Lipoteichoic Acids from<i>Lactobacillus johnsonii</i>Strain La1 and<i>Lactobacillus acidophilus</i>Strain La10 Antagonize the Responsiveness of Human Intestinal Epithelial HT29 Cells to Lipopolysaccharide and Gram-Negative Bacteria

Vidal, Karine; Donnet-Hughes, Anne; Granato, Dominique

doi:10.1128/iai.70.4.2057-2064.2002

Cited by 104 publications

(73 citation statements)

References 51 publications

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“…Even though at least two proinflammatory La1 proteins, GroEL and EF-Tu (16), are present at the bacterial surface, intact La1 bacteria do not stimulate IL-8 secretion from intestinal epithelium-like HT29 cells (54) and polarized Caco-2 cells (22) in the presence of sCD14 or peripheral blood mononuclear cells (1) in vitro. The global interpretation could be that the intestinal epithelial cells sense the bacterial surface with its proinflammatory components, like GroEL and EF-Tu, and its anti-inflammatory components, like lipoteichoic acid (53), process the information, and respond with a "consensus" pro-or anti-inflammatory response. In this sense, in vivo shedding of lipoteichoic acid from the La1 surface as a consequence of the stomach's acidic milieu may result in the exposure of the surface-associated proinflammatory molecules, thus favoring the activation of innate defenses.…”

Section: Discussionmentioning

confidence: 99%

“…Cell culture. Nondifferentiated human adenocarcinoma HT29 cells (American Type Culture Collection) were cultured in glucose-containing Dulbecco's modified Eagle's medium (DMEM) as previously described (31,53), and HT29-MTX (methotrexate treated) cells were grown according to Lesuffleur (32). Human peripheral blood mononuclear cells were isolated by density centrifugation on Ficoll (Histopaque-1077; Sigma) from fresh blood obtained from healthy donors.…”

Section: Methodsmentioning

confidence: 99%

“…Cell viability was determined using a cytotoxicity kit (Roche Diagnostic). Detection of IL-8 release was performed as described previously (53).…”

Section: La1 Rgroel Sequence Analysis By Nano-esi-ms (Ms/ms)mentioning

confidence: 99%

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GroEL ofLactobacillus johnsoniiLa1 (NCC 533) Is Cell Surface Associated: Potential Role in Interactions with the Host and the Gastric PathogenHelicobacter pylori

et al. 2006

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Heat shock proteins of the GroEL or Hsp60 class are highly conserved proteins essential to all living organisms. Even though GroEL proteins are classically considered intracellular proteins, they have been found at the surface of several mucosal pathogens and have been implicated in cell attachment and immune modulation. The purpose of the present study was to investigate the GroEL protein of a gram-positive probiotic bacterium, Lactobacillus johnsonii La1 (NCC 533). Its presence at the bacterial surface was demonstrated using a whole-cell enzyme-linked immunosorbent assay and could be detected in bacterial spent culture medium by immunoblotting. To assess binding of La1 GroEL to mucins and intestinal epithelial cells, the La1 GroEL protein was expressed in Escherichia coli. We report here that La1 recombinant GroEL (rGroEL) binds to mucins and epithelial cells and that this binding is pH dependent. Immunomodulation studies showed that La1 rGroEL stimulates interleukin-8 secretion in macrophages and HT29 cells in a CD14-dependent mechanism. This property is common to rGroEL from other gram-positive bacteria but not to the rGroEL of the gastric pathogen Helicobacter pylori. In addition, La1 rGroEL mediates the aggregation of H. pylori but not that of other intestinal pathogens. Our in vitro results suggest that GroEL proteins from La1 and other lactic acid bacteria might play a role in gastrointestinal homeostasis due to their ability to bind to components of the gastrointestinal mucosa and to aggregate H. pylori.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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GroEL ofLactobacillus johnsoniiLa1 (NCC 533) Is Cell Surface Associated: Potential Role in Interactions with the Host and the Gastric PathogenHelicobacter pylori

et al. 2006

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“…The presence of sCD14 has been shown to enable intestinal epithelial cells to respond to LPS in vitro (9,10). Consequently, several immune functions have been proposed for breast milk sCD14 in preventing gastrointestinal Gram-negative infections and stimulating the newborn immune system (10,(17)(18)(19)(20). Despite all the beneficial roles envisaged for sCD14, the in vivo physiologic significance of this milk-borne immune protein remains to be elucidated: does breast milk sCD14 persist throughout the neonatal digestive tract to deliver immune protection?…”

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confidence: 99%

Killing the Messenger in the Nick of Time: Persistence of Breast Milk sCD14 in the Neonatal Gastrointestinal Tract

2006

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Human breast milk contains several proteins that supplement the newborn mucosal defense system and prevent gastrointestinal illnesses. One of these recently identified breast milk proteins is soluble CD14 (sCD14). By being an important component of the lipopolysaccharide (LPS) receptor complex, it has been suggested that breast milk sCD14 could stimulate the newborn immune system and help reduce gastrointestinal Gram-negative infections. However, to deliver its potential immune benefits to the neonate, sCD14 would have to survive the passage through the gastrointestinal tract and retain its biologic activity. We analyzed the presence of breast milk sCD14 in the neonatal digestive system and found breast milk sCD14 to be absent from the stools of breast-fed infants. In vitro digestion analysis with simulated gastric and pancreatic fluids revealed that sCD14 is likely to survive the pepsin digestion but is more prone to been nicked and digested by pancreatin. These findings suggest that the presence of intact breast milk sCD14 in the upper digestive system could promote innate immunity in this low bacteria density lumen. The low concentration of sCD14 in the LPS-rich environment of the distal gastrointestinal tract (i.e. commensal microflora) could prevent excessive inflammation.

