Motility and Chemotaxis in Tissue Penetration of Oral Epithelial Cell Layers by<i>Treponema denticola</i>

Lux, Renate; Miller, James N.; Park, No-Hee; Shi, Wenyuan

doi:10.1128/iai.69.10.6276-6283.2001

Cited by 120 publications

(126 citation statements)

References 61 publications

(42 reference statements)

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“…Spirochetes have outer and inner membranes, defining a peptidoglycan-containing periplasmic space that contains a species-characteristic number of flagellar filaments (Hovind-Hougen, 1976). All spirochetes have the ability to penetrate into dense media and some species can penetrate into tissues (Lux et al, 2001), a capability associated with the periplasmic location of the flagellar filaments (Limberger, 2004). The organization of the periplasm, particularly in relationship to the arrangement of the flagellar filaments in the presence of the peptidoglycan layer, is poorly understood.…”

Section: Introductionmentioning

confidence: 99%

Native cellular architecture of Treponema denticola revealed by cryo-electron tomography

Izard¹,

Hsieh²,

Limberger³

et al. 2008

Journal of Structural Biology

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Using cryo-electron tomography, we are developing a refined description of native cellular structures in the pathogenic spirochete Treponema denticola. Tightly organized bundles of periplasmic flagella were readily observed in intact plunge-frozen cells. The periplasmic space was measured in both wild-type and aflagellate strains, and found to widen by less than the diameter of flagella when the latter are present. This suggests that a structural change occurs in the peptidoglycan layer to accommodate the presence of the flagella. In dividing cells, the flagellar filaments were found to bridge the cytoplasmic cylinder constriction site. Cytoplasmic filaments, adjacent to the inner membrane, run parallel to the tightly organized flagellar filaments. The cytoplasmic filaments may be anchored by a narrow plate-like structure. The tapering of the cell ends was conserved between cells, with a patella-shaped structure observed in the periplasm at the tip of each cytoplasmic cylinder. Several incompletely characterized structures have been observed in the periplasm between dividing cells, including a cable-like structure linking two cytoplasmic cylinders and complex foil-shaped structures.

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Section: Introductionmentioning

confidence: 99%

Native cellular architecture of Treponema denticola revealed by cryo-electron tomography

Izard¹,

Hsieh²,

Limberger³

et al. 2008

Journal of Structural Biology

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“…This unique swimming ability enables these bacteria to penetrate into specific host connective tissues and ecological niches (43). The importance of motility as a virulence factor has been implicated in several spirochete species, including Treponema denticola (42), Brachyspira hyodysenteriae (54), Borrelia garinii (60), and B. burgdorferi (10,56).…”

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confidence: 99%

Borrelia burgdorferi Uniquely Regulates Its Motility Genes and Has an Intricate Flagellar Hook-Basal Body Structure

