Abstract
The presence of a diversity of virulence factors such as Chaperone-Usher (CU) fibers in uropathogenic Escherichia coli (UPEC) pathotypes virulome has offered these bacteria a unique opportunity to select the right factors in suitable condition. Understanding the structures and mechanisms of these infectious weapons enables us to prevent the occurrence of infections and/or to treat the urinary tract infections (UTIs) with effective methodologies. This review summarizes the current knowledge on the mechanisms of CU fimbriae (CUF) formation in UPEC. Several CU fibers including Auf, Dr, F1C, S, Type 9, Type 3, Type 1, and P fimbriae have been recognized in UPEC pathotypes. These fimbrial organelles may have cross-talk with each other in the presence of different environmental factors. In other words, the expression or the silence of their genes are associated with a wide range of items comprising environmental factors, genetical factors, physiological factors, etc. Recognition, detection, and identification of virulome and the related characteristics, properties, and mechanisms in UPEC enable us to create new methodologies to have a definite prevention and treatment for UTIs in this regard.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abby S, Cury J, Guglielmini J, Néron B, Touchon M, Rocha EP (2016) Identification of protein secretion systems in bacterial genomes. Sci Rep 6:23080. https://doi.org/10.1038/srep23080
Agarwal J, Srivastava S, Singh M (2012) Pathogenomics of uropathogenic Escherichia coli. Indian J Med Microbiol 30:141–149. https://doi.org/10.4103/0255-0857.96657
Anderson KL et al (2004) An atomic resolution model for assembly, architecture, and function of the Dr adhesins. Mol Cell 15:647–657. https://doi.org/10.1016/j.molcel.2004.08.003
Baby S, Karnaker VK, Geetha R (2016) Adhesins of Uropathogenic Escherichia coli (UPEC). Int J Med Microbiol Trop Dis 2:10–18
Balsalobre C, Morschhäuser J, Jass J, Hacker J, Uhlin BE (2003) Transcriptional analysis of the sfa determinant revealing multiple mRNA processing events in the biogenesis of S fimbriae in pathogenic Escherichia coli. J Bacteriol 185:620–629. https://doi.org/10.1128/JB.185.2.620-629.2003
Bao R, Fordyce A, Chen Y-X, McVeigh A, Savarino SJ, Xia D (2014) Structure of CfaA suggests a new family of chaperones essential for assembly of class 5 fimbriae. PLoS Pathog 10:e1004316. https://doi.org/10.1371/journal.ppat.1004316
Bao R et al (2013) Structural basis for the specific recognition of dual receptors by the homopolymeric pH 6 antigen (Psa) fimbriae of Yersinia pestis. Proc Natl Acad Sci U S A 110:1065–1070. https://doi.org/10.1073/pnas.1212431110
Barnhart MM, Sauer FG, Pinkner JS, Hultgren SJ (2003) Chaperone-subunit-usher interactions required for donor strand exchange during bacterial pilus assembly. J Bacteriol 185:2723–2730. https://doi.org/10.1128/JB.185.9.2723-2730.2003
Behzadi E, Behzadi P (2016) The role of toll-like receptors (TLRs) in urinary tract infections (UTIs). Cent European J Urol 69:404–410. https://doi.org/10.5173/ceju.2016.871
Behzadi E, Behzadi P, Sirmatel F (2009) Identification of 30-kDa heat shock protein gene in Trichophyton rubrum. Mycoses 52:234–238. https://doi.org/10.1111/j.1439-0507.2008.01561.x
Behzadi P (2018a) Introductory chapter: an overview on urinary tract infections, pathogens, and risk factors. In: Behzadi P (ed) Microbiology of urinary tract infections: microbial agents and predisposing factors. IntechOpen, Croatia, pp 1–6. https://doi.org/10.5772/intechopen.82230
Behzadi P (2018b) Uropathogenic Escherichia coli and fimbrial adhesins virulome. In: Jarzembowski DT (ed) Urinary tract infection - the result of the strength of the pathogen, or the weakness of the host, 1st edn. InTech, Croatia, pp 65–84. https://doi.org/10.5772/intechopen.71374