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“…LTA is thought to aid in bacterial attachment to host cells (Granato et al, 1999), and is also immunologically active, having previously been demonstrated to elicit proinflammatory cytokine secretion from macrophage cells (Standiford et al, 1994). In contrast to this, LTAs from strains of potentially probiotic lactobacilli were unable to stimulate a proinflammatory response in the HT29 intestinal epithelial cell line, but actively inhibited E. coli-and LPS-induced IL-8 release in these cells (Vidal et al, 2002). Additionally, oral ingestion of LTA (isolated from Staphylococcus aureus), prior to induction of experimental colitis via dextran sulfate sodium, conferred protection in mice with colons depleted of commensal microbiota, subsequently reducing mortality, morbidity and severe colonic bleeding (Rakoff-Nahoum ; therefore it can be hypothesized that the intestinal epithelium is able to distinguish between commensal and pathogenic flagellins simply by the physical exclusion of commensal bacteria.…”

Section: Lipoteichoic Acidmentioning

confidence: 75%

Exploring the immunomodulatory potential of microbial-associated molecular patterns derived from the enteric bacterial microbiota

Patten

Collett

2013

Microbiology

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The human intestinal lumen represents one of the most densely populated microbial niches in the biological world and, as a result, the intestinal innate immune system exists in a constant state of stimulation. A key component in the innate defence system is the intestinal epithelial layer, which acts not only as a physical barrier, but also as an immune sensor. The expression of pattern recognition receptors, such as Toll-like receptors, in epithelial cells allows innate recognition of a wide range of highly conserved bacterial moieties, termed microbial-associated molecular patterns (MAMPs), from both pathogenic and non-pathogenic bacteria. To date, studies of epithelial immunity have largely concentrated on inflammatory pathogenic antigens; however, this review discusses the major types of MAMPs likely to be produced by the enteric bacterial microbiota and, using data from in vitro studies, animal model systems and clinical observations, speculates on their immunomodulatory potential. IntroductionThe intestine represents the body's largest mucosal surface, with the adult human intestine estimated to cover an area of about 250 m 2 (Artis, 2008). The highly folded luminal surface of the intestinal wall significantly increases absorption efficiency and, as such, is the largest surface area of the body exposed to the environment and its high microbial load (DeSesso & Jacobson, 2001). Humans have co-evolved with indigenous microbial populations, termed microbiota, which inhabit various niches of the body (Hooper et al., 2012) and the adult intestine is one of the most densely populated microbial habitations in the biological world (Artis, 2008). The enteric microbiota predominantly consists of bacteria, with estimated populations of~10 14 bacteria, with up to 500 species represented (Gill et al., 2006;Guarner & Malagelada, 2003); however, methanogenic archaea, eukaryotes (yeasts) and viruses (mainly bacteriophages) are also present (Lozupone et al., 2012). Due to the vast expanse of intestinal tissue exposed to the microbiota, the local innate immune system is in a constant state of stimulation, and a chronic, low-level proinflammatory response is characteristic of enteric immune homeostasis (Macpherson & Harris, 2004;Artis, 2008).The intestinal epithelium plays an active role in innate immunity, and pattern recognition receptors (PRRs) are utilized to detect the presence of bacteria and their associated antigens. PRRs are germline-encoded, sensory molecules which recognize a range of highly conserved bacterial motifs, termed 'pathogen-associated molecular patterns' (PAMPs) (Medzhitov, 2001). However, the ability of PRRs to recognize these bacterial moieties is not limited to just pathogens, and so the term 'microbial-associated molecular patterns' (MAMPs) may be more accurate (Medzhitov, 2001; Sanderson & Walker, 2007) and will be used throughout this review. Epithelium-associated, enteric immune cells, such as macrophages, dendritic cells, T-cells and B-cells, differentially express two major groups of PRRs, th...

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Lipoteichoic Acids fromLactobacillus johnsoniiStrain La1 andLactobacillus acidophilusStrain La10 Antagonize the Responsiveness of Human Intestinal Epithelial HT29 Cells to Lipopolysaccharide and Gram-Negative Bacteria

Cited by 104 publications

References 51 publications

GroEL ofLactobacillus johnsoniiLa1 (NCC 533) Is Cell Surface Associated: Potential Role in Interactions with the Host and the Gastric PathogenHelicobacter pylori

GroEL ofLactobacillus johnsoniiLa1 (NCC 533) Is Cell Surface Associated: Potential Role in Interactions with the Host and the Gastric PathogenHelicobacter pylori

Killing the Messenger in the Nick of Time: Persistence of Breast Milk sCD14 in the Neonatal Gastrointestinal Tract

Exploring the immunomodulatory potential of microbial-associated molecular patterns derived from the enteric bacterial microbiota

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