An extended hydrophobic interactive surface of <i>Yersinia pestis</i> Caf1M chaperone is essential for subunit binding and F1 capsule assembly

MacIntyre, Sheila; Zyrianova, Irina M.; Chernovskaya, T.V.; Leonard, Mary E.; Rudenko, E.; Zav’yalov, V.P.; Chapman, Dave

doi:10.1046/j.1365-2958.2001.02199.x

Cited by 38 publications

(69 citation statements)

References 38 publications

(95 reference statements)

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“…Thus, the capsule represents a high-molecular-weight polymer consisting of linear fibers of a single protein subunit, Caf1, assembled on the surface of the bacterial cell (54). The assembly of such fibrillar organelles is accomplished by a highly conserved periplasmic chaperone/usher pathway in which caf1-encoded F1 fimbrial subunits are translocated from bacterial cytoplasm to periplasm, where they interact with Caf1M chaperone and dimerize prior to export onto the bacterial surface by the outer-membrane usher protein Caf1A (28,55). The further addition of Caf1 dimers results in capsule formation, and caf1 is one of the most highly expressed genes during infection in mammals (38).…”

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confidence: 99%

Characterization of an F1 Deletion Mutant of Yersinia pestis CO92, Pathogenic Role of F1 Antigen in Bubonic and Pneumonic Plague, and Evaluation of Sensitivity and Specificity of F1 Antigen Capture-Based Dipsticks

et al. 2011

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We evaluated two commercial F1 antigen capture-based immunochromatographic dipsticks, Yersinia Pestis (F1) Smart II and Plague BioThreat Alert test strips, in detecting plague bacilli by using whole-blood samples from mice experimentally infected with Yersinia pestis CO92. To assess the specificities of these dipsticks, an in-frame F1-deficient mutant of CO92 (⌬caf) was generated by homologous recombination and used as a negative control. Based on genetic, antigenic/immunologic, and electron microscopic analyses, the ⌬caf mutant was devoid of a capsule. The growth rate of the ⌬caf mutant generally was similar to that of the wild-type (WT) bacterium at both 26 and 37°C, although the mutant's growth dropped slightly during the late phase at 37°C. The ⌬caf mutant was as virulent as WT CO92 in the pneumonic plague mouse model; however, it was attenuated in developing bubonic plague. Both dipsticks had similar sensitivities, requiring a minimum of 0.5 g/ml of purified F1 antigen or 1 ؋ 10 5 to 5 ؋ 10 5 CFU/ml of WT CO92 for positive results, while the blood samples were negative for up to 1 ؋ 10 8 CFU/ml of the ⌬caf mutant. Our studies demonstrated the diagnostic potential of two plague dipsticks in detecting capsular-positive strains of Y. pestis in bubonic and pneumonic plague.

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Characterization of an F1 Deletion Mutant of Yersinia pestis CO92, Pathogenic Role of F1 Antigen in Bubonic and Pneumonic Plague, and Evaluation of Sensitivity and Specificity of F1 Antigen Capture-Based Dipsticks

et al. 2011

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“…The caf operon products constitute a fimbrial chaperone-usher system that acts to assemble and export F1 subunits on the bacterial surface. The caf1-encoded F1 fimbrial subunits are translocated from the cytoplasm into the periplasm, where they interact with the Caf1M chaperone and dimerize prior to exportation to the surface of the bacteria by the outer-membrane usher protein Caf1A (46,72). Further addition of Caf1 dimers results in capsule formation.…”

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TheYersinia pestis caf1M1A1Fimbrial Capsule Operon Promotes Transmission by Flea Bite in a Mouse Model of Bubonic Plague

Sebbane

Jarrett²,

Gardner

et al. 2009

Infect Immun

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Plague is a zoonosis transmitted by fleas and caused by the gram-negative bacterium Yersinia pestis. During infection, the plasmidic caf1M1A1 operon that encodes the Y. pestis F1 protein capsule is highly expressed, and anti-F1 antibodies are protective. Surprisingly, the capsule is not required for virulence after injection of cultured bacteria, even though it is an antiphagocytic factor and capsule-deficient Y. pestis strains are rarely isolated. We found that a caf-negative Y. pestis mutant was not impaired in either flea colonization or virulence in mice after intradermal inoculation of cultured bacteria. In contrast, absence of the caf operon decreased bubonic plague incidence after a flea bite. Successful development of plague in mice infected by flea bite with the caf-negative mutant required a higher number of infective bites per challenge. In addition, the mutant displayed a highly autoaggregative phenotype in infected liver and spleen. The results suggest that acquisition of the caf locus via horizontal transfer by an ancestral Y. pestis strain increased transmissibility and the potential for epidemic spread. In addition, our data support a model in which atypical caf-negative strains could emerge during climatic conditions that favor a high flea burden. Human infection with such strains would not be diagnosed by the standard clinical tests that detect F1 antibody or antigen, suggesting that more comprehensive surveillance for atypical Y. pestis strains in plague foci may be necessary. The results also highlight the importance of studying Y. pestis pathogenesis in the natural context of arthropod-borne transmission.