Behzadi P, Behzadi E (2006) Detection of apoptosis feature in ultraviolet light-exposed Trichophyton rubrum. Turkiye Klinikleri J Med Sci 26:607–610
Behzadi P, Behzadi E (2008) The microbial agents of urinary tract infections at central laboratory of Dr. Shariati Hospital, Tehran, Iran. Turk Klin Tip Bilim 28:445–449
Behzadi P, Behzadi E (2011) A study on apoptosis inducing effects of UVB irradiation in Pseudomonas aeruginosa. Roum Arch Microbiol Immunol 70:74–77
Behzadi P, Behzadi E (2012) Evaluation of UVB light efficacy for inducing apoptosis in Candida albicans cultures. Roum Arch Microbiol Immunol 71:39–42
Behzadi P, Behzadi E (2017) Uropathogenic Escherichia coli: an ideal resource for DNA microarray probe designing. In: Rojas I, Ortuño F (eds) International conference on bioinformatics and biomedical engineering (IWBBIO), Spain, 2017. Springer, Cham, pp 12–19. https://doi.org/10.1007/978-3-319-56154-7_2
Behzadi P, Behzadi E, Alavian SM (2017) DNA microarray technology in HBV genotyping. Minerva Med 108:473–476. https://doi.org/10.23736/S0026-4806.17.05059-5
Behzadi P, Behzadi E, Pawlak-Adamska EA (2019) Urinary tract infections (UTIs) or genital tract infections (GTIs)? It's the diagnostics that count. GMS Hyg Infect Control 14:Doc: 14 doi:https://doi.org/10.3205/dgkh000320
Behzadi P, Behzadi E, Ranjbar R (2015) Urinary tract infections and Candida albicans. Cent European J Urol 68:96–101. https://doi.org/10.5173/ceju.2015.01.474
Behzadi P, Behzadi E, Ranjbar R (2016a) IL-12 family cytokines: general characteristics, pathogenic microorganisms, receptors, and signalling pathways. Acta Microbiol Immunol Hung 63:1–25. https://doi.org/10.1556/030.63.2016.1.1
Behzadi P, Issakhanian L (2019) Gene regulation, an RNA network-dependent architecture. In: Behzadi P (ed) Gene regulation, 1st edn. IntechOpen, Croatia, pp 1–6. https://doi.org/10.5772/intechopen.84535
Behzadi P, Najafi A, Behzadi E, Ranjbar R (2016b) Microarray long oligo probe designing for Escherichia coli: an in-silico DNA marker extraction. Cent European J Urol 69:105–111. https://doi.org/10.5173/ceju.2016.654
Behzadi P, Ranjbar R (2019) DNA microarray technology and bioinformatic web services. Acta Microbiol Immunol Hung 66:19–30. https://doi.org/10.1556/030.65.2018.028
Berry AA et al (2014) Structural insight into host recognition by aggregative adherence fimbriae of enteroaggregative Escherichia coli. PLoS Pathog 10:e1004404
Bien J, Sokolova O, Bozko P (2012) Role of uropathogenic Escherichia coli virulence factors in development of urinary tract infection and kidney damage. Int J Nephrol 2012:681473. https://doi.org/10.1155/2012/681473
Buckles EL et al (2004) Identification and characterization of a novel uropathogenic Escherichia coli-associated fimbrial gene cluster. Infect Immun 72:3890–3901. https://doi.org/10.1128/IAI.72.7.3890-3901.2004
Busch A, Waksman G (2012) Chaperone–usher pathways: diversity and pilus assembly mechanism. Philos Trans R Soc Lond Ser B Biol Sci 367:1112–1122. https://doi.org/10.1098/rstb.2011.0206
Chahales P, Thanassi DG (2015) Structure, function, and assembly of adhesive organelles by uropathogenic bacteria. Microbiol Spectr 3. https://doi.org/10.1128/microbiolspec.UTI-0018-2013doi:10.1128/microbiolspec.UTI-0018-2013
Cheryl-lynn YO, Beatson SA, Totsika M, Forestier C, McEwan AG, Schembri MA (2010) Molecular analysis of type 3 fimbrial genes from Escherichia coli, Klebsiella and Citrobacter species. BMC Microbiol 10:183. https://doi.org/10.1186/1471-2180-10-183
Choudhury D, Thompson A, Stojanoff V, Langermann S, Pinkner J, Hultgren SJ, Knight SD (1999) X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science 285:1061–1066
