Show simple item record

Secretion of curli fibre subunits is mediated by the outer membrane-localized CsgG protein

dc.contributor.authorRobinson, Lloyd S.en_US
dc.contributor.authorAshman, Elisabeth M.en_US
dc.contributor.authorHultgren, Scott J.en_US
dc.contributor.authorChapman, Matthew R.en_US
dc.date.accessioned2010-06-01T18:29:29Z
dc.date.available2010-06-01T18:29:29Z
dc.date.issued2006-02en_US
dc.identifier.citationRobinson, Lloyd S.; Ashman, Elisabeth M.; Hultgren, Scott J.; Chapman, Matthew R. (2006). "Secretion of curli fibre subunits is mediated by the outer membrane-localized CsgG protein." Molecular Microbiology 59(3): 870-881. <http://hdl.handle.net/2027.42/71698>en_US
dc.identifier.issn0950-382Xen_US
dc.identifier.issn1365-2958en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/71698
dc.identifier.urihttp://www.ncbi.nlm.nih.gov/sites/entrez?cmd=retrieve&db=pubmed&list_uids=16420357&dopt=citationen_US
dc.description.abstractProduced by many Enterobacteriaceae spp., curli are biologically important amyloid fibres that have been associated with biofilm formation, host cell adhesion and invasion, and immune system activation. CsgA is the major fibre subunit and CsgE, CsgF and CsgG are non-structural proteins involved in curli biogenesis. We have characterized the role of CsgG in curli subunit secretion across the outer membrane. Directed mutagenesis of CsgG confirmed that its activity is dependent on localization to the outer membrane. Rotary Shadow electron microscopy of purified CsgG suggested that this protein assembles into an oligomeric complex with an apparent central pore. Oligomeric CsgG complexes were confirmed using co-purification experiments. Antibiotic sensitivity assays demonstrated that overexpression of CsgG rendered Escherichia coli susceptible to the antibiotic erythromycin. A 22-amino-acid sequence at the N-terminus of CsgA was sufficient to direct heterologous proteins to the CsgG secretion apparatus. Finally, we determined that CsgG participates in an outer membrane complex with two other curli assembly proteins, CsgE and CsgF.en_US
dc.format.extent357103 bytes
dc.format.extent30660 bytes
dc.format.extent3109 bytes
dc.format.mimetypeapplication/pdf
dc.format.mimetypeapplication/pdf
dc.format.mimetypetext/plain
dc.publisherBlackwell Science Ltden_US
dc.rights© 2005 The Authors; Journal compilation © 2005 Blackwell Publishing Ltden_US
dc.titleSecretion of curli fibre subunits is mediated by the outer membrane-localized CsgG proteinen_US
dc.typeArticleen_US
dc.subject.hlbsecondlevelMicrobiology and Immunologyen_US
dc.subject.hlbtoplevelScienceen_US
dc.description.peerreviewedPeer Revieweden_US
dc.contributor.affiliationumDepartment of Molecular, Cellular and Developmental Biology, University of Michigan, 830 North University, Ann Arbor, MI 48109, USA.en_US
dc.contributor.affiliationotherDepartment of Molecular Microbiology and Microbial Pathogenesis, Box 8230, Washington University School of Medicine, 660S. Euclid Ave, St Louis, MO 63110, USA.en_US
dc.identifier.pmid16420357en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/71698/1/j.1365-2958.2005.04997.x.pdf
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/71698/2/MMI4997TableS1.pdf
dc.identifier.doi10.1111/j.1365-2958.2005.04997.xen_US
dc.identifier.sourceMolecular Microbiologyen_US
dc.identifier.citedreferenceAugustus, A. M., Celaya, T., Husain, F., Humbard, M., Misra, R. ( 2004 ) Antibiotic-sensitive TolC mutants and their suppressors. J Bacteriol 186: 1851 – 1860.en_US
