Fimbriae: Classification and Biochemistry

David G. Thanassi; Sean-Paul Nuccio; Stephane Shu Kin So; Andreas J. Bäumler

doi:10.1128/ecosalplus.2.4.2.1

journal article Dec 31, 2007

Fimbriae: Classification and Biochemistry

David G. Thanassi Sean-Paul Nuccio Stephane Shu Kin So Andreas J. Bäumler

EcoSal Plus Vol. 2 No. 2 · American Society for Microbiology

View at Publisher Save 10.1128/ecosalplus.2.4.2.1

Abstract

Proteinaceous, nonflagellar surface appendages constitute a variety of structures, including those known variably as fimbriae or pili. Constructed by distinct assembly pathways resulting in diverse morphologies, fimbriae have been described to mediate functions including adhesion, motility, and DNA transfer. As these structures can represent major diversifying elements among
Escherichia
and
Salmonella
isolates, multiple fimbrial classification schemes have been proposed and a number of mechanistic insights into fimbrial assembly and function have been made. Herein we describe the classifications and biochemistry of fimbriae assembled by the chaperone/usher, curli, and type IV pathways.

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References

321

[1]

Holmgren A Brändén C. 1989. Crystal structure of chaperone protein PapD reveals an immunoglobulin fold. Nature 342:248–251. [PubMed][CrossRef] 10.1038/342248a0

[2]

Duguid JP Campbell I. 1969. Antigens of the type-1 fimbriae of salmonellae and other enterobacteria. J Med Microbiol 2:535–553. [PubMed][CrossRef] 10.1099/00222615-2-4-535

[3]

Duguid JP Anderson ES Campbell I. 1966. Fimbriae and adhesive properties in salmonellae. J Pathol Bacteriol 92:107–138. [PubMed][CrossRef] 10.1002/path.1700920113

[4]

Boylan M Smyth CJ Scott JR. 1988. Nucleotide sequence of the gene encoding the major subunit of CS3 fimbriae of enterotoxigenic Escherichia coli. Infect Immun 56:3297–3300.[PubMed] 10.1128/iai.56.12.3297-3300.1988

[5]

Brinton CC Jr. 1959. Non-flagellar appendages of bacteria. Nature 183:782–786. [PubMed][CrossRef] 10.1038/183782a0

[6]

Ørskov I F Ørskov. 1990. Serologic classification of fimbriae. Curr Top Microbiol Immunol 151:71–90.[PubMed] 10.1007/978-3-642-74703-8_4

[7]

Bradley DE. 1980. A function of Pseudomonas aeruginosa PAO polar pili: twitching motility. Can J Microbiol 26:146–154.[PubMed] 10.1139/m80-022

[8]

Duguid JP. 1959. Fimbriae and adhesive properties in Klebsiella strains. J Gen Microbiol 21:271–286. [PubMed][CrossRef] 10.1099/00221287-21-1-271

[9]

Donnenberg MS Giron JA Nataro JP Kaper JB. 1992. A plasmid-encoded type IV fimbrial gene of enteropathogenic Escherichia coli associated with localized adherence. Mol Microbiol 6:3427–3437. [PubMed][CrossRef] 10.1111/j.1365-2958.1992.tb02210.x

[10]

Kisiela D Sapeta A Kuczkowski M Stefaniak T Wieliczko A Ugorski M. 2005. Characterization of FimH adhesins expressed by Salmonella enterica serovar Gallinarum biovars Gallinarum and Pullorum: reconstitution of mannose-binding properties by single amino acid substitution. Infect Immun 73:6187–6190. [PubMed][CrossRef] 10.1128/iai.73.9.6187-6190.2005

[11]

Pugsley A. 1993. The complete general secretory pathway in Gram negative bacteria. Microbiol Rev 57:50–108.[PubMed] 10.1128/mr.57.1.50-108.1993

[12]

Jones CH Pinkner JS Nicholes AV Slonim LN Abraham SN Hultgren SJ. 1993. FimC is a periplasmic PapD-like chaperone that directs assembly of type 1 pili in bacteria. Proc Natl Acad Sci USA 90:8397–8401. [PubMed][CrossRef] 10.1073/pnas.90.18.8397