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“…In this respect, McuB is similar to Caf1M-like FGL chaperones. For Y. pestis Caf1M, the G1 donor strand contributes a run of five rather than three alternating hydrophobic residues (as with the PapDlike FGS chaperones) to complex with the Caf1 subunit (6,13,30).…”

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confidence: 99%

Characterization of McuB, a Periplasmic Chaperone-Like Protein Involved in the Assembly of Myxococcus Spore Coat

Zhu

Cao

et al. 2013

J Bacteriol

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The MXAN3885 to -3882 gene locus cluster (designated here mcuABCD) of Myxococcus xanthus encodes a member of the archaic chaperone-usher (CU) systems that functions in spore coat formation. We show here that McuD, a putative spore coat protein, affects cellular accumulation and cell surface localization of the spore coat protein McuA. We previously reported that genetic disruption of the putative usher McuC nearly eliminates surface display of McuA and show here that lack of the periplasmic chaperone-like protein McuB, which forms a complex with McuA, has a similar effect. Deletion mutation confirms that the G1 ␤ strand of McuB is absolutely essential for the stability and secretion of McuA. Site-directed mutagenesis identified two additional alternating hydrophobic residues Ile113 and Val115, together with the highly conserved proline within the G1 strand, as critical residues for chaperone function. These findings suggest that the assembly proteins McuB and McuC mediate the transport of McuA onto the cell surface and that McuA may interact with another spore coat protein, McuD, for its secretion. Importantly, although our data argue that the M. xanthus CU system is likely to use the basic principle of donor strand complementation (DSC), as in the cases of classical CU pathways, to promote folding and stabilization of the structural subunit(s), the periplasmic chaperone McuB appears to exhibit structural variation in mediating chaperone-subunit interaction. Many Gram-negative bacteria display nonflagellar proteinaceous organelles on their outer surfaces. These adhesive extracellular structures, called pili or fimbriae, mediate bacterial attachment to host cells and play a key role in the pathogenicity of a wide range of infectious diseases. It has now become clear that pili can be classified into five major groups based on their biosynthetic pathways and that the chaperone-usher (CU) pili form the most abundant group of bacterial cell surface appendages (1). The CU biosynthetic pathway involves two nonstructural assembly components: a specialized periplasmic chaperone and an outer membrane protein called the usher. The chaperone binds and facilitates folding of pilus structural subunits, prevents them from aggregation or degradation in the periplasm, and targets them to the usher. Interactions between the chaperone-subunit complex and the usher release pilus subunits, which are subsequently exported through the usher channel for assembly into pilus fibers and secretion into the cell surface (2,3,4). Based on phylogenetic analysis of usher sequences, CU pili are divided into six major clades designated ␣, ␤, ␥, , , and (5). The analysis also reveals that the -fimbriae comprise an archaic CU family whose members share limited or no sequence homology with members of the alternate (␣-fimbriae) or the classical (␤-, ␥-, -, and -fimbriae) CU families. Within the CU assembly class, the archaic CU system is the most widely distributed, with representatives being present not only in Alpha-, Beta-, Gamma-, and Deltaprote...

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An extended hydrophobic interactive surface of Yersinia pestis Caf1M chaperone is essential for subunit binding and F1 capsule assembly

Cited by 38 publications

References 38 publications

Characterization of an F1 Deletion Mutant of Yersinia pestis CO92, Pathogenic Role of F1 Antigen in Bubonic and Pneumonic Plague, and Evaluation of Sensitivity and Specificity of F1 Antigen Capture-Based Dipsticks

Characterization of an F1 Deletion Mutant of Yersinia pestis CO92, Pathogenic Role of F1 Antigen in Bubonic and Pneumonic Plague, and Evaluation of Sensitivity and Specificity of F1 Antigen Capture-Based Dipsticks

TheYersinia pestis caf1M1A1Fimbrial Capsule Operon Promotes Transmission by Flea Bite in a Mouse Model of Bubonic Plague

Characterization of McuB, a Periplasmic Chaperone-Like Protein Involved in the Assembly of Myxococcus Spore Coat

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