Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens

• Published in: Nature reviews. Microbiology Vol. 8; no. 3; pp. 171 - 184
• Main Authors: Lebeer, Sarah, Vanderleyden, Jos, De Keersmaecker, Sigrid C. J.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.03.2010; Nature Publishing Group
• Subjects: 631/250/262/2106; 631/326/41/2531; 631/326/41/547; 692/698/2741/2135; Acids; Animals; Antigens; Bacteria; Bacteria - metabolism; Bacteria, Pathogenic; Biomedical and Life Sciences; Comparative analysis; Gastrointestinal Tract - microbiology; Glycoproteins; Gram-negative bacteria; Gram-positive bacteria; Host-bacteria relationships; Host-Pathogen Interactions; Humans; Infectious Diseases; Life Sciences; Ligands; Lipids; Medical Microbiology; Microbiology; Microbiota; Microorganisms; Mutualism; Parasitology; Pathogens; Pattern recognition; Physiological aspects; Probiotics; Proteins; Receptors, Pattern Recognition - metabolism; review-article; Saccharides; Virology; Belgium
• ISSN: 1740-1526; 1740-1534; 1740-1534
• DOI: 10.1038/nrmicro2297

Key Points The interaction of probiotic surface molecules with host pattern recognition receptors (PRRs) and associated co-receptors plays a key part in the observed health benefits of probiotic bacteria. Flagella, fimbriae, secreted proteins, cell wall-associated polysaccharides (CPSs), lipoteichoic acid (LTA), lipopolysaccharide (LPS) and peptidoglycan (PG) are important probiotic surface molecules that contain microorganism-associated molecular patterns (MAMPs), which are recognized by PRRs. Documented PRRs that can transduce signals on interaction with probiotic surface molecules include Toll-like receptor 2 (TLR2) (in heterodimers with TLR1 or TLR6), TLR4 and TLR5, the C type lectin dentritic cell-specific intercellular adhesion molecule 3-grabbing non-integrin (DC-SIGN) and nucleotide-binding oligomerization domain-containing protein (NOD)-like receptors. These receptors do not function in isolation but cooperate with various co-receptors. PRRs transduce these signals, through associated adaptor proteins that are linked to nuclear factor-κB (NF-κB) and mitogen-activated protein kinase (MAPK) signalling cascades, to the cell nucleus to modulate the expression of response genes that include genes for cytokines, chemokines, antimicrobial peptides, cytoprotective factors and co-stimulatory molecules. Non-phagocytic intestinal epithelial cells and phagocytic DCs differ in their responsiveness for probiotic MAMPs. This is especially relevant for LTA, LPS and PG, as their MAMPs are normally embedded in the cell walls of whole bacterial cells. Some parallels can be drawn between the interactions of the isolated surface molecules of probiotics, commensals and pathogens. However, it is the coordinated sum of the interactions of the various bacterial surface and effector molecules with the PRRs and co-receptors that determines the final host cell response against a certain microorganism. Surface molecules of probiotic bacteria and their host receptors are subject to dynamic regulation as a function of time and space. Glycans are important in these dynamics, possibly modulating ligand–receptor interactions and providing an additional opportunity of discrimination between MAMPs of probiotics, commensals and pathogens. Interactions between host cell receptors and the surface molecules of bacteria are important determinants of the nature of the relationship between the two organisms. In this Review, Lebeer, Vanderleyden and De Keersmaecker examine the signalling interactions of probiotic bacterial cell surface molecules. How can probiotic bacteria transduce their health benefits to the host? Bacterial cell surface macromolecules are key factors in this beneficial microorganism–host crosstalk, as they can interact with host pattern recognition receptors (PRRs) of the gastrointestinal mucosa. In this Review, we highlight the documented signalling interactions of the surface molecules of probiotic bacteria (such as long surface appendages, polysaccharides and lipoteichoic acids) with PRRs. Research on host–probiotic interactions can benefit from well-documented host–microorganism studies that span the spectrum from pathogenicity to mutualism. Distinctions and parallels are therefore drawn with the interactions of similar molecules that are presented by gastrointestinal commensals and pathogens.