Segmented Filamentous Bacteria Interact with Intraepithelial Mononuclear Cells

Meyerholz, David K.; Stabel, Thomas J.; Cheville, N. F.

doi:10.1128/iai.70.6.3277-3280.2002

Cited by 34 publications

(28 citation statements)

References 30 publications

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“…Molecular analyses revealed a diverse bacterial composition in the small intestinal contents (data not shown), yet the repertoire of bacteria adherent to the gut epithelium was rather limited and dominated by uncultured anaerobes. Among these, SFB seem to be a major population that activates the immune system because (i) SFB strongly attach to the gut epithelium (19,20) and are the main (if not the only) bacterial species that could be detected in IEC suspension (data not shown).…”

Section: Discussionmentioning

confidence: 99%

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Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut

Suzuki

Meek

Doi

et al. 2004

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

621

457

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The mechanism to maintain homeostasis of the gut microbiota remains largely unknown despite its critical role in the body defense. In the intestines of mice with deficiency of activationinduced cytidine deaminase (AID), the absence of hypermutated IgA is partially compensated for by the presence of large amounts of unmutated IgM and normal expression levels of defensins and angiogenins. We show here a predominant and persistent expansion of segmented filamentous bacteria throughout the small intestine of AID ؊/؊ mice. Reconstitution of lamina propria IgA production in AID ؊/؊ mice recovered the normal composition of gut flora and abolished the local and systemic activation of the immune system. The results indicate that secretions of IgAs rather than innate defense peptides are critical to regulation of commensal bacterial flora and that the segmented filamentous bacteria antigens are strong stimuli of the mucosal immune system. M ucosal epithelial surfaces represent points of continuous and intimate interactions between the immune system and the outside environment. Under a constant antigenic pressure from Ͼ400 species of commensal bacteria, the gut immune system has developed highly sophisticated and efficient defensive as well as symbiotic mechanisms (1, 2). Secretion of antibiotic peptides by epithelial cells represents an important component of the innate immune system in the gut. Bacteria or bacterial antigens are capable of stimulating secretion of large amounts of antimicrobial peptides by crypt Paneth cells (3, 4). Also, transgenic (Tg) mice expressing a human intestinal defensin are protected against enteric salmonellosis (5), whereas mice deficient in the metalloproteinase matrilysin MMP-7 and thus lacking mature cryptdins show decreased resistance to some intestinal infections (6). Therefore, antimicrobial peptides appear to be involved in the maintenance of the symbiotic environment in the gut and protection of crypt stem cells from infections.Another front line body defense mechanism that provides protection against microbial agents at mucosal surfaces is production and secretion of IgA (7). Indeed, IgA is the most abundant Ig isotype in mucosal secretions, and at least 80% of all plasma cells in mice are located in the intestinal lamina propria (LP) (8). The gut IgA responses are initiated primarily in organized lymphoid structures present in the intestine, namely Peyer's patches (PP) (9) and the isolated lymphoid follicles (ILFs), which have architecture similar to PP (10, 11). These structures contain a large number of conventional B2 cells, which are derived from precursor cells generated in the bone marrow (BM) (9, 10). In addition, peritoneal cavity B1 cells contribute to intestinal IgA plasma cells. B1 cells are shown to generate large amounts of IgAs independent of T cells and germinal centers (GC) (12, 13). Both B1 and conventional B2 cells are most likely to switch in situ from IgM to IgA in the LP with the help of dendritic cells and factors secreted by stromal cells (14). However, it is...

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Section: Discussionmentioning

confidence: 99%

“…Once attached, SFB may trigger a series of events that begin with uptake and antigen presentation to intraepithelial immune cells (19), activation of local B and T cells (21)(22)(23), production of cytokines and chemokines responsible for accumulation of B cells, hyperplasia of ILF, and GC induction.…”

Section: Discussionmentioning

confidence: 99%

Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut

Suzuki

Meek

Doi

et al. 2004

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

621

457

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“…Morphologically comparable cell types have been described as segmented filamentous bacteria (SFB) (Davis & Savage, 1974). SFB live in the small intestine of arthropods, fish, birds and many mammalian species including humans, where they are anchored to the epithelial surface (Tannock et al, 1984;Smith, 1997;Meyerholz et al, 2002). They are considered to be noncultivable, species-specific, non-pathogenic, and potent activators of the mucosal immune system.…”

Section: Discussionmentioning

confidence: 99%

Uncultivated Tannerella BU045 and BU063 are slim segmented filamentous rods of high prevalence but low abundance in inflammatory disease-associated dental plaques

