Chaperone–usher pathways: diversity and pilus assembly mechanism

Büsch, Andreas; Waksman, Gabriel

doi:10.1098/rstb.2011.0206

Cited by 121 publications

(112 citation statements)

References 62 publications

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“…The components of T9SSs are not closely related to those of the well-studied type I to type VI secretion systems of Gram-negative bacteria (5,9,10). They are also unrelated to the components of the chaperone-usher pathway that has recently been called the type VII secretion system (11)(12)(13), to the components of the extracellular nucleation-precipitation pathway involved in secretion and assembly of curli amyloid fibers, which has been referred to as the type VIII secretion system (13,14), and to the mycobacterial ESX (ESAT-6) system (12,15). The T9SS is required for secretion of the cell surface motility proteins SprB and RemA and is thus needed for motility.…”

mentioning

confidence: 99%

Flavobacterium johnsoniae Chitinase ChiA Is Required for Chitin Utilization and Is Secreted by the Type IX Secretion System

Kharade

McBride

2013

Journal of Bacteriology

110

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Flavobacterium johnsoniae, a member of phylum Bacteriodetes, is a gliding bacterium that digests insoluble chitin and many other polysaccharides. A novel protein secretion system, the type IX secretion system (T9SS), is required for gliding motility and for chitin utilization. Five potential chitinases were identified by genome analysis. Fjoh_4555 (ChiA), a 168.9-kDa protein with two glycoside hydrolase family 18 (GH18) domains, was targeted for analysis. Disruption of chiA by insertional mutagenesis resulted in cells that failed to digest chitin, and complementation with wild-type chiA on a plasmid restored chitin utilization. Antiserum raised against recombinant ChiA was used to detect the protein and to characterize its secretion by F. johnsoniae. ChiA was secreted in soluble form by wild-type cells but remained cell associated in strains carrying mutations in any of the T9SS genes, gldK, gldL, gldM, gldNO, sprA, sprE, and sprT. Western blot and liquid chromatography-tandem mass spectrometry (LC-MS/MS) analyses suggested that ChiA was proteolytically processed into two GH18 domain-containing proteins. Proteins secreted by T9SSs typically have conserved carboxy-terminal domains (CTDs) belonging to the TIGRFAM families TIGR04131 and TIGR04183. ChiA does not exhibit strong similarity to these sequences and instead has a novel CTD. Deletion of this CTD resulted in accumulation of ChiA inside cells. Fusion of the ChiA CTD to recombinant mCherry resulted in secretion of mCherry into the medium. The results indicate that ChiA is a soluble extracellular chitinase required for chitin utilization and that it relies on a novel CTD for secretion by the F. johnsoniae T9SS.

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mentioning

confidence: 99%

Flavobacterium johnsoniae Chitinase ChiA Is Required for Chitin Utilization and Is Secreted by the Type IX Secretion System

Kharade

McBride

2013

Journal of Bacteriology

110

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“…Fimbrial adhesins assembled via the chaperone-usher pathway are the most extensively studied adherence factors (13,14). Indeed, the genes necessary to synthesize two chaperone-usher fimbriae, type 1 and P fimbriae (pyelonephritis-associated pili), were among the first cloned virulence factor genes (15,16) and are important during experimental and human UTIs, respectively (17)(18)(19)(20)(21)(22)(23).…”

mentioning

confidence: 99%

A Conserved PapB Family Member, TosR, Regulates Expression of the Uropathogenic Escherichia coli RTX Nonfimbrial Adhesin TosA while Conserved LuxR Family Members TosE and TosF Suppress Motility

2014

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A heterogeneous subset of extraintestinal pathogenic Escherichia coli (ExPEC) strains, referred to as uropathogenic E. coli (UPEC), causes most uncomplicated urinary tract infections. However, no core set of virulence factors exists among UPEC strains. Instead, the focus of the analysis of urovirulence has shifted to studying broad classes of virulence factors and the interactions between them. For example, the RTX nonfimbrial adhesin TosA mediates adherence to host cells derived from the upper urinary tract. The associated tos operon is well expressed in vivo but poorly expressed in vitro and encodes TosCBD, a predicted type 1 secretion system. TosR and TosEF are PapB and LuxR family transcription factors, respectively; however, no role has been assigned to these potential regulators. Thus, the focus of this study was to determine how TosR and TosEF regulate tosA and affect the reciprocal expression of adhesins and flagella. Among a collection of sequenced UPEC strains, 32% (101/317) were found to encode TosA, and nearly all strains (91% [92/101]) simultaneously carried the putative regulatory genes. Deletion of tosR alleviates tosA repression. The tos promoter was localized upstream of tosR using transcriptional fusions of putative promoter regions with lacZ. TosR binds to this region, affecting a gel shift. A 100-bp fragment 220 to 319 bp upstream of tosR inhibits binding, suggesting localization of the TosR binding site. TosEF, on the other hand, downmodulate motility when overexpressed by preventing the expression of fliC, encoding flagellin. Deletion of tosEF increased motility. Thus, we present an additional example of the reciprocal control of adherence and motility. U rinary tract infections (UTIs) are the second most common bacterial infection in humans (1). UTIs can be classified as complicated or uncomplicated infections. Uncomplicated UTIs, occurring in otherwise healthy individuals, are self-limited infections of the bladder, referred to as cystitis (2-4). However, upon bacterial ascension into the kidney, a more serious infection referred to as pyelonephritis can develop (2, 4). Pyelonephritis, in turn, can lead to the development of bacteremia and sometimes fatal urosepsis (5, 6).UTIs normally occur when uropathogens that colonize the intestine alongside commensal organisms gain access to the periurethral area and then ascend to the urinary bladder (7,8). A heterogeneous subset of extraintestinal pathogenic Escherichia coli (ExPEC) strains, referred to as uropathogenic E. coli (UPEC), causes the overwhelming majority of uncomplicated UTIs (4). UPEC strains carry a battery of virulence factors, including adhesins, toxins, and iron acquisition systems, which promote uropathogenesis (9, 10). However, no core set of virulence factors has been identified. Instead, any given UPEC strain appears to use various virulence factors from these three classes of virulence determinants to colonize the urinary tract (11,12). This thesis requires that we consider established, newly discovered, and putative virule...