[13]

Labigne-Roussel AF Lark D Schoolnik G Falkow S. 1984. Cloning and expression of an afimbrial adhesin (AFA-I) responsible for P blood group-independent mannose-resistant hemagglutination from a pyelonephritic Escherichia coli strain. Infect Immun 46:251–259.[PubMed] 10.1128/iai.46.1.251-259.1984

[14]

Norgren M Baga M Tennent JM Normark S. 1987. Nucleotide sequence regulation and functional analysis of the papC gene required for cell surface localization of Pap pili of uropathogenic Escherichia coli. Mol Microbiol 1:169–178. [PubMed][CrossRef] 10.1111/j.1365-2958.1987.tb00509.x

[15]

Normark S Lark D Hull R Norgren M Baga M O'Hanley P Schoolnik G Falkow S. 1983. Genetics of digalactoside-binding adhesin from a uropathogenic Escherichia coli strain. Infect Immun 41:942–949.[PubMed] 10.1128/iai.41.3.942-949.1983

[16]

Knutton S McConnell MM Rowe B McNeish AS. 1989. Adhesion and ultrastructural properties of human enterotoxigenic Escherichia coli producing colonization factor antigens III and IV. Infect Immun 57:3364–3371.[PubMed] 10.1128/iai.57.11.3364-3371.1989

[17]

Pallen MJ Wren BW. 1997. The HtrA family of serine proteases. Mol Microbiol 26:209–221. [PubMed][CrossRef] 10.1046/j.1365-2958.1997.5601928.x

[18]

Okamoto S Ohmori M. 2002. The cyanobacterial PilT protein responsible for cell motility and transformation hydrolyzes ATP. Plant Cell Physiol 43:1127–1136. [PubMed][CrossRef] 10.1093/pcp/pcf128

[19]

Karch H Heesemann J Laufs R O'Brien AD Tacket CO Levine MM. 1987. A plasmid of enterohemorrhagic Escherichia coli O157:H7 is required for expression of a new fimbrial antigen and for adhesion to epithelial cells. Infect Immun 55:455–461.[PubMed] 10.1128/iai.55.2.455-461.1987

[20]

Torres AG Kanack KJ Tutt CB Popov V Kaper JB. 2004. Characterization of the second long polar (LP) fimbriae of Escherichia coli O157:H7 and distribution of LP fimbriae in other pathogenic E. coli strains. FEMS Microbiol Lett 238:333–344. [PubMed][CrossRef] 10.1111/j.1574-6968.2004.tb09774.x

[21]

Roosendaal E Boots M de Graaf FK. 1987. Two novel genes fanA and fanB involved in the biogenesis of K99 fimbriae. Nucleic Acids Res 15:5973–5984. [PubMed][CrossRef] 10.1093/nar/15.15.5973

[22]

Jacob-Dubuisson F Pinkner J Xu Z Striker R Padmanhaban A Hultgren SJ. 1994. PapD chaperone function in pilus biogenesis depends on oxidant and chaperone-like activities of DsbA. Proc Natl Acad Sci USA 91:11552–11556. [PubMed][CrossRef] 10.1073/pnas.91.24.11552

[23]

Qadri F Svennerholm AM Faruque AS Sack RB. 2005. Enterotoxigenic Escherichia coli in developing countries: epidemiology microbiology clinical features treatment and prevention. Clin Microbiol Rev 18:465–483. [PubMed][CrossRef] 10.1128/cmr.18.3.465-483.2005

[24]

Loferer 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. [PubMed][CrossRef] 10.1046/j.1365-2958.1997.5231883.x

[25]

Grund S Seiler A. 1993. Electron microscopic studies of fimbriae and lectin phagocytosis of Salmonella typhimurium variety copenhagen (STMVC). Zentbl Veterinarmed B 40:105–112. (In German.) 10.1111/j.1439-0450.1993.tb00116.x

[26]