Clare D, Saibil HR (2013) ATP-driven molecular chaperone machines. Biopolymers 99:846–859. https://doi.org/10.1002/bip.22361
Conover MS et al (2016) Inflammation-induced adhesin-receptor interaction provides a fitness advantage to uropathogenic E. coli during chronic infection. Cell Host Microbe 20:482–492. https://doi.org/10.1016/j.chom.2016.08.013
Costa TR, Felisberto-Rodrigues C, Meir A, Prevost MS, Redzej A, Trokter M, Waksman G (2015) Secretion systems in gram-negative bacteria: structural and mechanistic insights. Nat Rev Microbiol 13:343–359. https://doi.org/10.1038/nrmicro3456
Ellis RJ (2013) Assembly chaperones: a perspective. Philos Trans R Soc Lond Ser B Biol Sci 368:20110398. https://doi.org/10.1098/rstb.2011.0398
Fronzes R, Remaut H, Waksman G (2008) Architectures and biogenesis of non-flagellar protein appendages in Gram-negative bacteria. EMBO J 27:2271–2280. https://doi.org/10.1038/emboj.2008.155
Geibel S, Procko E, Hultgren SJ, Baker D, Waksman G (2013) Structural and energetic basis of folded-protein transport by the FimD usher. Nature 496:243–246. https://doi.org/10.1038/nature12007
Geibel S, Waksman G (2014) The molecular dissection of the chaperone–usher pathway. Biochim Biophys Acta 1843:1559–1567. https://doi.org/10.1016/j.bbamcr.2013.09.023
Gerlach G-F, Clegg S, Allen BL (1989) Identification and characterization of the genes encoding the type 3 and type 1 fimbrial adhesins of Klebsiella pneumoniae. J Bacteriol 171:1262–1270
Gerlach RG, Hensel M (2007) Protein secretion systems and adhesins: the molecular armory of Gram-negative pathogens. Int J Med Microbiol 297:401–415. https://doi.org/10.1016/j.ijmm.2007.03.017
Godaly G, Ambite I, Svanborg C (2015) Innate immunity and genetic determinants of urinary tract infection susceptibility. Curr Opin Infect Dis 28:88–96. https://doi.org/10.1097/QCO.0000000000000127
Grohmann E, Christie PJ, Waksman G, Backert S (2018) Type IV secretion in gram-negative and gram-positive bacteria. Mol Microbiol 107:455–471. https://doi.org/10.1111/mmi.13896
Holmgren A, Bränden C (1989) Crystal structure of chaperone protein PapD reveals an immunoglobulin fold. Nature 342:248–251
Hospenthal MK, Costa TR, Waksman G (2017a) A comprehensive guide to pilus biogenesis in gram-negative bacteria. Nat Rev Microbiol 15:365–379. https://doi.org/10.1038/nrmicro.2017.40
Hospenthal MK et al (2016) Structure of a chaperone-usher pilus reveals the molecular basis of rod uncoiling. Cell 164:269–278. https://doi.org/10.1016/j.cell.2015.11.049
Hospenthal MK et al (2017b) The cryoelectron microscopy structure of the type 1 chaperone-usher pilus rod. Structure 25:1829–1838. e1824. https://doi.org/10.1016/j.str.2017.10.004
Houben EN, Korotkov KV, Bitter W (2014) Take five—type VII secretion systems of mycobacteria. Biochim Biophys Acta 1843:1707–1716. https://doi.org/10.1016/j.bbamcr.2013.11.003
Hung DL, Knight SD, Woods R, Pinkner J, Hultgren S (1996) Molecular basis of two subfamilies of immunoglobulin-like chaperones. EMBO J 15:3792–3805
Hung DL, Pinkner JS, Knight SD, Hultgren SJ (1999) Structural basis of chaperone self-capping in P pilus biogenesis. Proc Natl Acad Sci U S A 96:8178–8183. https://doi.org/10.1073/pnas.96.14.8178
Jacob-Dubuisson F, Striker R, Hultgren SJ (1994) Chaperone-assisted self-assembly of pili independent of cellular energy. J Biol Chem 269:12447–12455
Jahandeh N, Ranjbar R, Behzadi P, Behzadi E (2015) Uropathogenic Escherichia coli virulence genes: invaluable approaches for designing DNA microarray probes. Cent European J Urol 68:452–458. https://doi.org/10.5173/ceju.2015.625