dc.identifier.citedreferenceBen Nasr, A., Olsen, A., Sjobring, U., Muller-Esterl, W., Bjorck, L. ( 1996 ) Assembly of human contact phase proteins and release of bradykinin at the surface of curli-expressing Escherichia coli. Mol Microbiol 20: 927 – 935.en_US
dc.identifier.citedreferenceBian, Z., Normark, S. ( 1997 ) Nucleator function of CsgB for the assembly of adhesive surface organelles in Escherichia coli. EMBO J 16: 5827 – 5836.en_US
dc.identifier.citedreferenceBose, N., Taylor, R. K. ( 2005 ) Identification of a TcpC-TcpQ outer membrane complex involved in the biogenesis of the toxin-coregulated pilus of Vibrio cholerae. J Bacteriol 187: 2225 – 2232.en_US
dc.identifier.citedreferenceBrok, R., Van Gelder, P., Winterhalter, M., Ziese, U., Koster, A. J., de Cock, H., et al. ( 1999 ) The C-terminal domain of the Pseudomonas secretin XcpQ forms oligomeric rings with pore activity. J Mol Biol 294: 1169 – 1179.en_US
dc.identifier.citedreferenceCampbell, A. ( 1961 ) Sensitive mutants of bacteriophage lambda. Virology 14: 22 – 32.en_US
dc.identifier.citedreferenceCasadaban, M. J. ( 1976 ) Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J Mol Biol 104: 541 – 555.en_US
dc.identifier.citedreferenceChapman, M. R., Robinson, L. S., Pinkner, J. S., Roth, R., Heuser, J., Hammar, M., et al. ( 2002 ) Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295: 851 – 855.en_US
dc.identifier.citedreferenceChirwa, N. T., Herrington, M. B. ( 2003 ) CsgD, a regulator of curli and cellulose synthesis, also regulates serine hydroxymethyltransferase synthesis in Escherichia coli K-12. Microbiology 149: 525 – 535.en_US
dc.identifier.citedreferenceCollinson, S. K., Doig, P. C., Doran, J. L., Clouthier, S., Trust, T. J., Kay, W. W. ( 1993 ) Thin, aggregative fimbriae mediate binding of Salmonella enteritidis to fibronectin. J Bacteriol 175: 12 – 18.en_US
dc.identifier.citedreferenceCollinson, S. K., Parker, J. M., Hodges, R. S., Kay, W. W. ( 1999 ) Structural predictions of AgfA, the insoluble fimbrial subunit of Salmonella thin aggregative fimbriae. J Mol Biol 290: 741 – 756.en_US
dc.identifier.citedreferenceGerstel, U., Park, C., Romling, U. ( 2003 ) Complex regulation of csgD promoter activity by global regulatory proteins. Mol Microbiol 49: 639 – 654.en_US
dc.identifier.citedreferenceGuzman, L. M., Belin, D., Carson, M. J., Beckwith, J. ( 1995 ) Tight regulation, modulation, and high-level expression by vectors containing the arabinose P BAD promoter. J Bacteriol 177: 4121 – 4130.en_US
dc.identifier.citedreferenceHammar, M., Arnqvist, A., Bian, Z., Olsen, A., Normark, S. ( 1995 ) Expression of two csg operons is required for production of fibronectin- and congo red-binding curli polymers in Escherichia coli K-12. Mol Microbiol 18: 661 – 670.en_US
dc.identifier.citedreferenceHammar, M., Bian, Z., Normark, S. ( 1996 ) Nucleator-dependent intercellular assembly of adhesive curli organelles in Escherichia coli. Proc Natl Acad Sci USA 93: 6562 – 6566.en_US
dc.identifier.citedreferenceHardie, K. R., Seydel, A., Guilvout, I., Pugsley, A. P. ( 1996 ) The secretin-specific, chaperon-like protein of the general secretory pathway: separation of proteolytic protection and piloting functions. Mol Microbiol 22: 967 – 976.en_US
dc.identifier.citedreferenceHung, D. L., Raivio, T. L., Jones, C. H., Silhavy, T. J., Hultgren, S. J. ( 2001 ) Cpx signaling pathway monitors biogenesis and affects assembly and expression of P pili. EMBO J 20: 1508 – 1518.en_US
dc.identifier.citedreferenceKayed, R., Head, E., Thompson, J. L., McIntire, T. M., Milton, S. C., Cotman, C. W., Glabe, C. G. ( 2003 ) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300: 486 – 489.en_US
