The composition and function of M cell apical membranes: Implications for microbial pathogenesis

Neutra, Marian R.; Mantis, Nicholas J.; Frey, Andreas; Giannasca, Paul J.

doi:10.1006/smim.1999.0173

Cited by 99 publications

(57 citation statements)

References 69 publications

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“…38,39 M cells lack a developed microvillus border and glycocalyx coat, which facilitates access for luminal pathogens and thereby the uptake increases. 2,37 There are large differences between different species regarding markers for M cells. 6 For example, markers have been identified for pig, rabbit and mouse, 7 however, there is today no universal human M-cell marker, which hampers the possibility to elucidate the actual role of M cells in barrier function of the FAE.…”

Section: Discussionmentioning

confidence: 99%

Characterization of antigen and bacterial transport in the follicle-associated epithelium of human ileum

Keita¹,

Gullberg

Ericson

et al. 2006

Laboratory Investigation

100

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The follicle-associated epithelium (FAE), covering Peyer's patches, provides a route of entry for antigens and microorganisms. Animal studies showed enhanced antigen and bacterial uptake in FAE, but no study on barrier function of human FAE has been reported. Our aim was to characterize the normal barrier properties of human FAE. Specimens of normal ileum were taken from 30 patients with noninflammatory colonic disease. Villus epithelium (VE) and FAE were identified and mounted in Ussing chambers. Permeability to 51 Cr-EDTA, transmucosal flux of the protein antigen, horseradish peroxidase (HRP), and transport of fluorescent Escherichia coli (chemically killed K-12 and live HB101) were measured. Uptake mechanisms were studied by confocal-and transmission electron microscopy, and by using pharmacological inhibitors in an in vitro coculture model of FAE and in human ileal FAE. HRP flux was substantially higher in FAE than in VE, and was reduced by an amiloride analog. Electron microscopy showed HRP-containing endosomes. Transport of E. coli K-12 and HB101 was also augmented in FAE and was confirmed by confocal microscopy. In vitro coculture experiments and electron microscopy revealed actin-dependent, mainly transcellular, uptake of E. coli K-12 into FAE. 51 Cr-EDTA permeability was equal in FAE and VE. Augmented HRP flux and bacterial uptake but similar paracellular permeability, suggest functional variations of transcellular transport in the FAE. We show for the first time that FAE of human ileum is functionally distinct from regular VE, rendering the FAE more prone to bacterial-epithelial cell interactions and delivery of antigens to the mucosal immune system.

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Section: Discussionmentioning

confidence: 99%

Characterization of antigen and bacterial transport in the follicle-associated epithelium of human ileum

Keita¹,

Gullberg

Ericson

et al. 2006

Laboratory Investigation

100

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“…10). M cells are unique in that endocytosed materials are rapidly and efficiently delivered to the basolateral side of the epithelium by transcytosis (43). The virus is thereby provided access to JAM1, the viral receptor on basolateral membranes, which can promote infection of adjacent epithelial cells and probably other cells as well (3) (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…This possibility is suggested by the fact that the apical surfaces of absorptive enterocytes are coated with a 400-to 500-nm-thick glycoprotein layer, the filamentous brush border glycocalyx (40), that can serve as a diffusion barrier to particles as small as 30 nm in diameter (21). Most M cells lack this layer (43), and previous studies have shown that 30-and 100-nm particles coated with a ligand specific for membrane gangliosides are capable of binding to their receptors on M cells but not on enterocytes (21,39).…”

mentioning

confidence: 99%

The Viral σ1 Protein and Glycoconjugates Containing α2-3-Linked Sialic Acid Are Involved in Type 1 Reovirus Adherence to M Cell Apical Surfaces

Helander

Silvey

Mantis

et al. 2003

J Virol

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Reovirus is a nonenveloped, 85-nm icosahedral pathogen that enters the mouse intestinal Peyer's patch mucosa by adhering to M cells and then exploiting the antigen-transporting activity of these specialized epithelial cells (2,50,73). When introduced into the intestinal lumens of adult mice, reovirus type 1 Lang (T1L) adheres to the apical surfaces of M cells but generally not to those of enterocytes, which cover the vast majority of the mucosa. It is known that T1L infection of the mouse mucosa in vivo requires proteolytic processing of the viral outer capsid by enzymes in the intestinal lumen (6, 9, 45). The resulting infectious subviral particles (ISVPs) have a cleaved form of the membrane penetration protein 1, have lost the 1-protecting protein 3, and may have the viral hemagglutinin 1 in a more extended conformation than that found in virions (18,20,38,44,45,48). We have previously shown that conversion of T1L virions to ISVPs is required for adherence to M cells in adult mice (2), but neither the T1L protein that mediates binding nor the M cell component recognized by that protein has been identified.The 1 protein serves as the viral adhesin that mediates hemagglutination (HA) and binding to several different types of cultured cells (3,

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“…Microbes and large molecules are sampled on the apical (luminal) side of microfold cells, and their antigens presented at the basal side to mucosal lymphoid elements (26,27), including macrophages and DCs. DCs, the primary antigenpresenting cells of the body, present the antigens locally to T lymphocytes or travel through the lymphatic system and present the antigens, principally in the mesenteric lymph node.…”

Section: Intestinal Mucosamentioning

confidence: 99%

Protection of the Neonate by the Innate Immune System of Developing Gut and of Human Milk

2007

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ABSTRACT:The neonatal adaptive immune system, relatively naïve to foreign antigens, requires synergy with the innate immune system to protect the intestine. Goblet cells provide mucins, Paneth cells produce antimicrobial peptides, and dendritic cells (DCs) present luminal antigens. Intracellular signaling by Toll-like receptors (TLRs) elicits chemokines and cytokines that modulate inflammation. Enteric neurons and lymphocytes provide paracrine and endocrine signaling. However, full protection requires human milk. Breast-feeding reduces enteric infection and may reduce chronic disease in later life. Although human milk contains significant secretory immunoglobulin A (sIgA), most of its protective factors are constitutively expressed. Multifunctional milk components are nutrients whose partial digestion products inhibit pathogens. Cytokines, cytokine receptors, TLR agonists and antagonists, hormones, antiinflammatory agents, and nucleotides in milk modulate inflammation. Human milk is rich in glycans (complex carbohydrates): As prebiotics, indigestible glycans stimulate colonization by probiotic organisms, modulating mucosal immunity and protecting against pathogens. Through structural homology to intestinal cell surface receptors, glycans inhibit pathogen binding, the essential first step of pathogenesis. Bioactive milk components comprise an innate immune system of human milk whereby the mother protects her nursing infant. Interactions between human milk glycans, intestinal microflora, and intestinal mucosa surface glycans underlie ontogeny of innate mucosal immunity, pathobiology of enteric infection, and inflammatory bowel diseases. (Pediatr Res 61: 2-8, 2007)

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The composition and function of M cell apical membranes: Implications for microbial pathogenesis

Cited by 99 publications

References 69 publications

Characterization of antigen and bacterial transport in the follicle-associated epithelium of human ileum

Characterization of antigen and bacterial transport in the follicle-associated epithelium of human ileum

The Viral σ1 Protein and Glycoconjugates Containing α2-3-Linked Sialic Acid Are Involved in Type 1 Reovirus Adherence to M Cell Apical Surfaces

Protection of the Neonate by the Innate Immune System of Developing Gut and of Human Milk

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