Jalili Z, Saleh M, Bouzari S, Pooya M (2018) Characterization of killed but metabolically active uropathogenic Escherichia coli strain as possible vaccine candidate for urinary tract infection. Microb Pathog 122:184–190. https://doi.org/10.1016/j.micpath.2018.06.027
Jędrzejczak R et al (2006) Structure of DraD invasin from uropathogenic Escherichia coli: a dimer with swapped β-tails. Acta Crystallogr D Biol Crystallogr 62:157–164. https://doi.org/10.1107/S0907444905036747
Johnson D (2018) Bacterial virulence factors. In: Johnson DI (ed) Bacterial pathogens and their virulence factors. Springer, Cham, pp 1–38. https://doi.org/10.1007/978-3-319-67651-7_1
Johnson JR (1991) Virulence factors in Escherichia coli urinary tract infection. Clin Microbiol Rev 4:80–128
Kalas V et al (2018) Structure-based discovery of glycomimetic FmlH ligands as inhibitors of bacterial adhesion during urinary tract infection. Proc Natl Acad Sci U S A 115:E2819–E2828. https://doi.org/10.1073/pnas.1720140115
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
Khandige S, Møller-Jensen J (2016) Fimbrial phase variation: stochastic or cooperative? Curr Genet 62:237–241. https://doi.org/10.1007/s00294-015-0529-3
Klemm P, Hancock V, Schembri MA (2010) Fimbrial adhesins from extraintestinal Escherichia coli. Environ Microbiol Rep 2:628–640. https://doi.org/10.1111/j.1758-2229.2010.00166.x
Knight SD, Choudhury D, Hultgren S, Pinkner J, Stojanoff V, Thompson A (2002) Structure of the S pilus periplasmic chaperone SfaE at 2.2 Å resolution. Acta Crystallogr D Biol Crystallogr 58:1016–1022
Korotkova N, Yarova-Yarovaya Y, Tchesnokova V, Yazvenko N, Carl MA, Stapleton AE, Moseley SL (2008) Escherichia coli DraE adhesin-associated bacterial internalization by epithelial cells is promoted independently by decay-accelerating factor and carcinoembryonic antigen-related cell adhesion molecule binding and does not require the DraD invasin. Infect Immun 76:3869–3880. https://doi.org/10.1128/IAI.00427-08
Kudinha T (2017) The pathogenesis of Escherichia coli urinary tract infection. In: Samie A (ed) Escherichia coli-recent advances on physiology, pathogenesis and biotechnological applications, 1st edn. IntechOpen, Croatia, pp 45–70. https://doi.org/10.5772/intechopen.69030
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
Le Trong I et al (2010) Structural basis for mechanical force regulation of the adhesin FimH via finger trap-like β sheet twisting. Cell 141:645–655. https://doi.org/10.1016/j.cell.2010.03.038
Luterbach CL, Forsyth VS, Engstrom MD, Mobley HL (2018) TosR-mediated regulation of adhesins and biofilm formation in uropathogenic Escherichia coli. mSphere 3:e00222–e00218. https://doi.org/10.1128/mSphere.00222-18
Matuszewski MA, Tupikowski K, Dołowy Ł, Szymańska B, Dembowski J, Zdrojowy R (2016) Uroplakins and their potential applications in urology. Cent European J Urol 69:252–257. https://doi.org/10.5173/ceju.2016.638
Navarro-Garcia F, Ruiz-Perez F, Larzábal M, Cataldi A (2016) Secretion systems of pathogenic Escherichia coli. In: Torres A (ed) Escherichia coli in the Americas. Springer, Cham, pp 221–249. https://doi.org/10.1007/978-3-319-45092-6_10
Nishiyama M et al (2005) Structural basis of chaperone–subunit complex recognition by the type 1 pilus assembly platform FimD. EMBO J 24:2075–2086. https://doi.org/10.1038/sj.emboj.7600693
Nowicki B, Selvarangan R, Nowicki S (2001) Family of Escherichia coli Dr adhesins: decay-accelerating factor receptor recognition and invasiveness. J Infect Dis 183:S24–S27. https://doi.org/10.1086/318846
Nuccio S-P, Bäumler AJ (2007) Evolution of the chaperone/usher assembly pathway: fimbrial classification goes Greek. Microbiol Mol Biol Rev 71:551–575. https://doi.org/10.1128/MMBR.00014-07