dc.identifier.citedreferenceLashuel, H. A., Hartley, D., Petre, B. M., Walz, T., Lansbury, P. T., Jr. ( 2002 ) Neurodegenerative disease: amyloid pores from pathogenic mutations. Nature 418: 291.en_US
dc.identifier.citedreferenceLoferer, H., Hammar, M., Normark, S. ( 1997 ) Availability of the fibre subunit CsgA and the nucleator protein CsgB during assembly of fibronectin-binding curli is limited by the intracellular concentration of the novel lipoprotein CsgG. Mol Microbiol 26: 11 – 23.en_US
dc.identifier.citedreferenceMundy, R., Pickard, D., Wilson, R. K., Simmons, C. P., Dougan, G., Frankel, G. ( 2003 ) Identification of a novel type IV pilus gene cluster required for gastrointestinal colonization of Citrobacter rodentium. Mol Microbiol 48: 795 – 809.en_US
dc.identifier.citedreferenceNarita, S., Matsuyama, S., Tokuda, H. ( 2004 ) Lipoprotein trafficking in Escherichia coli. Arch Microbiol 182: 1 – 6.en_US
dc.identifier.citedreferenceNevesinjac, A. Z., Raivio, T. L. ( 2005 ) The Cpx envelope stress response affects expression of the type IV bundle-forming pili of enteropathogenic Escherichia coli. J Bacteriol 187: 672 – 686.en_US
dc.identifier.citedreferenceOlsen, A., Jonsson, A., Normark, S. ( 1989 ) Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 338: 652 – 655.en_US
dc.identifier.citedreferencePrigent-Combaret, C., Brombacher, E., Vidal, O., Ambert, A., Lejeune, P., Landini, P., Dorel, C. ( 2001 ) Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J Bacteriol 183: 7213 – 7223.en_US
dc.identifier.citedreferenceRamer, S. W., Bieber, D., Schoolnik, G. K. ( 1996 ) BfpB, an outer membrane lipoprotein required for the biogenesis of bundle-forming pili in enteropathogenic Escherichia coli. J Bacteriol 178: 6555 – 6563.en_US
dc.identifier.citedreferenceRomling, U., Bian, Z., Hammar, M., Sierralta, W. D., Normark, S. ( 1998a ) Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol 180: 722 – 731.en_US
dc.identifier.citedreferenceRomling, U., Sierralta, W. D., Eriksson, K., Normark, S. ( 1998b ) Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol Microbiol 28: 249 – 264.en_US
dc.identifier.citedreferenceRuiz, N., Silhavy, T. J. ( 2005 ) Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr Opin Microbiol 8: 122 – 126.en_US
dc.identifier.citedreferenceSchmidt, 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.en_US
dc.identifier.citedreferenceSjobring, U., Pohl, G., Olsen, A. ( 1994 ) Plasminogen, absorbed by Escherichia coli expressing curli or by Salmonella enteritidis expressing thin aggregative fimbriae, can be activated by simultaneously captured tissue-type plasminogen activator (t-PA). Mol Microbiol 14: 443 – 452.en_US
dc.identifier.citedreferenceThanassi, D. G., Hultgren, S. J. ( 2000 ) Assembly of complex organelles: pilus biogenesis in Gram-negative bacteria as a model system. Methods 20: 111 – 126.en_US
dc.identifier.citedreferenceThanassi, D. G., Saulino, E. T., Lombardo, M. J., Roth, R., Heuser, J., Hultgren, S. J. ( 1998 ) The PapC usher forms an oligomeric channel: implications for pilus biogenesis across the outer membrane. Proc Natl Acad Sci USA 95: 3146 – 3151.en_US
dc.identifier.citedreferenceZogaj, X., Nimtz, M., Rohde, M., Bokranz, W., Romling, U. ( 2001 ) The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol 39: 1452 – 1463.en_US
dc.identifier.citedreferenceZogaj, X., Bokranz, W., Nimtz, M., Romling, U. ( 2003 ) Production of cellulose and curli fimbriae by members of the family Enterobacteriaceae isolated from the human gastrointestinal tract. Infect Immun 71: 4151 – 4158.en_US
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

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.