2007

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Uncultivated clones BU045 and BU063 and Tannerella forsythia, a 'consensus periodontal pathogen', are the closest known relatives within the genus Tannerella. They have been described to inhabit different ecological niches of the human oral cavity. In this study, fluorescent in situ hybridization (FISH) and immunofluorescence were combined to investigate the prevalence and abundance of BU045 and BU063 in comparison to T. forsythia in plaques from gingivitis, necrotizing ulcerative gingivitis (NUG) and chronic periodontitis. Phylotype-specific FISH probes identified BU045 and BU063 as elongated thin rods with a segmented structure. Two structurally similar and previously unknown, rare phylotypes (127 + and 997 + ) were also identified due to partial 16S rRNA sequence identity with T. forsythia. In gingivitis, NUG and periodontitis patients, BU045, BU063, 127 + , 997 + and T. forsythia were detected with prevalences of 50/83/71/14 and 81 %, 100/100/86/17 and 53 %, and 100/100/12/0 and 100 %, respectively. Supragingivally, colonization density of all five organisms was generally low, rarely exceeding 0.1 % of the total biota. In periodontal pocket samples, however, cell numbers of T. forsythia, but not of the uncultivable phylotypes, were greatly elevated. Our data demonstrate that Tannerella phylotypes BU045, BU063, 127 + and 997 + consist of long slim rods with segments, which, with respect to FISH stainability, often behaved as independent units. The phylotypes are frequent but low-level colonizers of various periodontal disease-associated plaques. Their apparent inability to proliferate to high density seems to exclude any relevance for the pathogenesis of periodontal diseases. INTRODUCTIONRelying on comprehensive culture analyses, Moore & Moore (1994) estimated that, on a population basis, the human oral cavity might harbour some 500 bacterial species. With the emergence of culture-independent methods for the identification of microbial biota (see Amann et al., 1995 for a review) it became clear that probably less than 50 % of the oral taxa have been cultured so far (Wilson et al., 1997). During the last decade hundreds of previously unknown phylotypes and clones have been identified in studies investigating 16S rRNA diversity in different forms of dental plaque (Paster et al., 2001(Paster et al., , 2002Munson et al., 2004;Aas et al., 2005;Kumar et al., 2005;de Lillo et al., 2006). Among the many uncultivable human oral phylotypes two clones with an apparently supragingival habitat, BU045 and BU063, attracted some interest, because their 16S rRNA gene sequence groups them within the genus Tannerella (Paster et al., 2001;Leys et al., 2002;de Lillo et al., 2004), which otherwise contains, besides some uncultivated clones from soil, only a single species, Tannerella forsythia (also known as Tannerella forsythensis) (Tanner et al., 1986;Tanner & Izard, 2006). T. forsythia is a 'consensus periodontal pathogen ' (Haffajee & Socransky, 2006) and associated with subgingival plaque from chronic and occasionally aggress...

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“…Specific sugar expression on the surface of the most luminal portions of mucosa throughout the rat alimentary tract in long, coccal-or rod-shaped chains between the intestinal villi of the lower part of small intestine, but never in the upper alimentary tract of rats [35]. Segmented filamentous bacteria (SFB), provisionally named Candidatus arthromitus [41], are apathogenic indigenous bacteria that colonize the lower alimentary canals, but never the upper alimentary tract of a wide range of animal species, including rats [25,27]. On the other hand, various bacterial species can bind to specific sugars on the host mucosal surface using bacterial surface lectins.…”

Section: Discussionmentioning

confidence: 99%

Lectin Histochemical Detection of Special Sugars on the Mucosal Surfaces of the Rat Alimentary Tract

Yamamoto

Yokoo

et al. 2010

The Journal of Veterinary Medical Science

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ABSTRACT. Surfaces of the most luminal positions of mucosae are fundamental settlement sites of indigenous bacteria throughout the rat alimentary tract. In these positions, also epithelial cell-shedding sites, the special sugar expression in the glycocalyx is very important as it provides possible ligands of bacterial lectins for attachment to epithelial cells. Therefore, the sugar expression in glycocalyx of epithelial cells was lectin-histochemically surveyed using 21 lectins throughout the rat alimentary tract. From the tongue to the nonglandular part of the stomach, -D-Man, -D-Glc and -D-GalNAc were detected on the surface of the keratinized stratified squamous epithelium. In the glandular part of the stomach,(1-4)GlcNAc and bisected triantennary N-glycans were detected on the surface of gastric superficial epithelial cells. From the duodenum to the ileum, (GlcNAc) 2-4 was expressed exclusively on the epithelial cells in the apical portions of the intestinal villi. From the cecum to the rectum,GalNAc) n and NeuNAc were expressed on the intestinal superficial epithelial cells. These results suggest that special sugars are expressed on the most luminal portions of mucosae as exclusive epithelial cell-shedding sites, and that sugar expression differs among the various segments of the alimentary tract. These site differences might reflect differences in resident bacterial species in the rat alimentary tract.KEY WORDS: alimentary tract, indigenous bacteria, lectin histochemistry, rat, sugar expression.

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Segmented Filamentous Bacteria Interact with Intraepithelial Mononuclear Cells

Cited by 34 publications

References 30 publications

Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut

Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut

Uncultivated Tannerella BU045 and BU063 are slim segmented filamentous rods of high prevalence but low abundance in inflammatory disease-associated dental plaques

Lectin Histochemical Detection of Special Sugars on the Mucosal Surfaces of the Rat Alimentary Tract

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