et al. 2008

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Borrelia burgdorferi is a flat-wave, motile spirochete that causes Lyme disease. Motility is provided by periplasmic flagella (PFs) located between the cell cylinder and an outer membrane sheath. The structure of these PFs, which are composed of a basal body, a hook, and a filament, is similar to the structure of flagella of other bacteria. To determine if hook formation influences flagellin gene transcription in B. burgdorferi, we inactivated the hook structural gene flgE by targeted mutagenesis. In many bacteria, completion of the hook structure serves as a checkpoint for transcriptional control of flagellum synthesis and other chemotaxis and motility genes. Specifically, the hook allows secretion of the anti-sigma factor FlgM and concomitant late gene transcription promoted by 28 . However, the control of B. burgdorferi PF synthesis differs from the control of flagellum synthesis in other bacteria; the gene encoding 28 is not present in the genome of B. burgdorferi, nor are any 28 promoter recognition sequences associated with the motility genes. We found that B. burgdorferi flgE mutants lacked PFs, were rod shaped, and were nonmotile, which substantiates previous evidence that PFs are involved in both cell morphology and motility. Although most motility and chemotaxis gene products accumulated at wild-type levels in the absence of FlgE, mutant cells had markedly decreased levels of the flagellar filament proteins FlaA and FlaB. Further analyses showed that the reduction in the levels of flagellin proteins in the spirochetes lacking FlgE was mediated at the posttranscriptional level. Taken together, our results indicate that in B. burgdorferi, the completion of the hook does not serve as a checkpoint for transcriptional regulation of flagellum synthesis. In addition, we also present evidence that the hook protein in B. burgdorferi forms a high-molecular-weight complex and that formation of this complex occurs in the periplasmic space.Borrelia burgdorferi, the causative agent of Lyme disease, is a spirochete with a characteristic flat-wave morphology (24, 25; for a review, see reference 12). As a result of their unusual morphology, B. burgdorferi and other spirochete species have a highly specialized ability that allows them to traverse viscous gellike media (8). This unique swimming ability enables these bacteria to penetrate into specific host connective tissues and ecological niches (43). The importance of motility as a virulence factor has been implicated in several spirochete species, including Treponema denticola (42), Brachyspira hyodysenteriae (54), Borrelia garinii (60), and B. burgdorferi (10, 56).Motility in B. burgdorferi is provided by bundles of between 7 and 11 periplasmic flagella (PFs) that are subterminally attached near the cell ends. These PFs extend inward along the cell cylinder beneath an outer membrane sheath (6,24,28,46). B. burgdorferi PFs have a structure similar to that of flagella of other bacteria; a PF is composed of a basal body, a hook, and a filament containing a single major ...

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“…Several compounds and media components have been shown to serve as attractants and repellents for S. aurantia (20) and to a lesser degree for Treponema denticola (21,22) and B. burgdorferi (23). Disruption of the cheA and chemoreceptor genes dmcA and dmcB in T. denticola results in cells that fail to penetrate monolayers of eukaryotic cells (18,24). Genomic analysis of B. burgdorferi, T. denticola, and Treponema pallidum indicate that these spirochetes contain flagellar and chemotaxis gene homologs common to other bacteria (refs.…”

mentioning

confidence: 99%

Asymmetrical flagellar rotation in Borrelia burgdorferi nonchemotactic mutants

Bakker

Motaleb

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

219

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The Lyme disease spirochete Borrelia burgdorferi has bundles of periplasmic flagella subpolarly located at each cell end. These bundles rotate in opposite directions during translational motility. When not translating, they rotate in the same direction, and the cells flex. Here, we present evidence that asymmetrical rotation of the bundles during translation does not depend upon the chemotaxis signal transduction system. The histidine kinase CheA is known to be an essential component in the signaling pathway for bacterial chemotaxis. Mutants of cheA in flagellated bacteria continually rotate their flagella in one direction. B. burgdorferi has two copies of cheA designated cheA1 and cheA2. Both genes were found to be expressed in growing cells. We reasoned that if chemotaxis were essential for asymmetrical rotation of the flagellar bundles, and if the flagellar motors at both cell ends were identical, inactivation of the two cheA genes should result in cells that constantly flex. To test this hypothesis, the signaling pathway was completely blocked by constructing the double mutant cheA1::kan cheA2::ermC. This double mutant was deficient in chemotaxis. Rather than flexing, it failed to reverse, and it continually translated only in one direction. Video microscopy of mutant cells indicated that both bundles actively rotated. The results indicate that asymmetrical rotation of the flagellar bundles of spirochetes does not depend upon the chemotaxis system but rather upon differences between the two flagellar bundles. We propose that certain factors within the spirochete localize at the flagellar motors at one end of the cell to effect this asymmetry.spirochete ͉ periplasmic flagella ͉ Lyme disease ͉ chemotaxis ͉ motility

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Motility and Chemotaxis in Tissue Penetration of Oral Epithelial Cell Layers byTreponema denticola

Cited by 120 publications

References 61 publications

Native cellular architecture of Treponema denticola revealed by cryo-electron tomography

Native cellular architecture of Treponema denticola revealed by cryo-electron tomography

Borrelia burgdorferi Uniquely Regulates Its Motility Genes and Has an Intricate Flagellar Hook-Basal Body Structure

Asymmetrical flagellar rotation in Borrelia burgdorferi nonchemotactic mutants

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