Sauer FG Remaut H Hultgren SJ Waksman G. 2004. Fiber assembly by the chaperone-usher pathway. Biochim Biophys Acta 1694:259–267. [PubMed][CrossRef] 10.1016/j.bbamcr.2004.02.010

[27]

Bieber D Ramer SW Wu CY Murray WJ Tobe T Fernandez R Schoolnik GK. 1998. Type IV pili transient bacterial aggregates and virulence of enteropathogenic Escherichia coli. Science 280:2114–2118. [PubMed][CrossRef] 10.1126/science.280.5372.2114

[28]

Tukel C Raffatellu M Humphries AD Wilson RP Andrews-Polymenis HL Gull T Figueiredo JF Wong MH Michelsen KS Akcelik M Adams LG Baumler AJ. 2005. CsgA is a pathogen-associated molecular pattern of Salmonella enterica serotype Typhimurium that is recognized by Toll-like receptor 2. Mol Microbiol 58:289–304. [PubMed][CrossRef] 10.1111/j.1365-2958.2005.04825.x

[29]

Horiuchi T Komano T. 1998. Mutational analysis of plasmid R64 thin pilus prepilin: the entire prepilin sequence is required for processing by type IV prepilin peptidase. J Bacteriol 180:4613–4620.[PubMed] 10.1128/jb.180.17.4613-4620.1998

[30]

Strom MS Lory S. 1992. Kinetics and sequence specificity of processing of prepilin by PilD the type IV leader peptidase of Pseudomonas aeruginosa. J Bacteriol 174:7345–7351.[PubMed] 10.1128/jb.174.22.7345-7351.1992

[31]

Torres AG Giron JA Perna NT Burland V Blattner FR Avelino-Flores F Kaper JB. 2002. Identification and characterization of lpfABCC'DE a fimbrial operon of enterohemorrhagic Escherichia coli O157:H7. Infect Immun 70:5416–5427. [PubMed][CrossRef] 10.1128/iai.70.10.5416-5427.2002

[32]

Kuehn MJ Heuser J Normark S Hultgren SJ. 1992. P pili in uropathogenic E. coli are composite fibres with distinct fibrillar adhesive tips. Nature 356:252–255. [PubMed][CrossRef] 10.1038/356252a0

[33]

Khan AS Kniep B Oelschlaeger TA Van Die I Korhonen T Hacker J. 2000. Receptor structure for F1C fimbriae of uropathogenic Escherichia coli. Infect Immun 68:3541–3547. [PubMed][CrossRef] 10.1128/iai.68.6.3541-3547.2000

[34]

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. [PubMed][CrossRef] 10.1046/j.1365-2958.1998.00677.x

[35]

Martin C Rousset E De Greve H. 1997. Human uropathogenic and bovine septicaemic Escherichia coli strains carry an identical F17-related adhesin. Res Microbiol 148:55–64. [PubMed][CrossRef] 10.1016/s0923-2508(97)81900-6

[36]

Donnenberg MS Zhang HZ Stone KD. 1997. Biogenesis of the bundle-forming pilus of enteropathogenic Escherichia coli: reconstitution of fimbriae in recombinant E. coli and role of DsbA in pilin stability: a review. Gene 192:33–38. [PubMed][CrossRef] 10.1016/s0378-1119(96)00826-8

[37]

Vetsch M Puorger C Spirig T Grauschopf U Weber-Ban EU Glockshuber R. 2004. Pilus chaperones represent a new type of protein-folding catalyst. Nature 431:329–333. [PubMed][CrossRef] 10.1038/nature02891

[38]

Froehlich BJ Karakashian A Sakellaris H Scott JR. 1995. Genes for CS2 pili of enterotoxigenic Escherichia coli and their interchangeability with those for CS1 pili. Infect Immun 63:4849–4856.[PubMed] 10.1128/iai.63.12.4849-4856.1995

[39]

Duguid JP. 1968. The function of bacterial fimbriae. Arch Immunol Ther Exp (Warsz) 16:173–188.[PubMed]

[40]

Nowicki B Hart A Coyne KE Lublin DM Nowicki S. 1993. Short consensus repeat-3 domain of recombinant decay-accelerating factor is recognized by Escherichia coli recombinant Dr adhesin in a model of a cell-cell interaction. J Exp Med 178:2115–2121. [PubMed][CrossRef] 10.1084/jem.178.6.2115

[41]

Immunoglobulin-like PapD chaperone caps and uncaps interactive surfaces of nascently translocated pilus subunits.