Omattage NS, Deng Z, Pinkner JS, Dodson KW, Almqvist F, Yuan P, Hultgren SJ (2018) Structural basis for usher activation and intramolecular subunit transfer in P pilus biogenesis in Escherichia coli. Nat Microbiol 3:1362–1368. https://doi.org/10.1038/s41564-018-0255-y
Ong C-LY et al (2008) Identification of type 3 fimbriae in uropathogenic Escherichia coli reveals a role in biofilm formation. J Bacteriol 190:1054–1063. https://doi.org/10.1128/JB.01523-07
Pakharukova N et al (2015) Structural insight into archaic and alternative chaperone-usher pathways reveals a novel mechanism of pilus biogenesis. PLoS Pathog 11:e1005269. https://doi.org/10.1371/journal.ppat.1005269
Pakharukova N et al (2018) Archaic and alternative chaperones preserve pilin folding energy by providing incomplete structural information. J Biol Chem 293:17070–17080. https://doi.org/10.1074/jbc.RA118.004170
Pakharukova N et al (2016) Structural basis for Myf and Psa fimbriae-mediated tropism of pathogenic strains of Yersinia for host tissues. Mol Microbiol 102:593–610. https://doi.org/10.1111/mmi.13481
Parkkinen J, Hacker J, Korhonen TK (1991) Enhancement of tissue plasminogen activator-catalyzed plasminogen activation by Escherichia coli S fimbriae associated with neonatal septicaemia and meningitis. Thromb Haemost 65:483–486
Phan G et al (2011) Crystal structure of the FimD usher bound to its cognate FimC–FimH substrate. Nature 474:49–53. https://doi.org/10.1038/nature10109
Piatek R et al (2013) Pilicides inhibit the FGL chaperone/usher assisted biogenesis of the Dr fimbrial polyadhesin from uropathogenic Escherichia coli. BMC Microbiol 13:131. https://doi.org/10.1186/1471-2180-13-131
Puorger C, Eidam O, Capitani G, Erilov D, Grütter MG, Glockshuber R (2008) Infinite kinetic stability against dissociation of supramolecular protein complexes through donor strand complementation. Structure 16:631–642. https://doi.org/10.1016/j.str.2008.01.013
Ranjbar R, Behzadi P, Mammina C (2016) Respiratory tularemia: Francisella tularensis and microarray probe designing. Open Microbiol J 10:176–182. https://doi.org/10.2174/1874285801610010176
Ranjbar R, Behzadi P, Najafi A, Roudi R (2017a) DNA microarray for rapid detection and identification of food and water borne Bacteria: from dry to wet lab. Open Microbiol J 11:330–338. https://doi.org/10.2174/1874285801711010330
Ranjbar R, Tabatabaee A, Behzadi P, Kheiri R (2017b) Enterobacterial repetitive intergenic consensus polymerase chain reaction (ERIC-PCR) genotyping of Escherichia coli strains isolated from different animal stool specimens. Iran J Pathol 12:25–34
Remaut H, Rose RJ, Hannan TJ, Hultgren SJ, Radford SE, Ashcroft AE, Waksman G (2006) Donor-strand exchange in chaperone-assisted pilus assembly proceeds through a concerted β strand displacement mechanism. Mol Cell 22:831–842. https://doi.org/10.1016/j.molcel.2006.05.033
Remaut H et al (2008) Fiber formation across the bacterial outer membrane by the chaperone/usher pathway. Cell 133:640–652. https://doi.org/10.1016/j.cell.2008.03.033
Ribić R, Meštrović T, Neuberg M, Kozina G (2018) Effective anti-adhesives of uropathogenic Escherichia coli. Acta Pharma 68:1–18. https://doi.org/10.2478/acph-2018-0004
Roy SP, Rahman MM, Yu XD, Tuittila M, Knight SD, Zavialov AV (2012) Crystal structure of enterotoxigenic Escherichia coli colonization factor CS 6 reveals a novel type of functional assembly. Mol Microbiol 86:1100–1115. https://doi.org/10.1111/mmi.12044
Sauer F, Fütterer K, Pinkner J, Dodson K, Hultgren S, Waksman G (1999) Structural basis of chaperone function and pilus biogenesis. Science 285:1058–1061
Sauer FG, Mulvey MA, Schilling JD, Martinez JJ, Hultgren SJ (2000) Bacterial pili: molecular mechanisms of pathogenesis. Curr Opin Microbiol 3:65–72
