies on gonococcus infection IV. Pili: their role in attachment of gonococci to tissue culture cells. J Exp Med 137: 571 – 589.en_US
dc.identifier.citedreferenceSwanson, J. ( 1978 ) Studies on gonococcus infection XII, Colony color and opacity variants of gonococci. Infect Immun 19; 320 – 331.en_US
dc.identifier.citedreferenceSwanson, J., Bergstrom, S., Robbins, K., Barrera, O., Corwin, O., and Koomey, M. ( 1986 ) Gene conversion involving the pilin structural gene correlates with pilus +→ pilus- changes in Neisseria gonorrhoeae. Cell 47; 267 – 276.en_US
dc.identifier.citedreferenceSwanson, J., Kraus, S.J., and Gotschlich, E.C. ( 1971 ) Studies on gonococcus infection. L Pili and zones of adhesion: their relation to gonococcal growth patterns. J Exp Med 134; 886 – 906.en_US
dc.identifier.citedreferenceSwanson, J., Robbins, K., Barrera, O., Corwin, D., Boslego, J., Ciak, J., Blake, M., and Koomey, M. ( 1987 ) Gonococcal pilin variants in experimental gonorrhoea. J Exp Med 165: 1344 – 1357.en_US
dc.identifier.citedreferenceTinsley, C.R., and Heckels, J.E. ( 1986 ) Variation in the expression of pili and outer membrane protein by Neisseria meningitidis during the course of meningococcal infection. J Gen Microbiol 132: 106 – 113.en_US
dc.identifier.citedreferenceTØnjum, T., Caugant, D.A., and BØvre, K. ( 1992 ) Differentiation of Moraxella nonliquefaciens, M. lacunata, and M. bovis by using multilocus enzyme electrophoresis and hybridization with pilin-specific DNA probes. J Clin Microbiol 30: 3099 – 3107.en_US
dc.identifier.citedreferenceTØnjum, T., Weir, S., BØvre, K., Progulske-Fox, A., and Mans, C.F. ( 1993 ) Sequence divergence in two tandemly lockated pilin genes of Eikenella corrodens. Infect Immun 61: 1909 – 1916.en_US
dc.identifier.citedreferenceVirji, M., Saunders, J.R., Sims, G., Makepeace, K., Maskell, D., and Ferguson, D.J.P. ( 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 glycosylation. Mol Microbiol 10: 1013 – 1028.en_US
dc.identifier.citedreferenceWeiss, A.A., Johnson, F.D., and Burns, D.L. ( 1993 ) Molecular characterization of an operon required for pertudssis toxin secretion Proc Natl Acad Sci USA 90; 2970 – 2974.en_US
dc.identifier.citedreferenceWhitchurch, C.B., Hobbs, M., Livingston, S.P., Krishnapillai, V., and Mattick, J.S. ( 1991 ) Characterization of a Pseudomonas aeruginosa twitching motility gene and evidence for a specialized protein export system widespread in eubacteria. Gene 101; 33 – 44.en_US
dc.identifier.citedreferenceZhang, O.Y., DeRyckere, D., Lauer, P., and Komey, M. ( 1992 ) Gene conversion in Neisseria gonorrhoeae: evidence for its role in pilus antigenic variation. Proc Natl Acad Sci USA 89; 5366 – 5370.en_US
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Name:
j.1365-2958.1995.tb02410.x.pdf
Size:
5.082MB
Format:
PDF
View/Open

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.