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“…Multiple fimbriae of the chaperone/usher assembly pathway are encoded in the genomes of a wide variety of pathogenic and nonpathogenic Gram-negative bacteria (32). In recent years, extensive knowledge about fimbrial structure and assembly has been generated, including classification schemes and phylogenetic analyses that have increased our understanding of their diversity and evolution (22,32,33).…”

Section: Discussionmentioning

confidence: 99%

“…In recent years, extensive knowledge about fimbrial structure and assembly has been generated, including classification schemes and phylogenetic analyses that have increased our understanding of their diversity and evolution (22,32,33). Despite our current knowledge, the biological relevance of having a wide repertoire of chaperone/usher operons (e.g., whether they play a differential, synergistic, or redundant role during the colonization process of host or reservoir niches) (2), and gcf3-cat (3) transcriptional fusions were assayed in WT (B) or ⌬hns1::Km mutant (C) C. rodentium, as described for Fig.…”

Section: Discussionmentioning

confidence: 99%

Identification and Regulation of a Novel Citrobacter rodentium Gut Colonization Fimbria (Gcf)

et al. 2015

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The Gram-negative enteric bacterium Citrobacter rodentium is a natural mouse pathogen that has been extensively used as a surrogate model for studying the human pathogens enteropathogenic and enterohemorrhagic Escherichia coli. All three pathogens produce similar attaching and effacing (A/E) lesions in the intestinal epithelium. During infection, these bacteria employ surface structures called fimbriae to adhere and colonize the host intestinal epithelium. For C. rodentium, the roles of only a small number of its genome-carried fimbrial operons have been evaluated. Here, we report the identification of a novel C. rodentium colonization factor, called gut colonization fimbria (Gcf), which is encoded by a chaperone-usher fimbrial operon. A gcfA mutant shows a severe colonization defect within the first 10 days of infection. The gcf promoter is not active in C. rodentium under several in vitro growth conditions; however, it is readily expressed in a C. rodentium ⌬hns1 mutant lacking the closest ortholog of the Escherichia coli histone-like nucleoid structuring protein (H-NS) but not in mutants with deletion of the other four genes encoding H-NS homologs. H-NS binds to the regulatory region of gcf, further supporting its direct role as a repressor of the gcf promoter that starts transcription 158 bp upstream of the start codon of its first open reading frame. The gcf operon possesses interesting novel traits that open future opportunities to expand our knowledge of the structure, regulation, and function during infection of these important bacterial structures. IMPORTANCEFimbriae are surface bacterial structures implicated in a variety of biological processes. Some have been shown to play a critical role during host colonization and thus in disease. Pathogenic bacteria possess the genetic information for an assortment of fimbriae, but their function and regulation and the interplay between them have not been studied in detail. This work provides new insights into the function and regulation of a novel fimbria called Gcf that is important for early establishment of a successful infection by C. rodentium in mice, despite being poorly expressed under in vitro growth conditions. This discovery offers an opportunity to better understand the individual role and the regulatory mechanisms controlling the expression of specific fimbrial operons that are critical during infection. The natural mouse pathogen Citrobacter rodentium and the human pathogens enterohemorrhagic Escherichia coli (EHEC) and enteropathogenic E. coli (EPEC) represent a family of enteric pathogenic bacteria that adhere to the host intestinal epithelial cells and inject effector proteins through a specialized type III secretion system (T3SS), subverting or hijacking several cell functions and leading to the formation of a distinctive histopathology known as the attaching and effacing (A/E) lesion (1, 2). These three pathogens produce similar lesions in the intestinal epithelium of their respective hosts, which are characterized by the intimate atta...

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Chaperone–usher pathways: diversity and pilus assembly mechanism

Cited by 121 publications

References 62 publications

Flavobacterium johnsoniae Chitinase ChiA Is Required for Chitin Utilization and Is Secreted by the Type IX Secretion System

Flavobacterium johnsoniae Chitinase ChiA Is Required for Chitin Utilization and Is Secreted by the Type IX Secretion System

A Conserved PapB Family Member, TosR, Regulates Expression of the Uropathogenic Escherichia coli RTX Nonfimbrial Adhesin TosA while Conserved LuxR Family Members TosE and TosF Suppress Motility

Identification and Regulation of a Novel Citrobacter rodentium Gut Colonization Fimbria (Gcf)

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