Sauer FG, Pinkner JS, Waksman G, Hultgren SJ (2002) Chaperone priming of pilus subunits facilitates a topological transition that drives fiber formation. Cell 111:543–551
Sauer FG, Remaut H, Hultgren SJ, Waksman G (2004) Fiber assembly by the chaperone–usher pathway. Biochim Biophys Acta 1694:259–267. https://doi.org/10.1016/j.bbamcr.2004.02.010
Servin AL (2005) Pathogenesis of Afa/Dr diffusely adhering Escherichia coli. Clin Microbiol Rev 18:264–292. https://doi.org/10.1128/CMR.18.2.264-292.2005
Soto GE, Hultgren SJ (1999) Bacterial adhesins: common themes and variations in architecture and assembly. J Bacteriol 181:1059–1071
Spurbeck RR, Mobley HLT (2013) Uropathogenic Escherichia coli. In: Donnenberg MS (ed) Escherichia coli: pathotypes and principles of pathogenesis, 2nd edn. Elsevier, Chian, pp 275–297. https://doi.org/10.1016/B978-0-12-397048-0.00009-7
Stork C et al (2018) Characterization of asymptomatic bacteriuria Escherichia coli isolates in search of alternative strains for efficient bacterial interference against uropathogens. Front Microbiol 9:214. https://doi.org/10.3389/fmicb.2018.00214
Stubenrauch CJ, Dougan G, Lithgow T, Heinz E (2017) Constraints on lateral gene transfer in promoting fimbrial usher protein diversity and function. Open Biol 7:170144. https://doi.org/10.1098/rsob.170144
Subashchandrabose S, Mobley HLT (2015) Virulence and fitness determinants of uropathogenic Escherichia coli. Microbiol Spectr 3. https://doi.org/10.1128/microbiolspec.UTI-0015-2012doi:10.1128/microbiolspec.UTI-0015-2012
Taheri M et al (2016) Antibiotic resistance pattern and phylogenetic groups of the Uropathogenic Escherichia coli isolates recovered from the urinary catheters of the hospitalized patients. JoMMID 4:76–82
Tajbakhsh E, Tajbakhsh S, Khamesipour F (2015) Isolation and molecular detection of gram negative bacteria causing urinary tract infection in patients referred to Shahrekord hospitals. Iran Iran Red Crescent Med J 17:e24779. https://doi.org/10.5812/ircmj.17(5)2015.24779
Terlizzi ME, Gribaudo G, Maffei ME (2017) UroPathogenic Escherichia coli (UPEC) infections: virulence factors, bladder responses, antibiotic, and non-antibiotic antimicrobial strategies. Front Microbiol 8:1566. https://doi.org/10.3389/fmicb.2017.01566
Tomasello G (2017-2019) 3dproteinimaging. Tomasello, Gianluca. https://3dproteinimaging.com/. Accessed 26 Jan 2019
Totsika M et al (2012) Uropathogenic Escherichia coli mediated urinary tract infection. Curr Drug Targets 13:1386–1399
Tsirigotaki A, De Geyter J, Šoštaric N, Economou A, Karamanou S (2017) Protein export through the bacterial sec pathway. Nat Rev Microbiol 15:21–36. https://doi.org/10.1038/nrmicro.2016.161
Ulett GC, Mabbett AN, Fung KC, Webb RI, Schembri MA (2007) The role of F9 fimbriae of uropathogenic Escherichia coli in biofilm formation. Microbiology 153:2321–2331. https://doi.org/10.1099/mic.0.2006/004648-0
Väisänen-Rhen V (1984) Fimbria-like hemagglutinin of Escherichia coli O75 strains. Infect Immun 46:401–407
Van Gerven N, Waksman G, Remaut H (2011) Pili and flagella: biology, structure, and biotechnological applications. Prog Mol Biol Transl Sci 103:21–72. https://doi.org/10.1016/B978-0-12-415906-8.00005-4
Waksman G (2017) Structural and molecular biology of a protein-polymerizing nanomachine for pilus biogenesis. J Mol Biol 429:2654–2666. https://doi.org/10.1016/j.jmb.2017.05.016
Waksman G, Hultgren SJ (2009) Structural biology of the chaperone–usher pathway of pilus biogenesis. Nat Rev Microbiol 7:765–774. https://doi.org/10.1038/nrmicro2220
Werneburg G, Thanassi D (2018) Pili assembled by the chaperone/usher pathway in Escherichia coli and Salmonella. EcoSal Plus 8. https://doi.org/10.1128/ecosalplus.ESP-0007-2017