Meta J. Kuehn, S Normark, S J Hultgren

Proceedings of the National Academy of Sciences 10.1073/pnas.88.23.10586

[42]

Old DC Payne SB. 1971. Antigens of the type-2 fimbriae of salmonellae: “cross-reacting material” (CRM) of type-1 fimbriae. J Med Microbiol 4:215–225. [PubMed][CrossRef] 10.1099/00222615-4-2-215

[43]

Salmonella enterica Serovar Typhi Possesses a Unique Repertoire of Fimbrial Gene Sequences

Stacy M. Townsend, Naomi E. Kramer, Robert Edwards et al.

Infection and Immunity 10.1128/iai.69.5.2894-2901.2001

[44]

Lee YM DiGiuseppe PA Silhavy TJ Hultgren SJ. 2004. P pilus assembly motif necessary for activation of the CpxRA pathway by PapE in Escherichia coli. J Bacteriol 186:4326–4237. [PubMed][CrossRef] 10.1128/jb.186.13.4326-4337.2004

[45]

Manting EH Driessen AJ. 2000. Escherichia coli translocase: the unravelling of a molecular machine. Mol Microbiol 37:226–238. [PubMed][CrossRef] 10.1046/j.1365-2958.2000.01980.x

[46]

Low D Braaten B van der Woude M. 1996. Fimbriae p 146–157. In Neidhardt FC Curtiss R III Ingraham JL Lin ECC Low KB Magasanik B Reznikoff WS Riley M Schaechter M and Umbarger HE (ed) Escherichia coli and Salmonella: Cellular and Molecular Biology 2nd ed. ASM Press Washington DC.

[47]

The PapG protein is the alpha-D-galactopyranosyl-(1----4)-beta-D-galactopyranose-binding adhesin of uropathogenic Escherichia coli.

B Lund, F Lindberg, B I Marklund et al.

Proceedings of the National Academy of Sciences 10.1073/pnas.84.16.5898

[48]

Ramboarina S Fernandes PJ Daniell S Islam S Simpson P Frankel G Booy F Donnenberg MS Matthews S. 2005. Structure of the bundle-forming pilus from enteropathogenic Escherichia coli. J Biol Chem 280:40252–40260. [PubMed][CrossRef] 10.1074/jbc.m508099200

[49]

Jacob-Dubuisson F Heuser J Dodson K Normark S Hultgren SJ. 1993. Initiation of assembly and association of the structural elements of a bacterial pilus depend on two specialized tip proteins. EMBO J 12:837–847.[PubMed] 10.1002/j.1460-2075.1993.tb05724.x

[50]

Evans DG Evans DJ Jr Clegg S Pauley JA. 1979. Purification and characterization of the CFA/I antigen of enterotoxigenic Escherichia coli. Infect Immun 25:738–748.[PubMed] 10.1128/iai.25.2.738-748.1979

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Details

Published: Dec 31, 2007
Vol/Issue: 2(2)
License: View

Authors

D

David G. Thanassi

Center for Infectious Diseases, Department of Molecular Genetics and Microbiology, Stony Brook University, Stony Brook, NY 11794-5120

S

Sean-Paul Nuccio

Department of Medical Microbiology and Immunology, School of Medicine, University of California at Davis, One Shields Ave., Davis, CA 95616-8645

Department of Medical Microbiology and Immunology, School of Medicine, University of California at Davis, One Shields Ave., Davis, California 95616-8645

Cite This Article

David G. Thanassi, Sean-Paul Nuccio, Stephane Shu Kin So, et al. (2007). Fimbriae: Classification and Biochemistry. EcoSal Plus, 2(2). https://doi.org/10.1128/ecosalplus.2.4.2.1

Fimbriae: Classification and Biochemistry

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