Wright KJ, Hultgren SJ (2006) Sticky fibers and uropathogenesis: bacterial adhesins in the urinary tract. Future Microbiol 1:75–87. https://doi.org/10.2217/17460913.1.1.75
Wurpel D, Totsika M, Allsopp L, Webb R, Moriel D, Schembri MA (2016) Comparative proteomics of uropathogenic Escherichia coli during growth in human urine identify UCA-like (UCL) fimbriae as an adherence factor involved in biofilm formation and binding to uroepithelial cells. J Proteome 131:177–189. https://doi.org/10.1016/j.jprot.2015.11.001
Wurpel DJ, Beatson SA, Totsika M, Petty NK, Schembri MA (2013) Chaperone-usher fimbriae of Escherichia coli. PLoS One 8:e52835. https://doi.org/10.1371/journal.pone.0052835
Wurpel DJ et al (2014) F9 fimbriae of uropathogenic Escherichia coli are expressed at low temperature and recognise Galβ1-3GlcNAc-containing glycans. PLoS One 9:e93177. https://doi.org/10.1371/journal.pone.0093177
Yu X, Visweswaran GR, Duck Z, Marupakula S, MacIntyre S, Knight SD, Zavialov AV (2009) Caf1A usher possesses a Caf1 subunit-like domain that is crucial for Caf1 fibre secretion. Biochem J 418:541–551. https://doi.org/10.1042/BJ20080992
Yu XD, Dubnovitsky A, Pudney AF, MacIntyre S, Knight SD, Zavialov AV (2012a) Allosteric mechanism controls traffic in the chaperone/usher pathway. Structure 20:1861–1871. https://doi.org/10.1016/j.str.2012.08.016
Yu XD et al (2012b) Large is fast, small is tight: determinants of speed and affinity in subunit capture by a periplasmic chaperone. J Mol Biol 417:294–308. https://doi.org/10.1016/j.jmb.2012.01.020
Zalewska-Piątek B, Kur M, Wilkanowicz S, Piątek R, Kur J (2010) The DraC usher in Dr fimbriae biogenesis of uropathogenic E. coli Dr+ strains. Arch Microbiol 192:351–363. https://doi.org/10.1007/s00203-010-0564-x
Zav’yalov V, Zavialov A, Zav’yalova G, Korpela T (2010) Adhesive organelles of gram-negative pathogens assembled with the classical chaperone/usher machinery: structure and function from a clinical standpoint. FEMS Microbiol Rev 34:317–378. https://doi.org/10.1111/j.1574-6976.2009.00201.x
Zav’yalov VP, Zav’yalova GA, Denesyuk AI, Korpela T (1995) Modelling of steric structure of a periplasmic molecular chaperone Caf1M of Yersinia pestis, a prototype member of a subfamily with characteristic structural and functional features. FEMS Immunol Med Microbiol 11:19–24. https://doi.org/10.1111/j.1574-695X.1995.tb00074.x
Zavialov A, Zav’yalova G, Korpela T, Zav’yalov V (2007) FGL chaperone-assembled fimbrial polyadhesins: anti-immune armament of gram-negative bacterial pathogens. FEMS Microbiol Rev 31:478–514. https://doi.org/10.1111/j.1574-6976.2007.00075.x
Zavialov AV, Berglund J, Pudney AF, Fooks LJ, Ibrahim TM, MacIntyre S, Knight SD (2003) Structure and biogenesis of the capsular F1 antigen from Yersinia pestis: preserved folding energy drives fiber formation. Cell 113:587–596
Zavialov AV, Knight SD (2007) A novel self-capping mechanism controls aggregation of periplasmic chaperone Caf1M. Mol Microbiol 64:153–164. https://doi.org/10.1111/j.1365-2958.2007.05644.x
Zavialov AV et al (2005) Resolving the energy paradox of chaperone/usher-mediated fibre assembly. Biochem J 389:685–694. https://doi.org/10.1042/BJ20050426
Zaw MT, Lin Z (2014) Uropathogenic Escherichia coli: a pathogen producing multiple virulence factors. Borneo Journal of Medical Sciences (BJMS) 8:35–46
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author declare that they have no conflicts of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Behzadi, P. Classical chaperone-usher (CU) adhesive fimbriome: uropathogenic Escherichia coli (UPEC) and urinary tract infections (UTIs). Folia Microbiol 65, 45–65 (2020). https://doi.org/10.1007/s12223-019-00719-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12223-019-00719-x